Igbeneghu and Lamikanra BMC Research Notes 2014 7859httpwwwbiomedcentralcom1756-05007859

RESEARCH ARTICLE Open Access

The bacteriological quality of different brands ofbottled water available to consumers in Ile-Ifesouth-western NigeriaOluwatoyin A Igbeneghu and Adebayo Lamikanra

Abstract

Background The upsurge in the demand for bottled water has prompted the interest of many manufacturers inthe production of bottled water and very many water bottling companies are therefore involved in its productionThese range from large scale multinational companies to medium scale business enterprises institutional andgovernment business investment companies as well as small scale entrepreneurs There is however little informationon the comparative quality of bottled water brands produced by different classes of water bottling companies inNigeria This study was undertaken to determine the bacteriological quality of brands of bottled water available toconsumers in Ile-Ife

Methods Forty-three samples of bottled water comprising of three batches each of thirteen bottled water brandsand two batches of two brands were purchased and analyzed for total bacterial count presence of coliform and thepresence of other bacterial indicators of drinking water quality

Results Only 674 of the water samples representing the products of 10 companies or 667 of the brands hadheterotrophic counts within the acceptable limits Coliforms present in 100 ml of water were detected in 267 of thebottled water brands Other indicator organisms detected included Staphylococci isolated from 279 of the samples(333 of the brands) and specifically Staphylococcus aureus found in four brands constituting 14 of the samplesPseudomonas strains were consistently detected in consecutive batches of three brands of the water samples

Conclusions Bottled water samples produced by the large scale multinational producers were of acceptablebacteriological quality unlike those produced by most small companies Significance and Impact of Study There isneed for a greater control of water bottling processes carried out by commercial bottled water producers in Nigeria

Keywords Bottled water Water quality Coliforms Indicator organisms Water bottling companies

BackgroundWater is indispensible to life as it is required for allphysiological processes which demand that all living or-ganisms have ready access to water This need is no lessimportant to human beings who have to drink plenty ofwater every day [1] Apart from drinking man uses waterfor many domestic industrial and recreational purposeswhich include washing bathing cooking food processingbrewing and beverage bottling as well as sporting activ-ities This means that there is a need for the constant sup-ply of potable water to all human communities and inareas where such supplies are lacking a great deal of time

Correspondence oaigbeneoauifeedungDepartment of Pharmaceutics Obafemi Awolowo University Ile-Ife Nigeria

copy 2014 Igbeneghu and Lamikanra licensee Bithe Creative Commons Attribution License (htdistribution and reproduction in any medium

and effort are devoted to finding a suitable source of supplyUnfortunately such water sources even when they areavailable are seldom safe or reliable and waters obtainedthere from need to be treated appropriately in order tomake them potableIn all urban areas in the developed countries reliance

is placed on the supply of adequately treated water bymunicipal authorities In developing countries howeverthere is little or no access to such treated water and sopotable water is usually difficult or even impossible toget This is because very little money has been madeavailable for the appropriate municipal infrastructureand this being so a large percentage of people in thesecountries have to depend on their own individual efforts

oMed Central Ltd This is an Open Access article distributed under the terms oftpcreativecommonsorglicensesby20) which permits unrestricted use provided the original work is properly credited

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to get the water which they need One of the means ofsatisfying the need for potable water especially in urbancommunities is to consume packaged water which inNigeria is sold in plastic sachets called pure water or inplastic bottles [2] Bottled water is drinking water whichhas been packaged in plastic bottles ranging in size fromsmall single serving polyethylene terephthalate bottles of500 ml minus15 L capacity to large carboys (20 L) for watercoolers [3] In Nigeria bottled water is regarded as beingsafer than water dispensed and sold in sachets but it isalso about ten times more expensive which is why it ispatronized mainly by people with a relatively large dis-posable incomeApart from microbiological considerations the upsurge

in the demand for bottled water has prompted the interestof many manufacturers in the production of bottled waterClose to two decades ago bottled water was a product ofa few multinational and large scale food processing andbeverage producing companies in Nigeria Presently how-ever there is the involvement of very many water bottlingcompanies ranging from large scale multinational com-panies to medium scale business enterprises institutionaland government business investment companies as well assmall scale entrepreneurs [4] These water bottling com-panies use various water purification methods which maybe one of or a combination of two of filtration ozonisa-tion ultra violet irradiation and chlorinationBottled water has been reported to be associated with

outbreaks of infections in the last few years In 2006Salmonella enterica serovar Kottbus from bottled waterwas significantly associated with 41 cases in an outbreakin infants in Gran Canaria Nineteen of the cases hadunderlying disease or were immuno-compromised Theorganism was isolated from bottled water randomly se-lected from the markets and in the local factory wherethe water was bottled [5] Eckmanns et al (2008) havedescribed an outbreak of hospital-acquired P aeruginosainfection caused by contaminated bottled water in inten-sive care units in a hospital in Germany [6] In the hos-pital the bottled water was used for the preparation oforally administered medications and oral fluid replace-ment Some unopened bottles of water were found tocontain the outbreak strain of P aeruginosa Cases suchas these underscore the need for continual surveillanceor monitoring of quality of bottled water Studies on thequality of bottled water in many parts of the world in-cluding Canada South Africa Iran Egypt and Nigeriahave shown that bottled water samples are not always ofthe required microbiological quality [7-15] This studywas therefore carried out to determine the bacterio-logical quality of all available brands of bottled watersold in a popular shopping centre in Ile-Ife an urbansettlement which is home to both the Obafemi AwolowoUniversity and the Obafemi Awolowo University Teaching

Hospitals Complex as well as many commercial bankswithin which a large number of potential users of bottledwater work This study reports the comparative quality ofbottled water brands produced by different classes ofwater bottling companies in south-western Nigeria

MethodsSamplingA total of 43 bottled water samples representing threebatches of 13 brands of bottled water and two batches oftwo brands purchased on three different occasionswithin a period of 6 months were tested for bacterio-logical quality On the first sampling occasion samplesof all brands of bottled water available for sale in shopslocated in Mayfair Hotel Shopping centre in Ile-Ife werepurchased The samples were inspected and ascertainedto be in good condition with the caps and protective sealintact before purchase The dates of production as wellas the batch numbers were documented They weretaken to the laboratory and analyzed for total bacterialload and the presence of bacterial indicators of drinkingwater qualityThe sampling was repeated two more times at inter-

vals of 3 months to include representative samples ofthree different batches of each brand of bottled wateravailable for sale in Ile-Ife On the third sampling occa-sion two of the brands were not available and so onlytwo batches of these brands were represented in thestudyThe brands were coded A-O for the purpose of this

study and also categorized into three groups based onthe size or class of the companies producing the wateras shown in Table 1

Test for the presence of chlorine in the samplesThe caps and necks of the bottles were swabbed withethanol before breaking the seals and opening the bottlesTwo drops of 5 nitric acid was then added to 15mls ofeach water sample followed by two drops of 01 M silvernitrate solution The cloudiness of the water samplestreated with silver nitrate was taken to be indicative of thepresence of chlorine in the water samples

Inactivation of chlorine in chlorinated samplesThe disinfectant activity of chlorine in chlorinated sampleswas neutralized by the addition of 01 ml of 3vv sterilesodium thiosulphate solution to 100 ml of each chlori-nated sample

Determination of total heterotrophic bacterial countThe enumeration of total heterotrophic bacterial countwas carried out using both the serial dilution and thepour plate technique Serial 10 fold dilutions in sterilewater were carried out and 1 ml of each dilution was

Table 1 Tested brands of bottled water samplesproduced by different classes of companies

Producers Brand Location ofproductionplant

No ofbatches

Method ofdisinfection

Multinational companies A Ibadan 3 Chlorination

B Lagos 3 Chlorination

C Lagos 3 Filtrationand UV

Medium scale andinstitutional bottlingcompanies

D Ibadan 3 Chlorination

E Ile-Ife 3 Ozonisation

F Osogbo 3 Filtrationandozonisation

Small scale businessentrepreneurs

G Ile-Ife 2 Filtrationandozonisation

H Ile-Ife 2 Unspecified

I Ile-Ife 3 Filtrationandozonisation

J Ile-Ife 3 Unspecified

K Ile-Ife 3 Unspecified

L Ile-Ife 3 Chlorination

M Ile-Ife 3 Chlorination

N Ile-Ife 3 Ozonisation

O Ilesa 3 Filtration

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aseptically placed in sterile petri-dishes in triplicates20 ml of molten plate count agar (Oxoid) cooled to 45degCwas then added to each of the plates and mixed thor-oughly The mixture was allowed to solidify and theplates incubated at 22degC and 37degC for 24ndash72 hours Thenumber of bacterial colonies were counted and reportedas colony-forming units per millilitre

The determination of presence of coliform bacteriaThe presence of coliform bacteria was determined bypassing 100 ml volumes of each sample (in triplicate)through membrane filter units (Millipore) (045 μm poresize 47 mm diameter) The filter membranes wereplaced on MacConkey agar plates and incubated at 37degCfor 24 h

Isolation of other indicator organismsThe presence of other indicator organisms which in-cluded Pseudomonas aeruginosa and Staphylococcusaureus was determined by filtering 100 ml volumes ofeach sample (in triplicate) as described above The filtermembranes were placed on nutrient agar plates and in-cubated at 37degC for 24ndash48 hours Colonies arising afterincubation were observed and streaked onto fresh agarplates

Identification of indicator organismsAn overnight Nutrient agar culture of each isolate fromeach water sample was taken through Grams stain andbiochemical tests for the identification of each of the or-ganisms The biochemical tests carried out on the Gramnegative organisms included MRVP citrate utilizationindole growth in Triple Sugar Iron agar and catalaseThe growth characteristic of the Gram positive cocci onMannitol Salt agar was observed and the cocci weretested for catalase and coagulase production The Grampositive rods were observed for sporulation characteristics

Maintenance of strainsDistinct colonies of each isolate from the samples werestored in nutrient agar at 4degC and cryo-preserved inglycerol-nutrient broth in a deep freezerStatistical analysis Descriptive statistical analysis of

the data obtained from the study was carried out usingthe Microsoft excel 2007 version

ResultsThe total heterotrophic bacterial count of the samples at37degC ranged between zero and 1000 cfumlminus1 674 ofthe water samples representing the products of 10 com-panies or 667 of the brands had heterotrophic countswithin the acceptable limits Coliforms present in 100 mlof water were detected in 163 of the samples and267 of the bottled water brands The coliforms de-tected included Enterobacter agglomerans from twobrands and Citrobacter freundi from another two brandsof the samples Other indicator organisms detected in-cluded Staphylococci isolated from 279 of the samples(333 of the brands) and specifically Staphylococcusaureus found in four brands constituting 14 of thesamples Pseudomonas strains were consistently detectedin consecutive batches of three brands of the water sam-ples The acceptability status of the bottled water samplesin relation to the WHO guidelines are as shown inTable 2

DiscussionDrinking water is not expected to be sterile thereforemicroorganisms may be found in potable water There ishowever a limit to the number and kinds of organismspermissible in drinking water with the WHO stipulatingthat the heterotrophic bacteria present in bottled watershould not exceed 50 cfumlminus1 and that there should beno coliform present per 100 ml of water [16]In this study different batches of bottled water pro-

duced by 15 different bottling companies were investi-gated These samples used were the products of largemultinational water bottling companies government andinstitutional bottling companies as well as the smallscale bottling companies which are likely to have been

Table 2 The acceptability status of the bottled watersamples in relation to the WHO guidelines

Brand Coliforms100 ml

TBC Other indicatorspresent

Acceptability

A _ 0 ndash 10 None +

B _ 0 ndash 10 None +

C _ 0 ndash 10 None +

D _ 0 ndash 10 Pseudomonas spp _

E + 11 ndash 100 Staphylococcus spp _

F _ 11 ndash 100 Staphylococcus aureus _

Enterococcus spp

G _ 101 ndash 500 Pseudomonas spp _

H _ 11 ndash 100 Salmonella spp _

I + 11 ndash 100 None _

J + 101 ndash 500 Staphylococcus spp _

Listeria spp

K _ 101 ndash 500 Staphylococcus aureus _

L _ 11 ndash 100 Staphylococcus aureus _

Listeria spp

M + 501 ndash 1000 Listeria spp _

N _ 501 ndash 1000 Pseudomonas spp _

Staphylococcus spp

O _ 0 ndash 10 None +

TBC Total Bacterial Count

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attracted to the packaging of water by a combination ofhigh demand and the possibility of making quick returnson investment [4] From the results of this study thethree batches of samples produced by only four compan-ies were of acceptable quality One other company pro-duced one acceptable batch out of the three batchessampled while the water samples from the other 10companies were found not to be acceptable on all threesampling occasions The acceptability of the products wasdetermined on the bases of the total bacterial load as wellas the presence of coliforms and other indicator organismsOn the basis of total heterotrophic bacterial load

674 of the 43 water samples representing the productsof 10 companies or 667 of the brands had hetero-trophic counts within the acceptable limits for drinkingor bottled water while samples from the other five waterbottling companies had counts above the acceptablelimits and should therefore be considered unfit fordrinking In most cases these are bacteria that areconsidered to be relatively harmless components of theenvironment and can be found on the skin in soil andin very high numbers in food products such as fruitsvegetables meats cheeses yogurt and pasteurized milk[3] Tens of thousands to millions of such bacteria areconsumed on a regular basis in these foods unnoticed[1718] The presence of these organisms in large

numbers even when they are non pathogenic is howeverof significance in immuno-compromised persons inwhom they could cause opportunistic infections Suchpersons include young children the elderly pregnantwomen people with diseases such as cancer diabetesand people on such medications as the corticosteroidswhich possess immunosuppressive properties [19] It hasbeen pointed out that high numbers of heterotrophicbacteria in bottled water might arise when unsterilizedand uncapped plastic bottles are transported to the bot-tling plants in cardboard cartons which expose the inte-riors of the bottles to airborne contaminants [20] It hasalso been pointed out that the presence of large numbersof heterotrophic bacteria in bottled water is an indica-tion of poor manufacturing practices involved in theprocessing of such water [10] and must therefore bedeemed to be unacceptableOn the basis of the coliform count it is required that

drinking water must not contain any coliform in 100mlsof water [16] However coliforms in 100 ml of waterwere detected in seven (163) of the samples represent-ing products from four (267) of the producers makingthese brands unacceptable for drinking The detected co-liforms were from one of the three samples produced bythe institutional water bottling business ventures andthree of the nine small scale producers None of the ninesamples produced by the three multinational large scaleproducers were contaminated with coliform bacteriaColiforms have similarly been reported to occur in bot-tled water sampled in Egypt and some other locations inNigeria ([1012] The presence of coliforms in bottledwater samples is not a confirmation of recent fecal con-tamination as E coli the indicator of recent fecal con-tamination was not detected in any of the samplestested Since coliforms are among the group of organ-isms that have been reported to have the capacity toform biofilms on the items of equipment used in thebottling process [16] they are not only indicators ofproblems with the quality of water source but also ofpossible contamination during the process of bottlingwater and are significant from the point of view ofhygiene [21] Some possible reasons for the presence ofcoliforms in bottled water samples include poor hygienicpractices of the producers poor hand hygiene illiteracyand unhygienic practices of vendors In a study carriedout in Egypt [10] coliforms were detected in 286 of 84bottled water samples examined and they were not offaecal origin as E coli was absent in the samplesOn the basis of the presence of other indicator organ-

isms bottled water samples from 10 of the producerswere found not to be acceptable for drinking Apartfrom coliforms other indicator organisms includingStaphylococcus aureus and Pseudomonas species wereisolated from water samples obtained from ten of the

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fifteen producers studied As pointed out by Addo et al(2009) these are common environmental contaminantswhich are likely to reduce the efficiency of any treatmentprocess [22] Pseudomonads including Pseudomonasaeruginosa have been shown to be persistent contami-nants of water plants [23] This organism is an oppor-tunistic pathogen the ingestion of which can causeinfections in the immuno-compromised subjects [24]Pseudomonas aeruginosa is also known for its resistanceto many antimicrobial agents making the treatment ofinfections caused by the organism a difficult task This iswhy it has been suggested that test for the presence ofPseudomonas species in drinking water should be usedas a means of monitoring the hygienic quality of drinkingwater [16] The two brands with all batches contaminatedby Pseudomonas species were products of two small scaleproducersStaphylococci which are the other indicator organisms

detected in some of the samples were found in 11(256) of the samples and six of the brands while thespecies aureus was found in three brands Staphylococcusaureus is an indicator of poor hygienic practices duringwater bottling [16] and is more likely to have been intro-duced into the samples by the personnel involved in waterprocessing Its presence in the water samples is suggestiveof the fact that the bottled water samples in this studywere contaminated not only by the factory surroundingsbut also by the people who came in contact with any partof the bottling procedure [25] The use of bare hands atdifferent stages in the production of the bottled water is aprobable source of this bacterial contaminant This is sug-gestive of the fact that the bottles were filled manually asis often the case with small scale producers such as thosewhose samples were found to be contaminated withS aureus in this studyThe deficiencies observed in these samples suggest

that most of the producers of the bottled water samplesexamined in this study do not follow stipulated guide-lines in their production processes This is howeveravoidable if there is adequate control or monitoring ofthe practices of the bottling companies The observationfrom this study is an indication of the lack of requiredinfrastructure within the manufacturing outfits Require-ments such as clean rooms automatic bottle filling ma-chines clean water source adequately trained personneland the need for staff supervision by personnel who areknowledgeable in the science of water purification anddispensing must be met by companies which are in-volved in the production of water packaged for humanconsumption This implies that the capital needed by aprospective water bottling company in order to put allthese things in place must be quite high It is not sur-prising therefore to observe that virtually all the bottledwater brands (A B and C) produced by the large scale

multinational companies were of acceptable qualityThese companies are multimillion dollar companies whichalso produce a wide range of consumable products Theyare therefore strictly regulated and their production facil-ities are equipped with a wide range of sophisticatedequipment operated by qualified personnel and their ac-tivities supervised by adequately trained professionals Onthe other hand brands G to O were products of smallscale business ventures located within Ile-Ife and itsenvirons and all except brand O fell short of stipulatedstandards in terms of either the total bacterial load or thepresence of coliforms and indicator organisms Resultsfrom this study suggest that these companies have lesssophisticated water bottling facilities none to a few yearsof experience and most probably employ cheap labourwith little or no technical knowledge in water processingThis phenomenon has been pointed out earlier by authors[26] who found out that body creams produced by largecompanies had better microbiological quality than creamsproduced by small scale producers which may not havebeen able to put in place the entire infrastructure neededfor the production of large quantities of products withdemonstrable quality

ConclusionsThe findings from this study indicate that the water pro-duced by the 10 institutional medium and small scaleproducers ought not to be in the market for public con-sumption underscoring the relevance of regulatory agenciesThere is a need for a rigorous inspection and follow-upof water bottling facilities so that only those companieswhich consistently produce water of acceptable bac-teriological quality are allowed to produce water forpublic consumption

Competing interestsThe authors declare that they have no competing interests

Authorsrsquo contributionsOAI carried out the microbiological analysis performed the statistical analysisand prepared the manuscript AL conceived of the study and participated in itsdesign and coordination and supervised the preparation of the manuscriptAll authors read and approved the final manuscript

Authorsrsquo informationOAI is a post Ph D candidate in the Department of Pharmaceutics ObafemiAwolowo University Ile-Ife Nigeria Pharmaceutical Microbiology is her areaof specialization AL is a professor of Pharmaceutical Microbiology in theDepartment of Pharmaceutics of the same university

Received 6 September 2013 Accepted 18 November 2014Published 28 November 2014

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The Molecules of life In Microbiology A Human perspective 4th editionNew York McGraw Hill 2004

2 Omoniyi BB Abu Z The economic analysis of the profitability of small-scale pure water production in Nigeria (a case study of Jabu packagedwater factory) Afro Asian J Soc Sci 2012 31ndash24

Igbeneghu and Lamikanra BMC Research Notes 2014 7859 Page 6 of 6httpwwwbiomedcentralcom1756-05007859

3 Reynolds KA The microbial quality and safety of bottled water WaterCond Purif 2005 4739ndash40

4 Babatunde MA Biala MI Externality Effects of Sachet Water Consumptionand the Choice of Policy Instruments in Nigeria Evidence from KwaraState J Economics 2010 1(2)113ndash131

5 Palmera-Suarez R Garcia P Garcia A Barrasa A Herrera D Salmonella kottbusoutbreak in infants in Gran Canaria (Spain) caused by bottled waterAugust- November 2006 Eurosurveillance 2007 12(28)3235 Available onlinehttpwwweurosurveillanceorgViewArticleaspxArticleId=3235

6 Eckmanns T Oppert M Martin M Amorosa R Zuschneid I Frei U Ruden HWeist K An outbreak of hospital acquired Pseudomonas aeruginosainfection caused by contaminated bottled water in intensive care unitsClin Microbiol Infec 2008 14454ndash458

7 Martins CHG Microbiological monitoring of mineral watercommercialized in Brazil Braz J Microbiol 2011 42554ndash559

8 Varga L Bacteriological quality of bottled natural mineral waterscommercialized in Hungary Food Control 2011 22591ndash595

9 Kassenga GR The health-related microbiological quality of bottleddrinking water sold in Dar es Salaam Tanzania J Water and Health 20075(Suppl 1)179ndash185

10 Magda MA Engy MA Mohamed MK Quality of Bottled Water Brands inEgypt Part II Biological Water Examination J Egypt Public Health Assoc2008 83(Suppl 5 amp 6)467ndash486

11 Gholam K Ahmaad Z Abolfazi K Mehdi F Mansoor G Asma ZBacteriological evaluation of bottled water from domestic brands inTehran market Iran World Applied Sci J 2010 8(Suppl 3)274ndash278

12 Onweluzo JC Akuagbazie CA Assessment of the bacteriological quality ofbottled and sachet water sold in Nsuka town Agro-Sci J Trop Agr FoodEnviron Ext 2010 9(Suppl 2)96ndash102

13 Oyedeji O Olutiola PO Moninuola MA Microbiological quality of packageddrinking water brands marketed in Ibadan metropolis and Ile-Ife city inSouth Western Nigeria Afr J Microbiol Res 2010 4(Suppl 1)96ndash102

14 Marzano MA Ripamonti B Balzaretti CMMonitoring the bacteriological qualityof Italian bottled spring water from dispensers Food Control 2011 22(2)333ndash336

15 Semerjian LA Quality assessment of various bottled waters marketed inLebanon Environ Monit Assess 2011 172(1ndash4)275ndash285

16 WHO Guidelines for Drinking-Water Quality 4th edition Geneva WorldHealth Organization 2011

17 Wadhwa SG Khaled GH Edberg SC Comparative microbial character ofconsumed food and drinking water Crit Rev Microbiol 2002 28249ndash279

18 Stine SW Pepper IL Gerba CP Contribution of drinking water to theweekly intake of heterotrophic bacteria from diet in the United StatesWater Res 2005 39257ndash263

19 Bartram J Cotruvo J Exner M Fricker C Glasmacher A Heterotrophic PlateCounts and Drinking-water Safety London UK World Health Organization(WHO) Published by IWA Publishing 2003

20 United States Environmental Protection Agency (USEPA) Bottled water vsbottleless water coolers Canada Pure Natural System INC 2008

21 Food Safety Authority of Ireland (FSAI) 3rd National Microbiological Survey2007 (07NS3) Microbiological safety and quality of bottled water wwwenvirocentreieincludesFSAIreportbottled_water2008[1]pdf

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23 Morais PV Mesquita C Andrade J-L da Costa MS Investigation of persistentcolonization by Pseudomonas aeruginosa ndash like strains in a spring waterbottling plant App Environ Microbiol 1997 63(Suppl 3)851ndash856

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26 Okeke IN Lamikanra A Bacteriological quality of skin-moisturizing creamsand lotions distributed in a tropical developing country J Appl Microbiol2001 91922ndash928

doi1011861756-0500-7-859Cite this article as Igbeneghu and Lamikanra The bacteriological qualityof different brands of bottled water available to consumers in Ile-Ifesouth-western Nigeria BMC Research Notes 2014 7859

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