The Open Microbiology Journal




ISSN: 1874-2858 ― Volume 14, 2020
RESEARCH ARTICLE

Degradation of Bacterial Water Quality in Drinking Water after Bottling



Ali Shahryari1, Charlotte D. Smith2, Abolfazl Amini3, *
1 Environmental Health Research Center, School of Health, Golestan University of Medical Sciences, Gorgan, Iran.
2 Division of Environmental Health Sciences, School of Public Health, University of California, Berkeley, CA94720, United States.
3 Laboratory Sciences Research Center, Golestan University of Medical Sciences, Gorgan, Iran.

Abstract

Background:

The consumption of bottled water globally, including Iran, has increased tremendously in recent years. This study was designed to assess the bacteriological quality of bottled water and its compliance with the drinking water regulations. In addition, we evaluated bottled waters for the presence of a variety of genera of bacteria and the effect of storage duration on the extent of bacterial contamination.

Methods:

Four hundred samples of bottled water belonging to ten different Iranian brands with various production dates were purchased from supermarkets in Gorgan, Iran, from 2017 to 2018. Bacterial quality of bottled water was assessed using heterotrophic plate count (HPC) followed by usual biochemical tests for identification of bacterial genera, and by the API system.

Results:

The average HPC of bottled water was 9974 colony-forming units per milliliter (CFU/ml). Twelve genera were isolated, among which Bacillus spp. and Escherichia coli were the most and least abundant, respectively. Statistical analysis showed that there was a positive association between water quality and storage duration so that the highest microbial load occurred within the first to third months after bottling. Furthermore, the highest rate of contamination was observed in May when ambient air temperatures commonly reached 40 °C.

Conclusion:

The bacterial quality of bottled water was not according to the standard of drinking water quality. This study demonstrated the variation in bacterial levels after bottling, which indicates the presence of waterborne heterotrophic bacteria, some of which can pose severe health risks to consumers.

Keywords: Bacteria, Drinking water, Heterotrophic plate count, Water Quality, Bottled Water, Escherichia coli.


Article Information


Identifiers and Pagination:

Year: 2020
Volume: 14
First Page: 78
Last Page: 83
Publisher Id: TOMICROJ-14-78
DOI: 10.2174/1874285802014010078

Article History:

Received Date: 20/01/2020
Revision Received Date: 30/03/2020
Acceptance Date: 02/04/2020
Electronic publication date: 16/05/2020
Collection year: 2020

© 2020 Shahryari et al.

open-access license: This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International Public License (CC-BY 4.0), a copy of which is available at: (https://creativecommons.org/licenses/by/4.0/legalcode). This license permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.


* Address correspondence to this author at the Laboratory Sciences Research Center, Golestan University of Medical Sciences, Gorgan, Iran, Tel: +98 1732454340, E-mail: amini_ab@msn.com





1. INTRODUCTION

The production and consumption of bottled drinking water are increasing all around the world with public concern rising regarding the safety and quality of the water, particularly with respect to the possibility of water-borne diseases [1Zamberlan dSM, Santana RG, Guilhermetti M. Comparison of the bacteriological quality of tap water and bottled mineral water. Int J Hyg Environ Health 2008; 211(5-6): 504-9.]. Similar to other countries, there is an increasing demand for consumption of bottled water among Iranian people [2Mohammadi Kouchesfahani M, Alimohammadi M, Nabizadeh Nodehi R, Aslani H, Rezaie S, Asadian S. Pseudomonas aeruginosa and Heterotrophic Bacteria Count in Bottled Waters in Iran. Iran J Public Health 2015; 44(11): 1514-9.
[PMID: 26744709]
]. The most important factors affecting the consumption of bottled water are organoleptic chemicals such as nitrate and nitrite, hardness, taste, odor and risk of water-borne diseases [3Moazeni M, Atefi M, Ebrahimi A, Razmjoo P, Vahid Dastjerdi M. Evaluation of chemical and microbiological quality in 21 brands of Iranian bottled drinking waters in 2012: a comparison study on label and real contents. J Environ Public Health 2013; 2013469590
[http://dx.doi.org/10.1155/2013/469590] [PMID: 23690802]
, 4Bedada TL, Dera FA, Edicho RM, et al. Mycological and bacteriological quality and safety of bottled water in Ethiopia. Open Microbiol J 2018; 12: 200-8.
[http://dx.doi.org/10.2174/1874285801812010200] [PMID: 30069259]
]. Bottled water is drinking water packaged in glass or plastic bottles, most often after advanced treatment processes including microfiltration, reverse osmosis, ultraviolet radiation and/or ozonation [5Doria MF. Bottled water versus tap water: understanding consumers’ preferences. J Water Health 2006; 4(2): 271-6.
[http://dx.doi.org/10.2166/wh.2006.0023] [PMID: 16813019]
-7Diduch M, Polkowska Ż, Namieśnik J. The role of heterotrophic plate count bacteria in bottled water quality assessment. Food Control 2016; 61: 188-95.
[http://dx.doi.org/10.1016/j.foodcont.2015.09.024]
]. For this reason, many individuals, especially elderly persons, pregnant women, children and immune-compromised individuals, prefer to drink bottled water for assured microbiological quality and safety of the water [8Venieri D, Vantarakis A, Komninou G, Papapetropoulou M. Microbiological evaluation of bottled non-carbonated (“still”) water from domestic brands in Greece. Int J Food Microbiol 2006; 107(1): 68-72.
[http://dx.doi.org/10.1016/j.ijfoodmicro.2005.08.013] [PMID: 16271413]
, 9Falcone-Dias MF, Vaz-Moreira I, Manaia CM. Bottled mineral water as a potential source of antibiotic resistant bacteria. Water Res 2012; 46(11): 3612-22.
[http://dx.doi.org/10.1016/j.watres.2012.04.007] [PMID: 22534119]
]. Contrary to expectations, some studies have detected waterborne bacteria such as Escherichia coli (E. coli), Pseudomonas aeruginosa, Staphylococcus spp., Micrococcus spp. and Corynebacterium spp. in bottled water [1Zamberlan dSM, Santana RG, Guilhermetti M. Comparison of the bacteriological quality of tap water and bottled mineral water. Int J Hyg Environ Health 2008; 211(5-6): 504-9., 10Rosenberg FA. The microbiology of bottled water. Clin Microbiol Newsl 2003; 25(6): 41-4.
[http://dx.doi.org/10.1016/S0196-4399(03)80019-3]
].

The fecal indicator bacterium E. coli has been adopted by the World Health Organization (WHO) and many countries as the standard for assessing the microbial safety of drinking water [11Ashbolt NJ, Grabow WO, Snozzi M. Indicators of Microbial Water Quality: Guidelines, Standards, and Health 2001., 12Blokker M, Smeets P, Medema G. Quantitative microbial risk assessment of repairs of the drinking water distribution system. Microb Risk Anal 2018; 8: 22-31.
[http://dx.doi.org/10.1016/j.mran.2017.12.002]
]. The number of heterotrophic bacteria as measured by the Heterotrophic Plate Count (HPC) is also used as a criterion of microbiological water quality assessment [6Diduch M, Polkowska Ż, Namieśnik J. Factors affecting the quality of bottled water. J Expo Sci Environ Epidemiol 2013; 23(2): 111-9.
[http://dx.doi.org/10.1038/jes.2012.101] [PMID: 23093103]
]. For example, in the United States of America, when a distribution system sample does not have detectable chlorine residual, the HPC concentration less than 500 CFU/mL (using plate count agar) can be a surrogate for a detectable disinfectant residual [13Hilborn ED, Covert TC, Yakrus MA, et al. Persistence of nontuberculous mycobacteria in a drinking water system after addition of filtration treatment. Appl Environ Microbiol 2006; 72(9): 5864-9.
[http://dx.doi.org/10.1128/AEM.00759-06] [PMID: 16957205]
]. Heterotrophic Plate Count is also used as a process management indicator in municipal systems in particular, when chloramine is used as the distribution system disinfectant [14American Water Works Association. Manual of Water Supply Practices (M56): Nitrification Prevention and Control in Drinking Water 2nd ed. 2013.], and for bottled water production [15Allen MJ, Edberg SC, Reasoner DJ. Heterotrophic plate count bacteria--what is their significance in drinking water? Int J Food Microbiol 2004; 92(3): 265-74.
[http://dx.doi.org/10.1016/j.ijfoodmicro.2003.08.017] [PMID: 15145585]
]. Heterotrophic bacteria are a group of non-pathogenic and pathogenic microorganisms including, Escherichia coli, Bacillus spp, Corynebacterium spp, Streptococcus spp, Enterobacter spp, Streptomyces spp, and opportunistic bacterial pathogens (i.e., Klebsiella spp, Legionella spp, Moraxella spp, Pseudomonas spp.) [6Diduch M, Polkowska Ż, Namieśnik J. Factors affecting the quality of bottled water. J Expo Sci Environ Epidemiol 2013; 23(2): 111-9.
[http://dx.doi.org/10.1038/jes.2012.101] [PMID: 23093103]
]. Previous clinical and epidemiological studies have not documented that the consumption of water with high HPC poses a significant health risk to consumers [6Diduch M, Polkowska Ż, Namieśnik J. Factors affecting the quality of bottled water. J Expo Sci Environ Epidemiol 2013; 23(2): 111-9.
[http://dx.doi.org/10.1038/jes.2012.101] [PMID: 23093103]
, 16Bartram J, Cotruvo J, Exner M, Fricker C, Glasmacher A. Heterotrophic Plate Counts and Drinking-Water Safety: The Significance of HPCs for Water Quality and Human Health 2003., 17Shahryari A, Nikaeen M, Hatamzadeh M, Vahid Dastjerdi M, Hassanzadeh A. Evaluation of bacteriological and chemical quality of dialysis water and fluid in isfahan, Central Iran. Iran J Public Health 2016; 45(5): 650-6.
[PMID: 27398338]
]. Nevertheless, in a survey conducted by Pavlov et al., a possible link was observed between HPC bacteria and the incidence of gastroenteritis due to opportunistic bacterial pathogens [18Pavlov D, de Wet CM, Grabow WO, Ehlers MM. Potentially pathogenic features of heterotrophic plate count bacteria isolated from treated and untreated drinking water. Int J Food Microbiol 2004; 92(3): 275-87.
[http://dx.doi.org/10.1016/j.ijfoodmicro.2003.08.018] [PMID: 15145586]
].

Contamination of drinking water is one of the most important public health concerns and it is necessary to know the microbial quality of bottled water. The HPC method is a reliable and cost-effective procedure for assessing the bacterial quality of drinking water, particularly for water with high quality such as bottled water [16Bartram J, Cotruvo J, Exner M, Fricker C, Glasmacher A. Heterotrophic Plate Counts and Drinking-Water Safety: The Significance of HPCs for Water Quality and Human Health 2003., 17Shahryari A, Nikaeen M, Hatamzadeh M, Vahid Dastjerdi M, Hassanzadeh A. Evaluation of bacteriological and chemical quality of dialysis water and fluid in isfahan, Central Iran. Iran J Public Health 2016; 45(5): 650-6.
[PMID: 27398338]
, 19Sartory DP. Heterotrophic plate count monitoring of treated drinking water in the UK: a useful operational tool. Int J Food Microbiol 2004; 92(3): 297-306.
[http://dx.doi.org/10.1016/j.ijfoodmicro.2003.08.006] [PMID: 15145588]
]. This study was design to assess the bacteriological quality of bottled water and its compliance with the drinking water regulations. In addition, we evaluated bottled waters for the presence of a variety of genera of bacteria and the effect of storage duration on the extent of bacterial contamination.

2. MATERIALS AND METHODS

2.1. Bottled Water Samples

Four hundred samples of bottled water (500ml and 1.5Lit) produced by ten different Iranian brands were collected from numerous supermarkets in Gorgan, Iran, during the period May 2017 to April 2018. The number of samples was determined based on the sample size formula for descriptive studies (n=(z_(1-∝/2)^2)/d^2 ), and a comparative study in Isfahan [3Moazeni M, Atefi M, Ebrahimi A, Razmjoo P, Vahid Dastjerdi M. Evaluation of chemical and microbiological quality in 21 brands of Iranian bottled drinking waters in 2012: a comparison study on label and real contents. J Environ Public Health 2013; 2013469590
[http://dx.doi.org/10.1155/2013/469590] [PMID: 23690802]
]. In our study, samples were randomly taken from the refrigerator from which they were ordinarily purchased by consumers. All the samples were transferred to the microbiology laboratory in the school of public health of Golestan university of medical sciences in an insulated cooler (T≤ 5 °C) within 2 hours after collection and were analyzed upon arrival at the laboratory. This laboratory was highly efficient due to a number of factors, including modern equipment and suitable testing facilities. The HPC values were categorized into seven subgroups depending on the time difference between bottling at the factory and the testing date (≤30, 31-60, 61-90, 91-120, 121-150, 151-180, and >180 days).

2.2. HPC Bacteria Analysis

For heterotrophic bacteria, the samples were vortexed for 15 seconds and ten-fold serial dilutions were prepared for each sample, using sterile 0.85% saline. The spread plate method using R2A agar (Merck, Germany) was used for enumeration of HPC bacteria as described in Standard Methods, except that the plates were incubated at 28 °C for at least 72 h and up to 7 days [20Rice E, Baird R, Eaton A. Standard Methods for the Examination of Water and Wastewater 23rd ed. 2017.]. All the experiments were carried out in duplicate and the mean values were recorded as total heterotrophic bacteria (CFU/ml) for each sample.

2.3. Identification of Heterotrophic Bacteria

The isolated bacteria from R2A plates were identified using several biochemical tests, including gram-staining, oxidase production and catalase tests, glucose and lactose fermentation, hydrogen sulfide production, indole production, methyl red, Voges-Proskauer, citrate utilization, motility, urea hydrolysis, ONPG hydrolysis, ornithine and lysine decarboxylase, arginine dihydrolase, gelatin hydrolysis, Schaeffer-Fulton staining, all according to standard methods [20Rice E, Baird R, Eaton A. Standard Methods for the Examination of Water and Wastewater 23rd ed. 2017.]. In addition, to confirm the bacteria, the API 20E/NE, Staph, Coryne and CHB Medium tests were performed in a manner conforming to the manufacturer’s protocol (BioMérieux, 69280, Marcy I’Etoile, France).

2.4. Statistical Analysis

The data was analyzed using IBM SPSS Statistics v16. Descriptive statistical parameters (mean and standard deviation) were used to describe the heterotrophic bacteria population in different bottled water brands. The Chi-square test was used to determine the variation in the bacterial population after bottling. A p-value of <0.05 was considered significant.

3. RESULTS

The mean HPC level of bottled water was 9974 CFU/ml and ranged from less than one up to 2×105 CFU/ml. The highest and lowest amount of bacterial contamination was observed in brands 8 and 7, respectively (Table 1). The statistical analysis revealed a significant difference between some brands and the amount of bacterial contamination (p<0.001).

In Table 2, the results of HPC are presented based on the storage duration. Our study revealed that the highest percentage of samples with HPC higher than 500 CFU/ml was found within the first to ninety days after bottling. The statistical analysis also showed a difference between the HPC value and the duration of storage (p<0.001).

Ten genera of HPC bacteria were identified from the HPC plates. Bacillus spp. were the predominant genera followed by Acinetobacter spp., Pseudomonas spp., Micrococcus spp., Enterobacter spp., Flavobacterium spp., Corynebacterium spp., Stenotrophomonas spp., Staphylococcus spp., and Escherichia coli. A statistically significant difference was not observed between the presence of the bacterial genera and bottle brands (p=0.428) (Table 3); whereas, a positive association was found between the HPC level of >1000 CFU/ml and the presence of bacteria listed above (p<0.001) (Table 4). We observed a positive association between storage duration and HPC (p<0.001).

4. DISCUSSION

This study assessed the quality of different brands of Iranian bottled water with respect to microbiological quality. We found that more than 84% and 98% of the samples had a HPC of over 500 and 100 CFU/ml, respectively. These values were much higher than the recommended microbiological value for bottled water (HPC<500 CFU/ml) in the USA [9Falcone-Dias MF, Vaz-Moreira I, Manaia CM. Bottled mineral water as a potential source of antibiotic resistant bacteria. Water Res 2012; 46(11): 3612-22.
[http://dx.doi.org/10.1016/j.watres.2012.04.007] [PMID: 22534119]
] and some European countries (HPC<100 CFU/ml) [21Stine SW, Pepper IL, Gerba CP. Contribution of drinking water to the weekly intake of heterotrophic bacteria from diet in the United States. Water Res 2005; 39(1): 257-63.
[http://dx.doi.org/10.1016/j.watres.2004.09.010] [PMID: 15607184]
]. However, it should be noted that higher values for HPC will occur on minimal nutrient media such as R2A as opposed to standard plate count agar [22Bugno A, Almodóvar AAB, Pereira TC. Enumeration of heterotrophic bacteria in water for dialysis: Comparison of the efficiency of reasoner’2 agar and plate count agar. Braz J Microbiol 2010; 41(1): 15-8.
[http://dx.doi.org/10.1590/S1517-83822010000100003] [PMID: 24031456]
]. Nevertheless, the American Public Health Association (APHA) recommended that R2A agar in combination with a longer incubation period and lower incubation temperature can improve the recovery of stressed and chlorine-tolerant bacteria. This medium may yield higher counts than high-nutrient formulations. However, it is preferable to other media such as m-HPC agar and Plate count agar [20Rice E, Baird R, Eaton A. Standard Methods for the Examination of Water and Wastewater 23rd ed. 2017.]. Attempted cultivation on plate count agar can result in nutrient shock resulting in lower concentrations. Regulatory norms are based on plate count agar, primarily as a matter of tradition.

Other studies have also reported the high HPC in bottled water. Moazeni et al., and Kouchesfahani et al., reported high numbers of HPC bacteria in bottled water sold in Isfahan and Tehran [2Mohammadi Kouchesfahani M, Alimohammadi M, Nabizadeh Nodehi R, Aslani H, Rezaie S, Asadian S. Pseudomonas aeruginosa and Heterotrophic Bacteria Count in Bottled Waters in Iran. Iran J Public Health 2015; 44(11): 1514-9.
[PMID: 26744709]
, 3Moazeni M, Atefi M, Ebrahimi A, Razmjoo P, Vahid Dastjerdi M. Evaluation of chemical and microbiological quality in 21 brands of Iranian bottled drinking waters in 2012: a comparison study on label and real contents. J Environ Public Health 2013; 2013469590
[http://dx.doi.org/10.1155/2013/469590] [PMID: 23690802]
]. The quantity of heterotrophic bacteria in bottled water is generally dependent on the type of source water, the availability of organic carbon, the autochthonic microorganisms and methods employed in the disinfection process [6Diduch M, Polkowska Ż, Namieśnik J. Factors affecting the quality of bottled water. J Expo Sci Environ Epidemiol 2013; 23(2): 111-9.
[http://dx.doi.org/10.1038/jes.2012.101] [PMID: 23093103]
].

Variations in heterotrophic bacterial populations revealed that storage duration affected the rate of bacterial contamination. In the current survey, the highest rate of samples with HPC higher than 1000 CFU/ml and the presence of heterotrophic bacteria were found within the first to ninety days following bottling (Tables 2 and 4). Our finding is consistent with the findings of other studies, which reported that the number of HPC bacteria can increase logarithmically during storage time to 105 CFU/ml [10Rosenberg FA. The microbiology of bottled water. Clin Microbiol Newsl 2003; 25(6): 41-4.
[http://dx.doi.org/10.1016/S0196-4399(03)80019-3]
, 23Nsanze H, Babarinde Z, Al Kohaly H. Microbiological quality of bottled drinking water in the uae and the effect of storage at different temperatures. Environ Int 1999; 25(1): 53-7.
[http://dx.doi.org/10.1016/S0160-4120(98)00097-X]
]. Zeenat et al., revealed that death and autolysis of microflora provide nutrients and further support to the growth of heterotrophic bacteria to high levels after prolonged storage [24Zeenat A, Hatha AA, Viola L, Vipra K. Bacteriological quality and risk assessment of the imported and domestic bottled mineral water sold in Fiji. J Water Health 2009; 7(4): 642-9.
[http://dx.doi.org/10.2166/wh.2009.137] [PMID: 19590131]
].

All bottled water had a variety of genera of heterotrophic bacteria. The results of the biochemical tests for speciation showed that Bacillus spp. and Pseudomonas spp. were detected in 61.8 and 34.5 percent of all samples. The presence of these bacteria in bottled water is due to failure to de-contaminate (properly disinfect) the source water, or the introduction of contaminants during the bottling process [25Joseph N, Bhat S, Mahapatra S, et al. Bacteriological assessment of bottled drinking water available at major transit places in mangalore city of South India. J Environ Public Health 2018; 20187472097
[http://dx.doi.org/10.1155/2018/7472097] [PMID: 30498514]
]. The WHO reported that Bacillus spp., Pseudomonas aeruginosa, Acinetobacter spp., Staphylococcus spp. and other pathogenic bacteria may be found in drinking waters [6Diduch M, Polkowska Ż, Namieśnik J. Factors affecting the quality of bottled water. J Expo Sci Environ Epidemiol 2013; 23(2): 111-9.
[http://dx.doi.org/10.1038/jes.2012.101] [PMID: 23093103]
]. Both norms and customer expectations require that drinking water that leaves a bottling plant must be free from opportunistic pathogens [26Leclerc H, Moreau A. Microbiological safety of natural mineral water. FEMS Microbiol Rev 2002; 26(2): 207-22.
[http://dx.doi.org/10.1111/j.1574-6976.2002.tb00611.x] [PMID: 12069884]
].

The presence of Pseudomonas spp. is countrary the standards established by the European Union water regulations, citing that this bacterium should not be detected in 250 ml bottled water samples [2Mohammadi Kouchesfahani M, Alimohammadi M, Nabizadeh Nodehi R, Aslani H, Rezaie S, Asadian S. Pseudomonas aeruginosa and Heterotrophic Bacteria Count in Bottled Waters in Iran. Iran J Public Health 2015; 44(11): 1514-9.
[PMID: 26744709]
]. The level of Pseudomonas spp. detected in the present study was in line with what detected by Kouchesfahani et al., who described samples purchased from retailers in Tehran, Iran [2Mohammadi Kouchesfahani M, Alimohammadi M, Nabizadeh Nodehi R, Aslani H, Rezaie S, Asadian S. Pseudomonas aeruginosa and Heterotrophic Bacteria Count in Bottled Waters in Iran. Iran J Public Health 2015; 44(11): 1514-9.
[PMID: 26744709]
]. In that study, contamination with E. coli and Enterobacter spp. was also observed in 4.5% and 27.5% of the samples, respectively. Although, these bacteria are considered nonpathogenic, their presence in bottled water indicates a failure in disinfecting the source water or contamination within the bottling plant [27Fewtrell L, Bartram J. Water Quality: Guidelines, Standards and Health Assessment of Risk Management for Water-related Infectious Diseases 2001.]. Farhadkhani et al., and Otterholt et al., showed a significant association between the heterotrophic bacteria level and the presence of opportunistic bacteria [28Farhadkhani M, Nikaeen M, Akbari Adergani B, Hatamzadeh M, Nabavi BF, Hassanzadeh A. Assessment of drinking water quality from bottled water coolers. Iran J Public Health 2014; 43(5): 674-81.
[PMID: 26060769]
, 29Otterholt E, Charnock C. Microbial quality and nutritional aspects of Norwegian brand waters. Int J Food Microbiol 2011; 144(3): 455-63.
[http://dx.doi.org/10.1016/j.ijfoodmicro.2010.10.034] [PMID: 21095035]
]. Fortunately, Vibrio chlorae, Salmonella spp., Shigella spp. and Aeromonas spp. were not found in any of the bottled water samples in our study.

Table 1
Heterotrophic bacterial count (CFU/ml) of bottled water of different brands.


Table 2
Heterotrophic bacterial count (CFU/ml) result for bottled water stored at different duration (days).


Table 3
Bacteria isolated from bottled water at different heterotrophic bacterial count (CFU/ml).


Table 4
Bacteria isolated from bottled water at different storage duration (days).


Our findings also indicated that storage influenced the bacterial quality of bottled water. The highest and lowest rate of contamination was observed in months of May and October when ambient air temperatures are relatively high and low compared to other months. The environmental temperature could be one important reason for the growth of heterotrophic bacteria in bottled water. Falcone-Dias et al., reported that the regrowth of bacteria increases at temperatures higher than 37 °C [30Falcone-Dias MF, Farache Filho A. Quantitative variations in heterotrophic plate count and in the presence of indicator microorganisms in bottled mineral water. Food Control 2013; 31(1): 90-6.
[http://dx.doi.org/10.1016/j.foodcont.2012.09.038]
]. In our study area, ambient environmental air temperatures and air temperatures inside stores commonly reached to 40 °C and occasionally 50 °C (in summer). This finding is similar to the result obtained by Nsanze et al., who reported a significant association between high numbers of HPC and bottled water stored at 25 °C and 37 °C [23Nsanze H, Babarinde Z, Al Kohaly H. Microbiological quality of bottled drinking water in the uae and the effect of storage at different temperatures. Environ Int 1999; 25(1): 53-7.
[http://dx.doi.org/10.1016/S0160-4120(98)00097-X]
].

CONCLUSION

The quality of bottled water reported in this study is of concern for the health of consumers. In our study, all the samples were collected only from supermarkets and not from the manufacturers. Therefore, it is difficult to determine whether the contamination was a result of improper disinfection of the source water, or contamination in the bottling plants; both could result in increased bacterial concentrations over time. The findings point to the need for monitoring of bottled water as well as the adoption of Hazard Assessment Critical Control Points (HACCP) programs, which focus on the most vulnerable aspects of food and water processing to ensure consumer safety.

LIST OF ABBREVIATIONS

E. coli  = Escherichia coli
WHO  = World Health Organization
HPC  = Heterotrophic Plate Count
CFU  = Colony-Forming Unit
ONPG  = Ortho-Nitrophenyl-β-Galactoside
API  = Analytical Profile Index
HACCP  = Hazard Assessment Critical Control Points

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

Not applicable.

HUMAN AND ANIMAL RIGHTS

No animals/humans were used in the study that is the basis of this research.

CONSENT FOR PUBLICATION

Not applicable.

AVAILABILITY OF DATA AND MATERIALS

The data supporting the findings of the article is available in the manuscript.

FUNDING

This research was conducted with funding from the vice chancellery for research at the Golestan University of Medical Sciences (Grant no. 66788).

CONFLICTS OF INTEREST

The authors declare no conflict of interest, financial or otherwise.

ACKNOWLEDGEMENTS

The authors thank the deputy of research and technology of Golestan University of Medical Sciences for financial support.

REFERENCES

[1] Zamberlan dSM, Santana RG, Guilhermetti M. Comparison of the bacteriological quality of tap water and bottled mineral water. Int J Hyg Environ Health 2008; 211(5-6): 504-9.
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[PMID: 26744709]
[3] Moazeni M, Atefi M, Ebrahimi A, Razmjoo P, Vahid Dastjerdi M. Evaluation of chemical and microbiological quality in 21 brands of Iranian bottled drinking waters in 2012: a comparison study on label and real contents. J Environ Public Health 2013; 2013469590
[http://dx.doi.org/10.1155/2013/469590] [PMID: 23690802]
[4] Bedada TL, Dera FA, Edicho RM, et al. Mycological and bacteriological quality and safety of bottled water in Ethiopia. Open Microbiol J 2018; 12: 200-8.
[http://dx.doi.org/10.2174/1874285801812010200] [PMID: 30069259]
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[http://dx.doi.org/10.2166/wh.2006.0023] [PMID: 16813019]
[6] Diduch M, Polkowska Ż, Namieśnik J. Factors affecting the quality of bottled water. J Expo Sci Environ Epidemiol 2013; 23(2): 111-9.
[http://dx.doi.org/10.1038/jes.2012.101] [PMID: 23093103]
[7] Diduch M, Polkowska Ż, Namieśnik J. The role of heterotrophic plate count bacteria in bottled water quality assessment. Food Control 2016; 61: 188-95.
[http://dx.doi.org/10.1016/j.foodcont.2015.09.024]
[8] Venieri D, Vantarakis A, Komninou G, Papapetropoulou M. Microbiological evaluation of bottled non-carbonated (“still”) water from domestic brands in Greece. Int J Food Microbiol 2006; 107(1): 68-72.
[http://dx.doi.org/10.1016/j.ijfoodmicro.2005.08.013] [PMID: 16271413]
[9] Falcone-Dias MF, Vaz-Moreira I, Manaia CM. Bottled mineral water as a potential source of antibiotic resistant bacteria. Water Res 2012; 46(11): 3612-22.
[http://dx.doi.org/10.1016/j.watres.2012.04.007] [PMID: 22534119]
[10] Rosenberg FA. The microbiology of bottled water. Clin Microbiol Newsl 2003; 25(6): 41-4.
[http://dx.doi.org/10.1016/S0196-4399(03)80019-3]
[11] Ashbolt NJ, Grabow WO, Snozzi M. Indicators of Microbial Water Quality: Guidelines, Standards, and Health 2001.
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