assessment of hand washing with new abstrat · and inadequate control is one of the factors...

J Egypt Public Health Assoc Vol. 84 No. 1 & 2, 2009

Corresponding Author: Dr Mohamed Fawzi Department of Nutrition, High Institute of Public Health, Alexandria University e.mail: [email protected]

Assessment of Hand Washing Facilities, Personal Hygiene and the Bacteriological Quality of Hand

Washes in Some Grocery and Dairy Shops in Alexandria, Egypt

Mohamed Fawzi*, Naglaa F. Gomaa*, Wafaa M.K. Bakr**

* Department of Nutrition, High Institute of Public Health, Alexandria University

** Department of Microbiology, High Institute of Public Health, Alexandria

University

ABSTRACT

Food produced with satisfactory hygienic standards is one of the

essential conditions for promoting and preserving health. A total of

15 grocery and dairy shops were randomly selected from Alexandria,

Egypt to assess their hand washing facilities and personal hygiene of

food handlers using a pre-designed sanitation checklist. Also the

bacteriological profile of the handlers’ hand washes was determined.

Only 20% of these shops were acceptable concerning their hand

washing facilities (≥≥≥≥ 50% score percentages). Observing 29 food

handlers revealed that only 3.4% of them were acceptable in their

personal hygiene with a mean score percentage of only 31.0 ± 9.2.

Although the hand washing method followed by the food handlers

significantly decreased both aerobic mesophilic and staphylococci

counts, they were still high. Moreover, fecal coliforms increased

insignificantly from 5 to 7 MPN/100ml indicating that the hand

washing was improperly done due several pitfalls. Most of the

handlers who washed their hands for less than 10 seconds (41.4%) had

higher counts of aerobic mesophiles and staphylococci than those

who washed for more 10 seconds. Most of the handlers (93.1%) did

not avoid contamination from the tap after hand washing.


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Moreover, their hand washes were contaminated with fecal

coliforms (8 MPN/100ml) and with slightly higher staphylococci

counts than those who avoid contamination either by rinsing a tap

or closing it by elbow. Recommendations: Much effort should be

done from the responsible authority to improve the sanitation inside

these shops and food handlers should be given in-service training to

know how to efficiently wash their hands.

Key words: Dairy shops, sanitation checklist, hand washing, personal hygiene,

food handlers, hand washing , staphylococci.

INTRODUCTION

Food elaborated with satisfactory hygienic standards is one

of the essential conditions for promoting and preserving health,

and inadequate control is one of the factors responsible for the

occurrence of foodborne disease outbreaks.(1) Milk and milk

products were the highest incriminated foods in microbial food

poisoning outbreaks admitted to Alexandria Poison Center from

1991-1994 (915 cases) and from August 1997 till July 1998 (103

cases).(2,3) The increasing number of food poisoning outbreaks

has led to calls for better hygiene and quality practices.(4) A study

on 30 supermarkets in Alexandria reported that only 13% of

them were acceptable concerning personal hygiene.(5)

Poor personal hygiene by food handlers frequently

contributes to outbreaks of foodborne illnesses caused by

Staphylococcus aureus (S. aureus) and gram negative bacilli such

as Salmonella spp., Shigella spp., Campylobacter jejuni,

Enterotoxigenic E. coli as well as viral agents, such as hepatitis

A, and Norovirus.(6-8) The importance of hand hygiene in the

control of infection cannot be under-emphasized.(9) Although

hand-washing may seem trivial to the food staff, failing to do it

can have tragic consequences.(10) It is generally accepted that the


73

hands of food handlers are an important vehicle of food cross-

contamination and that improved personal hygiene and

scrupulous hand washing would lead to the basic control of

feces-to-hand to-mouth spread of potentially pathogenic

transient microorganisms.(11,12)

Microorganisms on the human skin can be divided into two

groups: permanent and transitory; and the only pathogenic

microorganism in the permanent group of bacteria associated

with the human skin is S. aureus. It is not possible to fix an

acceptable contamination level for S. aureus after proper hand

washing.(13) Detection and enumeration of indicator organisms

are widely used to assess the efficacy of sanitation programs.(14)

Indicator organisms associated with hygiene practices include,

amongst others, total viable counts, total coliforms, E. coli,

members of the family Enterobacteriaceae and S. aureus.(15)

People in the food production and foodservice industries

should be well trained and motivated to follow good personal

hygiene practices, to use correct hand washing procedures and

to follow these procedures while working in order to prevent the

spread of infection.(16) The aim of the current study was to assess

the sanitary condition of the hand washing facilities in some

grocery and dairy shops in Alexandria and the level of personal

hygiene among their food handlers. Also it was designed to

explore the level of hand bacterial contamination of food

handlers and evaluate the effectiveness of their commonly used

hand-washing method in reducing hand contamination levels.

MATERIAL AND METHODS

A total of 15 shops were randomly selected from five zones of

Alexandria (El-Montazah, East, Middle, West and El-Gomrouk)


74

where three shops were selected from each zone. For each shop,

the following methods were conducted:

1- Assessment of hand washing facilities and personal hygiene

of the food handlers.

2- Determination of the bacteriological profile of the handlers’

hand washes.

1. Assessment of hand washing facilities and personal hygiene

of the food handlers

A pre-designed sanitation checklist was used for

investigating two main parameters in each shop:

- Hand washing facilities.

- Personal hygiene of the food handlers.

● Hand washing facilities

This parameter was evaluated through inspecting the hand

washing sink in each shop for the following items:

- Sink condition and design (sink material, curved corners,

cleaning, designed solely for hand washing, its repair status

and tap design).

- Water and cleaning agent.

- Hand drying method.

- Availability of posters demonstrating proper hand washing

and drying.

● Personal hygiene

This parameter was evaluated through observing 29 food

handlers who were in direct contact with the food products for

the following items and sub-items:

- Health certificates (presence and validity).


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- Uniform (head covering, protective clothing, footwear).

- Hands (clean hands, nails, presence of wounds, jewelry and

gloves).

- Effective hand washing where each handler was observed

during his usual followed way to wash and dry hands with

special attention to the following:

● Using a detergent.

● Friction of the hands, and whether it covered three

important areas namely between fingers, the finger tips

and around the wrist.

● Period of hand washing (seconds).

- Avoidance of post washing contamination from taps.

- Hand drying.

All questions in the checklist were either yes/no questions or

multiple options. Each yes/no question was scored by giving one

for the right item and zero for the wrong one. The multiple

options questions were scored from 0 to 5 with higher scores for

better options. The score of each parameter was calculated by

summing the scores of its questions that were transformed into

percentages. Shops with ≥ 50% score percentages were

considered acceptable while those with <50% were

unacceptable.(17)

2. Determination of the bacteriological profile of the handlers’

hand washes

Samples from hands of each of the 29 food handlers were

collected by asking each one to thoroughly wash his hands in a

sterile polyethylene plastic bag containing 100-ml sterile peptone

saline (0.1%) focusing on his finger tips, between fingers and

around wrist. Then, he was asked to wash his hands in his

usual way then to rewash them in another 100-ml sterile


76

peptone saline (0.1%). Ten fold serial dilutions from each sample

were prepared and subjected to the following bacteriological

examinations according to the method described in ISO 6687

(1980):(18)

● Aerobic mesophilic plate count. Standard plate count (SPC)

agar was drop plated and incubated at 30oC for 72 hours

according to ISO/DIS 4833, 1989.(19)

● Enumeration of fecal coliforms using the most probable

number technique (MPN) according to Harrigan (1998).(20)

Brilliant Green Bile broth was inoculated and incubated at

30°C for 4 hours then at 44 ± 0.2oC for 20 hours and

examined for gas production that denoted the presence of

fecal coliforms.

● Enumeration of Coagulase positive Staphylococci

according to ISO/CD 6888-1 (1995).(21) Baird-Parker agar

base supplemented with egg tullerite emulsion was surface

plated and incubated at 35-37oC for 48 hours. The suspected

colonies were transferred into brain heart infusion, incubated

for 24 hours at 37°C and subjected to tube coagulase test

according to Collee et al., (1989).(22)

Statistical Analysis

Data was statistically analyzed using SPSS program version

9.0. The cutoff point for statistical significance was P value <0.05

and all tests were two-sided. Kruskal-Wallis test was used for

comparing bacterial counts (aerobic mesophiles, staphylococci

and fecal coliforms) and score percentages of the two parameters

among different zones of Alexandria. Monte Carlo proportion was

used for comparing the percentages of acceptable shops and

handlers among different zones. Paired samples t test was used


77

to compare between mean bacterial counts before and after hand

washing while McNemar test was used to compare between

samples contaminated with fecal coliforms or coagulase positive

staphylococci. Spearman test was used to measure the

correlation between mean bacterial counts and mean score

percentages given to the used detergent, friction during washing,

period of washing and avoidance of post washing

contamination.(23)

RESULTS

Table (1) shows that only 20% of the visited shops were

acceptable concerning the parameter of hand washing facilities

with a mean score percentage of 39.2 ± 13.8. Moreover, none of

the shops in El-Montazah, West and El-Gomrouk were

acceptable. Higher acceptable percentages were found among

two of its items, 53.3% in sink condition and design and 40% in

the water and cleaning agent with higher mean score

percentages (50.9 ± 24.7 and 51.1 ± 28.5 respectively). There

were insignificant differences among different zones in the mean

score and acceptable percentages of the hand washing facilities.

A hand drying method or a poster demonstrating proper hand

washing was not available near the sink of any visited shop.

Table (2) demonstrates that only 3.4% of the observed 29

handlers were acceptable in personal hygiene with a mean score

percentage of 31.0 ± 9.2. Among its items, avoidance of post

washing contamination had the lowest acceptability (3.4%) and

none of the observed handlers wore acceptable uniforms with the

lowest mean score percentages (4.1 ± 18.8 and 5.6 ± 12.2;

respectively). The highest percentages of acceptable personal

hygiene of handlers (65.5%) were in the presence of valid health


78

certificates with the highest mean score percentages (65.5 ±

48.4). There were insignificant differences among different zones

except in the mean score of both uniform and hand drying as

well as in the percentages of acceptable handlers in hand drying

and using a detergent (p<0.05).

Table (3) shows the bacteriological profile of hand washes

before and after ordinary hand washing. Ordinary hand washing

regimes practiced by the food handlers improved the

bacteriological profile of their hand washes except the

percentages of coagulase positive staphylococci in East and EL-

Gomrouk zones that remained constant after washing (28.6%

and 14.3% respectively). The percentage and level of

contamination with fecal coliforms in the Middle zone worsened

and increased to 40% and 50 MPN/100ml respectively. Also the

level of contamination of all samples with fecal coliforms

increased insignificantly from 5 to 7 MPN/100ml. There were

insignificant differences in either the mean bacterial counts or

percentages of samples contaminated with coagulase positive

staphylococci and fecal coliforms among different zones except in

case of staphylococci count before hand washing.

Table (4) illustrates that most of the food handlers (48.3%)

washed their hands using bar soap followed by those who did

not use any detergent (34.5%) with approximately similar

bacteriological profile of their hand washes. They were

contaminated with mean fecal coliform counts of 6 and 14

MPN/100ml respectively. The bacteriological profile of the hand

washes of the two handlers (6.9%) practicing friction between

fingers, finger tips and around wrist and the five handlers

(17.2%) who rubbed two areas was approximately similar and

better than those either not practicing rubbing at all (41.4%) or


79

rubbed only one area (34.5%). Most of the handlers who washed

their hands for less than 10 seconds (41.4%) had higher counts

of aerobic mesophiles (4.3 x 106 CFU/100ml) and staphylococci

(8.5 x 105 CFU/100ml) than those who washed their hands

either for 20 seconds and more (2.4 x 106 and 7.1 x 105

CFU/100ml respectively) or for 10- 19 seconds (1.9 x 106 and 3.3

x 105 CFU/100ml). The Majority of the handlers (93.2%) did not

avoid contamination during closing the tap and their hand

washes were contaminated with fecal coliforms (8 MPN/100ml)

and slightly higher staphylococci counts (6.8 x 105 CFU/100ml)

than those who avoided contamination either by rinsing the tap

or closing it by elbow (6.0 x 105 and 2.0 x 105 CFU/100ml

respectively). There were insignificant differences among the

mean bacterial counts in hand washes collected either after

using different types of detergents, friction regimes, periods of

washing, or after different ways to avoid post washing

contamination. There were negative correlations between mean

fecal coliform counts and mean score percentages of all items of

effective hand washing, between staphylococci counts and both

of the periods of washing and avoidance of post washing

contamination as well as between aerobic mesophilic counts and

both of the periods of washing and friction during washing.

DISCUSSION

Food handlers are an important vehicle for microorganisms

and improper handling practices may cause food contamination

and consequently foodborne diseases, which pose a potential

risk to public health.(1) The present study revealed that the

visited 15 grocery and dairy shops in Alexandria confronted

problems in both sanitation of their hand washing facilities and


80

personal hygiene where only one fifth of these facilities and

about three percent of their handlers were acceptable. Also, their

followed ways to wash hands were not proper since the microbial

contamination level though reduced was still high.

Hand washing facilities

Hand washing sinks can be sources of pathogenic bacteria

because they usually contain stagnant water that supports the

growth of microorganisms, which can be transferred to hands

during hand hygiene practices.(24) The present study revealed

that only 20% of the visited shops were acceptable concerning

their hand washing facilities with a mean score percentage of

only 39.2. Moreover, about half of the shops had acceptable sink

condition and design with a mean score percentage of 50.9. The

majority of sinks were unclean, most were made of pottery with a

lot of cracks and none of them was used solely for hand washing.

Also, one of the shops was not provided with a hand washing

sink and washing hands was through using a hose.

Both bar soaps and liquid soaps may become contaminated

with bacteria during use, with bar soaps being associated with

heavier contamination compared to liquid soaps.(25) However,

other studies have suggested that these bacteria are unlikely to

be transferred to hands.(26) A lower acceptability percentage (40%)

was found in the item water and hand cleaning agent with a

mean score percentage of 51.1 since more than half of the sinks

were provided with bar soap and none of them was provided with

hot water. The FDA specifies that in order to clean their hands,

food employees shall use running warm water during their hand

washing.(27)

A sign or poster that notifies food employees to wash their

hands shall be provided at all hand washing sinks and shall be


81

clearly visible, also each sink shall be provided with disposable

towels or a heated-air hand drying device.(27) The unavailability of

a hand drying method or a poster demonstrating proper hand

washing in any of the visited shops contributed in lowering the

acceptability and the mean score percentage of the hand

washing facilities parameter. It has been reported that all food

handlers in 74.1% of the surveyed schools in Brazil did not

practice correct hand hygiene, mainly because most of the sinks

(81.5%) did not have antiseptic liquid soap or paper towels but

instead they were provided with bar soap and cloth towels that

are important vehicles for food contamination.(1)

Personal hygiene

The word hygiene usually refers to cleanliness and especially

to any practice which leads to the removal or reduction of

harmful infectious agents.(9) A study in the USA suggested that

improper food handling practices in food serving establishments

contributed to 97% of foodborne illnesses, thus employees

should pay attention to their personal hygiene.(28) The level of

personal hygiene in the visited shops needs rapid intervention

from both of the responsible authorities and food handlers to

ensure the safety of their food products. The mean score

percentage of this parameter was only 31 with a very low

percentage of acceptability among shops (3.4%). This can be

attributed to several serious defects in the uniform, hand

washing, avoidance of post washing contamination and hand

drying items.

None of the observed handlers wore acceptable uniforms

with a mean score percentage of 5.6 since few handlers wore

clean and light colored uniforms. Others reported that only 6.7%

of the food handlers were wearing clean light colored uniform.(5)


82

Many of the studies conducted have proven that it is

imperative to care about personal hygiene, and especially hand

cleanliness.(29,30) Hand-washing which is a simple and effective

way to cut down on cross-contamination is too often forgotten.(31)

It seems that the hand washing method followed in the present

study was improper since its mean score percentage was only

39.2, and the practices of less than one third of the handlers

(31%) were acceptable. All observed food handlers washed their

hands with tap water, about half of them (48.3%) used bar soap

and friction of the hand areas (between fingers, finger tips,

around wrist) was either not practiced at all (41.4%) or only one

area was rubbed (34.5%). Moreover, only 37.9% of the observed

handlers washed their hands for more than 20 seconds. The US

FDA stated that food employees shall clean their hands and

exposed portions of their arms for at least 20 seconds while

paying attention to removing soil from underneath the fingernails

and creating friction on the surfaces of the hands and arms,

finger tips, and areas between the fingers.(27)

It is worth mentioning that the majority of the observed

handlers failed to avoid contamination of their hands after

washing (93.1%) and the rest used to either closing the tap by

elbow or rinsed the tap with water alone that is considered

insufficient to remove the microbial contaminants. To avoid

recontaminating hands after washing, food employees may use

disposable paper towels or similar clean barriers when touching

surfaces such as manually operated faucet handles. (27)

Hand drying is an essential component of effective

handwashing. Damp hands as a result of ineffective hand drying

can lead to skin excoriation which in turn leads to higher

numbers of bacteria colonizing the skin and facilitating the


83

spread of microorganisms.(9) Less than half of the observed

handlers (48.3%) had acceptable level concerning their hand

drying with a mean score percentage of 33.1 since most of them

dried their hands either in papers used for wrapping food

products, in a piece of clothes or in a yellow towel where their

microbial quality is questionable and requires further studies.

Cloth towels are not recommended because of evidence that

microorganisms are less effectively removed. There is also the

risk of cross contamination.(32) Soft, absorbent paper towels are

more acceptable to users and may contribute to compliance with

hand hygiene recommendations.(33)

None of the observed handlers wore gloves during handling

of food products but instead use bare hands, knives or the

wrapping plastic sheaths. A considerably significant amount of

bacteria have been found on bare hands compared with the

amount of bacteria on gloved hands.(34) In 2003, the investigation

of 18 dairy shops in Alexandria showed that all food handlers

used ungloved hands during handling of dairy products.(17) So

much efforts are required from the responsible food control

authority to enforce careful use of gloves.

Bacteriological profile of the handlers’ hand washes

Microorganisms are transferred to the hands in the process

of handling food and through poor personal hygiene resulting in

the hands being heavily contaminated with enteric pathogens.(35)

Although the hand washing method followed by the food

handlers significantly decreased both aerobic mesophilic and

staphylococci counts, they were still high. Moreover, fecal

coliforms increased insignificantly from 5 to 7 MPN/100ml

indicating that the hand washing was improperly done due to

several pitfalls in one or more of the followings; the type of the


84

used detergent, friction regimes during hand washing, the period

of hand washing or avoidance of post hand washing

contamination. A study in Iran (2006) reported that correct hand

hygiene resulted in a microbial reduction from 72.7% to 32%.(10)

Most of the observed handlers washed their hands either

without any detergent at all (34.5%) or used bar soap (48.3%)

where washes collected after their hand washing were


MPN/100ml; respectively.

Regarding friction regimes during hand washing, about three

quarters of handlers were either not practicing rubbing between

fingers, finger tips and around wrist or rubbed only one area.

Their hand washes were contaminated with higher aerobic

mesophilic and staphylococci counts than washes collected from

those who rubbed three or two areas. Also they were


MPN/100ml; respectively. Detection of fecal coliforms

characterizes a situation of potential risk, owing to the

interrelation of these bacteria and the possible occurrence of

enteric pathogens.(1)

Concerning the period of hand washing, 41.4% of the

handlers washed their hands for less than 10 seconds while

20.7% washed for 10-19 seconds and those who washed for less

than 10 seconds were contaminated with higher counts of

aerobic mesophilic and staphylococci than those who washed

their hands either for 20 seconds and more or for 10-19 seconds

but without significant variations among them. Washes collected

after hand washing for these three periods were unfortunately

contaminated with fecal coliforms ranging between 5 and 8

MPN/100ml. This suggests a problem of post hand washing


85

contamination that was unfortunately observed among 93.1% of

the handlers where their hand washes were contaminated with a

mean fecal coliform count of 8 MPN/100ml.

Staphylococci are ubiquitously distributed in the

environment and strains present in the nose often contaminate

the back of hands, fingers and face, and nasal carriers could

therefore easily become skin carriers.(35) Although the hand

washing followed in the present study reduced the

contamination with coagulase positive Staphylococci, 10.3% of

the hand washes were still contaminated. Information from

staphylococcal food poisoning outbreaks indicates that strains of

Staphylococcus aureus isolated from specimens of vomitus and

faeces were identical with those from the implicated food and

from the hands and often the nose of a food handler.(36)

Fecal coliforms are among the transient hand flora that can

be easily removed by hand washing.(9) Their presence indicates

fecal contamination and food handlers are not taking enough

care in hand hygiene.(13) The hand washing regime followed by

the food handlers in the present study failed to free their hands

from the fecal coliforms but instead it increased the percentage

of contaminated hand washes to reach about 14%. This can be

attributed to either inefficient hand washing or post hand

washing contamination. Another study reported that Escherichia

coli was isolated from 7.8% of the hand samples.(37)

RECOMMENDATIONS

Much effort should be done from the responsible authority to

improve the sanitation inside the grocery and dairy shops in Alexandria

focusing on personal hygiene of their handlers. Food handlers should

be given in-service training to know how to efficiently wash their hands.


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