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 firstname.lastname@example.org 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. Filtration process is carried out by fabric, sand and anthra- Abdel-Monem MO, Al-Zubeiry AH, AL-Gheethi AAS (2008a) Sur- cite. Disinfection process is carried out by chlorine, sodium vival of enteric indicators and pathogenic bacteria in sewage sludge after thermal treatment. J Botany 27(1):171–183 hypochlorite and UV irradiation. However, the concentra- Abdel-Monem MO, Al-Zubeiry AH, AL-Gheethi AAS (2008b) Elim- tions of FC in treated sewage at six STPs were more than the ination of Salmonella and faecal indicator bacteria in sewage WHO guidelines. In the light of the aforementioned, Ener- sludge by quick lime stabilization. J Environ Sci 36:281–297 hall and Stenmark (2012) also reported that TC and entero- Abdel-Raouf N, Al-Homaidan AA, Ibraheem IBM (2012) Microalgae and wastewater treatment. Saudi J Biol Sci 19(3):257–275 cocci were 5.8 and 5.08 log CFU/100 mL, respectively in Acra A, Jurdi H, Mu’allem Y, Karahagopian Y, Raffoul Z (1990) Water treated sewage generated from STP in Sweden, which used disinfection by solar radiation: assessment and application. Inter- filtration system during the disinfection process. Viau and national Development Research Centre (IDRC), Ottawa Peccia (2009) stated that the concentrations of FC in biosol- ACWUA (2010) Wastewater reuse in Arab Countries, working group on wastewater reuse. Arab Countries Water Utility Association ids generated from 29 STPs in USA, which use mesophilic (ACEUA), Amman anaerobic digestion (MAD), temperature-phased anaerobic Ahmed AU, Sorensen DL (1995) Kinetics of pathogen destruction digestion (TPAD), composting the biosolids after anaerobic during storage of dewatered biosolids. Water Environ Res digestion (COM) corresponded to US EPA regulatory limits 67(2):143–150 Aksu Z, Tunc O (2005) Application of biosorption for penicillin G for each biosolids Class A and Class B. removal: comparison with activated carbon. Process Biochem 40(2):831–847 Alamanos Y, Maipa V, Levidiotou S, Gessouli E (2000) A com- munity waterborne outbreak of gastro-enteritis attributed to Conclusion Shigella sonnei. J Epidemiol Infect 125(3):499–503 Al-Asbahi QY (2005) Water resources information in Yemen. IWG- Environmental International Work Session on Water Statistics, The reuse of sewage-treated effluent and biosolids for agri- Vienna cultural purpose has increased extensively in the last few Al-Ashwal AM, Basalah AO (2012) Energy conservation indica- decades in the Middle East countries. Those countries face a tors in Southern Mediterranean countries. Country report for severe shortage of water resources and tertiary sewage treat- Yemen. Plan Bleu UNEP/MAP Regional Activity Centre, Sophia Antipolis ment plants are not available. Treated sewage and biosolids Alcalde L, Oron G, Gillerman L, Salgot M, Manor Y (2003) Removal are rich with nitrogen and phosphate that would improve of faecal coliforms, somatic coliphages and F-specific bacte- plant growth and soil properties. However, it has also a large riophages in a stabilization pond and reservoir system in arid diversity of pathogenic bacteria, which represent a potential regions. Water Sci Technol 3(4):177–184 Al-Enezi G, Hamoda MF, Fawzi N (2004) Heavy metals content of risk for human and animal. Most of these pathogens could municipal wastewater and sludges in Kuwait. J Environ Sci survive for a long time in the environment, because these 39(2):397–407 pathogens produce endospores and others can survive in Al-Gheethi AAS (2008) Bacteriological studies on sludge from some VBNC state. Therefore, further treatment of sewage efflu- municipals wastewater treatment plants in Yemen. MS.c The- sis, Department of Applied Microbiology, Faculty of Applied ents and biosolids generated from secondary treatment is Science, Taiz University, Taiz, Yemen necessary to reduce the pathogenic bacteria before reuse for Al-Gheethi AAS (2014) Screening of bacterial isolates from sew- agricultural purpose. Further treatment using technologies age treated effluent with potential to remove heavy metals and such as SODIS, air-drying and lime treatment appears to β-lactam antibiotics. Ph.D. Thesis, Environmental Technology Division, School of Industrial Technology, University Science be more suitable to the nature and climate of Middle East Malaysia. Penang, Malaysia countries and can vouch for their efficiencies. These pro- Al-Gheethi AAS, Ismail N (2014) Biodegradation of pharmaceu- cesses have the potential to reduce pathogenic bacteria in tical wastes in treated sewage effluents by Bacillus subtilis 1556WTNC. Environ Process 1(4):459–489 treated sewage and biosolids. Economically, the processes 1 3 Applied Water Science (2018) 8:74 Page 19 of 25 74 Al-Gheethi AAS, Norli I, Kadir MO (2013a) Elimination of enteric APHA (1998) Standard methods for the examination of water and indicators and pathogenic bacteria in secondary effluents and wastewater, 20th edn. American Public Health Association, lake water by solar disinfection (SODIS). J Water Reuse Desal- Washington ination 3(1):39–46 Ashbolt NJ, Grabow WOK, Snozzi M (2001) Indicators of microbial Al-Gheethi AAS, Norli I, Lalung J, Azieda T, Kadir MO (2013b) water Association, Washington Reduction of faecal indicators and elimination of pathogens Astals S, Venegas C, Peces M, Jofre J, Lucena F, Mata-Alvarez J from treated sewage by heat treatment. Caspian J Appl Sci (2012) Balancing hygienization and anaerobic digestion of raw Res 2(2):29–45 sewage sludge. Water Res 46(19):6218–6227 Al-Gheethi AAS, Norli I, Lalung J, Azieda T, Efaq AN, Kadir MO Avery LM, Killham K, Jones DL (2005) Survival of E. coli O157: H7 (2013c) Susceptibility for antibiotics among faecal indicators in organic wastes destined for land application. J Appl Microbiol and pathogenic bacteria in sewage treated effluents. Water 98:814–822 Pract Technol 8(1):1–6 Bala JD, Yusuf IZ, Tahir F (2012) Bacteriological assessment of phar- Al-Gheethi AAS, Abdul-Monem MO, AL-Zubeiry AHS, Efaq AN, maceutical wastewater and its public health implications in Nige- Shamar AM, Al-Amery RMA (2014) Effectiveness of selected ria. IUP J Biotechnol 6(1):34–50 wastewater treatment plants in Yemen for reduction of faecal Baloda SB, Krovacek K (1994) Use of polymerase chain reaction indicators and pathogenic bacteria in secondary effluents and (PCR) technology in the detection of foodborne pathogens: an sludge. Water Pract Technol 3(3):293–306 overview. In: Proceedings of International Congress on “Qual- Al-Gheethi AA, Norli I, Efaq AN, Bala JD, Al-Amery R (2015) ity of Veterinary Services for the 21st Century”; Kuala Lumpur, Solar Disinfection and lime treatment processes for reduction 1994; pp 123–126 of pathogenic bacteria in sewage treated effluents and biosolids Barbagallo S, Brissaud F, Cirelli GL, Consoli S, Xu P (2003) Modeling before reuse for agriculture in Yemen. Water Reuse Desalina- of bacterial removal in wastewater storage reservoir for irriga- tion 5(3):419–429 tion purposes: a case study in Sicily, Italy. Water Sci Technol Al-Gheethi AA, Mohamed RMS, Efaq AN, Norli I, Amir Hashim 3(4):169–175 MO, Kadir Ab (2016a) Bioaugmentation Process of Sewage Bataller M, Veliz E, Fernandez LA, Hernandez C, Fernandez I, Alvarez Effluents for the Reduction of Pathogens, heavy metals and C, Sanchez E (2005) Secondary effluent treatment with ozone. antibiotics. J Water Health 14(5):780–795 In: IOA 17th World Ozone Congress Straboung 2005. p 1–9 Al-Gheethi AA, Mohamed RM, Efaq AN, Amir HK (2016b) Reduction Baudišová D (2009) Microbial pollution of water from agriculture. Pant of microbial risk associated with greywater utilized for irrigation. Soil Environ 55(10):429–435 Water Health J 14(3):379–398 Berney M, Weilenmann HU, Simonetti A, Egli T (2006) Efficacy of Al-Gheethi AA, Mohamed RM, Efaq AN, Adib MR, Ismail N (2017) solar disinfection of E. coli, S. flexneri , S. typhimurium and V. Reduction of bacteria in storage system of sewage effluents. J cholera. J Appl Microbiol 101(4):828–836 Sustain Water Resour Manag 3:193–203 Bina B, Movahedian H, Kord I (2004) The effect of lime stabiliza- Al-Jaboobi M, Bouksaim M, Tijane M, EL-Ariqi S (2013) Agricultural tion on the microbiological quality of sewage sludge. Iranian quality evaluation of wastewater, used in Yemen vegetables pro- J Environ Health Sci Eng 1(1):34–38 duction. Mid East J Sci Res 16(5):667–677 Bitton G (2005a) Wastewater microbiology, 3rd edn. Wiley, Hobo- Al-Jasser AO (2011) Saudi wastewater reuse standards for agricultural ken, p 746 irrigation: riyadh treatment plants effluent compliance. J King Bitton G (2005b) Microbial indicator of faecal contamination: Appli- Saud Univ Eng Sci 23(1):1–8 cation to microbial source tracking. Report submitted to the Alonso E, Santos A, Riesco P (2004) Microorganism regrowth waste- Florida Storm water Association. Association 719 East Park water disinfected by UV radiation and ozone: a microbiological Avenue, Tallahassee, 32301. University of Florida study. Environ Technol 25(4):433–441 Block SS (2001) Disinfection, sterilization, and preservation, 5th Al-Rekabi WS, Qiang H, Qiang WW (2007) Improvements in waste- edn. Lippincott Williams and Wilkins, Lippincott Williams water treatment technology. Pak J Nutr 6(2):104–110 and Wilkins Al-Sabahi E, Abdul-Rahim S, Wan-Zuhairi WY, Alshaebi F, Al Bohm R (2004) Hygienic safety in organic waste management. Nozaily F (2009) Assessment of groundwater and surface In: Lens P, Hamerels B, Hoitink H, Bidlingmaier W (eds) water pollution at Mitm Area, Ibb City, Yemen. Am J Appl Sci Resource, recovery and reuse in organic solid waste manage- 6(4):772–783 ment. IWA Publishing, London Al-Saed R (2007) Pathogens assessment in reclaimed effluent used Brenner DJ, Krieg NR, Staley JT (2005) Bergey’s manual of sys- for industrial crops irrigation. Int J Environ Res Public Health tematic bacteriology, vol 2, proteobacteria, Parts A, B and C. 4(1):68–75 Williams and Wilkins Awaverly Co, Philadelphia Al-Sharabee R (2009) The effect of using wastewater on microbio- Burtscher C, Wuertz S (2003) Evaluation of the use of PCR and logical pollution for vegetable crops, MSc Thesis, Faculty of reverse transcriptase PCR for detection of pathogenic bacteria Agriculture, Sana’a University, Yemen in biosolids from anaerobic digestors and aerobic composters. Alvarez-Ordonez A, Begley M, Prieto M, Messens M, Lopez M, Ber- Appl Environ Microbiol 69(8):4618–4627 nardo A, Hill C (2011) Salmonella spp. survival strategies within Byappanahalli MN, Fujioka RS (1998) Evidence that tropical soil the host gastrointestinal tract. J Microbiol 157(12):3268–3281 environment can support the growth of E. coli. Water Sci Tech- Al-Zubeiry AHS (2005) Microflora inhabiting raw sewage, secondary nol 38(12):171–174 eu ffl ent and dewatered sludge in Ibb, Yemen Republic. Ass Univ Carlander A (2006) Assessment of microbial health hazards associ- Bull Environ Res 8(1):1–16 ated with wastewater application to willow coppice, conifer- Amer AA (1997) Destruction of sludge pathogenic bacteria using quick ous forest and wetland systems. Ph. D. Thesis. University of lime and cement dust. J Soil Sci 37:343–354 Agricultural Sciences, Swedish APHA (1989) Standard methods for the examination of water and Carrington EG, Davis RD, Hall JE, Pike EB, Smith SR, Unwin RJ wastewater, 17th edn. American Public Health Association, (1998) Review of the scientific evidence relating to the con- Washington trols on the agricultural use of sewage sludge. Report DETR 4415/3 [part1] and Report DETR 4454/4 [part 2] WRc plc, Medmenham 1 3 74 Page 20 of 25 Applied Water Science (2018) 8:74 Carvalho FG, Teixeira L (2002) History, taxonomy, biochemical char- Dumontet S, Scopa A, Kerje S, Krovacek K (2001) The importance of acteristics, and antibiotic susceptibility testing of enterococci. pathogenic organisms in sewage and sewage sludge. J Air and The enterococci: pathogenesis, molecular biology, and antibiotic Waste Manag Assoc 51:848–860 resistance. ASM Press, Washington Dungeni M, Merwe RR, Momba MNB (2010) Abundance of patho- Casey TJ (1997) Unit treatment processes in water and wastewater genic bacteria and viral indicators in chlorinated effluents pro - engineering. Wiley, Chichester duced by four wastewater treatment plants in the Gauteng Prov- CDPH (2009) Treatment technology report for recycled water. Califor- ince, South Africa. Water SA 36(5):607–614 nia Department of Public Health, State of California Division of Dutta M, Dutta NN, Bhattacharya KG (1999) Aqueous phase adsorp- Drinking Water and Environmental Management, Sacramento tion of certain beta-lactam antibiotics onto polymeric resins and Celico F, Varcamonti M, Guida M, Naclerio G (2004) Influence of pre- activated carbon. Separ Purif Technol 16(3):213–224 cipitation and soil on transport of faecal enterococci in fractured Edberg SC, Allen MG, Smith DB, Kriz NJ (1990) Enumeration of total limestone aquifers. Appl Environ Microbiol 70(5):2843–2847 coliforms and E. coli from source water by the defined substrate Ceustermans A, De Clercq D, Aertsen A, Michiels C, Geeraerd A, Van technology. Appl Environ Microbiol 56(2):366–369 Impe J, Coosemans J, Ryckeboer J (2007) Inactivation of Salmo- Efaq AN, Rahman Nik Norulaini Nik Ab, Nagao H, Al-Gheethi AA, nella Senftenberg strain W 775 during composting of biowastes Shahadat Md, Kadir MO (2015) Supercritical carbon dioxide as and garden wastes. J Appl Microbiol 103(1):53–64 non-thermal alternative technology for safe handling of clinical CFR (1995) Standards for the use or disposal of sewage sludge. Title wastes. J Environ Process 2(4):797–822 40, Part 503 Efaq AN, Ab Nik Norulaini Nik, Rahman Nagao H, Al-Gheethi AA, Chen YC, Higgins MJ, Beightol SM, Murthy SN, Toffey WE (2011) Kadir MO (2017) Inactivation of aspergillus spores in clinical Anaerobically digested biosolids odor generation and pathogen wastes by supercritical carbon dioxide. AJSE 42(1):39–51 indicator regrowth after dewatering. Water Res 45(8):2616–2626 Ellafi A, Abdallah F, Bakhrouf A (2010) Effect of starvation on sur - Chen Y, Fu B, Wang Y, Jiang Q, Liu H (2012) Reactor performance vival and adhesion ability of Shigella spp. in domestic treatment and bacterial pathogen removal in response to sludge retention plant effluent microcosms. J Ann Microbiol 60(3):383–389 time in a mesophilic anaerobic digester treating sewage sludge. El-Lathy MA, El-Taweel GE, El-Sonosy WM, Samhan FA, Moussa Biores Technol 106:20–26 TAA (2009) Determination of pathogenic bacteria in wastewa- Choi JW, Sherr EB, Sherr BF (1996) Relation between presence- ter using conventional and PCR techniques. Environ Biotechnol absence of a visible nucleoid and metabolic activity in bacterio- 5(2):73–80 plankton cells. Limnol Oceanogr 41:1161–1168 Enerhall C, Stenmark E (2012) Disc Filters to Reduce Wastewater Choi JW, Sherr BF, Sherr EB (1999) Dead or alive? A large fraction Pathogen Levels in Raw Water Sources. Master of Science Thesis of ETS-inactive marine bacterioplankton cells, as assessed by in the Master’s Programme Geo and Water Engineering. Depart- reduction of CTC, can become ETS-active with incubation and ment of Civil and Environmental Engineering Division of Water substrate addition. Aquat Microb Ecol 18(9):105–115 Environment Technology, Chalmers University of Technology. Cooper RC, Olivieri AW (1998) Infectious disease concerns in waste- Göteborg, Sweden 2012 water reuse. In: Asano T (ed) Wastewater reclamation and reuse. Espigares E, Bueno A, Espigares M, Galvez R (2006) Isolation of Sal- Technomic Publishing Company, Lancaster, pp 489–520 monella serotypes in wastewater and effluent: effect of treatment Coronel-Olivares C, Reyes-Gomez LM, Hernandez-Munoz A, Mar- and potential risk. Int J Hyg Environ Health 209:103–107 tinez-Falcon AP, Vazquez-Rodríguez GA, Iturbe U (2011) Chlo- Facile N, Barbeau B, Prevost M, Koudjonou B (2000) Evaluating rine disinfection of P. aeruginosa, total coliforms, E. coli and bacterial aerobic spores as a surrogate for Giardia and Crypto- E. faecalis: revisiting reclaimed water regulations. Water Sci sporidium inactivation by ozone. Water Res 34(12):3238–3246 Technol 64(11):2151–2157 FAO (2008) Irrigation in the Middle East region in figures. Aquastat Cotruvo JA, Rees ADG, Bartram J, Carr R, Cliver DO, Craun GF, survey 2008. In: Frenken K (Ed.) Land and Water Division. Food Fayer R, Gannon VPJ (2004) Waterborne zoonoses: identifica- and Agriculture Organization. FAO Water Reports 34 tion, causes and control. World Health Organization, London Farzadkia M, Bazrafshan E (2014) Lime stabilization of waste activated County K (2005) Biosolids quality summary. Department of Natural sludge. Health Scope J 3(1):1–5 Resources and Parks Wastewater Treatment. Division Technol- Fijalkowski KL, Kacprzak MJ, Rorat A (2014) Occurrence changes of ogy Assessment and Resource Recovery, 201. S. Jackson Street, Escherichia coli (including O157:H7 serotype) in wastewater and KSC-NR-0512 Seattle, Washington 98104-3855 sewage sludge by quantitation method of (EMA) real time-PCR. Crook J (1998) Water reclamation and reuse criteria. Water Sci Technol Desalination Water Treat 52:19–21 33(10–11):451–462 Fine P, Atzmon N, Adani F, Hass A (2006) Disposal of sewage effluent Cunault C, Pourcher AM, Burton CH (2011) Using temperature and and biosolids in eucalyptus plantations: a lysimeter simulation time criteria to control the effectiveness of continuous thermal study. Soil Water Pollut Monit Prot Rem 3(23):433–453 sanitation of piggery effluent in terms of set microbial indicators. Fittipaldi M, Nocker A, Codony F (2012) Progress in understand- J Appl Microbiol 111(6):1492–1504 ing preferential detection of live cells using viability dyes in Dalkmann P, Broszat M, Siebe C, Willaschek E, Sakinc T, Huebner combination with DNA amplification. J Microbiol Methods H, Amelung W, Grohmann E, Siemens J (2012) Accumula- 91(2):276–289 tion of pharmaceuticals, Enterococcus, and resistance genes in Fratamico PM, Bhunia AK, Smith JL (2005) Foodborne pathogens soils irrigated with wastewater for zero to 100 years in Central microbiology and molecular biology. Horizon Scientific Press, Mexico. PLoS One 7(9):e45397. https ://doi.org/10.1371/journ Poole al.pone.00453 97 Fujioka RS (1997) Indicators of marine recreational water quality. In: Dancer SJ (2004) How do we assess hospital cleaning? A proposal Hurst CJ, Knudsen GR, McInerney MJ, Stezenbach LD, Walter for microbiological standards for surface hygiene in hospitals. J MV (eds) Manual of environmental microbiology. ASM Press, Hospital Infect 56:10–15 Washington, pp 176–183 Dumontet S, Dinel H, Baloda SB (1999) Pathogen reduction in sewage Garcia-Armisen T, Vercammen K, Passerat J, Triest D, Servais P, Cor- sludge by composting and other biological treatments: a review. nelis P (2011) Antimicrobial resistance of heterotrophic bacteria Biol Agric Hortic 16(4):409–430 in sewage-contaminated rivers. Water Res 45(2):788–796 1 3 Applied Water Science (2018) 8:74 Page 21 of 25 74 Gasoll GM, Giorgio A, Massana R, Duarte CM (1995) Active versus organisms in surface water in Southwestern Finland, 2000–2001. inactive bacteria: size-dependence in a coastal marine plankton Appl Environ Microbiol 70(1):87–95 community. Mar Ecol Prog Ser 128:91–97 Ibenyassine K, Mhand RA, Karamoko Y, Anajjar B, Chouibani M, Gebra CP (1996) Microbial pathogens in municipal solid waste. In: Ennaj MM (2007) Bacterial pathogens recovered from veg- Palmisano AC, Barlaz MA (eds) Microbiology of solid waste. etables irrigated by wastewater in Morocco. J Environ Health CRC Press, Boca Raton, pp 71–104 69(10):47–51 Geldreich EE (1978) Bacterial populations and indicator concepts in Jagger J (1985) Solar-UV actions on living cells, 1st edn. Praeger Pub- feces, sewage, storm water and solid wastes. In: Berg G (ed) lishers, New York Indicators of viruses in food and water. Ann Arbor Science Pub- Janex ML, Savoye P, Xu P, Rodriguez J, Lazarova V (2000) Ozone lishers, Ann Arbor, pp 51–97 for Urban Wastewater Disinfection: A New Efficient Alternative Geldreich E (1996) Microbial quality of water supply in distribution Solution. In: Proceedings of the Specialized Conference on Fun- systems. CRC, Boca Raton, pp 76–78 damental and Engineering Concepts for Ozone Reactor Design, Ghazala S, Ramaswamy S, Smith JP, Simpson BK, Simpson MV Toulouse, France; International Ozone Association: Stamford, (1991) Establishing sous-vide processing schedules for spa- Connecticut; pp 95–98 ghetti/meat sauce and rice/salmon based on thermal destruction Jiang Q, Fu B, Chen Y, Wang Y, Liu H (2013) Quantification of viable of Streptococcus faecium. In: Proceedings of 18th International but nonculturable bacterial pathogens in anaerobic digested Congress of Refrigeration. Quebec, Montreal sludge. Appl Microbiol Biotechnol 97(13):6043–6050 Gomez M, Rua A, Garralon G, Plaza F, Hontoria E, Gomez MA (2006) Jin P, Jin X, Wang XC, Shi X (2013) An analysis of the chemical safety Urban wastewater disinfection by filtration technologies. Desali- of secondary effluent for reuse purposes and the requirement for nation 190(1–3):16–28 advanced treatment. Chemosphere 91(4):558–562 Gomez-Couso H, Fontan-Sainz M, Sichel C, Fernandez-Ibanez P, John MP (2005) The use of biosolids in Maine: A review. Biosolids Ares-Mazas E (2009) Efficacy of the solar water disinfection White Paper. Senator George J. Mitchell. Center for Environmen- method in turbid waters experimentally contaminated with tal and Watershed Research. University of Maine, Orono, Maine Cryptosporidium parvum oocysts under real field conditions. Jokinen CC, Schreier H, Mauro W, Taboada E, Isaac-Renton JL, Topp Trop Med Int Health 14(6):620–627 E, Edge T, Thomas JE, Gannon VPJ (2010) The occurrence and Gopakumar K, Ayyappan S, Jena JK (2000) Present status of integrated sources of Campylobacter spp., Salmonella enterica and Escheri- fish farming in India and wastewater treatment through aquacul- chia coli O157:H7 in the Salmon River, British Columbia, Can- ture proceedings of the national workshop on wastewater treat- ada. J Water Health 8(2):374–386 ment and integrated aquaculture, Edited, Kumar M.S. SARDI Joux F, LeBaron P (1997) Ecological implications of an improved Aquatic Sciences 17–19th pp. 22-37 direct viable count method for aquatic bacteria. Appl Environ Gordon DM, Bauer S, Johnson JR (2002) The genetic structure of E. Microbiol 63:3643–3647 coli populations in primary and secondary habitats. J Microbiol Jury KL, Vancov T, Stuetz RM, Khan SJ (2010) Antibiotic resistance 148(5):1513–1522 dissemination and sewage treatment plants. In: Current Research Gupta RA, Khan P, Saxena S, Mohapatra H (2000) Microbial biosor- Technology and Education Topics in Applied Microbiology and bents: meeting challenges of heavy metal pollution in aqueous Microbial Biotechnology. A Mendez–Vilas (Ed). pp 509–519 solutions. Review article. J Curr Sci 78(8):967–973 Kabrick RM, Jewell WJ (1982) Fate of pathogens in thermophilic aero- Haidar A (2005) Environmental impact to use wastewater in agricul- bic digestion. Water Res 16:1051–1060 tural irrigation (Ibb, Sana’a, Thammar), dar Al-Kutub Ministry Kaper JB, Nataro JP, Mobley HL (2004) Pathogenic E. coli. Nat Rev of Culture- Sana’a, 397: 1110 Microbiol 2:123–140 Han II, Congeevaram S, Ki D, Oh B, Park J (2011) Bacterial com- Katterman FRH, Day AD (1989) Plant growth factors in sewage sludge. munity analysis of swine manure treated with autothermal J BioCycle 30(3):64–65 thermophilic aerobic digestion. Appl Microbiol Biotechnol Keller R, Passamani F, Vaz L, Cassini ST, Goncalves RF (2003) Inac- 89(3):835–842 tivation of Salmonella spp. from secondary and tertiary effluents Hansen JJ, Warden PS, Margolin AB (2007) Inactivation of Adeno- by UV irradiation. Water Sci Technol 47(3):147–150 virus type 5, Rotavirus WA and male specific coliphage (MS ) Kim J, Hahn J, Franklin MJ, Stewart PS, Yoon J (2009) Tolerance in biosolids by lime stabilization. Int J Environ Res 4(1):61–67 of dormant and active cells in Pseudomonas aeruginosa PA01 Harrison EZ, McBride MB, Bouldin DR (1999) Land application of biofilm to antimicrobial agents. J Antimicrob Chem 63:129–135 sewage sludges: an appraisal of the US regulations. Int J Environ Kimberly LA, John EW, Valerie JH (2005) Persistence and differential Pollut 11(1):1–36 survival of faecal indicator bacteria in subtropical waters and Heng LY, Abdullah P, Yi CS, Mokhtar M, Ahmad R (2006) Develop- sediments. Appl Environ Microbiol 71(6):3041–3048 ment of possible indicators for sewage pollution for the assess- Klavarioti M, Mantzavinos D, Kassinos D (2009) Removal of residual ment of Langat river ecosystem health. Malaysia J Anal Sci pharmaceuticals from aqueous systems by advanced oxidation 10(1):15–26 processes. J Environ Int 35(2):402–417 Heritage J, Evans EG, Killington RA (2003) Microbiology in action. Koivunen J, Siitonen A, Heinonen-Tanski H (2003) Elimination of Cambridge University Press, New York, pp 10011–14211 enteric bacteria in biological–chemical wastewater treatment and Heyman D (2004) Control of communicable diseases manual, 18th edn. tertiary filtration units. Water Res 37(3):690–698 American Public Health Association, Washington Kollu K, Ormeci B (2012) Effect of particles and bio-flocculation on Himathongkham S, Riemann H (1999) Destruction of S. typhimurium, ultraviolet disinfection of E. coli. Water Res 46(3):750–760 E. coli O157:H7 and L. monocytogenes in chicken manure by Kowal NE (1983) An overview of public health effects. In: Page AL, drying and/or gassing with ammonia. FEMS Microbiol Lett Gleason TL, Smith JE, Iskander IK, Sommers LE (eds) Utiliza- 171(2):179–182 tion of municipal wastewater and sludge on land. University of Horman A, Rimhanen-Finne R, Maunula L, von Bonsdorff C, Torvela California, Riverside, pp 329–394 N, Heikinheimo A, Hanninen M (2004) Campylobacter spp., Laroche E, Pawlak B, Berthe T, Skurnik D, Petit F (2009) Occurrence Giardia spp., Cryptosporidium spp., Noroviruses, and indicator of antibiotic resistance and class 1, 2 and 3 integrons in E. coli 1 3 74 Page 22 of 25 Applied Water Science (2018) 8:74 isolated from a densely populated estuary (Seine, France). FEMS N’Dayegamiye A, Huard S, Thibault Y (2002) Paper mill sludge (bio- Microbiol Ecol 68(1):118–130 solids) applications in agriculture: agronomic and environmen- Leduc R, Gehr R (1990) Removal of coliform bacteria from aerated tal impacts. In: International Environmental Conference and stabilisation lagoons 1 Kinetics, modelling and biotic variable. Exhibit, TAPPI, Montreal, April 6–10, 2002, p 6 Water pollut Res J Can 25:231–263 Nasser AM, Paulman H, Sela O, Ktaitzer T, Cikurel H, Zuckerman I, Leeming R, Nichols PD, Ashbolt N (1998) Distinguishing sources Meir A, Aharoni A, Adin A (2006) UV disinfection of waste- of faecal pollution in Australia inland and coastal waters using water effluents for unrestricted irrigation. Water Sci Technol sterol biomarkers and microbial faecal indicators. UWRAA 54(3):83–88 Research Report 204, Water Services Association of Australia, Neis U, Blume (2002) Ultrasonic disinfection of wastewater effluents Melbourne, Australia for high-quality reuse. IWA Regional Symposium on Water Lepeuple AS, Gaval G, Jovic M, Recherche MR (2004) Literature Recycling in Mediterranean Region, Iraklio, Greece, 26.-29.09 review on levels of pathogens and their abatement in sludges, Nicholson FA, Hutchinson ML, Smith KA, Keevil CW, Chambers BJ, soil and treated biowaste. Horizontal WP3: Hygienic parameters Moore A (2000) A study on farms manure applications to agri- Lisle JT, Smith JJ, Edwards DD, Mcfeters GA (2004) Occurrence of cultural land and an assessment of the risks of pathogens transfer microbial indicators and Clostridium perfringens in wastewater, into the food chain. Report to MAFF, Project No. FS2526 water column samples, sediments, drinking water and weddell Niyogi SK (2005) Shigellosis. J Microbiol 43(2):133–143 seal feces collected at Memurdo station, Antarctica. Appl Envi- Nowak O (2007) Optimizing the use of sludge treatment facilities at ron Microbiol 70:7269–7276 municipal WWTPs. J Environ Sci Health 41(9):1807–1817 Liu C (2000) Pathogen inactivation in biosolids with lime and fly ash Oliver JD (2005) The viable but non-culturable state in bacteria. J addition. M. Sc. Thesis, Environmental Engineering University, Microbiol 43:93–100 Manitoba Onnis-Hayden A, Hsu BB, Klibanov AM, Gu AZ (2011) An antimi- Lucero-Ramirez B (2000) The effects of time and temperature on crobial polycationic sand filter for water disinfection. Water Sci the fate of pathogens and indicator bacteria during municipal Technol 63(9):1997–2003 wastewater sludge-mesophilic anaerobic digestion, air-drying Palmgren H (2002) Importance of wild birds in the spread of Salmo- and composting, Ph.D. Thesis, University of Texas, Austin, USA nella. Ph. D. Thesis. Umea University Luczkiewicz A, Jankowska K, Fudala-Ksiazek S, Olanczuk-Neyman K Paraskeva P, Graham NJD (2002) Ozonation of municipal WASTEWA- (2010) Antimicrobial resistance of faecal indicators in municipal TER EFflUENTS. Water Environ Res 74(6):569–580 wastewater treatment plant. Water Res 44(17):5089–5097 Pauwels B, Verstraete W (2006) The treatment of hospital wastewater: Luna GM, Manini E, Danovaro R (2002) Large fraction of dead and an appraisal. J Water Health 4(4):405–416 inactive bacteria in coastal marine sediments: comparison of Payment P, Franco E (1993) Clostridium perfringens and somatic protocols for determination and ecological significance. Appl coliphages as indicators of the efficacy of drinking water treat- Environ Microbiol 68(7):3509–3513 ment for viruses and protozoan cysts. Appl Environ Microbiol Markosyan LS, Vardanyan N, Paronyan AKH, Nikoghosyan VG, Dela- 59:2418–2424 lio A (2002) Microflora and chemical characteristics of wastewa- Payment P, Godfree A, Sartory D (2002) Clostridium. In: Bitton ter sludge. Biol J Armenia 54:31–41 G (ed) Encyclopedia of environmental microbiology. Wiley, Maynard HE, Ouki M, Williams SC (1999) Tertiary Lagoons: a review Hoboken, pp 861–871 of removal mechanisms and performance. Water Res 33(1):1–13 Pehlivanoglu-Mantas E, Elisabeth L, Hawley R, Deeb A, Sedlak DL Meierhofer R, Wegelin M (2002) Solar water disinfection –a guide (2006) Formation of nitrosodimethylamine (NDMA) during for the application of SODIS. Swiss Federal Institute of Envi- chlorine disinfection of wastewater effluents prior to use in ronmental Science and Technology (EAWAG/SANDEC), irrigation systems. Water Res 40(2):341–347 Switzerland Peng X, Luo W, Zhang J, Wang S, Lin S (2002) Rapid Detection Ministry of Agriculture and Irrigation (2012) A Promising sector for of Shigella Species in Environmental Sewage by an Immuno- Diversified Economy in Yemen: National Agriculture Sector capture PCR with Universal Primers. Appl Environ Microbiol Strategy 2012–2016, March 2012 68(5):2580–2583 Moce-Llivina L, Muniesa M, Pimenta-Vale H, Lucena F, Jofre J (2003) Placha I, Venglovsky J, Sasakova N, Svoboda IF (2001) The effect of Survival of bacterial indicator species and bacteriophages after summer and winter season on the survival of S. typhimurium thermal treatment of sludge and sewage. Appl Environ Microbiol and indicator microorganisms during the storage of solid frac- 69:1452–1456 tion of pig slurry. J Appl Microbiol 91:1–8 Mohamed RM, Al-Gheethi AA, Jackson AM, Amir HK (2016) Multi Plachy P, Placha I, Juris P (1996) Use of hydrated lime for disinfec- component filters for domestic greywater treatment in village tion of model pathogens S. typhimurium and Ascaris suum in houses. J Am Water Works Assoc (AWWA) 108(7):405–414 sewage sludge. In: Hygienic and ecological problems in rela- Mote BL, Turner JW, Lippa EK (2012) Persistence and growth of tion to veterinary medicine. Proceedings of International Con- the faecal indicator bacteria enterococci in detritus and natu- ference and Veterinary Medicine III. Kosice- Slovak Republic ral estuarine plankton communities. Appl Environ Microbiol Polo FMJ, Figueras I, Inza J, Sala JM, Fleisher JG (1998) Rela- 78(8):2569–2577 tionship between presence of Salmonella and indicators of Munir M, Wong K, Xagoraraki I (2010) Release of antibiotic resistant faecal pollution in aquatic habitats. FEMS Microbiol Lett bacteria and genes in the effluent and biosolids of five wastewater 160:253–256 utilities in Michigan. Water Res 45(2):681–693 Qing W, Yan L, Ming W, Xiao PP, Yong FT (2010) Fluorescence Munir M, Wong K, Xagoraraki I (2011) Release of antibiotic resistant in situ hybridization rapidly detects three different pathogenic bacteria and genes in the effluent and biosolids of five wastewater bacteria in urinary tract infection samples. J Microbiol Methods utilities in Michigan. Water Res 45(2):681–693 83:175–178 Myers DN, Stoeckel DM, Bushon RN, Francy DS, Brady AMG (2007) Rao DG, Senthilkumar R, Byrne A, Feroz S (2012) Wastewater treat- Faecal indicator bacteria. US Geological Survey Techniques of ment: Advanced processes and technologies. In: Thanikal V (ed) Water Resources Investigations. Book 9, chapter A7, section 7.1 Anaerobic fixed bed reactor for treatment of industrial wastewa- (version 2.0) ter Joseph. CRC Press, Boca Raton, pp 335–354 1 3 Applied Water Science (2018) 8:74 Page 23 of 25 74 Reimers RS (1997) Disinfection of pathogens by biosolids processing, (HACCP) to ensure the microbiological safety of sous vide US EPA Region VI. Biosolids stabilization and disinfection-what processed meat/pasta product. Food Microbiol 7(3):177–198 are our concerns. Water Environment Federation. Alexandria. Smith SR, Lang NL, Cheung KH, Spanoudaki K (2005) Factors VA (Dallas, TX). pp 1–4 controlling pathogen destruction during anaerobic digestion Reinosoa R, Alexandra L, Bécaresb TE (2008) Efficiency of natural of biowastes. Waste Manag 25(4):417–425 systems for removal of bacteria and pathogenic parasites from Spongberg AL, Witter JD (2008) Pharmaceutical compounds in the wastewater. J Sci Total Environ 395(2–3):80–86 wastewater process stream in Northwest Ohio. J Sci Environ Riley LW, Remis RS, Helgerson D, McGee HB, Wells JG, Davis BR, 397(1–3):148–157 Hebert RJ, Olcott ES, Johnson LM, Hargrett NT, Blake PA, Springthorpe S, Sattar SA (2004) The Biological issues related to use Cohen ML (1983) Hemorrhagic colitis associated with a rare of a pelletizer for the decontamination of biosolids in Toronto. Escherichia coli serotype. New Engl J Med 308(12):681–685 A report prepared for Jacques Whitford Environment Limited Rizzo L, Fiorentino A, Anselmo A (2013) Advanced treatment of urban July 2004 wastewater by UV radiation: effect on antibiotics and antibiotic- Straub TM, Pepper IL, Gerba CP (1993) Hazards from pathogenic resistant E. coli strains. Chemosphere 92(2):171–176 microorganisms in land-disposed sewage sludge. Rev Environ Ronner AB, Wong CL (1993) Biofilm development and sanitizer inac- Contam Toxicol 132:55–91 tivation of Listeria monocytogenes and Salmonella typhimurium Suresh DP, Kenneth WW, Scot ED, Steven CR (1996) Occurrence of on stainless steel and Bunan rubber. J Food Protect 56:750–758 airborne bacteria and pathogen indicators during land applica- Rose JB, Farrah SR, Harwood VJ, Levine AD, Lukasik J, Menendez P, tion of sewage sludge. Appl Environ Microbiol 1(62):296–299 Scott TM (2004) Reduction of pathogens, indicators bacteria and Svoboda IS, Carcluie C (2003) Anaerobic digestion, storage, oli- alternative indicators by wastewater treatment and reclamation golysis, lime, heat and aerobic treatment of livestock manures. processes. Water Environ Res Found, USA Provision of research and design of pilot schemes to minimize Rouch DA, Mondal T, Pai S, Glauche G, Fleming VA, Thurbon N, livestock pollution to the water environment in Scotland. QLC Blackbeard J, Smith SR, Deighton M (2011) Microbial safety of 9/2. FEC Services Ltd, Kenilworth, Warwickshire, pp 1–110 air-dried and rewetted biosolids. J Water Health 9(2):403–414 Synnott AJ, Kuang Y, Kurimoto M, Yamamichi K, Iwano H, Tanji Y Sahlstrom L, Aspan A, Bagge E, Danielsson-Tham ML, Albihn A (2009) Isolation from sewage influent and characterization of (2004) Bacterial pathogen incidences in sludge from Swedish novel S. aureus bacteriophages with wide host ranges and potent sewage treatment plants. Water Res 38:1989–1994 lytic capabilities. Appl Environ Microbiol 75(13):4483–4490 Sahlstrom L, De Jong B, Aspan A (2006) Salmonella isolated in sew- Telles CB, Tavares CRG, Filho BPD, Moitinho MLR (2002) Operation age sludge traced back to human cases of salmonellosis. Lett of a slow rate anaerobic digester treating municipal secondary Appl Microbiol 43:46–52 sludge. Electron J Biotechnol 5(3):216–227 Saleem A, Al-Malack MH, Bukhari AA (2001) Seasonal variation in Ting GM, Huang J, Hu H, Liu W (2011) Growth and repair potential the microbial population density present in biological sludge. of three species of bacteria in reclaimed wastewater after UV Environ Technol 22:55–259 disinfection. Biomed Environ Sci 24(4):400–407 Samhan AS, Al-Saed RM, Mahmoud NJ (2007) Removal of patho- Toth JD, Aceto HW, Rankin SC, DebRoy C, Dou Z (2012) Accelerat- genic microorganisms in pilot-scale uasb-septic tanks and ing the deactivation of Salmonella enterica serovar newport and Albireh urban wastewater treatment plant in Palestine. Water Escherichia coli O157:H7 in dairy manure by modifying pH or Int J 32(5):787–798 temperature. Open Waste Manag J 5:11–18 Santhiya G, Lakshumanan C, Selvin J, Asha D (2011) Microbio- Toze S (1997) Microbial pathogens in wastewater. Literature review for logical analysis of seawater and sediments in urban shorelines: urban water systems multi-divisional research program. Techni- occurrence of heavy metals resistance bacteria on Chennai cal report no 1/97 CSIRO, Australia beaches. Bay Bengal Microchem J 99(2):197–202 Tree JA, Adams MR, Lees DL (2003) Chlorination of Indicator bacte- Sasdkovd N, Vargov M, Ondraovidovd O, Ondraovic M, Kottferovd ria and viruses in primary sewage effluent. Appl Environ Micro- J, Venglovskf J, Culenova K, Hromada R, Papajovd I (2005) biol 69(4):2038–2043 The influence of the amendment of sewage sludge with zeolite Tripathi S, Pathak V, Tripathi DM, Tripathi BD (2011) Application of and lime from the microbiological point of view. Folia Vet ozone based treatments of secondary effluents. J Biores Technol 49(3):26–27 102(3):2481–2486 Schwartzbrod J, Gaspard P, Ambolet Y (1997) Urban sludge reused Tyagi VK, Chopra AK, Kazmi AA, Kumar A (2006) Alternative micro- for agricultural purposes: soils contamination and model devel- bial indicators of faecal pollution: current perspective. Iran J opment for the parasitological risk assessment. Bull Acad Med Environ Health Sci Eng 3(3):205–216 181:43–57 UN (2003) Economic and social commission for Western Asia waste- Scott TM, McLaughlin MR, Harwood VJ, Chivukula V, Levine A, water treatment technologies: a general review. United Nations, Gennaccaro A, Lukasik J, Farrah SR, Rosem JB (2003) Reduc- Distr. General E/ESCWA/SDPD tion of pathogens, indicator bacteria, and alternative indicators UN (2012) Status and new developments on the use of brackish water by wastewater treatment and reclamation processes. Water Sci for agricultural production in the Near East. Yemen Country Technol, Water Supply 3(4):247–252 Report. Prepared by: Eng. Abdulkarim Al-Sabri Edited by: Dr. Servais P, Passerat J (2009) Antimicrobial resistance of faecal bac- Mary K. Halim. United Nations, Cairo, Egypt, November 2012 teria in waters of the Seine river watershed (France). J Sci UNICEF (2013) Children dying daily because of unsafe water sup- Environ 408(2):365–372 plies and poor sanitation and hygiene. United Nations Children’s Sidhu JPS, Toze SG (2009) Human pathogens and their indicators Fund, USA in biosolids: a literature review. Environ Int 35(1):187–201 US EPA (1986a) Bacteriological ambient water quality criteria for Siti Khadijah E, Haque AM, Murshed MF (2013) Performance of marine and fresh recreational waters. EPA 440/5-84-002. US sewage oxidation pond in USM engineering campus. Caspian Environmental Protection Agency, Office of Research and Devel- J Appl Sci Res 2(12):219–225 opment, Cincinnati, OH Smith JP, Toupin C, Gagnon B, Voyer R, Fiset PP, Simpson MVA US EPA (1986b) Design manual municipal wastewater disinfection. (1990) Hazard analysis critical control point approach Environmental Protection Agency, EPA/625/1-86/021 1 3 74 Page 24 of 25 Applied Water Science (2018) 8:74 US EPA (1988) Occurrence of pathogens in distributed and marketing Vilanova X, Blanch AR (2005) Distribution and persistence of fae- municipal sludge project summary by Yanko, M. US Environ- cal bacterial populations in liquid and dewatered sludge from a mental Protection Agency. EPA/600/SI-87/014 biological treatment plant. J Gen Appl Microbiol 51(6):361–368 US EPA (1992) Environmental regulations technology control of path- Vital M, Stucki D, Egli T, Hammes F (2010) Evaluating the growth ogens and vector attraction in sewage sludge. EPA/625/R-92/01 potential of pathogenic bacteria in water. Appl Environ Microbiol US EPA (1993) The standards for the use of disposal of sewage sludge. 67(19):6477–6484 Final CFR Part 503 Rules. EPA 822/Z-93/001. USEPA, Office Wakelin S, Racz G, Oleszkiewicz J, Szoke N, Barsalou P (2003) Esti- of Water, Washington, DC mating the potential for disease in nearby residents as a result of US EPA (1995) Pathogen risk assessment methodology for munici- the city of Winnipeg biosolids land application program (Win pal sewage sludge land filling and surface disposal. US GRO). In: Presented at 2nd ed. Organic Residuals Recycling EPA/00/R-95-016. USA Conference, April 2003 US EPA (2000) Biosolids technology fact sheet alkaline stabilization Wang X, Hu X, Wang H, Hu C (2012) Synergistic effect of the sequen- of biosolids. Office of Water Washington, DC Environ. Prot. Age. tial use of UV irradiation and chlorine to disinfect reclaimed 832-F-00-052 water. Water Res 46(4):1225–1232 US EPA (2004a) Primer for municipal wastewater treatment systems. Wani D, Pandit AK, Kamili ZN (2013) Microbial assessment and effect US environmental protection agency municipal support, division of seasonal change on the removal efficiency of FAB based sew - office of wastewater management office of water Washington, age treatment plant. J Environ Eng Ecol Sci 2:1–3 DC, EPA 832-R-04-001 Ward RL, Yeager JG, Ashley CS (1981) Response of bacteria in waste- US EPA (2004b) Guidelines for Water Reuse, US Environmental Pro- water sludge to moisture loss by evaporation and effect of mois- tection agency municipal support, division office of wastewater ture content on bacterial inactivation by ionizing radiation. Appl management office of water Washington, DC, September 2004 Environ Microbiol 41(5):1123–1127 US EPA (2007) Pathogens, pathogen indicators and indicators of fecal WEF (1995) Wastewater residues stabilization. Manual of Practice contamination. Airlie Center, Warrenton, Virginiam US environ- FD-9. Water Environment Federation, USA mental protection agency, office of water, office of research and Wen Q, Tutuka C, Keegan A, Jin B (2009) Fate of pathogenic microor- development. EPA 823-R-07-006 ganisms and indicators in secondary activated sludge wastewater US EPA (2009) Terms of environment: glossary, abbreviations, and treatment plants. J Environ Manag 90(3):1442–1447 acronyms. Office of the Administrator/Office of External Affairs WHO (1989) Health guidelines for the use of wastewater in agricul- and Environmental Education ture and aquaculture. Technical Report Series 778, World Health US EPA (1989) Hazardous waste treatment, storage, and disposal facil- Organization, Geneva. Switzerland ities (TSDF), Air Emission Models, EPA-450/3-87-026. Environ- WHO (1993) Guidelines for drinking-water quality. Recommendations, mental Protection Agency, Research Triangle Park, Washington 2nd edn. WHO, Geneva. ISBN 9241544600 US EPA (1994) Standards for the use or disposal of sewage sludge. WHO (2001) Water quality. In: Fewtrell L, Bartram J (eds). Guidelines, Environmental protection agency; 40 CFR Part 503. Fed Regist standards and health: assessment of risk and risk management for 58:9248–9415 water-related infectious disease. IWA, London. (ISBN) US EPA (2003) Control of pathogens and vector attraction in sewage WHO (2002) Environmental health regional office for the Eastern Med- sludge; 40 CFR Part 503. Environmental Protection Agency, iterranean (EMRO). Regional Centre for Environmental Health Cincinnate, p 45268 Activities CEHA, Amman van Frankenhuyzen JK, Trevors JT, Lee H, Flemming CA, Habash MB Wilén BM, Johanssen A, Mattsson A (2012) Assessment of sludge (2011) Molecular pathogen detection in biosolids with a focus particle removal from wastewater by disc filtration. Chalmers on quantitative PCR using propidium monoazide for viable cell University of Technology and Gryaab, Göteborg, Water Practice enumeration. J Microbiol Methods 87(3):263–272 Technol. https ://doi.org/10.2166/wpt.2012.037 Veenstra G, Alaerts J, Bijlsma M (1997) Technology selection, chap- Wong K, Onan BM, Xagoraraki I (2010) Quantification of enteric ter 7. In: Helmer R, Hespanhol I (Eds.) Water pollution control— viruses, pathogen indicators, and salmonella bacteria in class b a guide to the use of water quality management principles. Pub- anaerobically digested biosolids by culture and molecular meth- lished on behalf of the United Nations Environment Programme, ods. Appl Environ Microbiol 76(196):441–6448 the Water Supply and Sanitation Collaborative Council and the Woteki CE, Kineman BD (2003) Challenges and approaches to reduc- World Health Organization by E. and F. Spon. 1997 WHO/ ing foodborne less. Ann Rev Nut 23:315–344 UNEP. ISBN, 0419229108 Xu P, Savoye P, Cockx A, Lazarova V (2002) Wastewater disinfec- Velickovic-Radovanovic R, Petrovic J, Kocic B (2009) Correlation tion by ozone: main parameters for process design. Water Res between antibiotic consumption and bacterial resistance as qual- 36(4):1043–1055 ity indicator of proper use of these drugs in inpatients. Vojnosanit Yachigo M, Sato S (2013) Leachability and vegetable absorption of Pregl 66(4):307–312 heavy metals from sewage sludge biochar (Chapter 15). In: Maria Viau E, Peccia J (2009) Survey of wastewater indicators and human C. Hernandez Soriano (Ed.) Soil processes and current trends pathogen genomes in biosolids produced by class a and class b in quality assessment. (ISBN 978-953-51-1029-3, CC BY 3.0 stabilization treatments. Appl Environ Microbiol 75(1):164–174 license) Vierheilig J, Frick C, Mayer RE, Kirschner AKT, Reischer GH, Derx Ye L, Zhang T (2011) Pathogenic bacteria in sewage treatment J, Mach RL, Sommer R, Farnleitner AH (2013) Clostridium plants as revealed by 454 pyrosequencing. Environ Sci Technol perfringens is not suitable for the indication of faecal pollution 45(17):7173–7179 from ruminant wildlife but is associated with excreta from non- Young KD, Thackston EL (1999) Housing density and bacterial load- herbivorous animals and human sewage. Appl Environ Microbiol ing in urban streams. J Environ Eng 125(12):1177–1180 79(16):5089–5092 Younis M, Soleiman HA, Abou-Elmagd K (2003) Microbiological and Vila J, Gascon J, Abdalla S, Gomez J, Marco F, Moreno A, Corachan chemical evaluation of bentonite as a new technique for sewage M, Jimenez T (1994) Antimicrobial resistance of Shigella iso- water treatment, Aswan city, Egypt. In: 7th International Water lates causing traveler’s diarrhea. Antimicrob Agents Chemother Technology Conference Egypt 1–3 April 2003: 323–343 38(11):2668–2670 Yurtsever D (2005) Use of treatment plant sludges as biosolids. M. Sc. Thesis, Dokuz Eylul University. IZMIR 1 3 Applied Water Science (2018) 8:74 Page 25 of 25 74 Zhou H, Smith DW (2002) Advanced technologies in water and waste- water treatment. J Environ Eng Sci 1:247–264 Ziemba C, Peccia J (2011) Net energy production associated with path- ogen inactivation during mesophilic and thermophilic anaerobic digestion of sewage sludge. Water Res 45(16):4758–4768 1 3
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