Contamination Of Bottles Used For Feeding Reconstituted Powdered Infant Formula And Implications For Public Health


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Contamination Of Bottles Used For Feeding Reconstituted Powdered Infant Formula And Implications For Public Health

  1. 1. Perspectives in Public Health Contamination of bottles used for feeding reconstituted powdered infant formula and implications for public health Elizabeth C Redmond, Christopher J Griffith and Steven Riley Perspectives in Public Health 2009; 129; 85 DOI: 10.1177/1757913908101606 The online version of this article can be found at: Published by: On behalf of: Royal Society for Public Health Additional services and information for Perspectives in Public Health can be found at: Email Alerts: Subscriptions: Reprints: Permissions: Citations Downloaded from by on September 6, 2009
  2. 2. PAPER Contamination of bottles used for feeding reconstituted powdered infant formula and implications for public health Contamination of bottles used for feeding reconstituted powdered infant formula and implications for public health Authors Elizabeth C Redmond Abstract PhD, Food Research and Aims: Microbial contamination of powdered infant formula (PIF) is known to cause gastrointestinal Consultancy Unit, University of Wales Institute, Cardiff, infections in infants. Of concern is intrinsic contamination of the formula with (for example) Western Avenue, Cardiff, Salmonella enterica as well as extrinsic contamination from inappropriate handling or ineffective CF5 2YB, UK disinfection. The aim of this study was to evaluate organic and microbial contamination of ‘in-use’ Tel: 02920416452 Fax: 02920416306 bottles used for feeding infants powdered formula milk in South Wales, UK. Email: eredmond@uwic. Methods: To establish baseline contamination levels of ‘in-use’ bottles, 75 ‘uncleaned’ and 150 ‘cleaned and ready to re-use’ bottles used for feeding infants PIF were analyzed. The microbiological analysis included aerobic colony counts (ACCs), presence/absence and Christopher J Griffith Food Research and counts of Enterobacteriaceae and Staphylococcus aureus. The level of residual adenosine Consultancy Unit, University tri-phosphate (ATP) was determined as an indicator of organic soiling. All bottles were sampled of Wales Institute, Cardiff, in four sites; inner screwcap, bottle interior; bottle outer rim and teat interior. UK Results: Microbial counts up to 105/area were sampled and ATP levels up to 100,051 relative light Steven Riley units (RLUs) were obtained from ‘uncleaned’ bottles. Findings varied according to bottle site. Laboratoires Rivadis, Enterobacteriaceae and Staphylococcus aureus were isolated from 12–15% of ‘unclean’ Immeuble Le Saint-Louis, bottles/components (up to 102 cfu/area sampled) and contamination was most frequently detected France from the screw cap and teat interiors. Data indicated that after use, prior to cleaning, considerable Corresponding author: microbial and organic soil remained in the cumulative bottles. Of the ready-to-use bottles reportedly Elizabeth C Redmond, as cleaned and disinfected, some had ACCs up to 5.8x104 cfu/area sampled. Staphylococcus aureus above was detected from 4% bottles/components but no Enterobacteriaceae were detected. Key words Conclusions: Cumulatively, findings indicate the presence of organic soiling and the potential powdered infant formula; for survival of bacteria between infant feeds. There is a need for effective education on effective bottle feeding; steriliza- bottle decontamination procedures. This may be achieved by using an audience-centred tion/disinfection; infant feed- ing; ATP approach to re-enforce messages to parents and caregivers to implement good hygiene bioluminescence; practices, effectively wash and rinse items before disinfection and follow manufacturers’ microbiological guidelines for disinfection. contamination INTRODUCTION behaviours, as well as effective decontamination In 2007 it was reported that nearly a quarter of of feeding bottles and components, is of UK mothers used infant formula as the sole significant importance to ensure microbiological source of nutrition for their baby from birth, and safety of reconstituted PIF feeds and thus is of the proportion of infants fed with formula relevance to parents and caregivers in homes, increased to 75% after six weeks from birth.1 hospitals and day nurseries. Implementation of recommended powdered Reconstituted PIF is considered high risk infant formula (PIF) preparation and handling because of the potential for microbial growth, the Copyright © Royal Society for Public Health 2009 March 2009 Vol 129 No 2 l Perspectives in Public Health 85 SAGE Publications ISSN 1757-9139 DOI: 10.1177/1757913908101606 Downloaded from by on September 6, 2009
  3. 3. PAPER Contamination of bottles used for feeding reconstituted powdered infant formula and implications for public health susceptibility of the infant population to cleaned and disinfected adequately, incentives, including the exchange of enteric bacterial pathogens and the subsequent formula made up in the each complete bottle with a packet of possibility of severe response to bottle may also become contaminated. surface wipes and a bottle of hand gel or enterotoxins. PIF is not a sterile product If the reconstituted feed is not used a new replacement bottle. and provides an ideal growth medium for immediately, storage at temperatures spoilage and pathogenic bacteria.2 >5oC for increased periods of time may Criteria for collection of feeding Micro-organisms of concern, with clear allow low numbers of microbial bottles evidence of causality, include contaminants to increase, thus Only plastic bottles with silicone teats Enterobacter sakazakii (Cronobacter potentially increasing the risk of used for feeding infants aged <9 months spp.) and Salmonella enterica. Other resultant infection. Therefore, with PIF were accepted for analysis for organisms associated with PIF include implementation of effective cleaning and this study. Collected bottles were other Enterobacterial strains, Bacillus disinfection procedures for all bottles required to be ‘clean’ or ‘unclean’. spp., Clostridium spp., Listeria and components are extremely ‘Clean’ bottles were defined as those monocytogenes and Staphylococcus important. Currently, little information is that were, in the parent’s/caregiver’s aureus.3 available on the adequacy of infant opinion, clean and ready to be filled with Vulnerable populations who are more feeding bottle cleaning and disinfection. a feed. Bottles and components susceptible to bacterial infections The limited information available is sampled from day nurseries and homes include young infants, who may be relatively dated7,8,9 and may not be had been reportedly cleaned and more likely to become infected with representative of the UK or practices of disinfected by day nursery staff and lower doses of infectious pathogens.4,5 other developed countries.10,11 parents respectively. ‘Unclean’ bottles Errors in the making up of feeds and Furthermore, recommended methods were defined as those that had just been poor hygiene behaviours are and advice on bottle decontamination used (within four hours) and had not considered to be particularly hazardous have changed considerably over the undergone any cleaning or disinfection. for infants aged < 6 months. Resultant past few decades. The aim of this study All of the unclean bottles were empty, gastroenteritis from hygiene was to evaluate organic and microbial with all of the feed reportedly having malpractices can be extremely contamination of ‘in-use’ bottles used been fed to one infant (no bottles dangerous to very young infants and for feeding infants PIF in South Wales, supplied for sampling were partially filled). remains a common reason for young UK. Organic and microbial As would be expected, small quantities babies to be admitted to hospital.6 contamination was determined for of feed residue remained in the ‘unclean’ Because of infants’ reduced immunity, bottles and components (including teat bottles and the screw cap and teat were the management of bottle cleaning and and screw cap) (a) sampled immediately reported to have not been removed from disinfection, followed by reconstitution after feeding (and subject to no cleaning unclean bottles post feeding, prior to of formula and subsequent storage and/or disinfection) and (b) considered sampling, thus preventing opportunity for prior to use, is particularly important. by parents and caregivers as ‘clean’ cross-contamination from the handler or Adequacy of bottle disinfection may be and ready to re-use, i.e. holding the environment. After collection, the especially significant when feeding reconstituted formula. Ready for use bottles were transported to the does not occur immediately after feed bottles were evaluated in relation to the laboratory in a refrigerated container preparation because time/temperature cleaning and disinfection methods used. (<5˚C). All bottles were collected within abuse can occur. To prevent this abuse four hours of (reported) use and sampled of reconstituted powdered formula within a further two hours. Therefore all feeds, the World Health Organization METHOD bottles were sampled within six hours of (WHO) has recommended for PIF to be Recruitment of parents and day nurs- reported use. freshly made up for immediate eries to provide ‘used’ feeding bottles At the time of bottle collection, all consumption (discarded if not Used infant feeding bottles were parents and day nurseries were asked to consumed within two hours). If, obtained from parents and day nurseries complete a short questionnaire to however, feeds need to be prepared in in South Wales using a convenience indicate the length of time that the bottle advance it is recommended that they sample.12 Sources of recruitment of and teat had been in use, frequency of are stored at the back of a refrigerator parents included members of a baby use and self-reported practices used to at no higher than 5oC for up to 24 club and parents of infants attending day clean the bottle (where appropriate). hours.5 nurseries in South Wales. All local If reconstituted infant formula is nurseries in the surrounding area were Bottle and component sampling contaminated, then logically the bottles contacted as part of the recruitment locations and components used for feeding the process. All parents and nurseries that Each feeding bottle (cleaned and formula can also become contaminated. supplied the study with used bottles and uncleaned) was sampled in four locations If these bottles and components are not components were provided with (in the following order for every bottle): 86 Perspectives in Public Health l March 2009 Vol 129 No 2 Downloaded from by on September 6, 2009
  4. 4. PAPER Contamination of bottles used for feeding reconstituted powdered infant formula and implications for public health 1. Outer rim of the bottle: Half of the (Oxoid, DR0595). Enterobacteriaceae particularly when coupled with potential outside rim was sampled using an counts were performed using violet red risks of temperature abuse and microbial ATP Clean-trace swab (3M-formally bile glucose agar (VRBGA) (Oxoid, growth within the formula during storage Biotrace Bridgend) and the other half CM485) with an overlay according to prior to consumption. sampled using a cotton tip swab HPA standard F23, 2006.14 (moistened using Maximum Recovery ATP measurements were presented as Analysis of data Diluent (MRD) (Oxoid CM733) with relative light units (RLU) obtained per Microsoft Access 2003 and Microsoft 0.05% sodium thiosulphate – surface area sampled. Microbial Excel 2003 were used for data analysis. neutraliser for hypochlorite). contamination was presented as colony Descriptive statistics were used to 2. Inner surface of the bottle: The whole forming units (cfu) per area sampled or describe frequency data. Significant surface area of each bottle was rinsed counts or presence/absence of statistical differences between ATP and with 20ml MRD (plus 0.05% sodium Staphylococcus aureus. No corrections microbiological data according to thiosulphate) (made using ATP free were made for the differences in size of reported disinfection method were H2O). The opening of each bottle was bottles or components sampled. determined using ANOVA (single factor). covered with Nesco film and a standard rinsing procedure was Classification of ‘satisfactory’ RESULTS used.13 and ‘unsatisfactory’ measures of Cumulatively, 150 ‘cleaned’ and 75 3. Inside of the screw cap: Before sampling the screw cap, the silicone cleanliness ‘unclean’ plastic feeding bottles with Standards of satisfactory and silicone teats were sampled. The average teat was removed using flamed unsatisfactory microbiological and ATP age of infants fed using sampled bottles tweezers. Half of the inside rim of the levels were required to classify findings. and components was 20 weeks. Ninety screw cap was sampled using and The manufacturers of the ATP system eight per cent of ‘unclean’ and 90% of ATP Clean-trace swab (3M) and the (3M) recommended that users determine ‘clean’ bottles and components were other half sampled using a cotton tip their own standards for cleanliness, exclusively used for feeding reconstituted swab (moistened using MRD with although they suggested for different PIF. Information regarding use history 0.05% sodium thiosulphate). sites and conditions, values between and self-reported methods of cleaning 4. Inner surface of silicone teat: Half of 200 and 1,000 RLU can be used. and disinfection of bottles and the inside of the silicone teat was Research has established that most components sampled for the study was sampled using an ATP Clean-trace surfaces after routine cleaning (but not provided for 79% of ‘unclean’ bottles swab (3M) and the other half sampled necessarily disinfection) can have an ATP and 97% of ‘clean’ bottles. The length of using a cotton tip swab (moistened level lower than 500 RLU.15 Previous PIF time bottles and teats had been in use using MRD with 0.05% sodium and feeding bottle/component work has prior to sampling was recorded (Figure thiosulphate). indicated that with good cleaning 1). The majority (78–82%) of ‘unclean’ techniques and disinfection equipment, a bottles and teats were reported to have Analysis of rinse and swab samples value lower than 200 RLU could routinely been in use for < 1 month, whereas the All ATP measurements were performed be attained.16 This value was therefore age of ‘clean’ bottles and teats sampled using 3M equipment and tests used throughout as a benchmark for was more evenly spread over six were implemented according to satisfactory residual organic soil levels months. Self-reported frequency data manufacturers’ recommendations. For and considered to be ‘clean’. indicated that 43% bottles/components ATP detection of the rinse samples, Previous work has demonstrated that, sampled had been in use one to five Aquatrace tests were used. For ATP for surfaces in good condition, microbial times a week, 29% in use six to 10 times detection of bottle, teat and screw cap levels <1 cfu/area sampled was routinely a week, 14% in use 10–15 times a week surfaces, Cleantrace tests were used. attainable when following UK and 18% in use more than 16 times a Aerobic colony counts (ACC) were Department of Health cleaning week. performed using oxoid plate count agar recommendations17 and manufacturer A large proportion of bottles and (PCA) (Oxoid CM325) and Health guidelines.16 This was used as a components considered, by parents and Protection Agency (HPA) standard benchmark value or ‘standard’ for a nurseries, to be ‘clean and ready to methods (F10, 2006).14 Staphylococcus ‘satisfactory’ clean bottle surface. This re-use’ had unsatisfactory levels of aureus counts were performed on Baird microbiological level for ‘satisfactory’ organic soiling. Overall, 81% of ‘clean’ Parker plates (spread plate) (Oxoid clean is more stringent than previously bottles had at least one sampled site in CM0275) (HPA standard F12, 2006).14 used older standards.9,12 However, the excess of 200 RLU, i.e. excess of that Determination of presence/absence of S. level used in this study can be justified which could be obtained and considered aureus was performed using Giolitti when considering the vulnerability of ‘clean’. Results showed that a large Cantioni broths (GC) (Oxoid, CM0523) young infants who will consume the proportion (55–62%) of sampled inner and confirmed using the Staphylase test reconstituted formula from the bottles, surface of screw caps and outer rim of March 2009 Vol 129 No 2 l Perspectives in Public Health 87 Downloaded from by on September 6, 2009
  5. 5. PAPER Contamination of bottles used for feeding reconstituted powdered infant formula and implications for public health ‘clean’ bottles and components. Eighty Figure 1 three per cent of ‘clean’ bottles sampled Age of bottles and teats sampled (i.e. length of time ‘in use’ prior to had reportedly been washed and sampling) disinfected and 17% were reportedly cleaned only using a hand wash 60 procedure or the dishwasher. The most ‘Clean’ bottles (n = 146) common disinfection method reportedly ‘Clean’ teats (n = 146) 50 ‘Unclean’ bottles (n = 59) used (by 43% of parents/nurseries) was ‘Unclean’ teats (n = 59) an electric steamer unit. All 40 parents/nurseries that provided disinfected bottles for the study reported No. bottles / teats 30 that they washed the bottles and components before disinfection. 20 However, 5% reported that they did not use detergent, 31% that they did not use hot water and 19% that they did not 10 rinse items after washing (Table 3). Data presented in Figure 2 indicated that the 0 0–3 weeks 4–11 weeks 12–19 weeks 20–27 weeks 28 weeks or more majority (80%) of bottles and Age of bottles and teats sampled components that were only hand washed or washed in the dishwasher had unsatisfactory levels of organic debris (ATP), compared to 18–23% of Table 1 bottles and components that had been subject to disinfection methods. Organic soiling (ATP) detected from ‘clean’ bottles per area sampled Results indicated that fewer bottles (n = 150 bottles) and components obtained Location of bottle unsatisfactory microbial counts when sampled disinfected using the microwave (no. of samples) Mean ATP (RLU) Range of RLU n (%) >200 RLU steamer unit (26% failure rate) and cold Outer rim (n = 150) 363 22–3,260 83 (55) water hypochlorite solution (31%). An unexpectedly high proportion (49%) of Rinse (n = 150) 46 6–285 4 (3) bottles and components disinfected in Screw cap (n = 150) 560 18–8,608 93 (62) steamer units were regarded as unsatisfactory. Despite this, no Inner teat (n = 150) 263 13–2,560 63 (42) significant difference (p < 0.05) was Cumulative bottle identified between different disinfection (n = 150) 308 6–8,608 121 (81) methods. However, a significant difference (p < 0.05) was identified between microbial counts from disinfected and non-disinfected ‘ready bottles had unsatisfactory ATP levels. excess of 104 cfu/area sampled. No to re-use’ bottles and components Organic soiling of rinse samples (inside Enterobacteriaceae were isolated from (ANOVA single factor). Cumulatively, bottle surfaces) was lower than other ‘ready to re-use’ bottles. Presence of results indicated that disinfected bottles sampled surfaces; 97% of clean bottle Staphylococcus aureus was detected and components had lower cfu counts. rinses attained a satisfactory ATP level from 4% of ‘clean’ bottles/components All of the ‘unclean’ bottles collected (Table 1). in at least one site. Three bottles had two immediately after feeding had residues of Overall, 61% of ‘clean and ready to or more positive locations, and six reconstituted formula. Findings indicated re-use’ bottles had at least one sampled bottles had counts in excess of that unclean bottles and components site in excess of 1 cfu/sampled area and 1 cfu/area sampled, with one bottle in had considerable organic soiling (ATP), thus were not considered to be excess of 102 cfu/area sampled. Positive particularly the inside surface of the satisfactorily clean (Table 2). The inside of samples were most frequently isolated screw caps and the inside surface of the the screw cap was the site most likely to from the outer rim of the bottle. teats. Results also showed some ATP have microbial contamination. All sites Microbiological and ATP results were levels in excess of 100,000 RLU (see recorded a mean count greater than 102 analyzed according to the method Table 4). Overall, >99% of bottles had at cfu/area sampled, with some counts in reportedly used for the preparation of least one or more sites with 88 Perspectives in Public Health l March 2009 Vol 129 No 2 Downloaded from by on September 6, 2009
  6. 6. PAPER Contamination of bottles used for feeding reconstituted powdered infant formula and implications for public health Table 2 Microbiological results from ‘clean’ bottles per area sampled (n = 150 bottles) n (%) bottles where Location of bottle ACC Mean ACC range % bottles S. aureus counts n (%) bottles where sampled cfu/area cfu/area where ACC positive for n (%) bottles detected >1 Enterobacteriaceae (no. of samples) sampled sampled <1 cfu S. aureus cfu/area sampled isolated (n = 75) Outer rim (n = 150) 1.4 × 102 <1 – 2.2 × 103 63% 4 (2.7) 3 (2.0) 0 (0) 2 3 Rinse (n = 150) 1.4 × 10 <1 – 4.4 × 10 63% 2 (1.3) 1 (0.7) 0 (0) 2 4 Screw cap (n = 150) 6.4 × 10 <1 – 5.8 × 10 67% 2 (1.3) 1 (0.7) 0 (0) Inner teat (n = 150) 1.4 × 102 <1 – 4.1 × 103 71% 1 (0.7) 1 (0.7) 0 (0) 2 4 Cumulative bottle 2.7 × 10 <1 – 5.8 × 10 61% 6 (4)* 5 (3)* 0 (0) (n = 150) * Positive/counts for S. aureus in at least one bottle site was in excess of 1 cfu/area sampled. Table 3 Staphylococcus aureus was isolated from all sampled sites but more frequently from Self-reported methods used for preparation of ‘clean’ bottles provided for the study the inside of the screw cap and outer rim (n = 146 responses) of the bottle; isolations sometimes Self-reported responses from exceeded 102 cfu/area sampled. Twelve parents and day nursery staff percent of bottles overall were positive for Method of cleaning and disinfection n (%) Enterobacteriaceae with the outer bottle Use of hot water (n = 146) 101 (69) rim and inner rim of the screw cap most likely to be contaminated, with counts Use of detergent (n = 146) 138 (95) sometimes exceeding 103 cfu/area Rinse (n = 146) 118 (81) sampled. Five percent of bottles yielded multiple site contamination with Reported disinfection Microwave unit 26 (17) Enterobacteriaceae. An additional method (n = 150) Steam unit 64 (43) analysis of the data indicated that sites where S. aureus was detected at an Cold water hypochlorite 35 (23) unsatisfactory level (>1 cfu/cm2), 86% solution were also contaminated with Dishwasher/handwash 25 (17) Enterobacteriaceae; ACCs for such samples all exceeded 103 cfu/area sampled and had unsatisfactory levels of organic debris (ATP). unsatisfactory (>200 RLU) organic soiling had at least one site contaminated with (ATP) levels. 105 cfu/area sampled, and 55 ‘unclean’ All sampled ‘unclean’ feeding bottles bottles had at least one site of 104 DISCUSSION had at least one or more site with an cfu/area sampled. Overall, 95% of outer Breastfeeding is reported by the WHO unsatisfactory microbial load (>1 cfu/area bottle rims, 99% of inside surface of teats and UNICEF to be ‘an unequalled way of sampled). Unclean bottles had mean and 100% of the inner bottle surfaces providing food for the healthy growth and ACCs in excess of 104 cfu/area sampled and inside rim of the screw cap failed to development of infants’.19 However, nine for the inside rim of the screw cap, inner attain satisfactory bacterial counts (<1 in 10 mothers in the UK have reported bottle surface and inside surface of the cfu/area sampled). Twelve percent of feeding their young infants aged <6 teat; the outer rim of the bottle having unclean bottles were positive for months with PIF, either exclusively or in marginally lower counts of 103 cfu/area Staphylococcus aureus from at least one combination with breastfeeding, a third sampled (Table 5). Eight ‘unclean’ bottles sampled location. In 8% of cases this of whom reported doing so since birth.1 March 2009 Vol 129 No 2 l Perspectives in Public Health 89 Downloaded from by on September 6, 2009
  7. 7. PAPER Contamination of bottles used for feeding reconstituted powdered infant formula and implications for public health to report adequate cleaning methods, Figure 2 whereas day nurseries reported Sampled bottle locations that failed to attain required ‘satisfactory’ adequate practice for all bottles provided microbiological levels (<1 cfu/area sampled) and ATP values (<200 RLU) for the study. It is recommended that according to disinfection method (n = 150 bottles) when using commercial disinfection/sterilizer units, 90 manufacturers’ instructions are 80 followed.25 The most common 70 disinfection method reported was use of 60 a steamer unit (43%), followed by a cold 50 water disinfection method (23%) and % 40 microwave unit (17%). Seventeen per 30 cent of bottles considered ‘ready to re- 20 use’ had only been hand washed or 10 washed in the dishwasher. 0 Microwave Steam unit Cold water Dishwasher/hand The microbiological analysis of 150 hypochlorite solution wash ‘ready to re-use’ bottles in this study Disinfection method indicated that a substantial number of No. samples obtaining unsatisfactory levels of ATP (>200 RLUs/area sampled) bottles and components had not been No. samples obtaining unsatisfactory microbiological counts (>1 cfu/area sampled) adequately cleaned or disinfected, especially the inner surface of screw caps, from where the more extensive contamination (up to 104 cfu/area sampled) was determined. Overall, 61% Table 4 of ‘ready to re-use’ bottles had at least Organic soiling (ATP) detected from ‘unclean’ bottles per area sampled one site in excess of 1 cfu/sampled area (n = 75 bottles) and thus were not considered to be satisfactorily clean. Data from this study Location of bottle % bottles with is comparable with previous bottle sampled Mean Range of unsatisfactory (no. of samples) ATP (RLU) RLU ATP levels (>200 RLU) contamination research from UK, Ireland and Sweden8,9,26 and findings from this Outer rim (n = 75) 1,822 183–7,946 99 study indicate a greater proportion of Rinse (n = 75) 1,204 224–4,253 100 satisfactorily clean inner teat and inner bottle surfaces. This may be due to Screw cap (n = 75) 6,628 452–100,051 100 the more stringent standards, Inner teat (n =75) 5,492 843–117,107 100 improvements in the efficacy of disinfection processes or quality of PIF used. Although the principles of disinfection have remained the same, Concerns about microbiological risks procedures and appropriate hygiene methods may have changed and associated with PIF use, preparation and behaviours during formula preparation improved in terms of potential efficiency storage have been investigated by WHO and use. Furthermore, there is a need for and convenience during the past 20–30 and the Food and Agriculture health professionals to provide parents years. For example, the required time for Organization (FAO) in recent years.3 and other caregivers with information immersing bottles and components into Consumption of PIF contaminated with and advice about safe preparation and cold water hypochlorite solutions has E. sakazakii (Cronobacter spp.) has been use of PIF from an early stage. reduced from (for example) at least 1½ epidemiologically linked with the cause of hours in 196527 to a minimum of 15 infant infections.20 This pathogen has Clean, ready to re-use feeding bottles minutes (for some brands) in 2008.28 In been isolated from 2–12% samples of In this study, a variety of cleaning addition, nowadays few parents report PIF21,22 as well as from a range of home, methods (prior to disinfection) were boiling bottles and components as a food production and healthcare reported by parents and day nursery means for disinfection and the use of environments.23,24 To reduce the potential employees and this may have influenced commercial steam and microwave units for implementation of malpractices that the subsequent effectiveness of the is a popular practice. could result in the possible illness of an disinfection methods used. Findings A comparison of findings from this infant, it is important for parents and indicated that 45% of parents who study with the Anderson and Gatherer caregivers to implement recommended provided ‘ready to re-use’ bottles failed study8 showed that 8–11% more teat 90 Perspectives in Public Health l March 2009 Vol 129 No 2 Downloaded from by on September 6, 2009
  8. 8. PAPER Contamination of bottles used for feeding reconstituted powdered infant formula and implications for public health Table 5 Microbiological results from ‘unclean’ bottles per area sampled (n = 75 bottles) n (%) bottles n (%) bottles n (%) bottles where n (%) bottles Location of bottle ACC Mean ACC range where ACC where S. aureus where sampled cfu/area cfu/area <1 cfu/area S. aureus >1 cfu/area Enterobacteriaceae (no. of samples) sampled sampled sampled isolated sampled isolated♦ Outer rim (n = 75) 3.3 × 103 0 – 7.8 × 104 4 (5) 6 (8) 5 (7) 7 (9) Rinse (n = 775) 2.6 × 104 1.0 × 102 – 2.1 × 105 0% 2 (3) 1 (1) 1 (1) Screw cap (n = 775) 2.3 × 104 50 – 2.9 × 105 0% 8 (11) 3 (4) 8 (11) Inner teat (n = 775) 1.4 × 104 0 – 1.2 × 105 1 (1) 3 (4) 2 (3) 2 (3) Cumulative bottle 1.6 × 104 0 – 2.9 × 105 5 (7) 9 (12)* 6 (8)* 11 (15) (n = 775) * Positive/counts for S. aureus in at least one bottle site Positive for Enterobacteriaceae in at least one bottle site ♦ All Enterobacteriaceae isolated were >1 cfu/area sample samples were more microbiologically Findings showed that a large proportion preparation.33 The same cross- contaminated than rinse samples (from of teats, screw caps and outer rim contamination issues are applicable inner bottle surfaces). This finding may surfaces (42–62%) had unsatisfactory during the preparation and feeding of PIF. not be surprising when considering the ATP levels, some in excess of 100,000 S. aureus was most frequently isolated practical implications of cleaning each RLU, whereas only 3% of rinse samples from the outer rim of bottles disinfected item, considering shape, structure and from the inner surface of bottles in an electric steamer unit. Observations composition of the teat and bottle. achieved unsatisfactory levels. This may of the decontamination process of such Furthermore, the cleanliness of a larger be because some teats, screw caps and bottles indicated that rather than failure proportion of teats sampled in this study outer rim surfaces have corners, of the cleaning or disinfection method, was considered to be ‘satisfactory’ than grooves, indented areas and curved contamination may have been from an in the Anderson and Gatherer study. 8 This edges that are awkward to clean, and extrinsic source, resulting from poor may be due not only to improved inadequate cleaning may have resulted in hygiene, post disinfection.34 In such disinfection processes now available, but an ineffective disinfection procedure. The instances, parents were observed to hold also the type of teats in use at the time of ease of cleaning all component parts of the outer rims of bottles with hands to study. UK market data suggests that bottles has important implications for remove it from the sterilizer/disinfection silicone teats are currently the most manufacturers involved in bottle and unit. Results for the same bottles popular type of teat purchased,29 component design. showed that, unsurprisingly, in some whereas years ago teats were A finding from this study that was of instances where S. aureus was isolated predominately made from latex. most concern was Staphylococcal from the outer rim, the pathogen was Nowadays, silicone is believed to be a contamination from ‘cleaned’, ready to also isolated from the inner rim of the more durable substance, which is better re-use bottles. This was most probably adjoining screw cap indicating microbial able to withstand repeated cleaning and derived from the hands of the people cross-contamination between bottle disinfection30 than latex alternatives. Latex cleaning and decontaminating the components, most probably originating teats are known to develop tiny cracks on bottles; however, it may have originated from poor hand hygiene. the surface after repeated use31 and thus from the environment or the infants Bottle sites (from unclean and ready to may be more difficult to clean effectively. themselves. Up to 30–50% of humans re-use bottles) associated with the most ATP bioluminescence is a method are carriers of S. aureus, found in the significant organic and microbial used in food processing, food nostrils, skin and hair,32 and the potential contamination (with ACCs, preparation and healthcare environments for associated illnesses have frequently Enterobacteriaceae and S. aureus) were to monitor surface cleanliness. In this been linked to cross-contamination the screw cap and the outer rim. Such study, the ATP detected most likely between hand- and food-contact sites included varying depths of thread originated from residual formula debris. surfaces, particularly during food (for attachment of the screw cap to the March 2009 Vol 129 No 2 l Perspectives in Public Health 91 Downloaded from by on September 6, 2009
  9. 9. PAPER Contamination of bottles used for feeding reconstituted powdered infant formula and implications for public health bottle), which may be difficult to clean, Unclean feeding bottles contamination. Alternatively, thus providing a location for harbouring An analysis of 75 ‘unclean’ bottles Enterobacteriaceae from the ‘unclean’ micro-organisms and a source of sampled immediately after use, before bottles may have come from human contamination for other bottle- or hand- any cleaning or disinfection, indicated contamination and be an indication of contact surfaces – and potentially the considerable organic soiling (high ATP inadequate personal hygiene behaviours reconstituted formula milk. The ease of levels) and microbial contamination. This implemented during preparation or cleaning and disinfection should be a was perhaps not surprising as the feeding. consideration for future design of feeding majority of such bottles contained visual The FAO/WHO3 have classified bottles whereby threads are shallow to residues of reconstituted formula when S. aureus as a ‘Category C organism’ – facilitate effective decontamination sampled. Given the nature of infant capable of causing infant illnesses (such procedures without difficulty. formula, elevated contamination levels is as systemic infection, necrotizing Cumulatively, results from this study perhaps to be expected. PIF is not, entercolitis and severe diarrhoea), but not indicate slight differences in contrary to considerable parent and yet previously identified in PIF or directly contamination levels depending on the healthcare professional belief, a sterile implicated in causing illness in infants. disinfection method used. Bottles product.38,39 However, recommendations Findings from this study showed that ‘disinfected’ in the microwave unit and in the UK indicate that the addition of overall, 12% of unclean feeding bottles using cold water hypochlorite methods boiled water, cooled to no less than were contaminated with S. aureus and attained the lowest microbiological 70oC, will destroy bacteria within the this was most likely as a result of counts. The most common disinfection powder, making the reconstituted extrinsic (human) contamination. Four method used to decontaminate bottles formula safe for consumption.38 per cent of inner teat surfaces were included use of a steamer unit and However, practices differ considerably in contaminated with S. aureus; this is a although measures of organic soiling other countries. Almost all of the total slightly smaller proportion than found in a were comparable with those bacterial counts obtained from all previous study where S. aureus was determined from microwave and cold ‘unclean’ bottles in this study are rated isolated from 12% of inner teats.10 water disinfection methods, samples as ‘unsatisfactory’, and would require However, environmental conditions, the associated with ‘unsatisfactory’ cleaning and disinfection before further quality of reconstituted formula and the microbiological counts were use. All parents and caregivers who type of bottles and teats sampled were unexpectedly high. A large proportion provided such bottles for the study different. (80%) of bottles that were not recognized the need for decontamination Identification of unsatisfactory levels of disinfected at all had unsatisfactory prior to further use. Total counts from organic and microbial contamination of levels of organic debris and nearly half sampled bottles in this study were Enterobacteriaceae and S. aureus on resulted in unsatisfactory microbial considerably less than counts used bottle components after feeding counts, illustrating the importance and determined in previous studies reaffirms the recommended need to need for disinfection, post cleaning. undertaken in developing countries, decontaminate bottles and components Great care needs to be taken when where counts of >106 cfu/ml were after use and before further use. cleaning and washing bottles in frequently (36–55%) enumerated from Decontamination procedures are dishwashers and washing-up water. bottles and teats.10,40 Greater required to remove pathogens to the Previous research studies have contamination levels in previous point where they are no longer capable detected up to 105 cfu/ml ACCs and studies may be a result of the quality of of being infectious. A two-component Enterobacteriacae in washing-up water PIF as well as the reported addition of process is required for the adequate from consumer homes,35 as well as corn starch, cereal, or rice starch to the decontamination of infant feeding bottles bacterial survival in washing-up water milk.40 and components. It is considered that and contamination of items washed in Another finding of particular concern the most critical step in the cleaning and contaminated water.36 Such findings from this study was that 15% of used, disinfection process is cleaning.42 Use of not only indicate the importance of unclean bottles were contaminated with clean, hot water and detergent, followed cleaning infant bottles and components Enterobacteriaceae in at least one site by rinsing, may result in a variable in previously unused washing-up water (<100 cfu/area sampled). A previous UK reduction of microbial load, but is but also the need for a subsequent study found that 65% of PIF samples important for the removal of organic disinfection procedure. The process of contained low levels (<100 cfu/g) of at debris. Inadequate cleaning of surfaces cleaning infant feeding bottles and least one Enterobacteriaceae species.20 may inhibit the effectiveness of components in a dishwasher may also Previous research has found that more disinfection procedures – for example, present risks of extrinsic contamination than 80% of homes are contaminated hypochlorite disinfectants (used for cold as high levels of total coliforms and with Enterobacteriaceae,41 frequently water disinfection processes) are faecal coliforms have been detected in from sites in the kitchen, thus presenting inactivated by food debris, organic dishwasher water.37 sources and opportunities for cross- matter and catonic detergents.42 92 Perspectives in Public Health l March 2009 Vol 129 No 2 Downloaded from by on September 6, 2009
  10. 10. PAPER Contamination of bottles used for feeding reconstituted powdered infant formula and implications for public health Furthermore, residues of food debris or unsatisfactory levels of organic and Previous research has indicated organic matter not removed during microbial contamination. discrepancies between self-reported cleaning may be ‘baked’ onto bottle Although only a relatively small and actual food safety/hygiene surfaces when using disinfection sample size of infant feeding bottles behaviours,45 whereby self-reported procedures involving heat. This makes from one geographical area in the UK data may represent an optimistic them more difficult to remove in the was investigated, there is no reason to portrayal of actual practices.46 There is a future and provides a focus for microbial believe this is atypical. The investigation need to determine consumer and growth. did not isolate pathogens known to be caregiver behaviours and underlying This research, based on an analysis of associated with causing illness among attitudes and beliefs associated with the ‘in-use’ feeding bottles and component infants as a result of the consumption of implementation of cleaning and parts used for PIF, provides important, reconstituted PIF, however, this is not disinfection practices. relevant and current data regarding the surprising given the sample size. Cumulatively, an improvement in microbiological status associated with Additional research including a consumer and caregiver cleaning and the need for cleaning and disinfection quantitative microbial risk assessment disinfection practices could result from a effectiveness. The findings expand on of a range of hazards linked to PIF and working partnership between disinfection previous studies by reporting organic feeding bottles would be useful but unit/product manufacturers, health debris contamination, which facilitates would require sampling of a much larger professionals, educators, caregivers and microbial survival and also provides number of bottles. This type of research parents. However, data from studies nutrients for microbial growth. Results would also include reviewing such as this, and further research have highlighted contamination of used microbiological effectiveness on different involving observation and psychological bottles and component parts after use methods of cleaning and disinfecting data, could be used to inform an (before cleaning and disinfection); this feeding bottles and equipment, used in audience-centred approach to re-enforce was not surprising, yet highlights the the home and caregiver environments, messages to parents and caregivers to need for effective decontamination which is known to be lacking.16,44 Self- implement good hygiene practices, before further use. However, a large reported data was collected from including the effective cleaning of items number of bottles and component parts parents and day nursery staff on the before disinfection and the need to follow considered ‘ready to re-use’, post history of feeding bottle use and manufacturers’ guidelines for the cleaning/disinfection, were found to have cleaning and disinfection practices. disinfection process. References 1 Bolling K, Grant C, Hamyln B, Thornton A. 7 Harmsen H, Gatherer A. Infant feeding 14 Health Protection Agency. National Infant Feeding Survey 2005: Part 5 The use bottle hygiene in two countries. The Standard Methods. London: Health of milk other than breast milk. London: Medical Officer 1968; 26 April: 226–227 Protection Agency, 2007. http://www.hpa- National Statistics/The Information Centre, 8 Anderson A, Gatherer A. Hygiene of infant 2007 feeding utensils. Practices and standards 15 Griffith CJ. Improving surface sampling and 2 Forsythe S. Enterobacter sakazakii and in the home. British Medical Journal 1970; detection of contamination. In: Lelieveld HLM, other bacteria in powdered infant formula 2: 20–23 Mostert MA, Holah J, editors. Handbook of milk. Maternal & Child Nutrition 2005; 1: 9 Creagh A, Foley B, O’Connor J, Barry R, Hygiene Control in the Food Industry. 44–50 Thackray P, Duke A. The domestic Cambridge: Woodhead Publishing, 2005 3 Food Agriculture Organization/World sterilization of feeding bottles. Journal of 16 Redmond EC, Griffith CJ. Comparison of Health Organization. Enterobacter sakazakii the Irish Medical Association 1978; 71(13); disinfection methods used for and other micro-organisms in powdered 452–454 decontamination of infant bottles used for infant formula: Meeting report, MRA Series 10 Tenssay LW, Tesfaye H. Bacteriological feeding powdered infant formula. Journal 6. Geneva: World Health Organization, quality of infant feeding bottle contents and of Family Health Care 2009;19(1): 26–31. 2004. teats in Addis Ababa, Ethiopia. Ethiopian 17 Department of Health. Bottlefeeding. publications/micro/mra6/en Medical Journal 1992; 30(2): 79–88 London: COI Publications, 2006 4 Smith JL. Review: Foodborne infections 11 Surjono D, Ismadi SD, Suwardji, Rohde JE. 18 Gatherer A, Wood N. Home standards of during pregnancy. Journal of Food Bacterial contamination and dilution of milk sterilization of infant feeding bottles and Protection 1999; 62(7): 818–829 in infant feeding bottles. Journal of Tropical teats. Monthly Bulletin of the Ministry of 5 World Health Organization. Guidelines: Pediatrics. 1980; 26(2): 58–61 Health and Public Health Laboratory Safe preparation, storage and handling of 12 Malhotra NK, Birks DF. Marketing Service 1966; 25: 126–130 powdered infant formula. Geneva: Research: An Applied Approach. London: 19 World Health Organization. Global trategy WHO/FAO, 2006. Prentice Hall, 2000 for Infant and Young Child Feeding. foodsafety/publications/micro/pif2007/en 13 Harrigan WF. Laboratory Methods in Food Geneva: World Health Organization, 2003. 6 Worsfold D. Food safety for babies. Microbiology. 3rd Edition. London: Nutrition & Food Science 1996; 6: 20–24 Academic Press, 1998 strategy/en/index.html March 2009 Vol 129 No 2 l Perspectives in Public Health 93 Downloaded from by on September 6, 2009
  11. 11. PAPER Contamination of bottles used for feeding reconstituted powdered infant formula and implications for public health 20 Mullane NR, Iversen C, Healy B, Walsh C, 29 Boots the Chemist. Personal London: Food Standards Ageny, 2006. Whyte P, Wall PG, Quinn T, Fanning S. Communication, 2007 Enterobacter sakazakii: An emerging 30 Choice. Bottlefeeding equipment. newsarchive/2006/dec/infantform bacterial pathogen with implications for Marrickville: Choice, 2007. 39 Central Office of Information, Food infant health. Minerva Pediatrics 2007; Standards Agency. Powdered Infant 59(2): 137–148 31 Mainstone A. Domestic hazard analysis of Formula Qualitative Research: Final Report. 21 Iversen C, Forsythe S. Isolation of infant feeding utensils. British Journal of Define Research and Insight. London: COI, Enterobacter sakazakii and other Midwifery 2004; 12(6): 368–372 2006. Enterobacteriaceae from powdered 32 Le Loir Y, Baron F, Gautier M. uk/multimedia/pdfs/powderinfantform.pdf infant milk formula and related Staphylococcus aureus food poisoning. 40 Morais TB, Morais MB, Sigulem DM. products. Food Microbiology 2004; 21: Genetics and Molecular Research 2003; Bacterial contamination of the lacteal 771–777 2(1): 63–76 contents of feeding bottles in metropolitan 22 Nazarowec-White M, Farber JM. 33 Chen Y, Jackson KM, Chea FP, Schaffer Sao Paulo, Brazil. Bulletin of the World Incidence, survival and growth of DW. Quantification and variability analysis Health Organization 1998; 76(2): 173–181 Enterobacter sakazakii in infant formula. of bacterial cross-contamination rates in 41 Worsfold D, Griffith CJ. An assessment of Journal of Food Protection 1997; 60(3): common food service tasks. Journal of cleanliness in domestic kitchens. Hygiene 226–230 Food Protection 2001; 64(1): 72–80 and Nutrition in Foodservice and Catering 23 Vasavada PC. Enterobacter sakazakii: The 34 Redmond EC, Griffith CJ. An analysis of 1996; 1: 163–173 quest for tests. Food Safety Magazine ‘in-use’ infant feeding bottles and a 42 European Society of Gastrointestinal 2005; August/September comparison of four bottle disinfection Endoscopy/European Society of 24 Kandhai MC, Reij MW, Gorris LG, methods. Confidential report. Thouars: Gastrointestinal Endoscopy Nursing and Guillaume-Gentil O, Van Schothorst M. Laboratoires Rivadis, 2007. Associates. Technical Note on Cleaning Occurrence of Enterobacter sakazakii in 35 Mattick K, Durham K, Hendrix M, Slader J, and Disinfection. St Laurent du Var Cedex: food production environments and Griffith C, Sen M, Humphrey T. The micro- ESGE, 2003. households. Lancet 2004; 363: biological quality of washing-up water and downloads/pdfs/guidelines/technical_ 39–40 the environment in domestic and commer- note_on_cleaning_and_disinfection.pdf 25 Chief Medical Officer. Revised guidance on cial kitchens. Journal of Applied 43 Ayliffe G, Collins B, Pettit F. Contamination preparation and storage of infant formula Microbiology 2003; 94(5): 842–848 of infant feeds in a Milton milk kitchen. milk. London: Department of Health, Social 36 Mattick K, Durham K, Domingue G, Lancet 1970; 14 March: 559–560 Services and Public Safety, 2006. Jørgensen F, Sen M, Schaffner D, 44 Renfrew MJ, McLoughlin M, McFadden A. Humphrey T. The survival of foodborne Cleaning and sterilization of infant feeding ph_hss(md)_11_-_2006.pdf pathogens during domestic washing up equipment: A systematic review. Public 26 Soderhjelm L. Infant feeding hygiene in and subsequent transfer onto washing-up Health and Nutrition 2008; 11(11): Sweden: A survey of bottle and teat sponges, kitchen surfaces and food. 1188–1199 hygiene. Acta Paediatrica Scandinavica International Journal of Food Microbiology 45 Redmond EC, Griffith CJ. Consumer 1972; 61; 565–570 2003; 85(3): 213–226 food-handling in the home: A review of 27 Farquhar JW, Gould JC, Schutt WH. A 37 Casanova LM, Gerba CP, Karpiscak M. food safety studies. Journal of Food ‘cold method’ of feed preparation for Chemical and microbial characterization of Protection 2003; 66(1): 130–161 newborn infants in a maternity hospital. household graywater. Journal of 46 Redmond EC, Griffith CJ. A comparison Lancet 1965; 1 May: 951–953 Environmental Science and Health 2001; and evaluation of research methods used 28 Anon. Milton Sterilizing Tablets – Hygiene 36: 395–401 in consumer food safety studies. for Baby Home. Thouars: Laboratoires 38 Food Standards Agency. Revised International Journal of Consumer Studies Rivadis, 2008 Guidance on Powdered Infant Formula. 2003; 27(1): 17–33 Health and Safety at Work – Best Practice and Partnerships Wednesday 17th June, 28 Portland Place, London, W1B 1DE CONFERENCE The RSPH conference will bring together experts in Hackitt, Chair of the Health and Safety Executive, Dr their field to learn about some recent outstanding health Luise Vassie, Head of Research and Technical Services and safety projects and their successful outcomes in IOSH, Trevor Todd, Health and Safety Section Manager, the areas of workplace violence, industrial estates, care Hull City Council and Ray Pearson of the Woodward homes, work experience students and flexible warrants. Group. There will also be an update on the Slips Trips The conference will focus on practical partnerships and and Falls Report 2008 and a focus on stress at work. how Local Authorities can work with other enforcing For more information and to book your place, bodies towards successful outcomes. It will be chaired by please contact Jennifer Tatman, Conference and David Clapham Principal Environmental Health Manager, Events Officer on 020 3177 1614 Bradford Metropolitan Council. Speakers include Judith or 94 Perspectives in Public Health l March 2009 Vol 129 No 2 Downloaded from by on September 6, 2009