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

Perspectives in Public Health
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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

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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
ac.uk ‘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

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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


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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


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‘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



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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



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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



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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



PAPER


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



PAPER


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.

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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 jtatman@rsph.org.uk



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

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