Since unsafe water is responsible for many illness, deaths, and economic failure, water quality monitoring is essential. A cross-sectional study was conducted on 218 drinking waters samples collected between February and June 2016 to assess water quality using phages by the help of CB390 E. coli host, plaque assay; multiple tube fermentation for coliforms and pour plate for heterotrophic bacteria at Ethiopian Public Health Institute. Heterotrophic plate count greater than 100 cfu/ml was noted in 41 samples and detections of total and thermotolerant coliforms and E. coli in 38, 24, and 10 samples, respectively, and no phages detection in chlorinated waters. While heterotrophic plate count greater than 100 cfu/ml was observed in 100 samples and detections of total and thermotolerant coliforms, E. coli, and phages in 75, 60, 42, and 5 samples, respectively, for untreated waters. The majority of the waters contained indicators above standard limits. This indicates that the sources are contaminated and they are potential threats for health. Hence, regular water monitoring should be a priority agenda. Keywords Indicators · Drinking water · Coliforms · Coliphage Introduction was previously not considered economically feasible (Salter 2012). Coliforms measure levels of fecal contamination in Lack of safe water results in untold suffering, diseases, infant water distribution systems. They are facultative anaerobic, mortality, stunted growth, and economic loss (Pathak 2015). rod-shaped, Gram-negative bacteria, lactose fermenters, and In developing countries, waterborne pathogens contribute produce acid and gas within 48 h at 35–37 °C (Rompre et al. 80% of health problems (Halvorson et al. 2010). 2002). Since coliforms respond to environment and water Since there is no universal indicator which has been iden- treatments, much less similar, and they have larger size com- tified (Skraber et al. 2004), testing of water using coliforms pared to viruses (Nkwe et al. 2015), they are not representa- and coliphages would give a more complete picture of water tive of viral contamination (Jurzik et al. 2010). Total coli- quality. Due to cost constraints and the complexity of ear- forms are mainly used for the assessment of sanitary water lier coliphages methods, requiring testing for both indicators quality after the water has been treated and disinfected. * Tesfaye Legesse Bedada Almaz Gonfa Biegna email@example.com firstname.lastname@example.org Walelign Dessie Mezemir Dejenie Shiferaw Teklu email@example.com firstname.lastname@example.org Firehiwot Abera Dera Kassu Desta Tullu email@example.com firstname.lastname@example.org Waktole Gobena Sima Public Health Microbiology Research Team, Ethiopian email@example.com Public Health Institute (EPHI), B. O. B: 1242, Addis Ababa, Samson Girma Gebre Ethiopia firstname.lastname@example.org Department of Medical Laboratory Science, CHS, School Redwan Muzeyin Edicho of Allied Health Science, Addis Ababa University, email@example.com Addis Ababa, Ethiopia Vol.:(0123456789) 1 3 70 Page 2 of 6 Applied Water Science (2018) 8:70 Thermotolerant coliforms are more closely related to fecal contamination. Five units of the same batch of produc- pollution. Escherichia coli is the most specific to fecal con- tion of carbonated and uncarbonated bottled waters of tamination (Odonkor and Ampofo 2013). eight brands produced in Ethiopia were collected to be Another fecal contamination monitoring tools in drink- analyzed as a single sample. Each bottle was thoroughly ing water are coliphages. Of two main groups of coliphages, mixed to have an even distribution of microbes, and then, male-specific coliphages are either DNA or RNA viruses equal volume of the sample from each bottle of water was that infect E. coli via pilli. Somatic coliphages are DNA taken and mixed together to have a composite sample of viruses that infect bacterial hosts by direct attachment to the desired volume. cell walls (Dryden et al. 2006). Single-agar layer CB390 The samples were stored at 4 °C. Microbiological inves- method reduces cost and workload to detect and quantify tigations were performed within 24 h after collection. All total coliphages in water (Price 2014). samples were tested for HPC, total and thermotolerant coli- A secondary indicator employed to evaluate water qual- forms, E. coli, male-specific, and somatic coliphages using ity is heterotrophic plate count (HPC). Heterotrophic bac- standard methods (Price 2014; HACH 2012; Cheesbrough teria are aerobic and facultative anaerobic organisms. The 2006); US Environmental Protection Agency 2001). large number of the bacteria may suggest the presence of opportunistic pathogens of non-fecal origin, which possibly indicate taste, odour, and corrosion problems in the water Hpc assay distribution system (Islam and Dey 2014). In Ethiopia, water quality is assessed using bacterial indicators. However, the One millilitre of each water sample was pipetted into the use of coliphage has not been assessed; hence, we set and sterile petri dish. After thoroughly mixing, the melted plate objective to determine the quality of drinking water using count agar was poured into the dish. The melted medium total coliphages, E. coli, thermotolerant and total coliforms, was mixed thoroughly with the sample and let them solidify. and heterotrophic bacteria in selected water samples in The plates were incubated for 48 h at 35 °C (HACH 2012). Ethiopia. Coliform assay Methods and materials The total coliform count test was based on the multiple tube A cross-sectional study was conducted on 218 drinking fermentation method to estimate the most probable number water samples at Public Health Microbiology Research (MPN) of total coliform, thermotolerant coliform and E. coli Team Laboratory in Ethiopian Public Health Institute in 100 ml of water. The test was carried out by incubating between February and June 2016. Water samples were col- at 37 °C for 48 h in measured quantities of sample water lected from 92 treated and 31 untreated piped, 69 untreated (50, 10, and 1 ml) into tubes of double and single-strength wells, 13 untreated rivers, and 13 bottled drinking water MacConkey broth (Difco). The tubes with acid and gas pro- samples from different locations of Addis Ababa, Oromia, duction were inoculated in brilliant green lactose bile broth Amhara, Afar and Southern Nations, Nationalities, and Peo- to observe gas production after 48 h of incubation at 37 °C. ples’ Region (SNNPR) regional states of Ethiopia by trained Then, E. coli and nutrient broths were inoculated and incu- professionals. bated at 44.5 °C for 48 h for gas production and indole test, The study areas for pipes, wells, and rivers are located in respectively. The coliforms were estimated per 100 ml of central, northern, and southern Ethiopia that extend between water using MPN tables (Cheesbrough 2006). latitude and longitude 8°00N and 38°00E, and present a diverse topography, ranging from 110 m below sea level to 4550 m above sea level. Coliphages assay The samples were collected into sterilized 500 ml bot- tles and transported on ice to the laboratory. The Samples For the simultaneous detection of both types of male-specific containing residual chlorine were neutralized by adding pre- and somatic Coliphages, single-agar layer plaque assay using sterilized 0.5 ml sodium thiosulphate per 500 ml of water coliphage host CB390 (obtained from University of North sample. Carolina, Chapel Hill) log phase containing 0.15% ampicil- Carbon dioxide and filtration were the major treatment lin was applied with magnesium chloride in double-strength methods employed to inactivate or remove microbes in the tryptic soy agar [Difco]. The coliphages were incubated for carbonated bottled water industry and ultraviolet, ozone, 16–24 h at 37 °C and the plaques were enumerated. The and filtration for the non-carbonated water. Sampling coliphage counted was computed per 100 ml of the sample site selection criteria were based on possible sources of (Price 2014; US Environmental Protection Agency 2001). 1 3 Applied Water Science (2018) 8:70 Page 3 of 6 70 (> 3.0 × 10 cfu/ml) were found in 22.5% (n = 49) of all Data analysis procedures samples for HPC; > 180 MPN/100 ml in 17% (n = 37) of the samples for total coliform and 11.5% (n = 25) of the The data were entered, cleaned, and analyzed using SPSS 20 for Windows (SPSS Inc. Version 20, Chicago, Illinois). The samples for thermotolerant coliforms. Of the total water samples for chlorinated water sam- Kruskall–Wallis test was used to find out the differences in indicators values by regions, water sources, and treatment ples, HPC > 100 Cfu/ml were observed in 41 (18.8%) samples; detections of total and thermotolerant coliforms types; and to observe the associations among the various indicators; the Spearman Rank Correlation was used to test and E. coli in 38 (17.4%), 24 (11.0%), and 10 (4.6%) sam- ples, respectively, and no detection of coliphages. While, the association between the variables. To check the normal- ity of data, Shapiro–Wilk test was used. The significance for untreated waters, HPC > 100 cfu/ml were observed in 100 (45.9%) samples; detections of total and thermotol- level was set at p value < 0.05. The results were compared with established Ethiopian standards and WHO guidelines erant coliforms, E. coli, and coliphages in 75 (34.4%), 60 (27.5%), 42 (19.3%), and 5 (2.3%) samples, respec- of drinking water. tively. In all coliphage-detected samples, all indicators, heterotrophic bacteria, and coliforms were also detected, Results inversely in the absence of thermotolerant coliforms, there were no coliphages detections. The detections of hetero- Microbial quality of water samples trophic bacteria, total coliforms, and thermotolerant coli- forms by treatment status of water samples were shown in Of the total 218 samples tested from various waters, het- Tables 1, 2, and 3. Rho values of HPC, and total and thermotolerant coli- erotrophic bacteria, total and thermotolerant coliforms, E. coli, and total coliphages were detected in 72.9% (n = 159), forms to coliphages were 0.202, 0.232, and 0.269; total and thermotolerant coliforms to HPC were 0.754 and 51.8% (n = 113), 38.5% (n = 84), 23.9% (n = 52), and 2.3% (n = 5) of the samples, respectively. HPC > 100 cfu/ 0.677, respectively, and total coliforms to thermotolerant was 0.816. p values for HPC, and total and thermotolerant ml were observed in 141 (64.7%) samples. High counts Table 1 Total heterotrophic Type of water Heterotrophic plate count (cfu/ml) bacteria counts in treated and untreated drinking water < 1 1–100 101–200 201–300 > 300 Total % samples using pouring method Chlorinated 41 10 26 6 9 92 42.2 in different regions of Ethiopia between February and June Unchlorinated 8 5 50 10 40 113 51.8 Bottled water 10 3 0 0 0 13 6 Total 59 18 76 16 49 218 100 % 27.1 8.3 34.9 7.3 22.5 100 100 Table 2 Estimation of total Type of water Total coliforms count (MPN/100 ml) coliforms in treated and untreated drinking water < 1 1–10 11–100 101–180 > 180 Total samples using MPN method Chlorinated 4 16 14 3 5 92 in different regions of Ethiopia between February and June Unchlorinated 8 18 23 2 32 113 Bottled water 13 0 0 0 0 13 Total 25 34 37 5 37 218 Table 3 Estimation of Type of water Thermotolerant coliforms (MPN/100 ml) thermotolerant coliform in treated and untreated drinking < 1 1–10 11–100 101–180 > 180 Total water samples using MPN Chlorinated 68 21 2 1 0 92 method in different regions of Ethiopia between February and Unchlorinated 53 23 11 1 25 113 June 2016 Bottled water 13 0 0 0 0 13 Total 134 44 13 2 25 218 1 3 70 Page 4 of 6 Applied Water Science (2018) 8:70 coliforms and coliphages using Kruskall–Wallis test for samples (64.7%) contained HPC above permissible limit the samples by region, source, and treatment type were of > 100 cfu/ml (WHO 2003) and total coliforms (51.8%), < 0.05. thermotolerant coliforms (38.5%), (23.9%), and coliphages (2.3%) above WHO guideline value of < 1/100 ml (WHO Bacteriological and virological indicator detection 2011) of the total water samples. The presence of these indi- in treated water sources cators may not cause illness, but used as one of the indicators of pathogens that can cause intestinal infections, hepatitis, Of chlorinated drinking waters, 41(44.6%) samples had typhoid fever, and other illnesses (Emmanuel et al. 2009). HPC > 100 cfu/ml and 38 (41.3%), 24 (26.1%), and 10 The findings observed in the present study about the inci- (10.9%) samples were positive for total and thermotoler- dences above the permissible limits of HPC and total coli- ant coliforms and E. coli, respectively, and no detection of forms in the total samples were lower than in some studies coliphages. All eight brands of 13 bottled drinking water done on drinking water samples in Peshawar, Pakistan (80 samples in Addis Ababa (N = 4) and Oromia (N = 9) had and 70%) (Ali et al. 2013) but higher than in one study in HPC < 100 cfu/ml; total and thermotolerant coliforms and E. Pakistan (45 and 25%) (Shar et al. 2010). coli of < 1 MPN/100 ml and coliphages of < 1 pfu/100 ml. The presence of total coliforms in the chlorinated drink- ing water samples indicates a serious treatment failure; Bacteriological and virological indicator distribution system may be vulnerable to contamination in untreated waters (Ainsworth 2004; Health Canada 2010). Out of water sam- ples positive for thermotolerant coliforms in the present Of untreated drinking waters, 100 (88.5%) samples had study, 28.6% were treated drinking waters which indicate HPC > 100 cfu/ml and 75 (66.4%), 60 (53.1%), 42 (37.2%), inadequate treatment and disinfection (Osman et al. 2011). and 5 (4.4%) samples were positive for total and thermo- The presence of E. coli in samples was more serious than tolerant coliforms, E. coli, and coliphages, respectively. other coliforms alone and possible presence of pathogens Untreated waters had HPC ranging from 100% for river to (Odonkor and Ampofo 2013). 80.6% for untreated piped water, total coliforms ranging The non-comply of 38.5% drinking water samples for from 92.3% for rivers to 60.9% for wells, thermotolerant thermotolerant coliforms is higher than the national survey, coliforms ranging from 92.3% for rivers to 45.1% for piped rapid assessment of drinking water quality in Ethiopia that waters, E. coli ranging from 84.6% for rivers to 29% for tested drinking water quality for thermotolerant coliforms wells, and coliphages ranging from 38.5% for rivers to no and found 28% of 1602 samples non-potable (Tadesse et al. detection for piped and well waters. 2010). Of unchlorinated piped waters, 25 (80.6%) samples had The finding observed in the present study about the pres- HPC > 100 cfu/ml; 21 (67.7%), 14 (45.1%), and 11 (35.5%) ence of thermotolerant coliforms or E. coli above the recom- samples were positive for total and thermotolerant coliforms mended limits was comparable to similar study conducted and E. coli, respectively and no detection of coliphages in in Bangladesh in various waters (Parvez et al. 2016) and the samples. lower than the study in India (100% and 78.1% (Borah et al. Of unchlorinated wells, 62 (89.9%) samples had 2010). Though, in one study, the detections of these bacte- HPC > 100 cfu/ml; 42 (60.9%) samples, 34 (49.3%) samples, rial indicators were higher than that from Lithuania (16.7%) and 20 (29%) samples were positive for total and thermotol- (Malakauskas et al. 2007). erant coliforms and E. coli, respectively and no detection of The detections above permissible limits for HPC, total coliphages in the samples. and thermotolerant coliforms, E. coli, and coliphages in Of the rivers, all samples had HPC > 100 cfu/ml and 12 untreated water samples were 2.7 times, 2.0 times, 2.5 times, (92.3%), 12 (92.3%), 11 (84.6%), and 5 (38.5%) samples 4.2 times, and 4.4 times more than the detections for chlo- were positive for total and thermotolerant coliforms, E. coli, rinated water samples, respectively. The non-detection of and coliphages respectively. The enumeration of coliphages coliphages in any treated water samples is consistent with analyzed in water samples from rivers were ranged between the study done in the United States on ground water (Plum- 1 2 2.2 × 10 and 5.3 × 10 pfu/100. mer et al. 2014). Spearman correlation test indicated statistically sig- nificant positive correlations between coliphages and all Discussion other bacterial indicators and agreed with a study done in the United States on drinking water samples (Wu et al. In the present investigation, virological and bacterio- 2011). HPC, and total and thermotolerant coliforms were logical quality of drinking water was assessed from vari- strongly related to each other, though the non-parametric ous sources in Ethiopia. As expected, the majority of the Kruskall–Wallis test showed that HPC, coliforms and total 1 3 Applied Water Science (2018) 8:70 Page 5 of 6 70 coliphages differed statistically by region, water source, and higher than that from Turkey (25% total coliform, 17.5% treatment type (p value < 0.05). thermotolerant coliforms and 15% E. coli (Aydin 2007). In the present study, the non-compliance of samples col- Thermotolerant coliforms in protected dug wells (49.3%) lected from chlorinated piped water for thermotolerant coli- were higher than untreated and treated piped waters and forms was high (26.1%) compared to 22.4% in survey of the comparable with the previous study in Ethiopia (Tadesse same country. This might be due to the increment of sanitary et al. 2010). Non-compliance of thermotolerant coliforms risk factors such as lack of maintenance, leaks in piped water in Addis Ababa protected dug wells (33.3%) and Oromia distribution system; poor site selection and failure to mini- protected dug wells (54.9%) was higher than the previous mize sanitary risks (Tadesse et al. 2010). study in Ethiopia (25%) for both regions (Tadesse et al. All the 13 samples from the eight brands of bottled water 2010). This level of contamination may be due to a source contained < 100 cfu/ml for HPC and no detectable organism of contamination which is nearby; otherwise, groundwater per 100 ml for coliforms and coliphages. This good quality sources are usually bacteriologically safe (Nkwe et al. 2015). may be due to the current follow-up and enforcement of the The non-compliance of HPC, total and thermotolerant bottled water companies to adhere to good manufacturing coliforms, E. coli, and total coliphages in 100, 92.3, 92.3, practice by the regulatory body. This is in consistent with 84.6, and 38.5%, respectively, in rivers indicates that they the study done in Ghana (Addo et al. 2009) which found are the most contaminated sources and unfit for consump- coliforms none detectable in any of the examined brands of tion. This poor quality of the source was consistent with the bottled drinking waters. study done in Kathmandu Valley, Nepal (Haramoto et al. Some investigations done in different countries have 2011). Rivers samples in SNNPR were more contaminated contained indicators in bottled drinking water. In Ethiopia, with the indicators than river samples in Oromia in the pre- 325 bottled water samples of 11 domestic and two imported sent study. The presences of coliphages in the rivers indicate brands contained HPC above the permissible limits in 16.9% the presence of enteric viruses (Plummer et al. 2014). of the samples (Tafere et al. 2014). In India, Jaipur city, 40 samples of various brands of bottled drinking water were tested for HPC, total coliforms and E. coli reported 50, 45, Conclusion and 20%, respectively (Gangil et al. 2013). In study done in Dar es Salaam, on 13 brands of 130 bottled drinking water, This study assessed bacterial and viral quality of drinking 92% was reported HPC, 4.6% total coliforms, and 3.6% ther- water sources in some regions of Ethiopia. Majority of the motolerant coliforms (Kassenga 2007). waters, mainly untreated sources contained bacterial indica- As expected, HPC non-compliance for treated piped tors and rivers contained viral indicators above the standards water was lower than untreated water sources. Non-com- permissible limits. This indicated that drinking waters are pliance of thermotolerant coliforms for treated piped water contaminated with environmental and fecal contaminants in Addis Ababa was lower than non-compliance in Oromia which are potential threats for human health, and probably, piped water but consistent with the previous national survey some of the waters sources may be unsafe for human con- of RADWQ (Tadesse et al. 2010). sumption. This shows the high risk of infection for consum- Large non-comply of untreated water sources for HPC ers and calls for immediate action. We recommend regular (88.5%), total coliforms (66.4%), thermotolerant coliforms microbiological assessment and strengthening the water (53.1%), E. coli (37.2%), and total coliphages (4.4%) signi- treatment system will reduce the risk of communicable fied the suggestion of WHO which states that surface water diseases. or shallow ground water should not be used as a source of drinking water without sanitary protection or treatment Open Access This article is distributed under the terms of the Crea- tive Commons Attribution 4.0 International License (http://creat iveco (WHO 2011). mmons.or g/licenses/b y/4.0/), which permits unrestricted use, distribu- The contamination of HPC and coliforms in untreated tion, and reproduction in any medium, provided you give appropriate piped water was higher than that of treated piped water. 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