Removal of pathogenic bacteria from sewage-treated effluent and biosolids for agricultural purposes

Removal of pathogenic bacteria from sewage-treated effluent and biosolids for agricultural purposes The reuse of treated sewage for irrigation is considered as an important alternative water source in the new water management strategy of the countries that face a severe dec fi iency of water resources such as the Middle East countries. The organic mate - rial and fertilizing elements contained in biosolids are essential for maintaining soil fertility. However, both treated sewage and biosolids contain a large diversity of pathogens that would be transmitted to the environment and infect human directly or indirectly. Therefore, those pathogens should be reduced from the treated sewage and biosolids before the reuse in the agriculture. This paper reviews the considerations for reuse of treated sewage and biosolids in agriculture and further treat- ments used for reduction of pathogenic bacteria. The treatment methods used for the reduction of pathogens in these wastes have reviewed. It appeared that the main concern associated with the reduction of pathogenic bacteria lies in their ability to regrow in the treated sewage and biosolids. Therefore, the effective treatment method is that it has the potential to destruct pathogens cells and remove the nutrients to prevent the regrowth or recontamination from the surrounded environment. The removal of nutrients might be applicable in the sewage but not in the biosolids due to high nutrient contents. However, the reduction of health risk in the biosolids might be carried out by regulating the biosolid utilization and selecting the plant species grown in the fertilized soil with biosolids. Keywords Treated sewage · Biosolids · Pathogenic bacteria · Reuse · Treatment technology · Pathogen growth potential Introduction Sewage effluent is defined as treated or untreated wastewa - ter generated from a treatment plant (US EPA 2009). The treated sewage is classified based on its origin in domestic sewage, hospital sewage and industrial wastewaters. Domes- * A. A. Al-Gheethi tic sewage is a complex mixture containing water together adel@uthm.edu.my with organic and inorganic constituents and large numbers Department of Water and Environmental Engineering, of pathogenic bacteria as well as viruses and parasites (US Faculty of Civil and Environmental Engineering, EPA 2003). Hospital sewage is that coming from the hos- Micro-pollution Research Centre (MPRC), Universiti Tun pitals and medical centres and includes sewage and waste- Hussein Onn Malaysia, Parit Raja, 86400 Batu Pahat, Johor, Malaysia water resulting from the cleaning of laboratories and other facilities. Antibiotics, disinfectants and antibiotic-resistant Environmental Technology Division, School of Industrial Technology, Universiti Sains Malaysia (USM), bacteria are the major constituents in these wastes (due to 11800 Penang, Malaysia their major use in hospital practice) (Pauwels and Verstraete Department of Microbiology, School of Life Sciences, 2006; Jury et al. 2010). Federal University of Technology, P.M.B 65, Minna, Industrial wastewaters are unwanted wastewater from the Niger State, Nigeria industrial operation such as chemical, electrochemical, elec- Botany Department, Faculty of Science, Benha University, tronic, petro-chemical and food-processing industries (US Banha, Egypt EPA 2009). These wastewaters are associated with high Department of Applied Microbiology, Faculty of Applied concentrations of dissolved metal salts (heavy metals) and Sciences, Taiz University, Taiz, Yemen Vol.:(0123456789) 1 3 74 Page 2 of 25 Applied Water Science (2018) 8:74 may include some domestic sewage, but the domestic sew- age is not the main component (Rao et al. 2012; Yachigo and Sato 2013). The sewage sludge is the solid, semisolid or liquid residue generated during the sewage treatment processes (US EPA 1993). The term sewage sludge has been replaced recently by the term biosolids. Biosolids represent sewage sludge that has been treated by advanced processes which included aerobic and anaerobic, heat or lime treatment and has met standards required for beneficial use. The particular characteristics of the biosolids vary depending on their origin (human, vegetable or animal) and the treatment process they have gone through (physical, chemical or biological, anaerobic or aerobic treat- ment, alkaline treatment by lime, etc.). The organic and inor- ganic contents of biosolids are essential for soil and plants (N’Dayegamiye et al. 2002 and Nowak 2007). Fig. 1 Treatment technology selection in relation to the origin of the Solids recovered from industrial processes are also called sewage (Veenstra et al. 1997) sludge and the term is often associated with potentially hazard- ous industrial wastes. Industrial sludge may have little or no agronomic value. Hence, it is important to distinguish those Importance of sewage treatment solids produced from sewage that have value as a fertilizer or soil amendment (John 2005). Human waste has increased tremendously with con- Treated sewage and biosolids contain high concentrations comitant rapid growth of communities and cities. Large of nutrients, which improve plant growth and soil properties. numbers of pathogenic microorganisms such as bacteria, However, it has pathogenic microorganisms such as bacteria, viruses and protozoa parasites have originated from the protozoa, viruses and parasites that can cause several diseases. sewage (US EPA 2003). Poor sanitation and contamina- Land application of treated sewage and biosolids creates tion of drinking water have led to the death of more than a potential for human exposure to these organisms through 2000 children every day under the age five worldwide direct and indirect contact. Therefore, to protect public health (UNICEF 2013). Hence, there is a need for sewage man- from these organisms, many countries have regulated the use agement to advert the magnitude of ecological degradation and disposal of treated sewage and biosolids (Al-Gheethi et al. due to untreated sewage in the environment. Therefore, the 2015). selection of an appropriate technology for the treatment In the field of biosolids, there are some technologies that and disposal of treated sewage requires an analysis of the have been developed which aimed to produce safe biosolids effects that the effluents would have on both agricultural that had to be used as fertilizer in agriculture. The develop- and the environment (Zhou and Smith 2002). ments in this area are less than that in the field of sewage efflu- Biosolid production has been estimated to be 20 × 10 ent treatment. However, some of the advanced technologies tons annually worldwide (Markosyan et al. 2002). Hence, including temperature-phased anaerobic digestion and auto- the management of sewage sludge has been a vital envi- thermal aerobic digestion processes have emerged (Wen et al. ronmental issue worldwide. However, in the Middle East 2009; Jin et al. 2013). Further, the membrane filtration, ionised countries, adoption of a practical, economic and accept- irradiation and oxidation processes by chemical disinfectants able approach in managing and disposing sewage sludge exhibited high treatment efficacy in the improvement of the is not applicable. The present practice is either to reuse for quality of biosolids (Dutta et al. 1999; Aksu and Tunc 2005; agricultural purpose or direct disposal in sea (UN 2003). Gomez et al. 2006; Dungeni et al. 2010; Tripathi et al. 2011). Sewage treatment system is a multistage process to In the present review, the main pathogenic bacteria that remove organic matter, heavy metals, causative agents of exist in treated sewage and biosolids are discussed. The diseases and other pollutants before its disposal or reuse treatment processes most common in the reduction of patho- for the agriculture (Al-Rekabi et  al. 2007; Wani et  al. genic bacteria in treated sewage and biosolids are revealed. 2013). The degree of treatment range from basic process Treatment processes that would produce treated sewage and such as individual septic tanks (ISTs), oxidation ponds, biosolids of higher quality for reuse in agriculture, as well as stabilization ponds, primary and secondary processes for their applicability in Middle East countries and other devel- heavily polluted waste to polishing process (advanced or oping countries, are highlighted. tertiary process) for removing the trace concentrations, 1 3 Applied Water Science (2018) 8:74 Page 3 of 25 74 which remain after the main treatment (Gupta et al. 2000; was recorded in an average of 2200 CFU/100 mL. E. coli Heritage et al. 2003). The final selection of sewage treat- increased from zero/100 mL in boreholes located before ment technology depends on the source of sewage and the plant to 1100 CFU/100 mL boreholes located after the its applicability (Fig. 1). The common sewage treatment plant. The study revealed the role of the treated sewage in processes can be presented as follows. the distribution of pathogenic bacteria into the natural waster system. Disposal and reuse of treated sewage and biosolids The reuse of treated sewage for irrigation is considered as an important alternative water source in the new water In the planning and designing of sewage treatment facili- management strategy of Middle East countries due to the ties, the disposal of treated sewage and biosolids is an inte- severe scarcity of water (UN 2012). In Jordan, 13.8% of all gral part of this structure. After the treatment, both treated water available for irrigation is sewage effluent, this per - sewage and biosolids are discharged into the environment centage is predicted to increase to 25% in 2020 (UN 2003; or reused for agricultural purposes (UN 2003). In Middle Al-Enezi et al. 2004). In Kuwait, approximately 43.9% of East countries, the common practices of treated sewage the sewage effluents are reused for agricultural irrigation. depend on the country’s economic structure. The discharge In Yemen, the farmers use sewage effluents directly from of treated sewage into the natural water is common in the stabilization ponds for irrigation of a wide range of vegeta- coastal cities which takes advantage of the self-purification bles and crops, especially the Qat farming which represents capacity of water bodies for the further treatment of treated about 22.3% of irrigated area (Haidar 2005; Al-Asbahi 2005; sewage (UN 2003; Fine et al. 2006). However, these prac- ACWUA 2010; Ministry of Agriculture and Irrigation 2012; tices are becoming unacceptable due to increase of the UN 2012). However, in Tunisia, Morocco and United Arab smells generated and the volume of the wastes involved as Emirates (UAE), the treated sewage has been used only well as risks to health (Heritage et al. 2003). The extreme for irrigation of gardens in urban centres and tourist facili- quantities of organic compounds may cause a reduction of ties (ACWUA 2010). It can be concluded that the reuse of the dissolved oxygen resources of the natural waters and treated sewage for the irrigation in the Middle East countries rapid bacterial growth. The changes in heavy metal concen- depends mainly on the geographic area and the develop- trations and pH values are harmful to organisms in these ment level for each country. Yemen, Jordan, Kuwait and water bodies (UN 2003). UAE are located in the same geographical area with arid and Recently, many water sources (e.g. seas, rivers, oceans semi-arid environment; however, UAE is more developed and surface water) started to represent health risks for than others. UEA has advanced technologies to the desali- humans due to the disposal of treated sewage contaminated nation of sea water, while Yemen is the least developed in with pathogenic bacteria (Wen et al. 2009; Garcia-Armisen the field of sewage treatment due to the economic status. et al. 2011). A wide variety of microbial pathogens that may Al-Sharabee (2009) reported that 95% of cultivated area in pose a risk to human health are known to be abundant in the zone around SSTP at Yemen (1.2–6.0 km) depends upon the treated sewage and considered the major source of fae- the sewage effluents. Animals in that zone have suffered due cal contamination in aquatic ecosystems (Scott et al. 2003; to intestinal diseases such as liver calcification, swelling of Tyagi et al. 2006). stomach, intestinal worms, diarrhoea, changes the taste of Transmission of infectious pathogenic organisms into milk and mouth blister and farmers are infected by many of rivers and water bodies from sewage effluent discharge pathogenic bacteria because they did not wear plant gloves increases the contamination by pathogenic bacteria such as during the irrigation process (Haidar 2005). Salmonella spp., Shigella spp., P. aeruginosa, S. aureus, E. The highly treated sewage from STPs is not necessarily a coli, V. cholerae, Y. enterocolitica and C. jejuni (US EPA pollutant, rather it represents a nutrient resource for use in 1988; WHO 1993; Santhiya et al. 2011). Discharge of pol- crop production (Gopakumar et al. 2000). The application of luted effluent frequently contaminated sea life, particularly treated sewage and biosolids at a controlled rate can improve fish, cockles and prawns; therefore, people who eat these the physical and chemical properties of soils (Katterman and contaminated seafood could become seriously ill (WHO Day 1989). However, the incessant use of sewage effluents 2001). and biosolids may produce detrimental effects on soil and Santhiya et al. (2011) revealed that the seawater and sedi- crops (US EPA 2004a; Al-Sa`ed 2007). ments polluted with discharged treated sewage in Morocco According to ACWUA (2010), two planning approaches were heavily contaminated with Vibrio sp., Pseudomonas for sewage reuse are applied. First, the intended reuse option sp., Salmonella spp., Shigella sp. and coliforms group. determines the water quality and, therefore, the required Al-Sabahi et  al. (2009) stated that the concentration of treatment technology. This approach allows structured E. coli in three surface water bodies located at the down- planning within a broader wastewater management master stream of treated sewage generated from STP in Ibb-Yemen plan and gives the greatest flexibility for reuse. Second, the 1 3 74 Page 4 of 25 Applied Water Science (2018) 8:74 available effluent qualities of existing treatment plants define increasing of microbial resistance that has occurred as one possible reuse option. This approach is widespread in Mid- of the eminent public health concerns of the twenty-first dle East countries, but considerably limits the reuse of sew- century (Klavarioti et  al. 2009: Velickovic-Radovanovic age and the development of new irrigation options. et al. 2009). Irrigation with treated sewage can lead to accu- Biosolids contain water, sand, organic matter, microor- mulation of pharmaceutical residues like antibiotics in the ganisms, trace metals and other chemicals. Their moisture irrigated soil (Dalkmann et al. 2012). content, humus-like characteristics and essential nutrients Sewage treatment plants are responsible for spreading for plants make biosolids beneficial and safe to use as a soil antibiotic resistance to the natural environment (Laroche conditioner and fertilizer for agriculture purpose (County et  al. 2009; Servais and Passerat 2009; Garcia-Armisen 2005). Nevertheless, the concerns in the reuse of treated et al. 2011). Therefore, the persistence of antibiotic-resistant sewage and biosolids in agriculture lie in the transfer of strains in the treated sewage should be considered if they pathogenic microorganisms to humans directly or indirectly, are used for land disposal or for water utilisation (Vilanova with the direct transmission of microbial pathogens taking and Blanch 2005). Al-Gheethi et al. (2013c) investigated the place via the consumption of effluent-irrigated vegetables prevalence of antibiotic resistance phenotypes among TC, (Heyman 2004). The irrigation of fresh vegetables by sew- E. coli, E. faecalis and Salmonella spp. in the treated sew- age effluents represents the main source of pathogenic bac- age generated from three sewage treatment plants in Penang teria. Some of those pathogens can survive even in washed Malaysia. The study found that TC and E. coli exhibited vegetables (Ronner and Wong 1993). Indirect transmission high resistance for cephalexin, ampicillin and ciprofloxacin of infection occurs when sewage effluents are discharged to compared to E. faecalis and Salmonella spp., respectively. the rivers, reservoirs and canals that supply irrigation water All E. coli strains, 76.18% of TC, 66.66% of E. faecalis and to farmlands (Cotruvo et al. 2004). Contamination of food, 35% of Salmonella spp. had multi-resistance for antibiotics. water and feed transmission may also occur through patho- Al-Gheethi and Ismail (2014) investigated the antimicro- gens in biosolids that are spread on land field areas (Car - bial resistance among total bacterial counts from sewage- lander 2006; Sahlstrom et al. 2006). The indirect pathway treated effluents. The report revealed that about 83.82% of concerns a larger proportion of the human and animal popu- the bacterial isolates were multi-resistant (resistant to three lation than the direct infection pathway. Pathogenic bacteria antibiotics or more). Gram-positive bacteria exhibited more may be taken up by plants and enter into the food chain. multi-resistance to antibiotics (cephalexin, amoxicillin, Movement through the soil and contamination of ground- ampicillin and cefuroxime) than Gram-negative bacteria. water with potential contamination of drinking water, runo ff Based on these studies it can be indicated that the sewage and erosion containing pathogens and contaminating surface effluents represent a rich source of antimicrobial resistance water has been reported (Sahlstrom et al. 2006). bacteria, perhaps due to the high nutrients contents. The potential of pathogenic bacteria to cause infection in human depends on the ability of bacteria to survive in the environment, which is highly dependent on numbers of environmental factors such as temperature, sunlight, mois- Frequently occurred pathogenic bacteria ture, the availability of organic matter, soil pH, soil particles in the treated sewage and biosolids and the presence of toxic substances as well as competi- tive organisms that influence bacterial survival in soils and Treated sewage and biosolids contain many pathogenic sewage (Ibenyassine et al. 2007). AL-Jaboobi et al. (2013) microorganisms, the most important are those transmitted evaluated the quality and suitability of canal sewage, shallow by the faecal–oral route, which includes bacteria, viruses and wells and ponds, in Bani Al-Harth area of Sana’a Yemen, parasites (US EPA 2003; Wen et al. 2009). However, bacte- when used to irrigate vegetable production. The results ria represent then concern due to their ability to increase in revealed high counts of total coliforms, faecal coliforms, E. the environment because it does not require a host cell for coli, E. amnigenus, E. intermedius, E. aerogenes, Klebsiella replication (Ceustermans et al. 2007). The actual species and sp., Citrobacter sp., Serratia sp., Proteus spp. Staphylococ- density of pathogenic bacteria in sewage depend on public cus spp., Vibrio spp., Salmonella spp., yeasts and moulds. health, the size of the local community and the presence of On the other hand, the treatment processes of sewage are hospitals, factories, as well as on sewage treatment processes insufficient to remove antibiotics. Many antibiotics have (Harrison et al. 1999; US EPA 2003; Bitton 2005a). been detected in large quantities in treated sewage and in There is a wide spectrum of pathogenic bacteria that has surface water receiving effluents (Spongberg and Witter been detected in the treated sewage and biosolids, many of 2008). Antibiotics represent an emerging environmental which are enteric in nature (Toze 1997). V. cholera, Lepto- problem due to their disposal into the aquatic ecosystem, spira spp., Salmonella spp., C. jejuni, E. coli O157:H7, Y. even at minimum inhibitory concentrations (MICs) and enterocolitica and Shigella sp. are considered as a major 1 3 Applied Water Science (2018) 8:74 Page 5 of 25 74 concern which could result in disease to the general popu- Salmonella spp. are resistant microorganisms that are lation, while B. cereus, Enterobacter spp., Klebsiella spp., readily adapt to extreme environmental conditions and have C. perfringens, L. monocytogenes, P. aeruginosa, S. aureus the ability to survive under hostile environmental condi- and Streptococcus spp. are the minor concerns which are tions (Espigares et al. 2006; Alvarez-Ordonez et al. 2011). considered opportunistic pathogens that cause disease only These characteristics make them the indicator of choice for in debilitated or immunologically compromised individuals monitoring the effectiveness of biosolid pathogen reduction (Kowal 1983; US EPA 1988; Synnott et al. 2009; Dungeni (US EPA 1995). US EPA (2003) also demonstrated that Sal- et al. 2010; Ellafi et al. 2010; Coronel-Olivares et al. 2011). monella spp. are bacteria of great concern as well as good Markosyan et al. (2002) detected different genera of Kleb- representatives of the reduction of other bacterial pathogens siella, Enterobacter, Hafnia, Serratia, Proteus, Providencia because they are typically present in higher densities than and Escherichia in the biosolids. Younis et al. (2003) iso- other bacterial pathogens and have the ability to survive for lated Salmonella spp., Shigella spp., Vibrio spp., Staphylo- a long time in the environment. coccus spp. and Listeria spp. from STP located in Aswan, Salmonella spp. are the most prevalent bacterial patho- Egypt. Lisle et al. (2004) observed that the untreated sewage gens of public healthcare concern that are frequently found at Memurdo station, Antarctica, contained relatively high in sewage (Dumontet et al. 2001; Espigares et al. 2006). concentrations of total coliforms, faecal coliforms, E. coli, Salmonella spp. can cause diseases to all organisms from enterococci and C. perfringens. Al-Zubeiry (2005) detected insects to mammals (Bohm 2004). Enteric fever is a col- S. aureus, S. pneumonia, E. coli, Salmonella spp. and P. lective term given to the invasive infections caused by S. aeruginosa in raw sewage and secondary effluent generated typhi and S. paratyphi causes paratyphoid fever. S. typhi is a from STP in Ibb, Yemen. El-Lathy et al. (2009) isolated pathogen that only has humans as its natural host (Heritage Salmonella spp., Listeria spp and Vibrio spp. (V. vulnificus, et al. 2003). V. parahaemolyticus and V. cholera) from sewage samples Burtscher and Wuertz (2003) reported that about 48% of from oxidation pond in El-Sadat, Egypt, and biosolids from the 46 biosolids samples tested were positive for Salmonella Zenin sewage treatment plant at Giza, Egypt. Ye and Zhang spp. which could be detected in both untreated and treated (2011) studied the presence of pathogenic bacteria in bio- waste samples during intermediate stages of treatment. How- solids from 14 STPs in China, USA, Canada and Singapore. ever, S. stanley was the only pathogen isolated after the ther- The study detected Aeromonas veronii, A. hydrophila, C. mophilic anaerobic digestion (Sahlstrom et al. 2004). perfringens and C. Diphtheria as most common. Bala et al. (2012) investigated pathogenic bacteria in pharmaceutical Shigella sp. wastewater in Nigeria. They noted that E. coli, Salmonella sp., Klebsiella sp., P. aeruginosa, S. aureus, P. vulgaris, This is a genus of gamma-Proteobacteria in the family Enter- Clostridium sp. and E. faecalis were predominant. obacteriaceae (Brenner et al. 2005), discovered by Kiyoshi Al-Gheethi et al. (2013a) reported that K. pneumonia, Shiga in 1896. They are rod-shaped, Gram-negative, non- E. coli, Shigella sp., Salmonella spp., S. aureus, E. faecalis spore-forming, non-motile bacteria that are very closely and P. aeruginosa are abundant in three STPs in Malaysia. related to E. coli and only humans are always the host (Gel- Al-Gheethi et al. (2014) also investigated the bacterial diver- dreich 1996). Members of the Shigella genus (S. dysente- sity in treated sewage and biosolid samples generated from riae, S. boydii, S. flexneri and S . sonnei) are the major cause five STPs in Yemen. The authors isolated hundred and sixty of dysentery, diarrhoea, fever, vomiting and cramps, which bacterial strains. Among those, E. coli was the most com- frequently occurred in countries that lack potable drinkable mon, followed by S. faecalis, K. pneumonia, E. aerogenes, water such as India (Niyogi 2005). The dysentery bacilli are S. typhi, S. typhimurium, S. sonni and Y. pestis. The most the most common infectious diseases in third world coun- concerned bacteria are discussed below; tries and among travellers to tropical countries (Vila et al. 1994). Shigella spp. are the second pathogenic bacteria that Salmonella spp. cause intestinal diseases in China (Peng et al. 2002). The infectious dose for Shigella sp. was determined to Salmonella spp. are rod-shaped, Gram-negative, non- be as few as 10–100 organisms (Fratamico et al. 2005) and spore-forming, facultatively anaerobic bacteria, discovered the waterborne transmission of shigellosis was documented by Salmon in 1880. This group consists of a range of very epidemiologically (Alamanos et al. 2000). Shigella sp. was closely related bacteria that belongs to the genus Salmonella isolated from pharmaceuticals wastewater, sewage effluents and the family Enterobacteriaceae. Salmonella spp. exhibit and biosolids (Bala et al. 2012; Al-Gheethi et al. 2013a). psychrotrophic properties and actively grow within a wide Chen et al. (2012) found that Shigella sp. survived more temperature range (10–54 °C) (Woteki and Kineman 2003). than Salmonella sp. and E. coli during mesophilic anaerobic digestion of sludge. However, it has been reported previously 1 3 74 Page 6 of 25 Applied Water Science (2018) 8:74 that Shigella sp. does not appear to survive long in the envi- an indicator organism. Thus, it could be useful as an indica- ronment (Gebra 1996). tor of past pollution and as a trace to follow the fate of patho- gens (Bitton 2005b). Vierheilig et al. (2013) investigated C. Escherichia coli O157:H7 perfringens in different faecal sources at Austria for 3 years. They stated that C. perfringens was not suitable as indicator Escherichia. coli is a rod-shaped Gram-negative bacterium, of faecal pollution but they suggested that it could be used which belongs to the family Enterobacteriaceae. They as a tracer for excreta from human sewage. are facultative, oxidase-negative anaerobes and produce gas from glucose. E. coli is a member of the physiologi- Faecal indicator bacteria cal gastrointestinal flora bacterium species for human and warm-blooded animals. Additionally, it belongs to the nor- Analytical techniques for the direct detection and identifi- mal intestinal flora and a facultative pathogen for human cation of many types of pathogenic bacteria in the sewage being (Kaper et al. 2004). However, some E. coli serotypes effluents require well-trained technicians. These techniques are pathogenic, among them enterohaemorrhagic strain E. are usually unpredictable, difficult, costly and time consum- coli O157:H7 which causes gastrointestinal disorders such ing. The faecal organisms which are used as pathogenic indi- as bloody diarrhoea, cramping and abdominal pain and the cator can determine the relative risk of biosolids (Toze 1997; infectious “hemolytic uremic syndrome” (Fijalkowski et al. Wen et al. 2009). 2014). E. coli O157:H7 was first reported as a gastrointes- The indicator bacteria are adapted to living in the gas- tinal pathogen in 1982 (Riley et al. 1983), they are able to trointestinal tract and can be harboured in other different survive in environment for long time without a host (Qing habitats, such as a septic system or sewage collection system et al. 2010). Isolation of E. coli from surface water, treated (Gordon et al. 2002). Indicator organisms are used as models sewage and biosolids has been reported by many investiga- for the behaviour of pathogens, for example, to determine tors (Al-Zubeiry 2005; Jokinen et al. 2010; Al-Gheethi et al. the efficiency of treatment processes, where their growth 2013a; Al-Gheethi et al. 2014). characteristics (temperature and pH) are similar to those of numerous pathogens for which detection and quantification Clostridium perfringens are difficult or sometimes impossible (Lepeuple et al. 2004). Many bacteria have been studied for their suitability as Clostridium. perfringens is an obligate anaerobic Gram- faecal indicators (Ashbolt et al. 2001; US EPA 2007). The positive bacterium, bacilli-shaped and endospore forming. first bacterial species, which had been used as faecal indica- It is a member of the Sulfite-Reducing Clostridia (SRC) tors, were K. pneumoniae and K. rhinoscleromatis, which group. C. perfringens has been isolated from sewage by was suggested by Von Fritsch in 1880 (Geldreich 1978). many researchers (Lisle et al. 2004; Ye and Zhang 2011), However, many bacterial species were also suggested as because it represents 0.5% of the faecal microflora (Leem- indicators. Dancer (2004) has proposed S. aureus as an ing et al. 1998; Payment et al. 2002). Payment and Franco indicator of hospital hygiene for microbiological stand- (1993) recommended this bacterium as an indicator for the ards. Jin et al. (2013) used S. aureus as indicator to evaluate presence of Giardia cysts in water treatment plants as well as the hydrothermal treatment process in achievement of the to evaluate the quality of recreational waters (Fujioka 1997). hygienic safety of food waste. Suresh et al. (1996) confirmed that the use of C. perfrin- Al-Gheethi et al. (2013a) studied the correlation between gens as well as faecal coliforms and faecal streptococci could the frequencies and the numbers of faecal indicators and serve as an excellent approach for identifying the presence of pathogenic bacteria. They found that E. coli has been cor- airborne pathogens and determining their origins or sources related significantly with all pathogenic bacteria investigated associated with the treatment and disposal of wastewater (K. pneumonia, P. aeruginosa, Shigella sp. and Salmonella and biosolids. spp.), E. faecalis has correlated by 75% while total coli- Lepeuple et al. (2004) reported that the C. perfringens is forms and faecal coliforms correlated by 50% with patho- common in raw sludge and resistant to heat, and hence their gens under study. removal can be related to removal of spore-forming spe- In general, the criteria for selection of faecal indicator cies such as Bacillus sp. C. perfringens has been reported as organisms have been documented as follows (Cooper and resistant to oxidizing agents and to UV disinfection (Alonso Olivieri 1998; Dumontet et al. 1999; Bitton 2005a; Myers et al. 2004). Rouch et al. (2011) indicated that C. perfringens et al. 2007): appeared to be a conservative indicator during their study on the air drying of sludge generated from two STPs in Victo- 1. Should be a member of the Enterobacteriaceae family. ria, Australia. However, some authors stated that the hardy 2. The presence of faecal indicators should be associated spores of this bacterium make it too resistant to be useful as with the presence of pathogens. 1 3 Applied Water Science (2018) 8:74 Page 7 of 25 74 3. Numbers should be greater than that of the pathogens. 1998). However, Bitton (2005b) reported that enterococci 4. It should be resistant to the disinfection processes as the are good indicators of faecal pollution like faecal coli- pathogens. forms. Enterococcus species (E. faecium, E. faecalis, E. 5. It should not increase in the environment. avium, E. gallinarum and E. durans) have the ability to 6. Should be easily detected by simple techniques. grow at both 10 and 45 °C, at high pH 9.6 and in medium 7. Should be non-pathogenic. containing 6.5% NaCl (Cooper and Olivieri 1998; Car- valho and Teixeira 2002). This group has been suggested Faecal indicators organisms are discussed below; as useful for indicating the presence of viruses, particu- Total coliforms are groups belonging to Enterobacte- larly in sludge, sea water and biosolids (Bitton 2005b), riaceae and include the aerobic and facultative anaerobic, because these organisms are relatively easy to enumer- rod-shaped, non-spore-forming, Gram-negative bacteria that ate and survive longer than faecal coliforms (Mote et al. ferment lactose with gas production within 48 h at 35 °C 2012). (APHA 1989). These characteristics are suitable for the Enterococci along with faecal coliforms have been used identification of this group and no confirmatory tests are to differentiate human faecal contamination from that of required (Edberg et al. 1990). other warm-blooded animals based on FC/FS ratio, if the Total coliforms include four genera, Escherichia sp., ratio less than 1.0 this means that the source of faecal Enterobacter sp., Klebsiella sp. and Citrobacter sp. Some contamination are all warm-blooded animals other than members of this group, e.g., Klebsiella sp. may grow in man, if the ratio was 4.0, this means the source of fae- industrial waste. They are the historic indicators of faecal cal contamination is human. Intermediate ratios indicate contamination since 100 years ago (Cooper and Olivieri contamination from both man and animals (Young and 1998). Total coliforms are one of the best indicators for treat- Thackston 1999; Baudišová 2009). Enterococci are a more ment efficiency of sewage treatment plants (Bitton 2005b). reliable indicator than faecal coliforms for the detection of Faecal coliforms (FC) are classified under the group of microbial pollution as they are more resistant to the envi- total coliforms and are more faecal specific in origin and ronment than faecal coliforms (Celico et al. 2004). It has include E. coli and other faecal (or thermotolerant) coliforms been frequently considered as reference microorganism that can ferment lactose at 44.5 °C (Kimberly et al. 2005). for thermal treatments to be applied in pasteurized foods The presence of these organisms more accurately correlates (Smith et al. 1990; Ghazala et al. 1991). However, US EPA with warm-blooded animal faecal discharges. However, even (US 2004a) and WHO (1989) did not regulate standards this group contains a genus, Klebsiella with species that are limits of enterococci in treated sewage if the effluents is to not necessarily faecal in origin. Klebsiella sp. is commonly be reused for irrigation or groundwater recharge. associated with textile, pulp and paper mill wastes (US EPA 1986a). According to the US EPA (1992), FC is faecal bacteria that are used as indicators to show probable presence of Regulations of treated sewage and biosolids pathogenic bacteria, because they are easily detected and their densities decline in the same proportion as pathogens To maintain safe reuse of sewage treated effluents, WHO during the treatment process. The EPA Part 503 regulations (1989) reported that the geometric mean of FC should “Standards for the use or disposal of sewage sludge” have be less than 1000 cells/100  mL (Table  1), these stand- established pathogen reduction requirements for FC (US ards are also used in Jordan and Palestine. However, US EPA 2003). EPA (2004b) recommended more stringent standards For recreational waters, FC was the primary bacterial for sewage-treated effluents. FC should not exceed 14 indicator until 1986, when the EPA began recommending cells/100 mL (Table 2). In Saudi Arabia, the standards for E. coli and enterococci as better indicators of health risk sewage effluents reuse in agricultural irrigation are issued from water contact (US EPA 1986a). FC is still being used by the Ministry of Municipal and Rural Affairs (MMRA). in many states of USA as the indicator bacteria. However, According to those standards, FC should be less than 2.2 Byappanahalli and Fujioka (1998) reported that tropical soil cells/100 mL of unrestricted irrigation and less than 1000 environments such as in Hawaii provide sufficient means to cells/100  mL of restricted irrigation (Al-Jasser 2011). support the growth of FC and E. coli. Polo et al. (1998) have The EPA part 503 regulations for the reuse of biosolids shown poor to no correlation between E. coli and Salmonella (CFR 1995) divided stabilization biosolids into “Class A” spp. to FC. Hörman et al. (2004) reported that there was no and ‘‘Class B’’. Class A biosolids must meet either FC correlation between E. coli and Campylobacter spp. limit of less than 1000 MPN g-1 TS or less than 3 Salmo- Enterococci bacteria have been considered useful as nella/4 g TS. Class B biosolids should be meet a FC limit 6 −1 secondary indicators of faecal contamination (APHA of less than 10  MPN g TS. The standards for reuse of 1 3 74 Page 8 of 25 Applied Water Science (2018) 8:74 Table 1 Guidelines for using treated wastewater in agriculture (WHO 1989) Category Reuse conditions Exposed group Intestinal nematode Coliforms Wastewater treatment expected (arithmetic mean no (geometric to achieve the required microbio- b b eggs/L) mean/100 mL) logical guideline A Irrigation of crops likely to be Workers, ≤ 1 ≤ 1000 A series of stabilization ponds eaten uncooked, sports fields, consumers, designed to achieve the micro- public parks public biological quality indicated, or equivalent treatment B Irrigation of cereal crops, Workers ≤ 1 No standard Retention in industrial crops, fodder crops, recommended stabilization ponds pasture and trees for 8–10 days or equivalent hel- minthic and FC removal C Localized irrigation of crops None Not applicable Not applicable Pre-treatment as required by irri- in category B if exposure to gation technology, but not less workers and the public does than primary sedimentation not occur Ascaris and Trichuris species and hookworms During the irrigation period A more stringent guideline (200 FC/100 mL) is appropriate for public lawns, such as hotel lawns, with which the public may come into direct contact In the case of fruit trees, irrigation should cease 2 weeks before fruit is picket, and no fruit should be picked off the ground. Sprinkler irrigation should be used Table 2 Microbiological requirements for reclaimed water (US EPA 2004b) Type of use Treatment Reclaimed water quality Urban uses, food crops eaten raw, recreational Secondary, filtration, disinfection pH = 6–9 impoundments no detectable FC/100 mL Restricted access area irrigation, processed Secondary, disinfection pH = 6–9 food crops, non-food crops, aesthetic 200 FC/100 mL impoundments, construction uses, industrial cooling, environmental reuse Groundwater recharge of potable aquifers by Site-specific secondary and disinfection Site-specific meet drinking water standards spreading (minimum) after percolation through vadose zone Groundwater recharge of potable aquifers by Includes: secondary, filtration, disinfection, Includes: pH = 6–8.5 no detectable FC/100 mL injection, augmentation of surface supplies advanced wastewater treatment Based on 7-day median value. Should not exceed 14 FC/100 mL in any sample Based on 7-day median value. Should not exceed 800 FC/100 mL in any sample sewage effluents and biosolids issued out by the Yemen could be transmitted into rivers and other environment agricultural sector have focused on the basic parameters of during the final disposal or reuse of the effluent (Spong- sewage such as COD, BOD, TS and TSS. However, these berg and Witter 2008). Rizzo et al. (2013) reported that standards are neither met nor controlled, because most of conventional disinfection processes might not be effective STPs are overloading, and Yemeni laboratories are not in the inactivation of antibiotic-resistant bacteria. There- equipped to measure all mentioned parameters (ACWUA fore, to achieve safe reuse of sewage-treated effluents, 2010). advanced treatment technologies have been applied to reduce various potentially harmful compounds that could not be effectively removed by conventional treatment pro- Further treatment of treated sewage cesses. Advanced treatment technologies have high poten- tial to produce an effluent of higher quality than normally Recent studies revealed that detectable amounts of pollut- achieved by secondary treatment processes (Zhou and ants remain in sewage effluents, even after secondary sew - Smith 2002; Jin et al. 2013). The techniques used for this age treatment processes are performed. These pollutants 1 3 Applied Water Science (2018) 8:74 Page 9 of 25 74 purpose include reduction of pathogens by disinfection Chlorination process (Al-Rekabi et al. 2007). Chlorination is the most common method used for disinfec- Disinfection processes of sewage‑treated effluents tion of treated sewage in Middle East countries because it is easily applied, readily available and cheaper than other oxi- The concentrations of faecal indicator bacteria in untreated dising agents. It can also be used to inhibit bacteria growth sewage are 8 log CFU/100  mL for TC, 7.48 log in treated sewage (Gomez et al. 2006). Tree et al. (2003) 10 10 CFU/100 mL for FC and 6.6 log CFU/100 mL for ente- found that chlorination has significant effect in the reduc- rococci (Wilén et  al. 2012). The conventional treatment tion of E. coli and E. faecalis in sewage-treated effluents. processes for sewage (primary and secondary processes) However, the occurrence of pathogenic bacteria in treated remove 95–99% of most microorganisms (Koivunen et al. sewage after chlorination has been observed. Dungeni et al. 2003). However, their numbers in the sewage effluent usu- (2010) stated that despite high free chlorine residual concen- ally remain higher than 4 log  CFU/100 mL (Luczkiewicz trations in sewage-treated effluents, the survival of E . coli, et al. 2010). The stabilization pond was reported to reduce S. typhimurium and V. cholerae was significantly high and 84% of total coliform, 96% of faecal coliform and 89% of they suggested an upgrading of the STPs by other processes enterococci (Reinosoa et al. 2008). The reduction efficacies to increase the inactivation of pathogenic bacteria. CDPH of faecal indicator bacteria by the septic tank and oxidation (2009) reported that the chlorination disinfection system is pond were reported to be 15 and 38% for FC and 11 and 16% the primary disinfection process, and the whole disinfection for FS, respectively (Samhan et al. 2007). of reclaimed water should be performed by the pasteurisa- Many studies have found that the concentrations of fae- tion system. cal indicators in the treated sewage and biosolids are still Moreover, one main disadvantage for utilization of more than the standard limits of US EPA and WHO guide- chlorine disinfection is the presence of free and combined lines. Heng et al. (2006) found that the concentrations of TC chlorine residues which is being toxic to aquatic organisms. in the treated sewage generated from two-oxidation ponds Therefore, the requirement to de-chlorinate or to remove at Kajang and UKM-Malaysia were 8.95 and 8.58 log chlorine residues from the treated sewage before it is dis- CFU/100 mL. Siti Khadijah et al. (2013) reported that the charged into the environment has increased in recent years concentration of FC in the treated sewage from the oxida- due to the potential health hazards of nitrosodimethylamine tion ponds in USM Engineering Campus, Malaysia, were (NDMA) which is reported as a probable human carcinogen also more than WHO guidelines, where FC concentrations (Pehlivanoglu-Mantas et al. 2006). ranged from 2.36 to 5.57 log  CFU/100 mL. Al-Gheethi et al. (2013a) revealed that the concentrations of FC at the three STPs in Penang, Malaysia were greater than the stand- Ozonation ard limits recommended by the WHO guideline for use of treated wastewater in agriculture and US EPA microbiologi- One of the most effective disinfectants used in water disin- cal requirements for wastewater reuse. fection is ozone. This is because ozone has high ability to According to those studies, it can be concluded that the destroy pathogenic cells through an irreversible physiochem- treated sewage still contains high concentrations of patho- ical action. Ozonation destroys the cell wall of the bacteria genic bacteria even after sewage treatment processes. The as well as semi-permeable membrane. The destruction in high bacteria levels in the natural water that received sew- the cell wall and membrane leads to the bacterial cell death age-treated effluent lead to increase in BOD, resulting in (Facile et al. 2000). Tripathi et al. (2011) claimed that 5 min −1 depletion of oxygen levels required for the various types of exposure at a concentration of 10 mg ozone L was suit- of living organisms supported by the estuary. Therefore, able for the inactivation of pathogenic bacteria by 95–98%. treated sewage needs to undergo further treatment to reduce Previous studies reported that ozone effectively removes TC the density of pathogenic bacteria to achieve a favourable and FC from sewage-treated effluents. Battaler et al. (2005) sanitary effluent quality (Koivunen et al. 2003; Jin et al. found that the ozone disinfection of secondary effluents at −1 2013). Disinfection process of effluents increases the reduc - concentration 4.7 mg L for 5 min had eliminated TC and −1 tion of pathogens for high-quality reuse (Crook 1998; Neis FC. At 21.4 mg L the bacteria that resisted for chlorine and Blume 2002). The tertiary treatment is able to achieve such as P. aeruginosa decreased by 2 log reduction after the guidelines of WHO and US EPA standards for pathogen 5 min of disinfection process by ozone. inactivation. The development of a tertiary treatment pro- Disinfection of treated sewage by ozone is applied cess includes all techniques that offer significantly higher because the use of ozone is cheap and low energy is needed. removal of pathogenic bacteria. The most common disinfec- Nonetheless, the effectiveness of disinfection using ozone tion processes of treated sewage are discussed below. depends on the ozone dose, the ozone demand, the quality 1 3 74 Page 10 of 25 Applied Water Science (2018) 8:74 of the effluent and the transfer efficiency of the ozone sys- on the UV radiation, photo-oxidation and temperature (Sect. tem (Paraskeva and Graham 2002). The COD and total sus- “Solar disinfection (SODIS)”). pended solids (TSS) of treated sewage might affect the effi- ciency of disinfection process by ozone (Janex et al. 2000). Filtration technology The properties of the treated sewage might induce the micro- bial resistance for the ozone as noted for Enterococcus sp., Filtration systems are designed to remove very small particu- Clostridium sp. and Salmonella spp. which exhibit resistance late or “suspended” solids from the treated sewage. Onnis- to ozonation (Xu et al. 2002). Hayden et al. (2011) evaluated sand filtration technology In USA, the disinfection of drinking water by ozona- in the disinfection of sewage generated by STPs and found tion process is more attractive disinfection method due to that the E. coli concentration reduced to below 2 logs in the promulgation of the EPA’s restrictions of disinfection the filtered sewage-treated effluents. Despite its high effi - by-products (DBPs) permitted in America’s drinking water ciency in the removal of pathogenic bacteria and producing attributable to chlorination. Nevertheless, ozonation can effluents with good microbiological quality, the effluents also lead to the formation of potentially harmful by-products would not be considered as sterile, since contamination of inclusive of bromate ions (BrO ), aldehydes and peroxides. permeation zones gave rise to the presence of pathogenic Vital et al. (2010) reported that the major concern associated bacteria (Gomez et al. 2006). At the same time, the mem- with the ozone application lies in the increase in microbial brane filtration systems are expensive with regard to con- regrowth due to the oxidation process which generates the struction and maintenance (Neis and Blume 2002). Different assimilable organic carbon (AOC). filtration systems have been developed which depend on the utilization of raw and low-cost materials such as sands and UV irradiation ceramic (Mohamed et al. 2016). These systema have exhib- ited high efficiency in the reduction of the main parameters Disinfection by ultraviolet irradiation has been reported as of wastewater such as COD, BOD and TSS, but their effi- a suitable technology for inactivating coliforms and Sal- ciency in the reduction of pathogenic bacteria still needs monella spp. (Keller et al. 2003). The principle of a UV more investigation. disinfection system is to destroy the genetic material of the bacterial cell and thus retard its ability to reproduce (US Storage of treated sewage EPA 1986b). The effectiveness of a UV disinfection system depends on the characteristics of the effluents including the Storage systems are used typically for accumulating waste- concentration of the sewage effluent, the intensity of the UV water before its ultimate disposal, or for temporarily holding radiation and the time of the treatment (Kollu and Ormeci batch streams before treatment (US EPA 1989). A storage 2012). basin was also used for treating effluent storage, especially Nasser et al. (2006) revealed that the treated sewage dis- during winter in temperate country. The stored effluents will infected by UV is suitable for the unrestricted irrigation of be released to environment normally during the rainy season food crops (FC < 1000 CFU/100 mL). Dungeni et al. (2010) where the dilution rate is higher (Al-Gheethi et al. 2017). suggested UV disinfection as an additional treatment process Storage of sewage has become the option selected in of effluents to increase the effective inactivation and removal European and Mediterranean countries because of the of pathogenic bacteria and viruses. However, Alonso et al. advantages they present in comparison with other treatment (2004) found that Clostridium spp., showed a greatest degree alternatives. This includes the coupling of two purposes: of resistance to UV treatment. Munir et al. (2010) indicated stabilization and seasonal regulation to regulate between that the disinfection of effluents by UV process did not con- sewage production and demand of treated wastewater for tribute to the significant reduction of antibiotic-resistant irrigation (Barbagallo et al. 2003). bacteria. Ting et al. (2011) observed a re-growth and repair Al-Gheethi et  al. (2013a) studied the effect of stor- potential of E. coli, FC and B. subtilis in reclaimed water age of treated sewage on survival of faecal indicators and after UV disinfection. Wang et al. (2012) suggested that Salmonella spp. and the susceptibility of these bacteria the higher number of particles in the treated sewage might to antibiotics during the storage period. The treated sew- have protected the bacteria against UV damage. Based on age was stored at room temperature for 28 days. The study those studies, it can be indicated that UV technology might noted that FC density in stored effluents dropped from have a limitation for the sewage disinfection. But it has to be 5.182  log  CFU/100 mL to below 2 log   CFU/100  mL 10 10 motioned that the disinfection processes of the treated sew- after 28 days and the treated sewage met WHO guidelines. age might be more effective as two methods have been used E. faecalis decreased to less than detection limits during the simultaneously such as the solar disinfection which depends storage period of 1 week. However, they observed that TC and Salmonella spp. which have survived during the storage 1 3 Applied Water Science (2018) 8:74 Page 11 of 25 74 period acquired more resistance to antibiotics. At the end of US EPA. The sewage effluents can be reused for irrigation the storage period, TC and Salmonella spp. were resistant purpose. to cephalexin, cefuroxime, ampicillin and amoxicillin. The study concluded that the storage system of treated sewage Solar disinfection (SODIS) would increase the distribution of antimicrobial resistance among bacterial population after the disposal or reuse of SODIS-based technologies are an efficient approach for the treated sewage for agricultural purposes. Indeed, the effi- reduction of pathogenic microorganism in the water due to ciency of the storage system on the reduction of pathogenic high availability of solar radiation and sustainable nature of bacteria depends mainly on the storage temperature, the stor- these water treatment methods (Gomez-Couso et al. 2009). age system at the room temperature might be effective for According to WHO (2002), SODIS depends on using trans- the reduction of pathogenic bacteria but it needs long time parent polyethylene terephthalate (PET) bottles and then to achieve high reduction of pathogens and then to meet exposing to the sun for a period between 4 and 8 h. Mei- the international standards required for the sewage disposal erhofer and Wegelin (2002) recommended that PET bot- or reuse of the sewage for the irrigations (Al-Gheethi et al. tles containing untreated raw water should be exposed to 2017). The mechanism which takes place in the storage direct sunlight for at least 6 h. Bacteria, viruses, Giardia system and leads to the reduction of pathogens might be and Cryptosporidium cysts, and parasite eggs could be the competition process between microorganisms due to inactivated through the combination of ultraviolet radiation the deficiency in the nutrients contents (Al-Gheethi et al. and elevated water temperature. Large field tests of SODIS 2016a). were conducted in a number of countries in South America, Africa, and Asia in the 90s (Acra 1990). Heat pasteurization The destruction of the bacterial cells takes place due to the combination of UV radiation and high temperature Heat disinfection is a proven technology in Europe that which has high potential to destroy the cell membrane (Al- requires skills such as boiler operation and the understand- Gheethi et al. 2015). However, SODIS has no efficiency ing of high-temperature and -pressure processes. The EPA for the reduction of chemical pollutants in the water. The Part 503 regulations (US EPA 2003) consider pasteurisa- sunlight has been reported as the single most important dis- tion as a process to further reduce pathogen (PFRP). CDPH infection factor in the stabilization pond (Leduc and Gehr (2009) reported that the use of pasteurisation is recognised 1990; Maynard et al. 1999). Three main mechanisms are as an acceptable disinfection process for meeting the inac- involved during the SODIS simultaneously, included the tivation criteria of coliform bacteria. It is a known fact that absorption of solar UV-B by microorganism DNA which pathogenic bacteria are inactivated during exposure to heat, causes direct damage by pyrimidine dimer formation. The especially when the temperature of the treatment is above process is independent of oxygen and other pond condi- the optimum temperature of growth (Himathongkham and tions. The second mechanism depends on the absorption of Riemann 1999). Lucero-Ramirez (2000) reported that path- UV-B and some shorter wavelength UV-A by cell constitu- ogenic bacteria are reduced to less than detectable levels ents including DNA (called endogenous photo-sensitisers). in properly operated heat-drying systems. Alcalde et  al. The activated constituents react with oxygen to form highly (2003) indicated that the retention time and temperature are reactive photo-oxidising species that damage genetic mate- the most important factors for the removal of pathogenic rial within the cell or viral particle. The third mechanism bacteria. involves absorption of a wide range of UV and visible wave- Bacteria can be classified into different groups based on lengths in sunlight by extra-cellular constituents of the pond optimum temperature. Most human pathogenic bacteria are medium (exogenous photo-sensitisers—notably humic mate- mesophilic (10–40  °C) with an optimum temperature of rial) (Jagger 1985). 37 °C. Metabolic enzymes of bacteria denature and inactive Al-Gheethi et al. (2013b) investigated the effect SODIS when exposed to temperature above its optimum. This even- on the survival of FC, E. faecalis, Salmonella spp. and S. tually led to the death of the bacterial cell. Removal of faecal aureus in treated sewage inside PET bottles. The study indicators (enterococci and E. coli) in piggery effluents to revealed high reduction of FC, Salmonella spp. and S. achieve hygiene standards could easily be met by treatment aureus by more than 4 log  CFU/100 mL after 6 h, while at 60 °C (Cunault et al. 2011). Al-Gheethi et al. (2013a) these pathogens were below the detection limits after 8 h investigated the heat treatment of treated sewage at different as detected by using the enrichment medium. The treated temperatures (45, 55 and 65 °C). They found that the sewage sewage met US EPA (2004a) standards after 6  h, where effluents disinfected at 45 °C for 192 h, 55 °C for 24 h and FC counts were less than 14  CFU/100  mL. SODIS has 65 °C for 30 min have met standard limits regulated by the several advantages to the reduction of faecal indicator in treated sewage compared to the others techniques such as 1 3 74 Page 12 of 25 Applied Water Science (2018) 8:74 chlorination, UV irradiation and ozonation. SODIS is com- matter (WHO 2002). Chemical treatment is sometimes used patible to meet the standards of the disinfection processes of and it encourages small particles and dissolved substances sewage treated effluents. This is because SODIS is effective, to form large particles which facilitate separation. This is more efficient, easily implementable and lower cost. SODIS called chemical precipitation. Sludge is formed when these is a natural process that produces no toxic by-product (Al- larger particles clump together during suitable separation Gheethi 2014). methods (Casey 1997). SODIS is more appropriate to be applied in the develop- All the sludge that is separated during these treatment ing countries that do not have the facilities to build typi- methods (mechanical, biological and chemical) is defined as cal sewage treatment plants. The climate of many Middle a raw sludge, which has to undergo various kinds of further East countries such as Yemen, Saudi Arabia, Oman, Jordan treatment for the improving the microbiological quality and and Egypt is semi-arid to arid and the temperatures during then for safe disposal or reuse. Physical, chemical and bio- summer season vary from 27 to 50 °C (FAO 2008). These logical processes accomplish the stabilization and disinfec- countries also have a large space of the deserts. The desert tion of sewage sludge. Stabilization refers to those processes temperatures range from 45 to 60 °C in summer and from that reduce the volatile solids content, pathogen levels and 7 to 35 °C in the winter and the sunlight intensity ranges odour. The biosolids generated from sewage treatment pro- from 5.2 to 6.8 kWh/m /day (Al-Ashwal and Basalah 2012). cesses must be subject to further treatment to reduce patho- Therefore, one of the proposals to reduce the environment genic bacteria which are still high in concentrations even pollution by sewage generated from STPs is by extending the after the treatment processes (Al-Gheethi et al. 2014). Dis- sewerage network to the desert. The desert provides many of infection processes emphasize the reduction of pathogenic the features of SODIS necessary to treat the sewage effluents bacteria below detectable limits. Major stabilization meth- such as the large areas and the temperature and the treated ods include anaerobic digestion, aerobic digestion, compost- sewage could be used in the land reclamation. ing, alkaline (lime) stabilization and air-drying. Disinfection includes pasteurization, long-term storage, irradiation, heat Reduction of pathogenic bacteria in biosolids drying and heat treatment (US EPA 2003). According to US EPA, there are two processes are used to Sewage treatment processes can be classified as primary and the reduction of pathogenic bacteria to comply the standards secondary processes. In primary treatment, solids are mainly limits of biosolids (Class A and B). These processes named removed mechanically from untreated sewage. Secondary Processes to Further Reduce Pathogens (PFRPs, Table 3) treatment is a biological process in which decomposers are and Processes to Significantly Reduce Pathogens (PSRPs, utilized to remove biodegradable pollutants. Decompos- Table 4). The details of the most common treatment pro- ers are organisms such bacteria and fungi that get energy cesses are described below. and nutrients by digesting waste matter in the sewage. In the activated sludge process, sewage is pumped into a large tank where aerobic microorganisms decompose the organic Table 3 Processes to Further Reduce Pathogens (PFRPs). Source; US EPA (2003) Treatment process Procedure of the treatment process Composting Using either the within-vessel composting method or the static aerated pile composting method, the tempera- ture of sewage sludge is maintained at 55 °C or higher for 3 consecutive days. Using the windrow composting method, the temperature of the sewage sludge is maintained at 55 °C or higher for 15 consecutive days or longer. During the period when the compost is maintained at 55 °C or higher, there shall be a minimum of five turnings of the windrow Heat drying Sewage sludge is dried by direct or indirect contact with hot gases to reduce the moisture content of the sewage sludge to 10% or lower. Either the temperature of the sewage sludge particles exceeds 80 °C or the wet bulb temperature of the gas in contact with the sewage sludge as the sewage sludge leaves the dryer exceeds 80 °C Heat treatment Liquid sewage sludge is heated to a temperature of 180 °C or higher for 30 min Thermophilic aerobic digestion Liquid sewage sludge is agitated with air or oxygen to maintain aerobic conditions and the mean cell residence time (i.e., the solids retention time) of the sewage sludge is 10 days at 55–60 °C Beta ray irradiation Sewage sludge is irradiated with beta rays from an electron accelerator at dosages of at least 1.0 megarad at room temperature (ca. 20 °C) Gamma-ray irradiation Sewage sludge is irradiated with gamma rays from certain isotopes, such as Cobalt 60 and Cesium 137, at dos- ages of at least 1.0 megarad at room temperature (ca. 20 °C) Pasteurization The temperature of the sewage sludge is maintained at 70 °C or higher for 30 min or longer 1 3 Applied Water Science (2018) 8:74 Page 13 of 25 74 Table 4 Processes to significantly reduce pathogens (PSRPs). Source; US EPA (2003) Treatment process Procedure of the treatment process Composting Using either the within-vessel, static aerated pile, or windrow composting methods, the temperature of the sewage sludge is raised to 40 °C (104 °F) or higher and remains at 40 °C or higher for 5 days. For 4 h during the 5 day period, the temperature in the compost pile exceeds 55 °C Aerobic digestion Sewage sludge is agitated with air or oxygen to maintain aerobic conditions for a specific mean cell residence time (i.e., solids retention time) at a specific temperature. Values for the mean cell residence time and temperature shall be between 40 days at 20 °C and 60 days at 15 °C Air drying Sewage sludge is dried on sand beds or on paved or unpaved basins. The sewage sludge dries for a minimum of 3 months. During 2 of the 3 months, the ambient average daily temperature is above 0 °C Anaerobic digestion Sewage sludge is treated in the absence of air for a specific mean cell residence time (i.e., solids retention time) at a specific temperature. Values for the mean cell residence time and temperature shall be between 15 days at 35–55 °C and 60 days at 20 °C Lime stabilization Sufficient lime is added to the sewage sludge to raise the pH of the sewage sludge to 12 for ≥ 2 h of contact Anaerobic digestion Ziemba and Peccia (2011) evaluated mesophilic, ther- mophilic, temperature-phase, and high-temperature (60 or Anaerobic digestion is a biological process that uses bacte- 70 °C) batch pre-treatment digester configurations for E . coli and E. faecalis inactivation potential. The results revealed ria that function in an oxygen-free environment to convert volatile solids into carbon dioxide, methane and ammo- that the inactivation rates have increased dramatically at temperatures above 55 °C. In mesophilic treatment, 1–2 log nia. Those reactions take place in an enclosed tank that may or may not be heated, because the biological activity inactivation was recorded, while was 2–5 log inactivation at 50–55 °C in thermophilic and temperature-phase treatments. consumes most of the volatile solids needed for further bacterial growth (US EPA 2003). The mesophilic anaero- Incorporating a 60 or 70 °C batch pre-treatment phase has achieved completed inactivation (over 100 log reductions) bic digestion (MAD) of biosolids has been reported to produce biosolids Class B, this treatment process is com- of E. coli and E. faecalis. Chen et al. (2012) investigated inactivation of Salmo- mon in USA (Wong et al. 2010). However, most Middle East countries used air-drying as will be presented below nella sp. E. coli and Shigella sp. during mesophilic anaero- bic digestion of biosolids. They found that the anaerobic (Sect. “Air drying”). Telles et al. (2002) investigated the reduction of TC, FC, digestion process efficiency reduces Salmonella sp. and E . coli during the retention time from 11 to 25 day. However, P. aeruginosa and FS by anaerobic digestion of sewage sludge generated from STP in Maringá-Paraná, Brazil. The the reduction of Shigella sp. was insignificant. However, the long period of the treatment process (25 days) might study showed that 99.9% of FS, 96.3% of TC and 95% of P. aeruginosa were reduced at the end of the treatment process. lead to increase the overload of the STP and thus required high capacity to store the received sewage before the treat- These findings revealed the potential of anaerobic digestion in the reduction of pathogenic bacteria from the biosolids. ment process. Astals et al. (2012) studied the mesophilic anaerobic digestion, thermophilic anaerobic digestion and Wakelin et al. (2003) showed that FC was reduced from −1 −1 7.5 log  CFU g in the raw sewage to 6.3 log  CFU g mesophilic anaerobic digestion followed by a 60 °C or by 10 10 an 80 °C hygienization treatment of sewage sludge. They in dewatered biosolids after mesophilic anaerobic digestion process. The main pathogen-reducing factor during thermo- recorded that both thermophilic anaerobic digestion and mesophilic anaerobic digestion followed by a hygieniza- philic anaerobic digestion is temperature in relation to time, while the competition among microorganisms for nutrients is tion step reduced E. coli to meet the standards limits rec- ommended by US EPA and the European legislation for the limiting factor that reduces pathogen amounts in anaero- bic mesophilic treatment of biosolids (Smith et al. 2005). It land application. According to aforementioned studies, the anaerobic can be noted that the thermophilic treatment is more efficient than the mesophilic because the biosolids have high contents digestion process of biosolids showed potential for effec- tive reduction of pathogenic bacteria to meet the stand- of nutrients; therefore, the competition between microorgan- isms in the biosolids is weak. Carrington (1998) also eluci- ards limits recommended by US EPA. However, Viau and Peccia (2009) detected Legionella pneumophila, S. aureus dated that temperature is not the main factor in mesophilic anaerobic digestion processes at 35 °C, but this process pro- and C. difficile in biosolids generated from 29 STPs in USA which was treated with mesophilic, temperature- duces fatty acids and other products that are lethal to many pathogenic bacteria. phase anaerobic digestion and composting process, which 1 3 74 Page 14 of 25 Applied Water Science (2018) 8:74 indicates to the ability of some pathogenic bacteria to process depends very much on the local climate. Drying survive in the biosolids even after the thermophilic treat- occurs faster and more completely in warm and dry weather ment. This might be due to the presence solids materials and slower and less completely in cold and wet weather. The which might protect the bacterial cells form the tempera- density of pathogenic bacteria is reduced by approximately ture actions. Chen et al. (2011) indicated that the patho- 2 log under these conditions of air drying. However, this genic bacteria in the treated biosolids could regrow again reduction is not enough to produce high quality of biosol- during the storage periods of biosolids. This is due to the ids for safe disposal. More disadvantage of air drying is the microbial response to substrate release and environmen- deficiency in the produce biosolids with only 38% volatile tal changes, such as oxygen, which favour the bacterial solids destruction (US EPA 2003). regrowth during 1–2 weeks of storage period. Ward et al. (1981) studied the response of Klebsiella, Enterobacter, Proteus mirabilis, S. typhimurium, E. coli Aerobic digestion and S. faecalis to the moisture loss through evaporation at 21 °C. In raw sterilized sludge with 5% solids, seeded enteric In aerobic digestion, biosolids are biochemically oxidized by bacteria initially increased in concentration with dewatering. bacteria in an open or enclosed vessel. Under proper operat- This increase was always followed by a consistent decrease ing conditions, the volatile solids in biosolids are converted in numbers with further dewatering, especially below 50% to CO and H O (US EPA 2003). The PSRPs described moisture. A 1–2 log reduction was seen for all bacterial 2 2 aerobic digestion as follows: Sewage sludge is agitated with strains except Proteus sp. which showed a 4 log reduction oxygen to maintain aerobic condition for indigenous cell. within 7 days as biosolids percent solids increased to 95%. Time and temperature shall be between 40 days at 20 °C and Rouch et al. (2011) examined the inactivation of E. coli 60 days at 15 °C. Aerobic digestion carried out according to and C. perfringens during the air-drying of anaerobically the part 503 requirement typically reduces pathogenic bac- digested biosolids generated from two STPs in Victoria, teria by 2 log (US EPA 2004a). Kabrick and Jewell (1982) Australia. The results found that E. coli were reduced to 2 −1 found that Salmonella spp. was reduced to undetectable below 10 CFU g dry solids after drying of 8–15 days and levels in an aerobic reactor at 35 °C in 24 h, while at 60 °C the biosolids met US EPA standards for Class A. C. perfrin- Salmonella spp. was eliminated in few hours. gens appeared to be a better indicator. Han et  al. (2011) studied the efficiency of anaerobic Air-drying of biosolids is common in Middle East coun- lagoon fermentation (ALF) and autothermal thermophilic tries because the climate is semi-arid to arid and the tem- aerobic digestion (ATAD) for removal of pathogenic bac- peratures range from 27 to 50 °C (FAO 2008). Besides, this teria in raw swine manure. The results revealed that in raw process is not expensive and easily implementable. However, swine manure, Dialister pneumosintes, Erysipelothrix rhu- one of the major disadvantages of this process is the vector siopathiae, Succinivibrioan dextrinosolvens, and Schine- attractions, which increase as result to volatile solids in the ria sp. were detected. ATAD exhibited more efficiency to biosolids. The pathogens are transmitted from air-drying eliminate of these pathogens than ALT. In the mesophilic basin by the vectors to animals and human (Palmgren 2002). ALF-treated swine manure, Schineria sp. and Succinivibrio STPs in Yemen overcame this problem by using pesticide dextrinosolvens were still detected, while were undetected in but this method leads to accumulate of pesticide in the lands ATAD. These findings support the superiority of ATAD in during land application of biosolids. To overcome the vec- selectively reducing potential human and animal pathogens tor attraction, US EPA recommended that the reduction of compared to ALF, which is a typical manure stabilization VS % should be more than 38%. The lime stabilization was method used in livestock farms. In a comparison between reported to achieve these standards as will be presented in aerobic and anaerobic treatment of biosolids, it can be indi- section 10.6. Another way to prevent the vector attraction cated that the anaerobic process is more efficient than the is by covering the air-drying basin by transparent polyeth- aerobic process, but the limitations to apply the anaerobic ylene terephthalate (PET) as in the case of SODIS of water treatment lie in the design and the maintenance in the devel- and wastewater. However, more research is needed in this oping countries. regards. Air‑drying Eec ff t of storage Air-drying allows partially digested biosolids to dry natu- Biosolids are stored inside buildings and outside enclosed rally in the open air. Wet biosolids are usually applied to in steel or concrete tanks. The storage duration of biosol- a depth of approximately 23 cm onto sand drying beds or ids could strongly affect the survival of pathogenic bac- even deeper (US EPA 2000). The sewage sludge is left to teria. During storage, the biosolids undergo biochemical dry by the evaporation. The effectiveness of the air-drying changes, which depend on the storage temperature. These 1 3 Applied Water Science (2018) 8:74 Page 15 of 25 74 changes effect on the survival of pathogenic bacteria. The growth temperature. The period of exposure is depended on storage of biosolids at low temperatures prolong pathogens the temperature as well as the bacterial species (Himathong- survival, while at high storage temperatures free ammonia kham and Riemann 1999). which would shorten the pathogens chances for survival is The total inactivation of pathogenic bacteria in biosol- produced (Svoboda and Carcluie 2003). ids requires a holding time of 4.78 h at 60 °C compared Ahmed and Sorensen (1995) evaluated pathogen inac- to 30 min at 70 °C (US EPA 1994). Moce-Llivina et al. tivation during storage of biosolids. The pathogens tested (2003) recorded significant reductions in indigenous E . coli included S. typhimurium, Y. enterocolitica, Campylobacter to below detectable levels after 30 and 90 min at 80 °C. The jejuni. Biosolids samples seeded with the pathogens were indigenous FS was only reduced between 1.4 and 1.8 log incubated under both anaerobic and aerobic conditions in units after 30 min but undetectable after 90 min. S. choler- reactors at 5, 22, 38 and 49.5 °C for up to 62 days. They aesuis cells that were added to sludge at high counts were revealed that pathogenic bacteria decreased in stored bio- reduced by approximately 6 log after 30 min at 80 °C and solids at all temperatures and survival decreased as the tem- by more than 8 log after 60 min at 80 °C. They concluded perature increased. that temperature of 80 °C for 30–60 min would probably Liu (2000) observed that FC in biosolids was inactivated qualify the biosolids product as Class A requirements. naturally by storing the sample in an airtight container The EPA Part 503 regulations consider heat drying as at room temperature (20–23  °C). This natural inactiva- PFRPs and suggest that, the temperature of the biosolids tion started after 17–28 days of storage and FC were not should exceed 80 °C but no time is given treatment period. detected after 100 days of storage. However, FC density in In other instances, it seems clear that processes using higher samples stored at − 22 and 4 °C had no significant reduc- than 60–70 °C can produce biosolids Class A (Springthorpe tion in 3 months. Nicholson et al. (2000) recorded that slight and Sattar 2004). increases in temperature during summer destroy E. coli Abdel-Monem et al. (2008a) investigated the inactivation O157 and radically decrease number of Salmonella after a of TC, FC, FS and Salmonella spp. in biosolids by thermal few months. treatment at 60 and 80 °C. The study revealed that the inac- Placha et  al. (2001) found that in pig slurry, S. typh- tivation of Salmonella spp. and FS was significantly greater imurium survived for 26 days in summer and 85 days in than the inactivation of TC at 80 °C for 90 min. After heat winter and FC were reduced by 90% in 35 and 233 days treatment at 80 °C for 120 min, TC reduced by 5.5 log during summer and winter time, respectively. However, stor- while FC, FS and Salmonella were undetected and the bio- age alone is not regarded as an effective way to inactivate solids met the US EPA, Class A standards for biosolids pathogens in sludge (Carrington 1998). Avery et al. (2005) reuse. monitored the decline in E. coli O157 in different wastes over 64 days. They concluded that the storage decreases the Lime stabilization treatments amount of E. coli O157 but does not eliminate the pathogen. According to Sahlstrom et al. (2006), the sludge is stored The principle objectives of alkaline stabilization are to usually for 6 months, in heaps outdoors on the ground or reduce the activity of pathogenic bacteria and inhibit their on a concrete surface, before being used. After 2 months regrowth and thus reduce the health hazard associated with of storage of sewage sludge, no Salmonella spp. could be the biosolids (WEF 1995). The most commonly used alka- isolated in the heaped material. Al-Gheethi et al. (2014) line is the quick lime (calcium oxide, CaO) and its derivative observed that the biosolids stored for 24 weeks at room tem- hydrated lime or slaked lime (calcium hydroxide, Ca(OH) ) perature (25 ± 2 °C) met the standards limits recommended which are used due to their low cost. Adding adequate vol- by US EPA, Class A, and suitable for reuse in the agriculture ume of CaO to the biosolids leads to increase of pH to 12 as fertilizers. (or higher) and temperature to be between 55 and 70 °C, and as results for these conditions the pathogenic bacteria are Heat treatments inactivated or destroyed (Hansen et al. 2007). Plachy et al. (1996) demonstrated that S. typhimurium Heat drying involves using active or passive dryers to was eliminated from biosolids after 60  min of hydrated destroy pathogens and remove water from biosolids. In this lime addition. Reimers (1997) found that the inactivation process, biosolids are dried with hot gases at temperatures of pathogenic bacteria by lime was not only because of the greater than 80 °C to reduce the moisture content to 10% or hydroxide ions but also because of silicate components in lower. Pathogenic bacteria, viruses, and helminth ova are lime. This conclusion was derived from studies by compar- reduced to below detectable levels in properly operated heat- ing pathogen inactivation effects of sodium hydroxide and drying systems (Lucero-Ramirez 2000). Pathogenic bacteria calcium hydroxide. According to Schwartzbrod et al. (1997) are inactivated during exposure to heat, above their optimum the raising of the pH to at least pH 12 by the use of lime has 1 3 74 Page 16 of 25 Applied Water Science (2018) 8:74 −1 −1 the effect to suspend microbiological activity and lime con- 42.65  g  kg TS and 91.41% with 133.52  g  kg after ditioning in specific conditions (pH of 12.5 for 2-4 months) 120 h. can cause helminths reduction by 98.5% and a virus inactiva- Toth et al. (2012) investigated the alkaline treatment of tion by 90%, while biosolids met the Class B requirements animal manures by hydrated lime (CaOH ) to eliminate when the pH was 12 or above after 2 h of contact. S. enterica and E. coli O157:H7. They found that both Amer (1997) studied the effect of quick lime (CaO) pathogens were killed when pH was more than 11.0 within and cement dust additions to biosolids on the reduction of 2 weeks. Farzadkia and Bazrafshan (2014) studied the lime pathogenic bacteria. Rapid reduction in TC, Salmonella stabilization of biosolids on the inactivation of FC. The and Shigella counts were achieved after the addition of study was conducted in a reactor for 6 weeks, the biosolids quick lime and cement dust. US EPA (2000) reported that stabilization with hydrated lime reduced FC more than biosolids Class A requirements can be achieved when the 99.99% and the stabilized biosolids met US EPA standards pH of the mixture is maintained at or above 12 for at least limits of class B. 72 h, with a temperature of 52 °C maintained for at least 12 h during the period. Bina et al. (2004) investigated the effect of liming on Pathogen growth potential (PGP) the microbiological quality of urban liquid raw biosolids. The lime was added to increase the pH of biosolids to pH PGP is defined as the ability of inactivated bacteria to re- 11 and 12 for 2, 24, 72 and 120 h. Salmonella spp. were grow again in the disinfected sample. The effectiveness inactivated completely in treated biosolids after 2 h. 99% of disinfection process for treated sewage and biosolids of FC reduction was obtained for two ranges of pH (pH 11 depends on inactivation of pathogenic bacteria. However, and 12). Biosolids treated with lime met US EPA stand- it is well known that under unfavourable conditions, bac- ards for Class B and Class A after 2 and 24 h, respec- teria may transfer into a dormant state called viable but tively. At pH higher than pH 11 and 12 treated biosolids non-culturable (VBNC), which mean the microorganism with lime met vector attraction reduction requirements has slow metabolic processes and no cell division (Oli- after 2 h. ver 2005). Therefore, the development of the detection, Sasdkovd et al. (2005) stored biosolids amended with enumeration and viability assessment of pathogenic bac- zeolite and lime for 42 days at a temperature between 14.5 teria in biosolids is required (Sidhu and Toze 2009). For and 17.9 °C. Samples were taken at 5-day intervals for the microbial cell, death is the irreversible loss of microbial determination of TC, FC and FS. The results revealed a cell to growth and reproduction. To verify this fact the decrease in plate counts of the observed bacteria in exper- isolation on solid culture medium is the suitable method. imental substrates compared to the control biosolids. The microbial cell is considered dead if they fail to form −1 Yurtsever (2005) found that about 150–200 g CaO kg colonies. However, the cultural based technique depends TS is satisfactory for keeping pH on recommended levels on culture medium used. Bacteria may fail to grow on and to reduce FC to less than detectable limits. solid media and need to be cultured first in enrichment In alkaline treatment study conducted by Abdel- media (Block 2001; Efaq et al. 2015). Monem et al. (2008b), the results revealed that 19.12 g The condition of storage for disinfected sample affect −1 of quicklime kg TS reduced FC to meet the require- the ability of bacteria to regrow, for example, bacterial ments of US EPA standards for Class B after 2  h and inactivation by UV irradiation may reach to 99.99%, but Class A criteria after 24 h. Salmonella spp. reduced to if the disinfected sample stored at optimal conditions the −1 meet Class A criteria after 120 h. At 29.41 g kg TS, FC regrowth of inactivated bacteria may reach to 90%. This and Salmonella spp. dropped to below US EPA Class A means the bacteria can repair damage caused by UV. Al- −1 limit after 24 h. At 42.65 g kg TS, FC has reduced to Gheethi et al. (2013b) found that Salmonella spp. S. aureus below detection level after 24 h and Salmonella after 2 h. and E. faecalis grow again in treated sewage exposed to US EPA requirements for Class B met after 2 h, while the SODIS for 6 h, when the samples were incubated at 37 °C requirements for Class A met for Salmonella spp. after for 4 days. The bacterial regrowth may occur if the treat- −1 2 h and FC after 24 h. Finally, 133.52 g kg TS of lime ment process did not lead to physical damage of bacterial was found to be very effective, Salmonella spp. and FC cell and PGP bioassay should be carried out (Al-Gheethi were inactivated completely after 2 h. To reduce vector et al. 2016a, b; Efaq et al. 2017). PGP has been used to attraction, US EPA recommended that the reduction of assay bacterial growth in drinking water disinfected by VS % should be more than 38% (US EPA 2003). In the ozonation and different bio-filter systems (Berney et al. study conducted by Al-Gheethi (2008), the mass of vola- 2006; Vital et al. 2010). tile solids in the biosolids has reduced by 63.47% with Choi et al. (1999) stated that the main factors, which convert dormant bacteria cell to be active, the factors 1 3 Applied Water Science (2018) 8:74 Page 17 of 25 74 included the incubation and substrate addition such as glu- some limitations especially when applied to environmental cose, amino acids or yeast extract. Luna et al. (2002) found samples. that after nutrient enrichment, a large fraction of dormant Some researchers used the culture method and the molec- bacteria (6–11% of the inactivated bacterial number) was ular analysis to investigate the presence of pathogenic bac- reactivated. teria in the VBNC state. Jiang et al. (2013) combined the The factors, which might induce bacterial cell to be standards culture method (MPN technique) with the reverse VBNC, are less nutrients, nucleotide, inactive cell mem- transcription quantitative PCR (RT-qPCR) assay for the brane, size of bacterial cells and presence of antibiotics, quantification of S . typhimurium, E. coli and S, flexneri in which inhibit DNA synthesis without affecting other cellu- the VBNC state during anaerobic digestion of biosolids. lar metabolic activities (Gasoll et al. 1995; Joux and LeB- They revealed that the cycle threshold (C ) values from RT- aron 1997; Luna et al. 2002; Kim et al. 2009). Therefore, qPCR assays have significant correlation to the counts of 2 2 some authors recommended using molecular techniques E. coli (R  = 0.9964), S. typhimurium (R  = 0.9938) and such as PCR to detect the presence of VBNC bacteria after S. flexneri ( R  = 0.997). In addition, they stated that the disinfection process (Straub et al. 1993; Choi et al. 1996). quantification results of VBNC pathogens using RT-qPCR Chen et al. (2012) determined log reduction of Salmonella could provide an improved evaluation of pathogen inactiva- sp., E. coli and Shigella sp. during mesophilic anaerobic tion efficiency and biological safety in the biosolids. digestion of sludge by MPN and PCR. They found that log Real-time quantitative polymerase chain reaction (qPCR) reduction determined by MPN was much higher than the is fast, sensitive, and specific molecular tool for enumera- data recorded by quantitative PCR. They explained their tion of pathogens in biosolids. However, the main limita- findings due to the presence of viable but non-culturable tion is that it amplifies all target DNAs, including that from pathogen cells. non-viable cells. Therefore, to overcome this limitation the However, other investigators reported that PCR technique authors suggested that the couple qPCR with PMA (van is not suitable after disinfection process as PCR can still Frankenhuyzen et al. 2011) or EMA (Fijalkowski et al. 2014) recognize or detect the DNA fragments of the bacterial cells can be used to monitor the presence of viable pathogens in that have been killed during disinfection processes, thus, several different matrices. yielding false positive results (Baloda and Krovacek 1994). Fijalkowski et al. (2014) detected the presence of E. coli O157:H7 in wastewater and sewage sludge in Poland by Current status of sewage treatment quantitation method of (EMA) real time-PCR. They found in Middle East countries that E. coli O157:H7 gene copies were detected in primary influents and final effluents in winter from municipal waste- In the Middle East countries, there is no plan to build ter- water treatment plant. However, the ethidium monoazide tiary treatment systems (except some STPs in Riyadh, Saudi bromide (EMA) application revealed false-positive detec- Arabia which use sand filters as a tertiary treatment process, tion of this bacterium in final effluents. They also detected Al-Jasser 2011). They focus on the basic standard of pri- large amount of “free DNA” derived from dead cells that mary and secondary treatment. Most sewage is reused for gave false-positive results. agricultural irrigation purpose. This is due to increase in In the last decades, authors have detected the viability of population growth rate, besides present expansion of water bacterial cells based on metabolic activity, such as detection networks in these countries without parallel construction of of RNA transcripts, a positive energy status and responsive- new sewage network, or rehabilitation of the existing ones ness. The detected RNA transcripts were used to detect via- (Abdel-Raouf et al. 2012). ble cells in combination with DNA amplification techniques. Most treated sewage and biosolids generated from STPs The technology depends on the treatment of bacterial cells in Middle East countries have not met the standards limits with photoactivatable, and cell membrane impermeant with required by WHO and US EPA. Saleem et al. (2001) inves- nucleic acid intercalating dyes propidium monoazide (PMA) tigated the counts FC during summer and winter seasons in or ethidium monoazide (EMA) followed by light exposure the drying biosolids generated from Al-Khobar sewage treat- prior to extraction of DNA and amplification. Light acti- ment plant in Saudi Arabia. They found that FC was more vation of DNA-bound dye molecules results in irreversible than standards limits required for US EPA, Class B. El-Lathy DNA modification and subsequent inhibition of its ampli- et al. (2009) reported that the concentrations of Salmonella fication. Sample pre-treatment with viability dyes has been spp., in biosolids generated from Zenin sewage treatment used in combination with PCR (leading to the term viability plant at Giza Governorate, Egypt were 330 CFU/mL, which PCR,v-PCR), and increasingly with isothermal amplifica- means the biosolids, has not met the standards limits recom- tion method (Fittipaldi et al. 2012). This technique still has mended by US EPA for biosolids Class A. AL-Jaboobi et al. (2013) stated that FC in the treated sewage canal generated 1 3 74 Page 18 of 25 Applied Water Science (2018) 8:74 from STP (primary and secondary processes) located in are efficient, easily implementable, natural, with no toxic Sana’a Yemen was more than WHO guidelines. Al-Gheethi by-products and most of all are of low cost. et al. (2014) evaluated the efficiency of five STPs in Yemen Open Access This article is distributed under the terms of the Crea- for reduction of faecal indicators and pathogenic bacteria in tive Commons Attribution 4.0 International License (http://creat iveco the secondary effluents and biosolids. They also found that mmons.or g/licenses/b y/4.0/), which permits unrestricted use, distribu- FC was more than WHO guidelines for sewage effluents as tion, and reproduction in any medium, provided you give appropriate well as US EPA Class A, and B for biosolids. credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. In comparison to developed countries, Rose et al. (2004) investigated the efficiency of six STPs in USA for reduction of FC. All STPs used primary treatment, four STPs used the biological treatment (activated sludge), one STP used References nitrification and one STP used biological nutrient removal. 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Removal of pathogenic bacteria from sewage-treated effluent and biosolids for agricultural purposes

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Earth Sciences; Hydrogeology; Water Industry/Water Technologies; Industrial and Production Engineering; Waste Water Technology / Water Pollution Control / Water Management / Aquatic Pollution; Nanotechnology; Private International Law, International & Foreign Law, Comparative Law
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10.1007/s13201-018-0698-6
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Abstract

The reuse of treated sewage for irrigation is considered as an important alternative water source in the new water management strategy of the countries that face a severe dec fi iency of water resources such as the Middle East countries. The organic mate - rial and fertilizing elements contained in biosolids are essential for maintaining soil fertility. However, both treated sewage and biosolids contain a large diversity of pathogens that would be transmitted to the environment and infect human directly or indirectly. Therefore, those pathogens should be reduced from the treated sewage and biosolids before the reuse in the agriculture. This paper reviews the considerations for reuse of treated sewage and biosolids in agriculture and further treat- ments used for reduction of pathogenic bacteria. The treatment methods used for the reduction of pathogens in these wastes have reviewed. It appeared that the main concern associated with the reduction of pathogenic bacteria lies in their ability to regrow in the treated sewage and biosolids. Therefore, the effective treatment method is that it has the potential to destruct pathogens cells and remove the nutrients to prevent the regrowth or recontamination from the surrounded environment. The removal of nutrients might be applicable in the sewage but not in the biosolids due to high nutrient contents. However, the reduction of health risk in the biosolids might be carried out by regulating the biosolid utilization and selecting the plant species grown in the fertilized soil with biosolids. Keywords Treated sewage · Biosolids · Pathogenic bacteria · Reuse · Treatment technology · Pathogen growth potential Introduction Sewage effluent is defined as treated or untreated wastewa - ter generated from a treatment plant (US EPA 2009). The treated sewage is classified based on its origin in domestic sewage, hospital sewage and industrial wastewaters. Domes- * A. A. Al-Gheethi tic sewage is a complex mixture containing water together adel@uthm.edu.my with organic and inorganic constituents and large numbers Department of Water and Environmental Engineering, of pathogenic bacteria as well as viruses and parasites (US Faculty of Civil and Environmental Engineering, EPA 2003). Hospital sewage is that coming from the hos- Micro-pollution Research Centre (MPRC), Universiti Tun pitals and medical centres and includes sewage and waste- Hussein Onn Malaysia, Parit Raja, 86400 Batu Pahat, Johor, Malaysia water resulting from the cleaning of laboratories and other facilities. Antibiotics, disinfectants and antibiotic-resistant Environmental Technology Division, School of Industrial Technology, Universiti Sains Malaysia (USM), bacteria are the major constituents in these wastes (due to 11800 Penang, Malaysia their major use in hospital practice) (Pauwels and Verstraete Department of Microbiology, School of Life Sciences, 2006; Jury et al. 2010). Federal University of Technology, P.M.B 65, Minna, Industrial wastewaters are unwanted wastewater from the Niger State, Nigeria industrial operation such as chemical, electrochemical, elec- Botany Department, Faculty of Science, Benha University, tronic, petro-chemical and food-processing industries (US Banha, Egypt EPA 2009). These wastewaters are associated with high Department of Applied Microbiology, Faculty of Applied concentrations of dissolved metal salts (heavy metals) and Sciences, Taiz University, Taiz, Yemen Vol.:(0123456789) 1 3 74 Page 2 of 25 Applied Water Science (2018) 8:74 may include some domestic sewage, but the domestic sew- age is not the main component (Rao et al. 2012; Yachigo and Sato 2013). The sewage sludge is the solid, semisolid or liquid residue generated during the sewage treatment processes (US EPA 1993). The term sewage sludge has been replaced recently by the term biosolids. Biosolids represent sewage sludge that has been treated by advanced processes which included aerobic and anaerobic, heat or lime treatment and has met standards required for beneficial use. The particular characteristics of the biosolids vary depending on their origin (human, vegetable or animal) and the treatment process they have gone through (physical, chemical or biological, anaerobic or aerobic treat- ment, alkaline treatment by lime, etc.). The organic and inor- ganic contents of biosolids are essential for soil and plants (N’Dayegamiye et al. 2002 and Nowak 2007). Fig. 1 Treatment technology selection in relation to the origin of the Solids recovered from industrial processes are also called sewage (Veenstra et al. 1997) sludge and the term is often associated with potentially hazard- ous industrial wastes. Industrial sludge may have little or no agronomic value. Hence, it is important to distinguish those Importance of sewage treatment solids produced from sewage that have value as a fertilizer or soil amendment (John 2005). Human waste has increased tremendously with con- Treated sewage and biosolids contain high concentrations comitant rapid growth of communities and cities. Large of nutrients, which improve plant growth and soil properties. numbers of pathogenic microorganisms such as bacteria, However, it has pathogenic microorganisms such as bacteria, viruses and protozoa parasites have originated from the protozoa, viruses and parasites that can cause several diseases. sewage (US EPA 2003). Poor sanitation and contamina- Land application of treated sewage and biosolids creates tion of drinking water have led to the death of more than a potential for human exposure to these organisms through 2000 children every day under the age five worldwide direct and indirect contact. Therefore, to protect public health (UNICEF 2013). Hence, there is a need for sewage man- from these organisms, many countries have regulated the use agement to advert the magnitude of ecological degradation and disposal of treated sewage and biosolids (Al-Gheethi et al. due to untreated sewage in the environment. Therefore, the 2015). selection of an appropriate technology for the treatment In the field of biosolids, there are some technologies that and disposal of treated sewage requires an analysis of the have been developed which aimed to produce safe biosolids effects that the effluents would have on both agricultural that had to be used as fertilizer in agriculture. The develop- and the environment (Zhou and Smith 2002). ments in this area are less than that in the field of sewage efflu- Biosolid production has been estimated to be 20 × 10 ent treatment. However, some of the advanced technologies tons annually worldwide (Markosyan et al. 2002). Hence, including temperature-phased anaerobic digestion and auto- the management of sewage sludge has been a vital envi- thermal aerobic digestion processes have emerged (Wen et al. ronmental issue worldwide. However, in the Middle East 2009; Jin et al. 2013). Further, the membrane filtration, ionised countries, adoption of a practical, economic and accept- irradiation and oxidation processes by chemical disinfectants able approach in managing and disposing sewage sludge exhibited high treatment efficacy in the improvement of the is not applicable. The present practice is either to reuse for quality of biosolids (Dutta et al. 1999; Aksu and Tunc 2005; agricultural purpose or direct disposal in sea (UN 2003). Gomez et al. 2006; Dungeni et al. 2010; Tripathi et al. 2011). Sewage treatment system is a multistage process to In the present review, the main pathogenic bacteria that remove organic matter, heavy metals, causative agents of exist in treated sewage and biosolids are discussed. The diseases and other pollutants before its disposal or reuse treatment processes most common in the reduction of patho- for the agriculture (Al-Rekabi et  al. 2007; Wani et  al. genic bacteria in treated sewage and biosolids are revealed. 2013). The degree of treatment range from basic process Treatment processes that would produce treated sewage and such as individual septic tanks (ISTs), oxidation ponds, biosolids of higher quality for reuse in agriculture, as well as stabilization ponds, primary and secondary processes for their applicability in Middle East countries and other devel- heavily polluted waste to polishing process (advanced or oping countries, are highlighted. tertiary process) for removing the trace concentrations, 1 3 Applied Water Science (2018) 8:74 Page 3 of 25 74 which remain after the main treatment (Gupta et al. 2000; was recorded in an average of 2200 CFU/100 mL. E. coli Heritage et al. 2003). The final selection of sewage treat- increased from zero/100 mL in boreholes located before ment technology depends on the source of sewage and the plant to 1100 CFU/100 mL boreholes located after the its applicability (Fig. 1). The common sewage treatment plant. The study revealed the role of the treated sewage in processes can be presented as follows. the distribution of pathogenic bacteria into the natural waster system. Disposal and reuse of treated sewage and biosolids The reuse of treated sewage for irrigation is considered as an important alternative water source in the new water In the planning and designing of sewage treatment facili- management strategy of Middle East countries due to the ties, the disposal of treated sewage and biosolids is an inte- severe scarcity of water (UN 2012). In Jordan, 13.8% of all gral part of this structure. After the treatment, both treated water available for irrigation is sewage effluent, this per - sewage and biosolids are discharged into the environment centage is predicted to increase to 25% in 2020 (UN 2003; or reused for agricultural purposes (UN 2003). In Middle Al-Enezi et al. 2004). In Kuwait, approximately 43.9% of East countries, the common practices of treated sewage the sewage effluents are reused for agricultural irrigation. depend on the country’s economic structure. The discharge In Yemen, the farmers use sewage effluents directly from of treated sewage into the natural water is common in the stabilization ponds for irrigation of a wide range of vegeta- coastal cities which takes advantage of the self-purification bles and crops, especially the Qat farming which represents capacity of water bodies for the further treatment of treated about 22.3% of irrigated area (Haidar 2005; Al-Asbahi 2005; sewage (UN 2003; Fine et al. 2006). However, these prac- ACWUA 2010; Ministry of Agriculture and Irrigation 2012; tices are becoming unacceptable due to increase of the UN 2012). However, in Tunisia, Morocco and United Arab smells generated and the volume of the wastes involved as Emirates (UAE), the treated sewage has been used only well as risks to health (Heritage et al. 2003). The extreme for irrigation of gardens in urban centres and tourist facili- quantities of organic compounds may cause a reduction of ties (ACWUA 2010). It can be concluded that the reuse of the dissolved oxygen resources of the natural waters and treated sewage for the irrigation in the Middle East countries rapid bacterial growth. The changes in heavy metal concen- depends mainly on the geographic area and the develop- trations and pH values are harmful to organisms in these ment level for each country. Yemen, Jordan, Kuwait and water bodies (UN 2003). UAE are located in the same geographical area with arid and Recently, many water sources (e.g. seas, rivers, oceans semi-arid environment; however, UAE is more developed and surface water) started to represent health risks for than others. UEA has advanced technologies to the desali- humans due to the disposal of treated sewage contaminated nation of sea water, while Yemen is the least developed in with pathogenic bacteria (Wen et al. 2009; Garcia-Armisen the field of sewage treatment due to the economic status. et al. 2011). A wide variety of microbial pathogens that may Al-Sharabee (2009) reported that 95% of cultivated area in pose a risk to human health are known to be abundant in the zone around SSTP at Yemen (1.2–6.0 km) depends upon the treated sewage and considered the major source of fae- the sewage effluents. Animals in that zone have suffered due cal contamination in aquatic ecosystems (Scott et al. 2003; to intestinal diseases such as liver calcification, swelling of Tyagi et al. 2006). stomach, intestinal worms, diarrhoea, changes the taste of Transmission of infectious pathogenic organisms into milk and mouth blister and farmers are infected by many of rivers and water bodies from sewage effluent discharge pathogenic bacteria because they did not wear plant gloves increases the contamination by pathogenic bacteria such as during the irrigation process (Haidar 2005). Salmonella spp., Shigella spp., P. aeruginosa, S. aureus, E. The highly treated sewage from STPs is not necessarily a coli, V. cholerae, Y. enterocolitica and C. jejuni (US EPA pollutant, rather it represents a nutrient resource for use in 1988; WHO 1993; Santhiya et al. 2011). Discharge of pol- crop production (Gopakumar et al. 2000). The application of luted effluent frequently contaminated sea life, particularly treated sewage and biosolids at a controlled rate can improve fish, cockles and prawns; therefore, people who eat these the physical and chemical properties of soils (Katterman and contaminated seafood could become seriously ill (WHO Day 1989). However, the incessant use of sewage effluents 2001). and biosolids may produce detrimental effects on soil and Santhiya et al. (2011) revealed that the seawater and sedi- crops (US EPA 2004a; Al-Sa`ed 2007). ments polluted with discharged treated sewage in Morocco According to ACWUA (2010), two planning approaches were heavily contaminated with Vibrio sp., Pseudomonas for sewage reuse are applied. First, the intended reuse option sp., Salmonella spp., Shigella sp. and coliforms group. determines the water quality and, therefore, the required Al-Sabahi et  al. (2009) stated that the concentration of treatment technology. This approach allows structured E. coli in three surface water bodies located at the down- planning within a broader wastewater management master stream of treated sewage generated from STP in Ibb-Yemen plan and gives the greatest flexibility for reuse. Second, the 1 3 74 Page 4 of 25 Applied Water Science (2018) 8:74 available effluent qualities of existing treatment plants define increasing of microbial resistance that has occurred as one possible reuse option. This approach is widespread in Mid- of the eminent public health concerns of the twenty-first dle East countries, but considerably limits the reuse of sew- century (Klavarioti et  al. 2009: Velickovic-Radovanovic age and the development of new irrigation options. et al. 2009). Irrigation with treated sewage can lead to accu- Biosolids contain water, sand, organic matter, microor- mulation of pharmaceutical residues like antibiotics in the ganisms, trace metals and other chemicals. Their moisture irrigated soil (Dalkmann et al. 2012). content, humus-like characteristics and essential nutrients Sewage treatment plants are responsible for spreading for plants make biosolids beneficial and safe to use as a soil antibiotic resistance to the natural environment (Laroche conditioner and fertilizer for agriculture purpose (County et  al. 2009; Servais and Passerat 2009; Garcia-Armisen 2005). Nevertheless, the concerns in the reuse of treated et al. 2011). Therefore, the persistence of antibiotic-resistant sewage and biosolids in agriculture lie in the transfer of strains in the treated sewage should be considered if they pathogenic microorganisms to humans directly or indirectly, are used for land disposal or for water utilisation (Vilanova with the direct transmission of microbial pathogens taking and Blanch 2005). Al-Gheethi et al. (2013c) investigated the place via the consumption of effluent-irrigated vegetables prevalence of antibiotic resistance phenotypes among TC, (Heyman 2004). The irrigation of fresh vegetables by sew- E. coli, E. faecalis and Salmonella spp. in the treated sew- age effluents represents the main source of pathogenic bac- age generated from three sewage treatment plants in Penang teria. Some of those pathogens can survive even in washed Malaysia. The study found that TC and E. coli exhibited vegetables (Ronner and Wong 1993). Indirect transmission high resistance for cephalexin, ampicillin and ciprofloxacin of infection occurs when sewage effluents are discharged to compared to E. faecalis and Salmonella spp., respectively. the rivers, reservoirs and canals that supply irrigation water All E. coli strains, 76.18% of TC, 66.66% of E. faecalis and to farmlands (Cotruvo et al. 2004). Contamination of food, 35% of Salmonella spp. had multi-resistance for antibiotics. water and feed transmission may also occur through patho- Al-Gheethi and Ismail (2014) investigated the antimicro- gens in biosolids that are spread on land field areas (Car - bial resistance among total bacterial counts from sewage- lander 2006; Sahlstrom et al. 2006). The indirect pathway treated effluents. The report revealed that about 83.82% of concerns a larger proportion of the human and animal popu- the bacterial isolates were multi-resistant (resistant to three lation than the direct infection pathway. Pathogenic bacteria antibiotics or more). Gram-positive bacteria exhibited more may be taken up by plants and enter into the food chain. multi-resistance to antibiotics (cephalexin, amoxicillin, Movement through the soil and contamination of ground- ampicillin and cefuroxime) than Gram-negative bacteria. water with potential contamination of drinking water, runo ff Based on these studies it can be indicated that the sewage and erosion containing pathogens and contaminating surface effluents represent a rich source of antimicrobial resistance water has been reported (Sahlstrom et al. 2006). bacteria, perhaps due to the high nutrients contents. The potential of pathogenic bacteria to cause infection in human depends on the ability of bacteria to survive in the environment, which is highly dependent on numbers of environmental factors such as temperature, sunlight, mois- Frequently occurred pathogenic bacteria ture, the availability of organic matter, soil pH, soil particles in the treated sewage and biosolids and the presence of toxic substances as well as competi- tive organisms that influence bacterial survival in soils and Treated sewage and biosolids contain many pathogenic sewage (Ibenyassine et al. 2007). AL-Jaboobi et al. (2013) microorganisms, the most important are those transmitted evaluated the quality and suitability of canal sewage, shallow by the faecal–oral route, which includes bacteria, viruses and wells and ponds, in Bani Al-Harth area of Sana’a Yemen, parasites (US EPA 2003; Wen et al. 2009). However, bacte- when used to irrigate vegetable production. The results ria represent then concern due to their ability to increase in revealed high counts of total coliforms, faecal coliforms, E. the environment because it does not require a host cell for coli, E. amnigenus, E. intermedius, E. aerogenes, Klebsiella replication (Ceustermans et al. 2007). The actual species and sp., Citrobacter sp., Serratia sp., Proteus spp. Staphylococ- density of pathogenic bacteria in sewage depend on public cus spp., Vibrio spp., Salmonella spp., yeasts and moulds. health, the size of the local community and the presence of On the other hand, the treatment processes of sewage are hospitals, factories, as well as on sewage treatment processes insufficient to remove antibiotics. Many antibiotics have (Harrison et al. 1999; US EPA 2003; Bitton 2005a). been detected in large quantities in treated sewage and in There is a wide spectrum of pathogenic bacteria that has surface water receiving effluents (Spongberg and Witter been detected in the treated sewage and biosolids, many of 2008). Antibiotics represent an emerging environmental which are enteric in nature (Toze 1997). V. cholera, Lepto- problem due to their disposal into the aquatic ecosystem, spira spp., Salmonella spp., C. jejuni, E. coli O157:H7, Y. even at minimum inhibitory concentrations (MICs) and enterocolitica and Shigella sp. are considered as a major 1 3 Applied Water Science (2018) 8:74 Page 5 of 25 74 concern which could result in disease to the general popu- Salmonella spp. are resistant microorganisms that are lation, while B. cereus, Enterobacter spp., Klebsiella spp., readily adapt to extreme environmental conditions and have C. perfringens, L. monocytogenes, P. aeruginosa, S. aureus the ability to survive under hostile environmental condi- and Streptococcus spp. are the minor concerns which are tions (Espigares et al. 2006; Alvarez-Ordonez et al. 2011). considered opportunistic pathogens that cause disease only These characteristics make them the indicator of choice for in debilitated or immunologically compromised individuals monitoring the effectiveness of biosolid pathogen reduction (Kowal 1983; US EPA 1988; Synnott et al. 2009; Dungeni (US EPA 1995). US EPA (2003) also demonstrated that Sal- et al. 2010; Ellafi et al. 2010; Coronel-Olivares et al. 2011). monella spp. are bacteria of great concern as well as good Markosyan et al. (2002) detected different genera of Kleb- representatives of the reduction of other bacterial pathogens siella, Enterobacter, Hafnia, Serratia, Proteus, Providencia because they are typically present in higher densities than and Escherichia in the biosolids. Younis et al. (2003) iso- other bacterial pathogens and have the ability to survive for lated Salmonella spp., Shigella spp., Vibrio spp., Staphylo- a long time in the environment. coccus spp. and Listeria spp. from STP located in Aswan, Salmonella spp. are the most prevalent bacterial patho- Egypt. Lisle et al. (2004) observed that the untreated sewage gens of public healthcare concern that are frequently found at Memurdo station, Antarctica, contained relatively high in sewage (Dumontet et al. 2001; Espigares et al. 2006). concentrations of total coliforms, faecal coliforms, E. coli, Salmonella spp. can cause diseases to all organisms from enterococci and C. perfringens. Al-Zubeiry (2005) detected insects to mammals (Bohm 2004). Enteric fever is a col- S. aureus, S. pneumonia, E. coli, Salmonella spp. and P. lective term given to the invasive infections caused by S. aeruginosa in raw sewage and secondary effluent generated typhi and S. paratyphi causes paratyphoid fever. S. typhi is a from STP in Ibb, Yemen. El-Lathy et al. (2009) isolated pathogen that only has humans as its natural host (Heritage Salmonella spp., Listeria spp and Vibrio spp. (V. vulnificus, et al. 2003). V. parahaemolyticus and V. cholera) from sewage samples Burtscher and Wuertz (2003) reported that about 48% of from oxidation pond in El-Sadat, Egypt, and biosolids from the 46 biosolids samples tested were positive for Salmonella Zenin sewage treatment plant at Giza, Egypt. Ye and Zhang spp. which could be detected in both untreated and treated (2011) studied the presence of pathogenic bacteria in bio- waste samples during intermediate stages of treatment. How- solids from 14 STPs in China, USA, Canada and Singapore. ever, S. stanley was the only pathogen isolated after the ther- The study detected Aeromonas veronii, A. hydrophila, C. mophilic anaerobic digestion (Sahlstrom et al. 2004). perfringens and C. Diphtheria as most common. Bala et al. (2012) investigated pathogenic bacteria in pharmaceutical Shigella sp. wastewater in Nigeria. They noted that E. coli, Salmonella sp., Klebsiella sp., P. aeruginosa, S. aureus, P. vulgaris, This is a genus of gamma-Proteobacteria in the family Enter- Clostridium sp. and E. faecalis were predominant. obacteriaceae (Brenner et al. 2005), discovered by Kiyoshi Al-Gheethi et al. (2013a) reported that K. pneumonia, Shiga in 1896. They are rod-shaped, Gram-negative, non- E. coli, Shigella sp., Salmonella spp., S. aureus, E. faecalis spore-forming, non-motile bacteria that are very closely and P. aeruginosa are abundant in three STPs in Malaysia. related to E. coli and only humans are always the host (Gel- Al-Gheethi et al. (2014) also investigated the bacterial diver- dreich 1996). Members of the Shigella genus (S. dysente- sity in treated sewage and biosolid samples generated from riae, S. boydii, S. flexneri and S . sonnei) are the major cause five STPs in Yemen. The authors isolated hundred and sixty of dysentery, diarrhoea, fever, vomiting and cramps, which bacterial strains. Among those, E. coli was the most com- frequently occurred in countries that lack potable drinkable mon, followed by S. faecalis, K. pneumonia, E. aerogenes, water such as India (Niyogi 2005). The dysentery bacilli are S. typhi, S. typhimurium, S. sonni and Y. pestis. The most the most common infectious diseases in third world coun- concerned bacteria are discussed below; tries and among travellers to tropical countries (Vila et al. 1994). Shigella spp. are the second pathogenic bacteria that Salmonella spp. cause intestinal diseases in China (Peng et al. 2002). The infectious dose for Shigella sp. was determined to Salmonella spp. are rod-shaped, Gram-negative, non- be as few as 10–100 organisms (Fratamico et al. 2005) and spore-forming, facultatively anaerobic bacteria, discovered the waterborne transmission of shigellosis was documented by Salmon in 1880. This group consists of a range of very epidemiologically (Alamanos et al. 2000). Shigella sp. was closely related bacteria that belongs to the genus Salmonella isolated from pharmaceuticals wastewater, sewage effluents and the family Enterobacteriaceae. Salmonella spp. exhibit and biosolids (Bala et al. 2012; Al-Gheethi et al. 2013a). psychrotrophic properties and actively grow within a wide Chen et al. (2012) found that Shigella sp. survived more temperature range (10–54 °C) (Woteki and Kineman 2003). than Salmonella sp. and E. coli during mesophilic anaerobic digestion of sludge. However, it has been reported previously 1 3 74 Page 6 of 25 Applied Water Science (2018) 8:74 that Shigella sp. does not appear to survive long in the envi- an indicator organism. Thus, it could be useful as an indica- ronment (Gebra 1996). tor of past pollution and as a trace to follow the fate of patho- gens (Bitton 2005b). Vierheilig et al. (2013) investigated C. Escherichia coli O157:H7 perfringens in different faecal sources at Austria for 3 years. They stated that C. perfringens was not suitable as indicator Escherichia. coli is a rod-shaped Gram-negative bacterium, of faecal pollution but they suggested that it could be used which belongs to the family Enterobacteriaceae. They as a tracer for excreta from human sewage. are facultative, oxidase-negative anaerobes and produce gas from glucose. E. coli is a member of the physiologi- Faecal indicator bacteria cal gastrointestinal flora bacterium species for human and warm-blooded animals. Additionally, it belongs to the nor- Analytical techniques for the direct detection and identifi- mal intestinal flora and a facultative pathogen for human cation of many types of pathogenic bacteria in the sewage being (Kaper et al. 2004). However, some E. coli serotypes effluents require well-trained technicians. These techniques are pathogenic, among them enterohaemorrhagic strain E. are usually unpredictable, difficult, costly and time consum- coli O157:H7 which causes gastrointestinal disorders such ing. The faecal organisms which are used as pathogenic indi- as bloody diarrhoea, cramping and abdominal pain and the cator can determine the relative risk of biosolids (Toze 1997; infectious “hemolytic uremic syndrome” (Fijalkowski et al. Wen et al. 2009). 2014). E. coli O157:H7 was first reported as a gastrointes- The indicator bacteria are adapted to living in the gas- tinal pathogen in 1982 (Riley et al. 1983), they are able to trointestinal tract and can be harboured in other different survive in environment for long time without a host (Qing habitats, such as a septic system or sewage collection system et al. 2010). Isolation of E. coli from surface water, treated (Gordon et al. 2002). Indicator organisms are used as models sewage and biosolids has been reported by many investiga- for the behaviour of pathogens, for example, to determine tors (Al-Zubeiry 2005; Jokinen et al. 2010; Al-Gheethi et al. the efficiency of treatment processes, where their growth 2013a; Al-Gheethi et al. 2014). characteristics (temperature and pH) are similar to those of numerous pathogens for which detection and quantification Clostridium perfringens are difficult or sometimes impossible (Lepeuple et al. 2004). Many bacteria have been studied for their suitability as Clostridium. perfringens is an obligate anaerobic Gram- faecal indicators (Ashbolt et al. 2001; US EPA 2007). The positive bacterium, bacilli-shaped and endospore forming. first bacterial species, which had been used as faecal indica- It is a member of the Sulfite-Reducing Clostridia (SRC) tors, were K. pneumoniae and K. rhinoscleromatis, which group. C. perfringens has been isolated from sewage by was suggested by Von Fritsch in 1880 (Geldreich 1978). many researchers (Lisle et al. 2004; Ye and Zhang 2011), However, many bacterial species were also suggested as because it represents 0.5% of the faecal microflora (Leem- indicators. Dancer (2004) has proposed S. aureus as an ing et al. 1998; Payment et al. 2002). Payment and Franco indicator of hospital hygiene for microbiological stand- (1993) recommended this bacterium as an indicator for the ards. Jin et al. (2013) used S. aureus as indicator to evaluate presence of Giardia cysts in water treatment plants as well as the hydrothermal treatment process in achievement of the to evaluate the quality of recreational waters (Fujioka 1997). hygienic safety of food waste. Suresh et al. (1996) confirmed that the use of C. perfrin- Al-Gheethi et al. (2013a) studied the correlation between gens as well as faecal coliforms and faecal streptococci could the frequencies and the numbers of faecal indicators and serve as an excellent approach for identifying the presence of pathogenic bacteria. They found that E. coli has been cor- airborne pathogens and determining their origins or sources related significantly with all pathogenic bacteria investigated associated with the treatment and disposal of wastewater (K. pneumonia, P. aeruginosa, Shigella sp. and Salmonella and biosolids. spp.), E. faecalis has correlated by 75% while total coli- Lepeuple et al. (2004) reported that the C. perfringens is forms and faecal coliforms correlated by 50% with patho- common in raw sludge and resistant to heat, and hence their gens under study. removal can be related to removal of spore-forming spe- In general, the criteria for selection of faecal indicator cies such as Bacillus sp. C. perfringens has been reported as organisms have been documented as follows (Cooper and resistant to oxidizing agents and to UV disinfection (Alonso Olivieri 1998; Dumontet et al. 1999; Bitton 2005a; Myers et al. 2004). Rouch et al. (2011) indicated that C. perfringens et al. 2007): appeared to be a conservative indicator during their study on the air drying of sludge generated from two STPs in Victo- 1. Should be a member of the Enterobacteriaceae family. ria, Australia. However, some authors stated that the hardy 2. The presence of faecal indicators should be associated spores of this bacterium make it too resistant to be useful as with the presence of pathogens. 1 3 Applied Water Science (2018) 8:74 Page 7 of 25 74 3. Numbers should be greater than that of the pathogens. 1998). However, Bitton (2005b) reported that enterococci 4. It should be resistant to the disinfection processes as the are good indicators of faecal pollution like faecal coli- pathogens. forms. Enterococcus species (E. faecium, E. faecalis, E. 5. It should not increase in the environment. avium, E. gallinarum and E. durans) have the ability to 6. Should be easily detected by simple techniques. grow at both 10 and 45 °C, at high pH 9.6 and in medium 7. Should be non-pathogenic. containing 6.5% NaCl (Cooper and Olivieri 1998; Car- valho and Teixeira 2002). This group has been suggested Faecal indicators organisms are discussed below; as useful for indicating the presence of viruses, particu- Total coliforms are groups belonging to Enterobacte- larly in sludge, sea water and biosolids (Bitton 2005b), riaceae and include the aerobic and facultative anaerobic, because these organisms are relatively easy to enumer- rod-shaped, non-spore-forming, Gram-negative bacteria that ate and survive longer than faecal coliforms (Mote et al. ferment lactose with gas production within 48 h at 35 °C 2012). (APHA 1989). These characteristics are suitable for the Enterococci along with faecal coliforms have been used identification of this group and no confirmatory tests are to differentiate human faecal contamination from that of required (Edberg et al. 1990). other warm-blooded animals based on FC/FS ratio, if the Total coliforms include four genera, Escherichia sp., ratio less than 1.0 this means that the source of faecal Enterobacter sp., Klebsiella sp. and Citrobacter sp. Some contamination are all warm-blooded animals other than members of this group, e.g., Klebsiella sp. may grow in man, if the ratio was 4.0, this means the source of fae- industrial waste. They are the historic indicators of faecal cal contamination is human. Intermediate ratios indicate contamination since 100 years ago (Cooper and Olivieri contamination from both man and animals (Young and 1998). Total coliforms are one of the best indicators for treat- Thackston 1999; Baudišová 2009). Enterococci are a more ment efficiency of sewage treatment plants (Bitton 2005b). reliable indicator than faecal coliforms for the detection of Faecal coliforms (FC) are classified under the group of microbial pollution as they are more resistant to the envi- total coliforms and are more faecal specific in origin and ronment than faecal coliforms (Celico et al. 2004). It has include E. coli and other faecal (or thermotolerant) coliforms been frequently considered as reference microorganism that can ferment lactose at 44.5 °C (Kimberly et al. 2005). for thermal treatments to be applied in pasteurized foods The presence of these organisms more accurately correlates (Smith et al. 1990; Ghazala et al. 1991). However, US EPA with warm-blooded animal faecal discharges. However, even (US 2004a) and WHO (1989) did not regulate standards this group contains a genus, Klebsiella with species that are limits of enterococci in treated sewage if the effluents is to not necessarily faecal in origin. Klebsiella sp. is commonly be reused for irrigation or groundwater recharge. associated with textile, pulp and paper mill wastes (US EPA 1986a). According to the US EPA (1992), FC is faecal bacteria that are used as indicators to show probable presence of Regulations of treated sewage and biosolids pathogenic bacteria, because they are easily detected and their densities decline in the same proportion as pathogens To maintain safe reuse of sewage treated effluents, WHO during the treatment process. The EPA Part 503 regulations (1989) reported that the geometric mean of FC should “Standards for the use or disposal of sewage sludge” have be less than 1000 cells/100  mL (Table  1), these stand- established pathogen reduction requirements for FC (US ards are also used in Jordan and Palestine. However, US EPA 2003). EPA (2004b) recommended more stringent standards For recreational waters, FC was the primary bacterial for sewage-treated effluents. FC should not exceed 14 indicator until 1986, when the EPA began recommending cells/100 mL (Table 2). In Saudi Arabia, the standards for E. coli and enterococci as better indicators of health risk sewage effluents reuse in agricultural irrigation are issued from water contact (US EPA 1986a). FC is still being used by the Ministry of Municipal and Rural Affairs (MMRA). in many states of USA as the indicator bacteria. However, According to those standards, FC should be less than 2.2 Byappanahalli and Fujioka (1998) reported that tropical soil cells/100 mL of unrestricted irrigation and less than 1000 environments such as in Hawaii provide sufficient means to cells/100  mL of restricted irrigation (Al-Jasser 2011). support the growth of FC and E. coli. Polo et al. (1998) have The EPA part 503 regulations for the reuse of biosolids shown poor to no correlation between E. coli and Salmonella (CFR 1995) divided stabilization biosolids into “Class A” spp. to FC. Hörman et al. (2004) reported that there was no and ‘‘Class B’’. Class A biosolids must meet either FC correlation between E. coli and Campylobacter spp. limit of less than 1000 MPN g-1 TS or less than 3 Salmo- Enterococci bacteria have been considered useful as nella/4 g TS. Class B biosolids should be meet a FC limit 6 −1 secondary indicators of faecal contamination (APHA of less than 10  MPN g TS. The standards for reuse of 1 3 74 Page 8 of 25 Applied Water Science (2018) 8:74 Table 1 Guidelines for using treated wastewater in agriculture (WHO 1989) Category Reuse conditions Exposed group Intestinal nematode Coliforms Wastewater treatment expected (arithmetic mean no (geometric to achieve the required microbio- b b eggs/L) mean/100 mL) logical guideline A Irrigation of crops likely to be Workers, ≤ 1 ≤ 1000 A series of stabilization ponds eaten uncooked, sports fields, consumers, designed to achieve the micro- public parks public biological quality indicated, or equivalent treatment B Irrigation of cereal crops, Workers ≤ 1 No standard Retention in industrial crops, fodder crops, recommended stabilization ponds pasture and trees for 8–10 days or equivalent hel- minthic and FC removal C Localized irrigation of crops None Not applicable Not applicable Pre-treatment as required by irri- in category B if exposure to gation technology, but not less workers and the public does than primary sedimentation not occur Ascaris and Trichuris species and hookworms During the irrigation period A more stringent guideline (200 FC/100 mL) is appropriate for public lawns, such as hotel lawns, with which the public may come into direct contact In the case of fruit trees, irrigation should cease 2 weeks before fruit is picket, and no fruit should be picked off the ground. Sprinkler irrigation should be used Table 2 Microbiological requirements for reclaimed water (US EPA 2004b) Type of use Treatment Reclaimed water quality Urban uses, food crops eaten raw, recreational Secondary, filtration, disinfection pH = 6–9 impoundments no detectable FC/100 mL Restricted access area irrigation, processed Secondary, disinfection pH = 6–9 food crops, non-food crops, aesthetic 200 FC/100 mL impoundments, construction uses, industrial cooling, environmental reuse Groundwater recharge of potable aquifers by Site-specific secondary and disinfection Site-specific meet drinking water standards spreading (minimum) after percolation through vadose zone Groundwater recharge of potable aquifers by Includes: secondary, filtration, disinfection, Includes: pH = 6–8.5 no detectable FC/100 mL injection, augmentation of surface supplies advanced wastewater treatment Based on 7-day median value. Should not exceed 14 FC/100 mL in any sample Based on 7-day median value. Should not exceed 800 FC/100 mL in any sample sewage effluents and biosolids issued out by the Yemen could be transmitted into rivers and other environment agricultural sector have focused on the basic parameters of during the final disposal or reuse of the effluent (Spong- sewage such as COD, BOD, TS and TSS. However, these berg and Witter 2008). Rizzo et al. (2013) reported that standards are neither met nor controlled, because most of conventional disinfection processes might not be effective STPs are overloading, and Yemeni laboratories are not in the inactivation of antibiotic-resistant bacteria. There- equipped to measure all mentioned parameters (ACWUA fore, to achieve safe reuse of sewage-treated effluents, 2010). advanced treatment technologies have been applied to reduce various potentially harmful compounds that could not be effectively removed by conventional treatment pro- Further treatment of treated sewage cesses. Advanced treatment technologies have high poten- tial to produce an effluent of higher quality than normally Recent studies revealed that detectable amounts of pollut- achieved by secondary treatment processes (Zhou and ants remain in sewage effluents, even after secondary sew - Smith 2002; Jin et al. 2013). The techniques used for this age treatment processes are performed. These pollutants 1 3 Applied Water Science (2018) 8:74 Page 9 of 25 74 purpose include reduction of pathogens by disinfection Chlorination process (Al-Rekabi et al. 2007). Chlorination is the most common method used for disinfec- Disinfection processes of sewage‑treated effluents tion of treated sewage in Middle East countries because it is easily applied, readily available and cheaper than other oxi- The concentrations of faecal indicator bacteria in untreated dising agents. It can also be used to inhibit bacteria growth sewage are 8 log CFU/100  mL for TC, 7.48 log in treated sewage (Gomez et al. 2006). Tree et al. (2003) 10 10 CFU/100 mL for FC and 6.6 log CFU/100 mL for ente- found that chlorination has significant effect in the reduc- rococci (Wilén et  al. 2012). The conventional treatment tion of E. coli and E. faecalis in sewage-treated effluents. processes for sewage (primary and secondary processes) However, the occurrence of pathogenic bacteria in treated remove 95–99% of most microorganisms (Koivunen et al. sewage after chlorination has been observed. Dungeni et al. 2003). However, their numbers in the sewage effluent usu- (2010) stated that despite high free chlorine residual concen- ally remain higher than 4 log  CFU/100 mL (Luczkiewicz trations in sewage-treated effluents, the survival of E . coli, et al. 2010). The stabilization pond was reported to reduce S. typhimurium and V. cholerae was significantly high and 84% of total coliform, 96% of faecal coliform and 89% of they suggested an upgrading of the STPs by other processes enterococci (Reinosoa et al. 2008). The reduction efficacies to increase the inactivation of pathogenic bacteria. CDPH of faecal indicator bacteria by the septic tank and oxidation (2009) reported that the chlorination disinfection system is pond were reported to be 15 and 38% for FC and 11 and 16% the primary disinfection process, and the whole disinfection for FS, respectively (Samhan et al. 2007). of reclaimed water should be performed by the pasteurisa- Many studies have found that the concentrations of fae- tion system. cal indicators in the treated sewage and biosolids are still Moreover, one main disadvantage for utilization of more than the standard limits of US EPA and WHO guide- chlorine disinfection is the presence of free and combined lines. Heng et al. (2006) found that the concentrations of TC chlorine residues which is being toxic to aquatic organisms. in the treated sewage generated from two-oxidation ponds Therefore, the requirement to de-chlorinate or to remove at Kajang and UKM-Malaysia were 8.95 and 8.58 log chlorine residues from the treated sewage before it is dis- CFU/100 mL. Siti Khadijah et al. (2013) reported that the charged into the environment has increased in recent years concentration of FC in the treated sewage from the oxida- due to the potential health hazards of nitrosodimethylamine tion ponds in USM Engineering Campus, Malaysia, were (NDMA) which is reported as a probable human carcinogen also more than WHO guidelines, where FC concentrations (Pehlivanoglu-Mantas et al. 2006). ranged from 2.36 to 5.57 log  CFU/100 mL. Al-Gheethi et al. (2013a) revealed that the concentrations of FC at the three STPs in Penang, Malaysia were greater than the stand- Ozonation ard limits recommended by the WHO guideline for use of treated wastewater in agriculture and US EPA microbiologi- One of the most effective disinfectants used in water disin- cal requirements for wastewater reuse. fection is ozone. This is because ozone has high ability to According to those studies, it can be concluded that the destroy pathogenic cells through an irreversible physiochem- treated sewage still contains high concentrations of patho- ical action. Ozonation destroys the cell wall of the bacteria genic bacteria even after sewage treatment processes. The as well as semi-permeable membrane. The destruction in high bacteria levels in the natural water that received sew- the cell wall and membrane leads to the bacterial cell death age-treated effluent lead to increase in BOD, resulting in (Facile et al. 2000). Tripathi et al. (2011) claimed that 5 min −1 depletion of oxygen levels required for the various types of exposure at a concentration of 10 mg ozone L was suit- of living organisms supported by the estuary. Therefore, able for the inactivation of pathogenic bacteria by 95–98%. treated sewage needs to undergo further treatment to reduce Previous studies reported that ozone effectively removes TC the density of pathogenic bacteria to achieve a favourable and FC from sewage-treated effluents. Battaler et al. (2005) sanitary effluent quality (Koivunen et al. 2003; Jin et al. found that the ozone disinfection of secondary effluents at −1 2013). Disinfection process of effluents increases the reduc - concentration 4.7 mg L for 5 min had eliminated TC and −1 tion of pathogens for high-quality reuse (Crook 1998; Neis FC. At 21.4 mg L the bacteria that resisted for chlorine and Blume 2002). The tertiary treatment is able to achieve such as P. aeruginosa decreased by 2 log reduction after the guidelines of WHO and US EPA standards for pathogen 5 min of disinfection process by ozone. inactivation. The development of a tertiary treatment pro- Disinfection of treated sewage by ozone is applied cess includes all techniques that offer significantly higher because the use of ozone is cheap and low energy is needed. removal of pathogenic bacteria. The most common disinfec- Nonetheless, the effectiveness of disinfection using ozone tion processes of treated sewage are discussed below. depends on the ozone dose, the ozone demand, the quality 1 3 74 Page 10 of 25 Applied Water Science (2018) 8:74 of the effluent and the transfer efficiency of the ozone sys- on the UV radiation, photo-oxidation and temperature (Sect. tem (Paraskeva and Graham 2002). The COD and total sus- “Solar disinfection (SODIS)”). pended solids (TSS) of treated sewage might affect the effi- ciency of disinfection process by ozone (Janex et al. 2000). Filtration technology The properties of the treated sewage might induce the micro- bial resistance for the ozone as noted for Enterococcus sp., Filtration systems are designed to remove very small particu- Clostridium sp. and Salmonella spp. which exhibit resistance late or “suspended” solids from the treated sewage. Onnis- to ozonation (Xu et al. 2002). Hayden et al. (2011) evaluated sand filtration technology In USA, the disinfection of drinking water by ozona- in the disinfection of sewage generated by STPs and found tion process is more attractive disinfection method due to that the E. coli concentration reduced to below 2 logs in the promulgation of the EPA’s restrictions of disinfection the filtered sewage-treated effluents. Despite its high effi - by-products (DBPs) permitted in America’s drinking water ciency in the removal of pathogenic bacteria and producing attributable to chlorination. Nevertheless, ozonation can effluents with good microbiological quality, the effluents also lead to the formation of potentially harmful by-products would not be considered as sterile, since contamination of inclusive of bromate ions (BrO ), aldehydes and peroxides. permeation zones gave rise to the presence of pathogenic Vital et al. (2010) reported that the major concern associated bacteria (Gomez et al. 2006). At the same time, the mem- with the ozone application lies in the increase in microbial brane filtration systems are expensive with regard to con- regrowth due to the oxidation process which generates the struction and maintenance (Neis and Blume 2002). Different assimilable organic carbon (AOC). filtration systems have been developed which depend on the utilization of raw and low-cost materials such as sands and UV irradiation ceramic (Mohamed et al. 2016). These systema have exhib- ited high efficiency in the reduction of the main parameters Disinfection by ultraviolet irradiation has been reported as of wastewater such as COD, BOD and TSS, but their effi- a suitable technology for inactivating coliforms and Sal- ciency in the reduction of pathogenic bacteria still needs monella spp. (Keller et al. 2003). The principle of a UV more investigation. disinfection system is to destroy the genetic material of the bacterial cell and thus retard its ability to reproduce (US Storage of treated sewage EPA 1986b). The effectiveness of a UV disinfection system depends on the characteristics of the effluents including the Storage systems are used typically for accumulating waste- concentration of the sewage effluent, the intensity of the UV water before its ultimate disposal, or for temporarily holding radiation and the time of the treatment (Kollu and Ormeci batch streams before treatment (US EPA 1989). A storage 2012). basin was also used for treating effluent storage, especially Nasser et al. (2006) revealed that the treated sewage dis- during winter in temperate country. The stored effluents will infected by UV is suitable for the unrestricted irrigation of be released to environment normally during the rainy season food crops (FC < 1000 CFU/100 mL). Dungeni et al. (2010) where the dilution rate is higher (Al-Gheethi et al. 2017). suggested UV disinfection as an additional treatment process Storage of sewage has become the option selected in of effluents to increase the effective inactivation and removal European and Mediterranean countries because of the of pathogenic bacteria and viruses. However, Alonso et al. advantages they present in comparison with other treatment (2004) found that Clostridium spp., showed a greatest degree alternatives. This includes the coupling of two purposes: of resistance to UV treatment. Munir et al. (2010) indicated stabilization and seasonal regulation to regulate between that the disinfection of effluents by UV process did not con- sewage production and demand of treated wastewater for tribute to the significant reduction of antibiotic-resistant irrigation (Barbagallo et al. 2003). bacteria. Ting et al. (2011) observed a re-growth and repair Al-Gheethi et  al. (2013a) studied the effect of stor- potential of E. coli, FC and B. subtilis in reclaimed water age of treated sewage on survival of faecal indicators and after UV disinfection. Wang et al. (2012) suggested that Salmonella spp. and the susceptibility of these bacteria the higher number of particles in the treated sewage might to antibiotics during the storage period. The treated sew- have protected the bacteria against UV damage. Based on age was stored at room temperature for 28 days. The study those studies, it can be indicated that UV technology might noted that FC density in stored effluents dropped from have a limitation for the sewage disinfection. But it has to be 5.182  log  CFU/100 mL to below 2 log   CFU/100  mL 10 10 motioned that the disinfection processes of the treated sew- after 28 days and the treated sewage met WHO guidelines. age might be more effective as two methods have been used E. faecalis decreased to less than detection limits during the simultaneously such as the solar disinfection which depends storage period of 1 week. However, they observed that TC and Salmonella spp. which have survived during the storage 1 3 Applied Water Science (2018) 8:74 Page 11 of 25 74 period acquired more resistance to antibiotics. At the end of US EPA. The sewage effluents can be reused for irrigation the storage period, TC and Salmonella spp. were resistant purpose. to cephalexin, cefuroxime, ampicillin and amoxicillin. The study concluded that the storage system of treated sewage Solar disinfection (SODIS) would increase the distribution of antimicrobial resistance among bacterial population after the disposal or reuse of SODIS-based technologies are an efficient approach for the treated sewage for agricultural purposes. Indeed, the effi- reduction of pathogenic microorganism in the water due to ciency of the storage system on the reduction of pathogenic high availability of solar radiation and sustainable nature of bacteria depends mainly on the storage temperature, the stor- these water treatment methods (Gomez-Couso et al. 2009). age system at the room temperature might be effective for According to WHO (2002), SODIS depends on using trans- the reduction of pathogenic bacteria but it needs long time parent polyethylene terephthalate (PET) bottles and then to achieve high reduction of pathogens and then to meet exposing to the sun for a period between 4 and 8 h. Mei- the international standards required for the sewage disposal erhofer and Wegelin (2002) recommended that PET bot- or reuse of the sewage for the irrigations (Al-Gheethi et al. tles containing untreated raw water should be exposed to 2017). The mechanism which takes place in the storage direct sunlight for at least 6 h. Bacteria, viruses, Giardia system and leads to the reduction of pathogens might be and Cryptosporidium cysts, and parasite eggs could be the competition process between microorganisms due to inactivated through the combination of ultraviolet radiation the deficiency in the nutrients contents (Al-Gheethi et al. and elevated water temperature. Large field tests of SODIS 2016a). were conducted in a number of countries in South America, Africa, and Asia in the 90s (Acra 1990). Heat pasteurization The destruction of the bacterial cells takes place due to the combination of UV radiation and high temperature Heat disinfection is a proven technology in Europe that which has high potential to destroy the cell membrane (Al- requires skills such as boiler operation and the understand- Gheethi et al. 2015). However, SODIS has no efficiency ing of high-temperature and -pressure processes. The EPA for the reduction of chemical pollutants in the water. The Part 503 regulations (US EPA 2003) consider pasteurisa- sunlight has been reported as the single most important dis- tion as a process to further reduce pathogen (PFRP). CDPH infection factor in the stabilization pond (Leduc and Gehr (2009) reported that the use of pasteurisation is recognised 1990; Maynard et al. 1999). Three main mechanisms are as an acceptable disinfection process for meeting the inac- involved during the SODIS simultaneously, included the tivation criteria of coliform bacteria. It is a known fact that absorption of solar UV-B by microorganism DNA which pathogenic bacteria are inactivated during exposure to heat, causes direct damage by pyrimidine dimer formation. The especially when the temperature of the treatment is above process is independent of oxygen and other pond condi- the optimum temperature of growth (Himathongkham and tions. The second mechanism depends on the absorption of Riemann 1999). Lucero-Ramirez (2000) reported that path- UV-B and some shorter wavelength UV-A by cell constitu- ogenic bacteria are reduced to less than detectable levels ents including DNA (called endogenous photo-sensitisers). in properly operated heat-drying systems. Alcalde et  al. The activated constituents react with oxygen to form highly (2003) indicated that the retention time and temperature are reactive photo-oxidising species that damage genetic mate- the most important factors for the removal of pathogenic rial within the cell or viral particle. The third mechanism bacteria. involves absorption of a wide range of UV and visible wave- Bacteria can be classified into different groups based on lengths in sunlight by extra-cellular constituents of the pond optimum temperature. Most human pathogenic bacteria are medium (exogenous photo-sensitisers—notably humic mate- mesophilic (10–40  °C) with an optimum temperature of rial) (Jagger 1985). 37 °C. Metabolic enzymes of bacteria denature and inactive Al-Gheethi et al. (2013b) investigated the effect SODIS when exposed to temperature above its optimum. This even- on the survival of FC, E. faecalis, Salmonella spp. and S. tually led to the death of the bacterial cell. Removal of faecal aureus in treated sewage inside PET bottles. The study indicators (enterococci and E. coli) in piggery effluents to revealed high reduction of FC, Salmonella spp. and S. achieve hygiene standards could easily be met by treatment aureus by more than 4 log  CFU/100 mL after 6 h, while at 60 °C (Cunault et al. 2011). Al-Gheethi et al. (2013a) these pathogens were below the detection limits after 8 h investigated the heat treatment of treated sewage at different as detected by using the enrichment medium. The treated temperatures (45, 55 and 65 °C). They found that the sewage sewage met US EPA (2004a) standards after 6  h, where effluents disinfected at 45 °C for 192 h, 55 °C for 24 h and FC counts were less than 14  CFU/100  mL. SODIS has 65 °C for 30 min have met standard limits regulated by the several advantages to the reduction of faecal indicator in treated sewage compared to the others techniques such as 1 3 74 Page 12 of 25 Applied Water Science (2018) 8:74 chlorination, UV irradiation and ozonation. SODIS is com- matter (WHO 2002). Chemical treatment is sometimes used patible to meet the standards of the disinfection processes of and it encourages small particles and dissolved substances sewage treated effluents. This is because SODIS is effective, to form large particles which facilitate separation. This is more efficient, easily implementable and lower cost. SODIS called chemical precipitation. Sludge is formed when these is a natural process that produces no toxic by-product (Al- larger particles clump together during suitable separation Gheethi 2014). methods (Casey 1997). SODIS is more appropriate to be applied in the develop- All the sludge that is separated during these treatment ing countries that do not have the facilities to build typi- methods (mechanical, biological and chemical) is defined as cal sewage treatment plants. The climate of many Middle a raw sludge, which has to undergo various kinds of further East countries such as Yemen, Saudi Arabia, Oman, Jordan treatment for the improving the microbiological quality and and Egypt is semi-arid to arid and the temperatures during then for safe disposal or reuse. Physical, chemical and bio- summer season vary from 27 to 50 °C (FAO 2008). These logical processes accomplish the stabilization and disinfec- countries also have a large space of the deserts. The desert tion of sewage sludge. Stabilization refers to those processes temperatures range from 45 to 60 °C in summer and from that reduce the volatile solids content, pathogen levels and 7 to 35 °C in the winter and the sunlight intensity ranges odour. The biosolids generated from sewage treatment pro- from 5.2 to 6.8 kWh/m /day (Al-Ashwal and Basalah 2012). cesses must be subject to further treatment to reduce patho- Therefore, one of the proposals to reduce the environment genic bacteria which are still high in concentrations even pollution by sewage generated from STPs is by extending the after the treatment processes (Al-Gheethi et al. 2014). Dis- sewerage network to the desert. The desert provides many of infection processes emphasize the reduction of pathogenic the features of SODIS necessary to treat the sewage effluents bacteria below detectable limits. Major stabilization meth- such as the large areas and the temperature and the treated ods include anaerobic digestion, aerobic digestion, compost- sewage could be used in the land reclamation. ing, alkaline (lime) stabilization and air-drying. Disinfection includes pasteurization, long-term storage, irradiation, heat Reduction of pathogenic bacteria in biosolids drying and heat treatment (US EPA 2003). According to US EPA, there are two processes are used to Sewage treatment processes can be classified as primary and the reduction of pathogenic bacteria to comply the standards secondary processes. In primary treatment, solids are mainly limits of biosolids (Class A and B). These processes named removed mechanically from untreated sewage. Secondary Processes to Further Reduce Pathogens (PFRPs, Table 3) treatment is a biological process in which decomposers are and Processes to Significantly Reduce Pathogens (PSRPs, utilized to remove biodegradable pollutants. Decompos- Table 4). The details of the most common treatment pro- ers are organisms such bacteria and fungi that get energy cesses are described below. and nutrients by digesting waste matter in the sewage. In the activated sludge process, sewage is pumped into a large tank where aerobic microorganisms decompose the organic Table 3 Processes to Further Reduce Pathogens (PFRPs). Source; US EPA (2003) Treatment process Procedure of the treatment process Composting Using either the within-vessel composting method or the static aerated pile composting method, the tempera- ture of sewage sludge is maintained at 55 °C or higher for 3 consecutive days. Using the windrow composting method, the temperature of the sewage sludge is maintained at 55 °C or higher for 15 consecutive days or longer. During the period when the compost is maintained at 55 °C or higher, there shall be a minimum of five turnings of the windrow Heat drying Sewage sludge is dried by direct or indirect contact with hot gases to reduce the moisture content of the sewage sludge to 10% or lower. Either the temperature of the sewage sludge particles exceeds 80 °C or the wet bulb temperature of the gas in contact with the sewage sludge as the sewage sludge leaves the dryer exceeds 80 °C Heat treatment Liquid sewage sludge is heated to a temperature of 180 °C or higher for 30 min Thermophilic aerobic digestion Liquid sewage sludge is agitated with air or oxygen to maintain aerobic conditions and the mean cell residence time (i.e., the solids retention time) of the sewage sludge is 10 days at 55–60 °C Beta ray irradiation Sewage sludge is irradiated with beta rays from an electron accelerator at dosages of at least 1.0 megarad at room temperature (ca. 20 °C) Gamma-ray irradiation Sewage sludge is irradiated with gamma rays from certain isotopes, such as Cobalt 60 and Cesium 137, at dos- ages of at least 1.0 megarad at room temperature (ca. 20 °C) Pasteurization The temperature of the sewage sludge is maintained at 70 °C or higher for 30 min or longer 1 3 Applied Water Science (2018) 8:74 Page 13 of 25 74 Table 4 Processes to significantly reduce pathogens (PSRPs). Source; US EPA (2003) Treatment process Procedure of the treatment process Composting Using either the within-vessel, static aerated pile, or windrow composting methods, the temperature of the sewage sludge is raised to 40 °C (104 °F) or higher and remains at 40 °C or higher for 5 days. For 4 h during the 5 day period, the temperature in the compost pile exceeds 55 °C Aerobic digestion Sewage sludge is agitated with air or oxygen to maintain aerobic conditions for a specific mean cell residence time (i.e., solids retention time) at a specific temperature. Values for the mean cell residence time and temperature shall be between 40 days at 20 °C and 60 days at 15 °C Air drying Sewage sludge is dried on sand beds or on paved or unpaved basins. The sewage sludge dries for a minimum of 3 months. During 2 of the 3 months, the ambient average daily temperature is above 0 °C Anaerobic digestion Sewage sludge is treated in the absence of air for a specific mean cell residence time (i.e., solids retention time) at a specific temperature. Values for the mean cell residence time and temperature shall be between 15 days at 35–55 °C and 60 days at 20 °C Lime stabilization Sufficient lime is added to the sewage sludge to raise the pH of the sewage sludge to 12 for ≥ 2 h of contact Anaerobic digestion Ziemba and Peccia (2011) evaluated mesophilic, ther- mophilic, temperature-phase, and high-temperature (60 or Anaerobic digestion is a biological process that uses bacte- 70 °C) batch pre-treatment digester configurations for E . coli and E. faecalis inactivation potential. The results revealed ria that function in an oxygen-free environment to convert volatile solids into carbon dioxide, methane and ammo- that the inactivation rates have increased dramatically at temperatures above 55 °C. In mesophilic treatment, 1–2 log nia. Those reactions take place in an enclosed tank that may or may not be heated, because the biological activity inactivation was recorded, while was 2–5 log inactivation at 50–55 °C in thermophilic and temperature-phase treatments. consumes most of the volatile solids needed for further bacterial growth (US EPA 2003). The mesophilic anaero- Incorporating a 60 or 70 °C batch pre-treatment phase has achieved completed inactivation (over 100 log reductions) bic digestion (MAD) of biosolids has been reported to produce biosolids Class B, this treatment process is com- of E. coli and E. faecalis. Chen et al. (2012) investigated inactivation of Salmo- mon in USA (Wong et al. 2010). However, most Middle East countries used air-drying as will be presented below nella sp. E. coli and Shigella sp. during mesophilic anaero- bic digestion of biosolids. They found that the anaerobic (Sect. “Air drying”). Telles et al. (2002) investigated the reduction of TC, FC, digestion process efficiency reduces Salmonella sp. and E . coli during the retention time from 11 to 25 day. However, P. aeruginosa and FS by anaerobic digestion of sewage sludge generated from STP in Maringá-Paraná, Brazil. The the reduction of Shigella sp. was insignificant. However, the long period of the treatment process (25 days) might study showed that 99.9% of FS, 96.3% of TC and 95% of P. aeruginosa were reduced at the end of the treatment process. lead to increase the overload of the STP and thus required high capacity to store the received sewage before the treat- These findings revealed the potential of anaerobic digestion in the reduction of pathogenic bacteria from the biosolids. ment process. Astals et al. (2012) studied the mesophilic anaerobic digestion, thermophilic anaerobic digestion and Wakelin et al. (2003) showed that FC was reduced from −1 −1 7.5 log  CFU g in the raw sewage to 6.3 log  CFU g mesophilic anaerobic digestion followed by a 60 °C or by 10 10 an 80 °C hygienization treatment of sewage sludge. They in dewatered biosolids after mesophilic anaerobic digestion process. The main pathogen-reducing factor during thermo- recorded that both thermophilic anaerobic digestion and mesophilic anaerobic digestion followed by a hygieniza- philic anaerobic digestion is temperature in relation to time, while the competition among microorganisms for nutrients is tion step reduced E. coli to meet the standards limits rec- ommended by US EPA and the European legislation for the limiting factor that reduces pathogen amounts in anaero- bic mesophilic treatment of biosolids (Smith et al. 2005). It land application. According to aforementioned studies, the anaerobic can be noted that the thermophilic treatment is more efficient than the mesophilic because the biosolids have high contents digestion process of biosolids showed potential for effec- tive reduction of pathogenic bacteria to meet the stand- of nutrients; therefore, the competition between microorgan- isms in the biosolids is weak. Carrington (1998) also eluci- ards limits recommended by US EPA. However, Viau and Peccia (2009) detected Legionella pneumophila, S. aureus dated that temperature is not the main factor in mesophilic anaerobic digestion processes at 35 °C, but this process pro- and C. difficile in biosolids generated from 29 STPs in USA which was treated with mesophilic, temperature- duces fatty acids and other products that are lethal to many pathogenic bacteria. phase anaerobic digestion and composting process, which 1 3 74 Page 14 of 25 Applied Water Science (2018) 8:74 indicates to the ability of some pathogenic bacteria to process depends very much on the local climate. Drying survive in the biosolids even after the thermophilic treat- occurs faster and more completely in warm and dry weather ment. This might be due to the presence solids materials and slower and less completely in cold and wet weather. The which might protect the bacterial cells form the tempera- density of pathogenic bacteria is reduced by approximately ture actions. Chen et al. (2011) indicated that the patho- 2 log under these conditions of air drying. However, this genic bacteria in the treated biosolids could regrow again reduction is not enough to produce high quality of biosol- during the storage periods of biosolids. This is due to the ids for safe disposal. More disadvantage of air drying is the microbial response to substrate release and environmen- deficiency in the produce biosolids with only 38% volatile tal changes, such as oxygen, which favour the bacterial solids destruction (US EPA 2003). regrowth during 1–2 weeks of storage period. Ward et al. (1981) studied the response of Klebsiella, Enterobacter, Proteus mirabilis, S. typhimurium, E. coli Aerobic digestion and S. faecalis to the moisture loss through evaporation at 21 °C. In raw sterilized sludge with 5% solids, seeded enteric In aerobic digestion, biosolids are biochemically oxidized by bacteria initially increased in concentration with dewatering. bacteria in an open or enclosed vessel. Under proper operat- This increase was always followed by a consistent decrease ing conditions, the volatile solids in biosolids are converted in numbers with further dewatering, especially below 50% to CO and H O (US EPA 2003). The PSRPs described moisture. A 1–2 log reduction was seen for all bacterial 2 2 aerobic digestion as follows: Sewage sludge is agitated with strains except Proteus sp. which showed a 4 log reduction oxygen to maintain aerobic condition for indigenous cell. within 7 days as biosolids percent solids increased to 95%. Time and temperature shall be between 40 days at 20 °C and Rouch et al. (2011) examined the inactivation of E. coli 60 days at 15 °C. Aerobic digestion carried out according to and C. perfringens during the air-drying of anaerobically the part 503 requirement typically reduces pathogenic bac- digested biosolids generated from two STPs in Victoria, teria by 2 log (US EPA 2004a). Kabrick and Jewell (1982) Australia. The results found that E. coli were reduced to 2 −1 found that Salmonella spp. was reduced to undetectable below 10 CFU g dry solids after drying of 8–15 days and levels in an aerobic reactor at 35 °C in 24 h, while at 60 °C the biosolids met US EPA standards for Class A. C. perfrin- Salmonella spp. was eliminated in few hours. gens appeared to be a better indicator. Han et  al. (2011) studied the efficiency of anaerobic Air-drying of biosolids is common in Middle East coun- lagoon fermentation (ALF) and autothermal thermophilic tries because the climate is semi-arid to arid and the tem- aerobic digestion (ATAD) for removal of pathogenic bac- peratures range from 27 to 50 °C (FAO 2008). Besides, this teria in raw swine manure. The results revealed that in raw process is not expensive and easily implementable. However, swine manure, Dialister pneumosintes, Erysipelothrix rhu- one of the major disadvantages of this process is the vector siopathiae, Succinivibrioan dextrinosolvens, and Schine- attractions, which increase as result to volatile solids in the ria sp. were detected. ATAD exhibited more efficiency to biosolids. The pathogens are transmitted from air-drying eliminate of these pathogens than ALT. In the mesophilic basin by the vectors to animals and human (Palmgren 2002). ALF-treated swine manure, Schineria sp. and Succinivibrio STPs in Yemen overcame this problem by using pesticide dextrinosolvens were still detected, while were undetected in but this method leads to accumulate of pesticide in the lands ATAD. These findings support the superiority of ATAD in during land application of biosolids. To overcome the vec- selectively reducing potential human and animal pathogens tor attraction, US EPA recommended that the reduction of compared to ALF, which is a typical manure stabilization VS % should be more than 38%. The lime stabilization was method used in livestock farms. In a comparison between reported to achieve these standards as will be presented in aerobic and anaerobic treatment of biosolids, it can be indi- section 10.6. Another way to prevent the vector attraction cated that the anaerobic process is more efficient than the is by covering the air-drying basin by transparent polyeth- aerobic process, but the limitations to apply the anaerobic ylene terephthalate (PET) as in the case of SODIS of water treatment lie in the design and the maintenance in the devel- and wastewater. However, more research is needed in this oping countries. regards. Air‑drying Eec ff t of storage Air-drying allows partially digested biosolids to dry natu- Biosolids are stored inside buildings and outside enclosed rally in the open air. Wet biosolids are usually applied to in steel or concrete tanks. The storage duration of biosol- a depth of approximately 23 cm onto sand drying beds or ids could strongly affect the survival of pathogenic bac- even deeper (US EPA 2000). The sewage sludge is left to teria. During storage, the biosolids undergo biochemical dry by the evaporation. The effectiveness of the air-drying changes, which depend on the storage temperature. These 1 3 Applied Water Science (2018) 8:74 Page 15 of 25 74 changes effect on the survival of pathogenic bacteria. The growth temperature. The period of exposure is depended on storage of biosolids at low temperatures prolong pathogens the temperature as well as the bacterial species (Himathong- survival, while at high storage temperatures free ammonia kham and Riemann 1999). which would shorten the pathogens chances for survival is The total inactivation of pathogenic bacteria in biosol- produced (Svoboda and Carcluie 2003). ids requires a holding time of 4.78 h at 60 °C compared Ahmed and Sorensen (1995) evaluated pathogen inac- to 30 min at 70 °C (US EPA 1994). Moce-Llivina et al. tivation during storage of biosolids. The pathogens tested (2003) recorded significant reductions in indigenous E . coli included S. typhimurium, Y. enterocolitica, Campylobacter to below detectable levels after 30 and 90 min at 80 °C. The jejuni. Biosolids samples seeded with the pathogens were indigenous FS was only reduced between 1.4 and 1.8 log incubated under both anaerobic and aerobic conditions in units after 30 min but undetectable after 90 min. S. choler- reactors at 5, 22, 38 and 49.5 °C for up to 62 days. They aesuis cells that were added to sludge at high counts were revealed that pathogenic bacteria decreased in stored bio- reduced by approximately 6 log after 30 min at 80 °C and solids at all temperatures and survival decreased as the tem- by more than 8 log after 60 min at 80 °C. They concluded perature increased. that temperature of 80 °C for 30–60 min would probably Liu (2000) observed that FC in biosolids was inactivated qualify the biosolids product as Class A requirements. naturally by storing the sample in an airtight container The EPA Part 503 regulations consider heat drying as at room temperature (20–23  °C). This natural inactiva- PFRPs and suggest that, the temperature of the biosolids tion started after 17–28 days of storage and FC were not should exceed 80 °C but no time is given treatment period. detected after 100 days of storage. However, FC density in In other instances, it seems clear that processes using higher samples stored at − 22 and 4 °C had no significant reduc- than 60–70 °C can produce biosolids Class A (Springthorpe tion in 3 months. Nicholson et al. (2000) recorded that slight and Sattar 2004). increases in temperature during summer destroy E. coli Abdel-Monem et al. (2008a) investigated the inactivation O157 and radically decrease number of Salmonella after a of TC, FC, FS and Salmonella spp. in biosolids by thermal few months. treatment at 60 and 80 °C. The study revealed that the inac- Placha et  al. (2001) found that in pig slurry, S. typh- tivation of Salmonella spp. and FS was significantly greater imurium survived for 26 days in summer and 85 days in than the inactivation of TC at 80 °C for 90 min. After heat winter and FC were reduced by 90% in 35 and 233 days treatment at 80 °C for 120 min, TC reduced by 5.5 log during summer and winter time, respectively. However, stor- while FC, FS and Salmonella were undetected and the bio- age alone is not regarded as an effective way to inactivate solids met the US EPA, Class A standards for biosolids pathogens in sludge (Carrington 1998). Avery et al. (2005) reuse. monitored the decline in E. coli O157 in different wastes over 64 days. They concluded that the storage decreases the Lime stabilization treatments amount of E. coli O157 but does not eliminate the pathogen. According to Sahlstrom et al. (2006), the sludge is stored The principle objectives of alkaline stabilization are to usually for 6 months, in heaps outdoors on the ground or reduce the activity of pathogenic bacteria and inhibit their on a concrete surface, before being used. After 2 months regrowth and thus reduce the health hazard associated with of storage of sewage sludge, no Salmonella spp. could be the biosolids (WEF 1995). The most commonly used alka- isolated in the heaped material. Al-Gheethi et al. (2014) line is the quick lime (calcium oxide, CaO) and its derivative observed that the biosolids stored for 24 weeks at room tem- hydrated lime or slaked lime (calcium hydroxide, Ca(OH) ) perature (25 ± 2 °C) met the standards limits recommended which are used due to their low cost. Adding adequate vol- by US EPA, Class A, and suitable for reuse in the agriculture ume of CaO to the biosolids leads to increase of pH to 12 as fertilizers. (or higher) and temperature to be between 55 and 70 °C, and as results for these conditions the pathogenic bacteria are Heat treatments inactivated or destroyed (Hansen et al. 2007). Plachy et al. (1996) demonstrated that S. typhimurium Heat drying involves using active or passive dryers to was eliminated from biosolids after 60  min of hydrated destroy pathogens and remove water from biosolids. In this lime addition. Reimers (1997) found that the inactivation process, biosolids are dried with hot gases at temperatures of pathogenic bacteria by lime was not only because of the greater than 80 °C to reduce the moisture content to 10% or hydroxide ions but also because of silicate components in lower. Pathogenic bacteria, viruses, and helminth ova are lime. This conclusion was derived from studies by compar- reduced to below detectable levels in properly operated heat- ing pathogen inactivation effects of sodium hydroxide and drying systems (Lucero-Ramirez 2000). Pathogenic bacteria calcium hydroxide. According to Schwartzbrod et al. (1997) are inactivated during exposure to heat, above their optimum the raising of the pH to at least pH 12 by the use of lime has 1 3 74 Page 16 of 25 Applied Water Science (2018) 8:74 −1 −1 the effect to suspend microbiological activity and lime con- 42.65  g  kg TS and 91.41% with 133.52  g  kg after ditioning in specific conditions (pH of 12.5 for 2-4 months) 120 h. can cause helminths reduction by 98.5% and a virus inactiva- Toth et al. (2012) investigated the alkaline treatment of tion by 90%, while biosolids met the Class B requirements animal manures by hydrated lime (CaOH ) to eliminate when the pH was 12 or above after 2 h of contact. S. enterica and E. coli O157:H7. They found that both Amer (1997) studied the effect of quick lime (CaO) pathogens were killed when pH was more than 11.0 within and cement dust additions to biosolids on the reduction of 2 weeks. Farzadkia and Bazrafshan (2014) studied the lime pathogenic bacteria. Rapid reduction in TC, Salmonella stabilization of biosolids on the inactivation of FC. The and Shigella counts were achieved after the addition of study was conducted in a reactor for 6 weeks, the biosolids quick lime and cement dust. US EPA (2000) reported that stabilization with hydrated lime reduced FC more than biosolids Class A requirements can be achieved when the 99.99% and the stabilized biosolids met US EPA standards pH of the mixture is maintained at or above 12 for at least limits of class B. 72 h, with a temperature of 52 °C maintained for at least 12 h during the period. Bina et al. (2004) investigated the effect of liming on Pathogen growth potential (PGP) the microbiological quality of urban liquid raw biosolids. The lime was added to increase the pH of biosolids to pH PGP is defined as the ability of inactivated bacteria to re- 11 and 12 for 2, 24, 72 and 120 h. Salmonella spp. were grow again in the disinfected sample. The effectiveness inactivated completely in treated biosolids after 2 h. 99% of disinfection process for treated sewage and biosolids of FC reduction was obtained for two ranges of pH (pH 11 depends on inactivation of pathogenic bacteria. However, and 12). Biosolids treated with lime met US EPA stand- it is well known that under unfavourable conditions, bac- ards for Class B and Class A after 2 and 24 h, respec- teria may transfer into a dormant state called viable but tively. At pH higher than pH 11 and 12 treated biosolids non-culturable (VBNC), which mean the microorganism with lime met vector attraction reduction requirements has slow metabolic processes and no cell division (Oli- after 2 h. ver 2005). Therefore, the development of the detection, Sasdkovd et al. (2005) stored biosolids amended with enumeration and viability assessment of pathogenic bac- zeolite and lime for 42 days at a temperature between 14.5 teria in biosolids is required (Sidhu and Toze 2009). For and 17.9 °C. Samples were taken at 5-day intervals for the microbial cell, death is the irreversible loss of microbial determination of TC, FC and FS. The results revealed a cell to growth and reproduction. To verify this fact the decrease in plate counts of the observed bacteria in exper- isolation on solid culture medium is the suitable method. imental substrates compared to the control biosolids. The microbial cell is considered dead if they fail to form −1 Yurtsever (2005) found that about 150–200 g CaO kg colonies. However, the cultural based technique depends TS is satisfactory for keeping pH on recommended levels on culture medium used. Bacteria may fail to grow on and to reduce FC to less than detectable limits. solid media and need to be cultured first in enrichment In alkaline treatment study conducted by Abdel- media (Block 2001; Efaq et al. 2015). Monem et al. (2008b), the results revealed that 19.12 g The condition of storage for disinfected sample affect −1 of quicklime kg TS reduced FC to meet the require- the ability of bacteria to regrow, for example, bacterial ments of US EPA standards for Class B after 2  h and inactivation by UV irradiation may reach to 99.99%, but Class A criteria after 24 h. Salmonella spp. reduced to if the disinfected sample stored at optimal conditions the −1 meet Class A criteria after 120 h. At 29.41 g kg TS, FC regrowth of inactivated bacteria may reach to 90%. This and Salmonella spp. dropped to below US EPA Class A means the bacteria can repair damage caused by UV. Al- −1 limit after 24 h. At 42.65 g kg TS, FC has reduced to Gheethi et al. (2013b) found that Salmonella spp. S. aureus below detection level after 24 h and Salmonella after 2 h. and E. faecalis grow again in treated sewage exposed to US EPA requirements for Class B met after 2 h, while the SODIS for 6 h, when the samples were incubated at 37 °C requirements for Class A met for Salmonella spp. after for 4 days. The bacterial regrowth may occur if the treat- −1 2 h and FC after 24 h. Finally, 133.52 g kg TS of lime ment process did not lead to physical damage of bacterial was found to be very effective, Salmonella spp. and FC cell and PGP bioassay should be carried out (Al-Gheethi were inactivated completely after 2 h. To reduce vector et al. 2016a, b; Efaq et al. 2017). PGP has been used to attraction, US EPA recommended that the reduction of assay bacterial growth in drinking water disinfected by VS % should be more than 38% (US EPA 2003). In the ozonation and different bio-filter systems (Berney et al. study conducted by Al-Gheethi (2008), the mass of vola- 2006; Vital et al. 2010). tile solids in the biosolids has reduced by 63.47% with Choi et al. (1999) stated that the main factors, which convert dormant bacteria cell to be active, the factors 1 3 Applied Water Science (2018) 8:74 Page 17 of 25 74 included the incubation and substrate addition such as glu- some limitations especially when applied to environmental cose, amino acids or yeast extract. Luna et al. (2002) found samples. that after nutrient enrichment, a large fraction of dormant Some researchers used the culture method and the molec- bacteria (6–11% of the inactivated bacterial number) was ular analysis to investigate the presence of pathogenic bac- reactivated. teria in the VBNC state. Jiang et al. (2013) combined the The factors, which might induce bacterial cell to be standards culture method (MPN technique) with the reverse VBNC, are less nutrients, nucleotide, inactive cell mem- transcription quantitative PCR (RT-qPCR) assay for the brane, size of bacterial cells and presence of antibiotics, quantification of S . typhimurium, E. coli and S, flexneri in which inhibit DNA synthesis without affecting other cellu- the VBNC state during anaerobic digestion of biosolids. lar metabolic activities (Gasoll et al. 1995; Joux and LeB- They revealed that the cycle threshold (C ) values from RT- aron 1997; Luna et al. 2002; Kim et al. 2009). Therefore, qPCR assays have significant correlation to the counts of 2 2 some authors recommended using molecular techniques E. coli (R  = 0.9964), S. typhimurium (R  = 0.9938) and such as PCR to detect the presence of VBNC bacteria after S. flexneri ( R  = 0.997). In addition, they stated that the disinfection process (Straub et al. 1993; Choi et al. 1996). quantification results of VBNC pathogens using RT-qPCR Chen et al. (2012) determined log reduction of Salmonella could provide an improved evaluation of pathogen inactiva- sp., E. coli and Shigella sp. during mesophilic anaerobic tion efficiency and biological safety in the biosolids. digestion of sludge by MPN and PCR. They found that log Real-time quantitative polymerase chain reaction (qPCR) reduction determined by MPN was much higher than the is fast, sensitive, and specific molecular tool for enumera- data recorded by quantitative PCR. They explained their tion of pathogens in biosolids. However, the main limita- findings due to the presence of viable but non-culturable tion is that it amplifies all target DNAs, including that from pathogen cells. non-viable cells. Therefore, to overcome this limitation the However, other investigators reported that PCR technique authors suggested that the couple qPCR with PMA (van is not suitable after disinfection process as PCR can still Frankenhuyzen et al. 2011) or EMA (Fijalkowski et al. 2014) recognize or detect the DNA fragments of the bacterial cells can be used to monitor the presence of viable pathogens in that have been killed during disinfection processes, thus, several different matrices. yielding false positive results (Baloda and Krovacek 1994). Fijalkowski et al. (2014) detected the presence of E. coli O157:H7 in wastewater and sewage sludge in Poland by Current status of sewage treatment quantitation method of (EMA) real time-PCR. They found in Middle East countries that E. coli O157:H7 gene copies were detected in primary influents and final effluents in winter from municipal waste- In the Middle East countries, there is no plan to build ter- water treatment plant. However, the ethidium monoazide tiary treatment systems (except some STPs in Riyadh, Saudi bromide (EMA) application revealed false-positive detec- Arabia which use sand filters as a tertiary treatment process, tion of this bacterium in final effluents. They also detected Al-Jasser 2011). They focus on the basic standard of pri- large amount of “free DNA” derived from dead cells that mary and secondary treatment. Most sewage is reused for gave false-positive results. agricultural irrigation purpose. This is due to increase in In the last decades, authors have detected the viability of population growth rate, besides present expansion of water bacterial cells based on metabolic activity, such as detection networks in these countries without parallel construction of of RNA transcripts, a positive energy status and responsive- new sewage network, or rehabilitation of the existing ones ness. The detected RNA transcripts were used to detect via- (Abdel-Raouf et al. 2012). ble cells in combination with DNA amplification techniques. Most treated sewage and biosolids generated from STPs The technology depends on the treatment of bacterial cells in Middle East countries have not met the standards limits with photoactivatable, and cell membrane impermeant with required by WHO and US EPA. Saleem et al. (2001) inves- nucleic acid intercalating dyes propidium monoazide (PMA) tigated the counts FC during summer and winter seasons in or ethidium monoazide (EMA) followed by light exposure the drying biosolids generated from Al-Khobar sewage treat- prior to extraction of DNA and amplification. Light acti- ment plant in Saudi Arabia. They found that FC was more vation of DNA-bound dye molecules results in irreversible than standards limits required for US EPA, Class B. El-Lathy DNA modification and subsequent inhibition of its ampli- et al. (2009) reported that the concentrations of Salmonella fication. Sample pre-treatment with viability dyes has been spp., in biosolids generated from Zenin sewage treatment used in combination with PCR (leading to the term viability plant at Giza Governorate, Egypt were 330 CFU/mL, which PCR,v-PCR), and increasingly with isothermal amplifica- means the biosolids, has not met the standards limits recom- tion method (Fittipaldi et al. 2012). This technique still has mended by US EPA for biosolids Class A. AL-Jaboobi et al. (2013) stated that FC in the treated sewage canal generated 1 3 74 Page 18 of 25 Applied Water Science (2018) 8:74 from STP (primary and secondary processes) located in are efficient, easily implementable, natural, with no toxic Sana’a Yemen was more than WHO guidelines. Al-Gheethi by-products and most of all are of low cost. et al. (2014) evaluated the efficiency of five STPs in Yemen Open Access This article is distributed under the terms of the Crea- for reduction of faecal indicators and pathogenic bacteria in tive Commons Attribution 4.0 International License (http://creat iveco the secondary effluents and biosolids. They also found that mmons.or g/licenses/b y/4.0/), which permits unrestricted use, distribu- FC was more than WHO guidelines for sewage effluents as tion, and reproduction in any medium, provided you give appropriate well as US EPA Class A, and B for biosolids. credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. In comparison to developed countries, Rose et al. (2004) investigated the efficiency of six STPs in USA for reduction of FC. All STPs used primary treatment, four STPs used the biological treatment (activated sludge), one STP used References nitrification and one STP used biological nutrient removal. 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