- Email: [email protected]
Bacterial assessment of food handlers in Sari City, Mazandaran Province, north of Iran
JIPH-575; No. of Pages 6
ARTICLE IN PRESS
Journal of Infection and Public Health (2016) xxx, xxx—xxx
Bacterial assessment of food handlers in Sari City, Mazandaran Province, north of Iran Mohtaram Nasrolahei a, Siavash Mirshafiee b,∗, Soudeh Kholdi a, Maryam Salehian a, Masoumeh Nasrolahei a a
Department of Microbiology, Mazandaran University of Medical Sciences, Sari 4847191971, Iran b Husbandry Department, Ghaemshahr Branch of Islamic Azad University, 8456491896, Iran Received 14 July 2015 ; received in revised form 11 February 2016; accepted 4 March 2016
KEYWORDS Food handlers; Hand washing practice; Nasal carrier; Fingernail contents
Abstract Food handlers with poor personal hygiene could be potential sources of infection due to pathogenic bacteria. This study was designed to determine the prevalence of bacterial infestation among the food handlers attending the public health center laboratory in Sari, northern Iran for annual check-up. This study was performed from September 2013 to August 2014. Stool samples, fingernail specimens of both hands and nasal swabs were collected from 220 male and female food handlers of different jobs, aged between 17—65 years. The samples were cultured on bacteriological culture media and bacterial species were identified following standard procedures. A structured questionnaire was used to record sociodemographic and behavioral data analysis of the food handlers. Of the total 220 subjects examined, 62.2% showed positive culture for different bacterial species from their fingernail contents, 65.4% were found to be harboring Staphylococcus aureus in their nostrils and 0.9% tested positive for Shigella boydii from stool samples. Staphylococcus aureus was the predominant bacteria isolated from fingernail specimens (46%), followed by Escherichia coli (29.2%), Coliforms (18.2%) and Pseudomonas aeruginosa (6.6%). This study showed a statistically significant difference in the rate of bacterial infestation between different occupational categories (p = 0.04). Butchers showed the highest prevalence of bacteria (86.6%) in their fingernail contents, followed by fast food workers (76.5%), bakers (73.5%), chicken store workers (73%), school cafeterias staff (53.3%), restaurant workers (46.9%) and fruit/vegetables sellers (42.5%). The highest rate of nasal carrier for Staphylococcus aureus was observed among chicken store workers 14/17(20.8%).
∗
Corresponding author at: Husbandry Department, Ghaemshahr Branch of Islamic Azad University, 8456491896, Iran. Tel.: +98 11456760314; fax: +98 2595435326. E-mail addresses: [email protected], dr.mirshafi[email protected] (S. Mirshafiee). http://dx.doi.org/10.1016/j.jiph.2016.03.006 1876-0341/© 2016 Published by Elsevier Limited on behalf of King Saud Bin Abdulaziz University for Health Sciences.
Please cite this article in press as: Nasrolahei M, et al. Bacterial assessment of food handlers in Sari City, Mazandaran Province, north of Iran. J Infect Public Health (2016), http://dx.doi.org/10.1016/j.jiph.2016.03.006
JIPH-575; No. of Pages 6
ARTICLE IN PRESS
2
M. Nasrolahei et al. These findings indicate the need for intensive training/retraining and health education of all food service employees and strengthening the existing screening methods to control the problem of bacterial infestation in food handlers. © 2016 Published by Elsevier Limited on behalf of King Saud Bin Abdulaziz University for Health Sciences.
Introduction Diarrheal diseases, mostly caused by foodborne or waterborne microbial pathogens, are considered as leading causes of illness and deaths in developing countries, killing an estimated 1.9 million people annually at the global level. Even in developed countries, an estimated one-third of the populations are affected by microbiological foodborne diseases each year [1]. Food handlers also known as food vendors are vital components in the interaction between the cooking environment and the food which is being either prepared or served. WHO (1989) defined food handlers as those who, in the course of their normal routine work, handle food or items that may come into contact with food, such as eating and drinking utensils not meant for their personal use [2]. Transmission of intestinal enteropathogenic bacteria is affected directly or indirectly through objects contaminated with feces. These include food, water, nails and fingers, indicating the importance of fecal-oral human-to-human transmission. Food handlers who harbor and excrete enteropathogenic bacteria may contaminate foods from their feces via their fingers, then to food processing, and finally to healthy individuals [3]. Compared to other parts of the hand, the area beneath fingernails can be the vector to spread harmful microorganisms through cross contamination [4]. A number of outbreaks of viral and bacterial infections have already been shown to have been initiated by infected food handlers [5,6]. Therefore, it is extremely important to have regularly scheduled check-ups so that infected employees can be immediately excluded from work involving direct contact with food products and can be appropriately treated. Accordingly, Food handlers with poor personal hygiene working in food service establishments could be potential sources of infection due to pathogenic organisms [7]. Therefore, a proper screening procedure is helpful to diagnose food handlers, thus preventing probable morbidity and protecting the health of the consumers. According to National Food Safety Standards in Iran, all food handlers should receive health
certificate annually. So, food handlers must go under annual microbial examination and should take part in training courses regarding food safety prior to receive their health certificate. This study was established to determine the prevalence of bacteria among food handlers working in food service setting attending the public health center for annual check-up in Sari, northern Iran.
Materials & methods This study was conducted on all 220 food handlers attending to Health Center Diagnostic Laboratory in Sari, northern Iran from September 2013 to August 2014. Sari lies at the center of Mazandaran province in northern Iran (lat.35◦ 58—36◦ 50 N, long. 52◦ 56—53◦ 59 E) and has a population of approximately 261,293 individuals. The study was carried out on food handlers of different jobs from different geographical areas in Sari city. Written consent was obtained from health center administration and participants. The food handlers who did not take treatment for any intestinal ailment within three months prior to the study were included. A structured questionnaire was used for collecting information on age, gender, educational status, income level and hand washing practices of the individuals under study. Stool, fingernail content samples and nasal swab were collected from each food handler and transferred to the microbiology laboratory at Sari Medical School for laboratory examinations. All the samples were cultured into the plates of Blood agar (Padtan- teb), MacConkey agar (Q-lab) and Salmonella-Shigella agar (Oxoid). Sorbitol—MacConkey agar (Oxoid) was added to identify Enterohemorrhagic Escherichia coli (E.coli). Bacteria were purified and identified using standard laboratory methods [8].
Statistical analysis Simple proportion, the Chi-square and Fisher’s exact tests were used to assess the difference
Please cite this article in press as: Nasrolahei M, et al. Bacterial assessment of food handlers in Sari City, Mazandaran Province, north of Iran. J Infect Public Health (2016), http://dx.doi.org/10.1016/j.jiph.2016.03.006
ARTICLE IN PRESS
JIPH-575; No. of Pages 6
Bacterial assessment of food handlers in Sari City, Mazandaran Province, north of Iran Table 1 Socio-demographic characteristics of food handlers in Sari City, northern Iran, 2013—2014. Variable Age group (years) <19 20—49 >50 Gender Male Female Educational status Illiterate Grade 1—6 Grade 7—12 University educated Occupation Bakers Chicken store workers School cafeterias staff Butchers Fruits/vegetables sellers Restaurant workers Fast food workers Hand washing practice after toilet use Yes No Income level ≤200 US $ >200 US $
Frequency
Percentage
5 173 42
2.3 78.7 19
150 70
68.2 31.8
38 33 131 18
17.3 15 59.5 8.5
49 37 30 15 40
22.3 16.8 13.6 6.8 18.2
32 17
14.5 7.8
90 130
41 59
142 78
64.5 35.4
between the variables. The significant level was 5%. SPSS 18 software was used for statistical analysis.
Results In this study, 150 (68.2%) males and 70 (31.8%) females with age range of 17—65 years (mean ages 33 ± 15 years) were examined. All Food handlers employing in different food establishments attending to Health Center Diagnostic Laboratory in Sari gave good response to take part in this survey. The majority of food handlers were young adults aged from 20 to 49 years (Table 1). The participants were divided into seven groups according to the nature of occupational duties. The subjects under study were 49 (22.3%) bakers, 40 (18.2%) fruits/vegetables sellers, 37 (16.8%) chicken store workers, 32 (14.5%) restaurant workers, 30 (13.6%) school cafeterias staff, 17 (7.8%) fast food workers and 15 (6.8%) butchers. Of the 220 food handlers examined, 62.2% (n = 137) were carrier of some pathogenic bacteria in their fingernails. The number of positive cultures from fingernail contents were higher among female
3
subjects (51/70, 72.8%) than those of male subjects (86/150, 57.3%), but the difference was not statistically significant (p > 0.05).The bacteria isolated were Staphylococcus aureus (46%), Escherichia coli (29.2%), Klebsiella species (5.8%), Pseudomonas aeruginosa (6.6%), Citrobacter species (5.1%), Enterobacter species (4.8%) and Proteus species (2.5%). None of the food handlers showed positive culture for Salmonella and Shigella in respect of their fingernail specimens (Table 2). About 65% of the subjects under study (n = 144) were carrier of S. aureus in their nostrils (Table 3). No more than one enteric bacterium was observed in the subject under study. The occurrence of bacterial infestation was different in seven occupational categories. Butchers had the highest number of carriers of bacteria in respect of their fingernail 13/15 (86.6%), followed by fast food workers 13/17 (76.5%), bakers 36/49 (73.5%), chicken store workers 27/37 (73%), school cafeterias staff 16/30 (53.3%), restaurant workers 15/32 (46.9%) and fruits/vegetables sellers 17/40 (42.5%). The highest number of nasal carrier for S. aureus was observed among chicken store workers 30/37 (20.8%), followed by bakers 27/49 (18.7%), school cafeterias staff 20/30 (13.8%), fruits/vegetables sellers 24/40 (16.6%), restaurant workers 20/32 (13.8%), fast food workers 14/17 (9.7%) and butchers 9/15 (6.25). As shown in Table 2, factors related to bacterial infestation included educational level (p = 0. 005), hand washing practice after using toilet (p = 0.001) and income level (p = 0.001). In this study, illiterate food handlers who comprised 17.3% of the total subjects under study, showed the highest rate of bacterial infestation (86.8%). Stool cultures revealed the isolation of Shigella boydii from two food handlers (0.9%). No other enteropathogenic bacteria were isolated from stools specimens.
Discussion Several authors have emphasized the importance of food handlers with poor personal hygiene as threats in the transmission of bacterial diseases [9—14]. In this survey of 220 food handlers examined, 62.2% (n = 137) were carrier of some pathogenic bacteria mainly S.aureus, P.aeroginosa and S.boydii in their fingernails and 65.4% (n = 144) were found to be harboring S.aureus in their nostrils. Our results are in agreement with previous studies reported from other parts of the country [15] and are similar to findings of Humodi et al. from
Please cite this article in press as: Nasrolahei M, et al. Bacterial assessment of food handlers in Sari City, Mazandaran Province, north of Iran. J Infect Public Health (2016), http://dx.doi.org/10.1016/j.jiph.2016.03.006
JIPH-575; No. of Pages 6
ARTICLE IN PRESS
4
M. Nasrolahei et al. Table 2 Frequency and type of bacteria isolated from fingernail contents of food handlers in Sari, northern Iran, 2013—2014. Variable
Gender Male Female Occupation Fast food workers Butchers Chicken store workers Restaurant workers Bakers School cafeterias staff Fruit/vegetables sellers Educational status Illiterate Grade 1—6 Grade 7—12 University educated Economic status ≤ 200 US $ >200 US $ Hand washing practice after toilet use Yes No Total
Bacteria frequency (%)
Total positive (%)
S.aureus
E.coli
35(40.7) 28(55)
30(34.9) 16(18.6) 10(19.6) 9(17.6)
Coliform
p value
P.aeroginosa 5(5.8) 4(7.8)
86(57.3) 51(72.8)
0.31
5(38.5) 2(15.3) 4(14.8) 3(9.4) 6(23) 2(12.5) 3(17.6)
— 1(8) 1(9) — 3(11.5) 1(6.2) 3(17.6)
13(76.5) 13(86.6) 27(73) 15(46.9) 36(73.5) 16(53.3) 17(42.5)
0.04*
20(60.6) 17(68) 25(34.2) 1(16.6)
4(12.1) 5(15.1) 5(20) 3(12) 30(41) 13(17.9) 1(16.6) 4(66.6)
4(12.1) — 5(6.8) —
33(86.8) 25(75.7) 73(55.7) 6(33.3)
0.005*
39(41.9) 24(54.5)
29(31.2) 19(20.4) 11(25) 6(13.6)
6(6.5) 3(6.8)
93(67.9) 44(32.1)
0.001*
11(36.7) 52(49) 63(46)
9(30) 6(20) 31(28.80 19(17.7) 40(29.2) 25(18.2)
4(13.3) 5(4.5) 9(6.6)
30(33.30 107(82.3) 137(62.2)
0.001*
3(23) 8(61.5) 13(20.6) 7(21.8) 20(55.5) 8(50) 4(23.5)
5(38.5) 2(15.3) 9(22.5) 5(15.6) 7(26.9) 5(31.2) 7(41.2)
*Statistically significant at p < 0.05.
Sudan who reported S. aureus as the most common pathogen isolated from food handlers [16]. However, some studies have reported a lower rate of infestation [17]. High prevalence of S. aureus in this study was because it is the true pathogenic bacteria included in the resident micro-flora of the skin and 40—50% of healthy peoples carry S .aureus in the anterior nostrils of the nose [18]. Food handlers
can easily contaminate food with S aureus (common cause of food poisoning), if they sneeze or cough during food preparation and if they do not wash their hands properly after making contact with their nose or after using toilet [19,20]. Our findings showed a significant difference in the rate of bacterial infestation between different occupational categories (Fisher exact p = 0.04) and
Table 3 The rate of nasal carrier for Staphylococcus aureus among seven occupational categories of 220 food handlers in Sari, northern Iran, 2013—2014. Variable Gender Male Female Occupation Bakers Chicken store workers School cafeterias staff Butchers Fruits/vegetables sellers Restaurant workers Fast food workers Total
Total examined n (%)
Positive (%)
150(68.2) 70(31.8)
95(63.3) 49(70)
49(22.3) 37(16.8) 30(13.6) 15(6.8) 40(18.2) 32(14.5) 17(7.8) 220(100)
27(55.1) 30(81) 20(66.6) 9(60) 24(60) 20(62.5) 14(82.3) 144(65.4)
p value 0.45
>0.05
Please cite this article in press as: Nasrolahei M, et al. Bacterial assessment of food handlers in Sari City, Mazandaran Province, north of Iran. J Infect Public Health (2016), http://dx.doi.org/10.1016/j.jiph.2016.03.006
JIPH-575; No. of Pages 6
ARTICLE IN PRESS
Bacterial assessment of food handlers in Sari City, Mazandaran Province, north of Iran the level of education (p = 0.005). Taking continuous training and health education, have good knowledge on food safety, presence of running water, access to toilet facilities and operate in clean area could lead to the difference in the rate of bacterial infestation between different categories of food handlers in this study as was shown by AbdulMutalib et al [21]. The presence of P. aeruginosa in the fingernails of the subjects may be as a result of contact with contaminated raw products such as raw meat, poultry, fish, unwashed fruits and vegetables as reported earlier [22]. In this study, subjects were supposed to be more health conscious than usual practice which was one of our survey limitations. Despite the awareness of annual check -up, the rate of bacterial infestation was high in food handlers, which reflects poor personal hygiene practice and environmental sanitation, lack of supply of safe water and ignorance of health promotion practices. According to our findings, food handlers, hand washing practices after toilet use, were lower (90/220, 41%) than those reported by others [23,24] and significantly increased the rate of bacterial infestation (p = 0.001). Reduced hand washing practice after using toilet in our investigation, might have been confounded by the fact that most food handlers were individuals from the lower socioeconomic class with a low income level. In this survey, the highest rate of bacterial infestation were identified among individuals with low income level (p = 0.001); hence, it is estimated that the better the living conditions, the lower the prevalence rates. In this study, no significant difference in the rate of bacterial infestation was identified between two sexes (p > 0.05). Stool cultures of two food handlers were positive for S.boydii. The low frequency of S.boydii recorded in this study, is in line with that previously reported by Alwia [25], who found that only 10 of 400 (2.5%) patients with diarrhea tested positive for the pathogen. However, these carriers may spread the pathogen via food to consumers and may lead to outbreaks of bacillary dysentery. One limitation of our study was that, although all food handlers were included in the study, the sample size was small, and it was thus unable to use advanced analysis to make associations.
5
bacterial infestation in food handlers was high in this survey. An effective means of preventing the transmission of pathogens from food handling personnel via food consumers is strict adherence to good personal hygiene and to hygienic food handling practices. These findings indicate the need for protective enforcement including rising awareness about foodborne diseases, intensive training/retraining and health education of all food service employees and strengthening the existing screening methods to control the problem of bacterial infestation in food handlers.
Funding source Research deputy of Mazandaran University of Medical Sciences, provided financial support for the conduct of the research but had no involvement in study design, in the collection of data, in the writing of the report and etc.
Competing interests None declared.
Ethical approval Annual check-up of food handlers is Public Health Center policy in the country. It is to notify that this survey is supported by the research deputy of Mazandaran University of Medical Sciences which attends Public Health Center and supervises annual check-up of food handlers in Sari city, so there was no need for approval ethics to be issued for this study.
Acknowledgments The authors acknowledge the research deputy and laboratory staff who helped us while performing this study. Sincere thanks also to the participating food handlers in Sari city and its suburb, for their kind cooperation during the study.
References Conclusions Although educational and legal efforts to promote food safety are active in this area, still the rate of
[1] Schlundt J, Toyofuku H, Jansen J. Emerging food-borne zoonoses. Rev Sci Tech 2004;23:513—5. [2] Fendler EJ, Dolan MJ, Williams RA. Hand washing and gloving for food protection: Part I. Examination of the evidence. Dairy Food Environ Sanit 1998;18:814—23.
Please cite this article in press as: Nasrolahei M, et al. Bacterial assessment of food handlers in Sari City, Mazandaran Province, north of Iran. J Infect Public Health (2016), http://dx.doi.org/10.1016/j.jiph.2016.03.006
JIPH-575; No. of Pages 6
ARTICLE IN PRESS
6
M. Nasrolahei et al.
[3] WHO- Prevention and control of intestinal parasitic infections. World Health Organization, Geneva.1987; pp. 7—18. (Technical report series no.749). [4] Bas M, Ersun AS, Kivanc G. The evaluation of food hygiene knowledge, attitudes and practices of food handlers in food business in Turkey. Food Control 2006;17(4):317—22. [5] Shinkawa N, Noda M, Yoshizumi S, Tokutake Y, Shiraishi T, Arita-Nishida T. Molecular epidemiology of noro viruses detected in food handler associated outbreaks of gastroenteritis in Japan. Intervirology 2008;51:422—6. [6] Stein-Zamir C, Tallen-Gozani E, Abramson N, Shoob H, Yishai R, Among V, et al. Salmonella enterica outbreak in a banqueting hall in Jerusalem: the unseen hand of the epidemiological triangle. Israel Med Assoc J 2008;11:94—6. [7] WHO- Health surveillace and management procedures of food-handling personnel. World Health Organization, Geneva 1989. pp. 1—46. (Technical Report Series no.785). [8] Barrow GI, Feltham RKA. Characters of gram- negative bacteria. In: Cowans, Steels, editors. Manual for identification of medical bacteria. UK: Cambridge University Press; 2003. p. 6, 130—1. [9] Al-Lahham AB, Abu-Saud M, Shehabi AA. Prevalence of Salmonella, Shigella and intestinal parasites in food handlers in Irbid, Jordan. J Diarrhoeal Dis Res 1990;8(4):160—2. [10] Oteri T, Ekanem EE. Food hygiene behavior among hospital food handlers. Public Health 1989;103(3):153—9. [11] Yamada S, Matushita S, Kudoh Y. Recovery and its evaluation of Shigella bacilli or Salmonella from healthy food handlers in Tokyo (1961—1997). Kansenshogaku Zasshi 1999;73:758—65. [12] Wiwanitkit V, Assawawitoontip S. High prevalence of positive culture and parasites in stool samples of food handlers in a Thai hospital setting. Med Gen Med 2002;4:8. [13] Hundy RL, Cameron S. An outbreak of infections with a new Salmonella phage type linked to a symptomatic food handler. Commun Dis Intell 2002;26:562—7. [14] Feglo PK, Frimpong EH, Essel-Ahun M. Salmonellae carrier status of food vendors in Kumasi, Ghana. East Afr Med J 2004;81:358—61. [15] Fallah M, Sadeghian S, Taherkhani H, Habibi F, Barghi ZH. Study of parasitic and bacterial infections in the
[16]
[17]
[18]
[19]
[20]
[21]
[22]
[23]
[24]
[25]
food-handling personnel, Hamadan, Iran. J Res Health Sci 2004;4:3—10. Humodi AS, Hatim HH. Bacteriological and parasitological assessment of food handlers in the Omdurman area of Sudan. J Micbiol Immunol Infect 2010;43(1):70—3. Soto A, Saldias ME, Oviedo P, Fernandez M. Prevalence of Staphylococcus aureus among food handlers from a metropolitan university in Chile. Rev Med Chile 1996;124:1142—6. Redway K, Knights B, Bozoky Z, Theobald A, Hardcastle S. Hand drying: a study of bacterial types associated with different hand drying methods and with hot air dryers. Applied Ecology Research Group, University of Westminster. London, UK. 14. Brodie, J 1965. Hand hygiene. Scot Med J 1994;10(1):115—25. Brooks GF, Butel JS, Morse SA. Medical microbiology. 21st ed. New York: Lange Medical Books/McGraw-Hill Medical publishing Division; 1998. p. 466. Isara AR, Isah EC, Lofor PVO, Ojide CK. Food contamination in fast food restaurants in Benin city, Edo state, Nigeria. Implication for food hygiene and safety. J Pub Health 2010:471. Abdul-Mutalib NA, Abdul-Rashid MF, Mustafa S, Amin-Nordin S, Hamat RA, Osman M. Knowledge, attitude and practices regarding food hygiene and sanitation of food handlers in Kuala Pilah, Malaysia. Food Control 2012:289—93. Larson EKJ, McGinley GL, Grove JJL, Talbot GH. Physiologic, microbiologic, and seasonal effects of hand washing on the skin of health care personnel. Am J Infect Control 1986;14(2):51—9. Nassiri V, Esmailnia K, Karimi G, Nasiri M, Akhavan O. Intestinal parasitic infections among inhabitants of Karaj city, Tehran province, Iran in 2006—2008. Korean J Parasitol 2009;47:265—8. Abera B, Biadegelgen F, Bezabih B. Prevalence of Salmonella typhi and intestinal parasites among food handlers in Bahir Dar town, Northwest Ethiopia. Ethiop J Health Dev 2010;24:46—50. Alwia M. Bacterial cause of diarrhea in children. University of Khartoum: Thesis submitted in partial fulfillment of MD in Clinical Pathology; 1994.
Available online at www.sciencedirect.com
ScienceDirect
Please cite this article in press as: Nasrolahei M, et al. Bacterial assessment of food handlers in Sari City, Mazandaran Province, north of Iran. J Infect Public Health (2016), http://dx.doi.org/10.1016/j.jiph.2016.03.006
ARTICLE IN PRESS
Journal of Infection and Public Health (2016) xxx, xxx—xxx
Bacterial assessment of food handlers in Sari City, Mazandaran Province, north of Iran Mohtaram Nasrolahei a, Siavash Mirshafiee b,∗, Soudeh Kholdi a, Maryam Salehian a, Masoumeh Nasrolahei a a
Department of Microbiology, Mazandaran University of Medical Sciences, Sari 4847191971, Iran b Husbandry Department, Ghaemshahr Branch of Islamic Azad University, 8456491896, Iran Received 14 July 2015 ; received in revised form 11 February 2016; accepted 4 March 2016
KEYWORDS Food handlers; Hand washing practice; Nasal carrier; Fingernail contents
Abstract Food handlers with poor personal hygiene could be potential sources of infection due to pathogenic bacteria. This study was designed to determine the prevalence of bacterial infestation among the food handlers attending the public health center laboratory in Sari, northern Iran for annual check-up. This study was performed from September 2013 to August 2014. Stool samples, fingernail specimens of both hands and nasal swabs were collected from 220 male and female food handlers of different jobs, aged between 17—65 years. The samples were cultured on bacteriological culture media and bacterial species were identified following standard procedures. A structured questionnaire was used to record sociodemographic and behavioral data analysis of the food handlers. Of the total 220 subjects examined, 62.2% showed positive culture for different bacterial species from their fingernail contents, 65.4% were found to be harboring Staphylococcus aureus in their nostrils and 0.9% tested positive for Shigella boydii from stool samples. Staphylococcus aureus was the predominant bacteria isolated from fingernail specimens (46%), followed by Escherichia coli (29.2%), Coliforms (18.2%) and Pseudomonas aeruginosa (6.6%). This study showed a statistically significant difference in the rate of bacterial infestation between different occupational categories (p = 0.04). Butchers showed the highest prevalence of bacteria (86.6%) in their fingernail contents, followed by fast food workers (76.5%), bakers (73.5%), chicken store workers (73%), school cafeterias staff (53.3%), restaurant workers (46.9%) and fruit/vegetables sellers (42.5%). The highest rate of nasal carrier for Staphylococcus aureus was observed among chicken store workers 14/17(20.8%).
∗
Corresponding author at: Husbandry Department, Ghaemshahr Branch of Islamic Azad University, 8456491896, Iran. Tel.: +98 11456760314; fax: +98 2595435326. E-mail addresses: [email protected], dr.mirshafi[email protected] (S. Mirshafiee). http://dx.doi.org/10.1016/j.jiph.2016.03.006 1876-0341/© 2016 Published by Elsevier Limited on behalf of King Saud Bin Abdulaziz University for Health Sciences.
Please cite this article in press as: Nasrolahei M, et al. Bacterial assessment of food handlers in Sari City, Mazandaran Province, north of Iran. J Infect Public Health (2016), http://dx.doi.org/10.1016/j.jiph.2016.03.006
JIPH-575; No. of Pages 6
ARTICLE IN PRESS
2
M. Nasrolahei et al. These findings indicate the need for intensive training/retraining and health education of all food service employees and strengthening the existing screening methods to control the problem of bacterial infestation in food handlers. © 2016 Published by Elsevier Limited on behalf of King Saud Bin Abdulaziz University for Health Sciences.
Introduction Diarrheal diseases, mostly caused by foodborne or waterborne microbial pathogens, are considered as leading causes of illness and deaths in developing countries, killing an estimated 1.9 million people annually at the global level. Even in developed countries, an estimated one-third of the populations are affected by microbiological foodborne diseases each year [1]. Food handlers also known as food vendors are vital components in the interaction between the cooking environment and the food which is being either prepared or served. WHO (1989) defined food handlers as those who, in the course of their normal routine work, handle food or items that may come into contact with food, such as eating and drinking utensils not meant for their personal use [2]. Transmission of intestinal enteropathogenic bacteria is affected directly or indirectly through objects contaminated with feces. These include food, water, nails and fingers, indicating the importance of fecal-oral human-to-human transmission. Food handlers who harbor and excrete enteropathogenic bacteria may contaminate foods from their feces via their fingers, then to food processing, and finally to healthy individuals [3]. Compared to other parts of the hand, the area beneath fingernails can be the vector to spread harmful microorganisms through cross contamination [4]. A number of outbreaks of viral and bacterial infections have already been shown to have been initiated by infected food handlers [5,6]. Therefore, it is extremely important to have regularly scheduled check-ups so that infected employees can be immediately excluded from work involving direct contact with food products and can be appropriately treated. Accordingly, Food handlers with poor personal hygiene working in food service establishments could be potential sources of infection due to pathogenic organisms [7]. Therefore, a proper screening procedure is helpful to diagnose food handlers, thus preventing probable morbidity and protecting the health of the consumers. According to National Food Safety Standards in Iran, all food handlers should receive health
certificate annually. So, food handlers must go under annual microbial examination and should take part in training courses regarding food safety prior to receive their health certificate. This study was established to determine the prevalence of bacteria among food handlers working in food service setting attending the public health center for annual check-up in Sari, northern Iran.
Materials & methods This study was conducted on all 220 food handlers attending to Health Center Diagnostic Laboratory in Sari, northern Iran from September 2013 to August 2014. Sari lies at the center of Mazandaran province in northern Iran (lat.35◦ 58—36◦ 50 N, long. 52◦ 56—53◦ 59 E) and has a population of approximately 261,293 individuals. The study was carried out on food handlers of different jobs from different geographical areas in Sari city. Written consent was obtained from health center administration and participants. The food handlers who did not take treatment for any intestinal ailment within three months prior to the study were included. A structured questionnaire was used for collecting information on age, gender, educational status, income level and hand washing practices of the individuals under study. Stool, fingernail content samples and nasal swab were collected from each food handler and transferred to the microbiology laboratory at Sari Medical School for laboratory examinations. All the samples were cultured into the plates of Blood agar (Padtan- teb), MacConkey agar (Q-lab) and Salmonella-Shigella agar (Oxoid). Sorbitol—MacConkey agar (Oxoid) was added to identify Enterohemorrhagic Escherichia coli (E.coli). Bacteria were purified and identified using standard laboratory methods [8].
Statistical analysis Simple proportion, the Chi-square and Fisher’s exact tests were used to assess the difference
Please cite this article in press as: Nasrolahei M, et al. Bacterial assessment of food handlers in Sari City, Mazandaran Province, north of Iran. J Infect Public Health (2016), http://dx.doi.org/10.1016/j.jiph.2016.03.006
ARTICLE IN PRESS
JIPH-575; No. of Pages 6
Bacterial assessment of food handlers in Sari City, Mazandaran Province, north of Iran Table 1 Socio-demographic characteristics of food handlers in Sari City, northern Iran, 2013—2014. Variable Age group (years) <19 20—49 >50 Gender Male Female Educational status Illiterate Grade 1—6 Grade 7—12 University educated Occupation Bakers Chicken store workers School cafeterias staff Butchers Fruits/vegetables sellers Restaurant workers Fast food workers Hand washing practice after toilet use Yes No Income level ≤200 US $ >200 US $
Frequency
Percentage
5 173 42
2.3 78.7 19
150 70
68.2 31.8
38 33 131 18
17.3 15 59.5 8.5
49 37 30 15 40
22.3 16.8 13.6 6.8 18.2
32 17
14.5 7.8
90 130
41 59
142 78
64.5 35.4
between the variables. The significant level was 5%. SPSS 18 software was used for statistical analysis.
Results In this study, 150 (68.2%) males and 70 (31.8%) females with age range of 17—65 years (mean ages 33 ± 15 years) were examined. All Food handlers employing in different food establishments attending to Health Center Diagnostic Laboratory in Sari gave good response to take part in this survey. The majority of food handlers were young adults aged from 20 to 49 years (Table 1). The participants were divided into seven groups according to the nature of occupational duties. The subjects under study were 49 (22.3%) bakers, 40 (18.2%) fruits/vegetables sellers, 37 (16.8%) chicken store workers, 32 (14.5%) restaurant workers, 30 (13.6%) school cafeterias staff, 17 (7.8%) fast food workers and 15 (6.8%) butchers. Of the 220 food handlers examined, 62.2% (n = 137) were carrier of some pathogenic bacteria in their fingernails. The number of positive cultures from fingernail contents were higher among female
3
subjects (51/70, 72.8%) than those of male subjects (86/150, 57.3%), but the difference was not statistically significant (p > 0.05).The bacteria isolated were Staphylococcus aureus (46%), Escherichia coli (29.2%), Klebsiella species (5.8%), Pseudomonas aeruginosa (6.6%), Citrobacter species (5.1%), Enterobacter species (4.8%) and Proteus species (2.5%). None of the food handlers showed positive culture for Salmonella and Shigella in respect of their fingernail specimens (Table 2). About 65% of the subjects under study (n = 144) were carrier of S. aureus in their nostrils (Table 3). No more than one enteric bacterium was observed in the subject under study. The occurrence of bacterial infestation was different in seven occupational categories. Butchers had the highest number of carriers of bacteria in respect of their fingernail 13/15 (86.6%), followed by fast food workers 13/17 (76.5%), bakers 36/49 (73.5%), chicken store workers 27/37 (73%), school cafeterias staff 16/30 (53.3%), restaurant workers 15/32 (46.9%) and fruits/vegetables sellers 17/40 (42.5%). The highest number of nasal carrier for S. aureus was observed among chicken store workers 30/37 (20.8%), followed by bakers 27/49 (18.7%), school cafeterias staff 20/30 (13.8%), fruits/vegetables sellers 24/40 (16.6%), restaurant workers 20/32 (13.8%), fast food workers 14/17 (9.7%) and butchers 9/15 (6.25). As shown in Table 2, factors related to bacterial infestation included educational level (p = 0. 005), hand washing practice after using toilet (p = 0.001) and income level (p = 0.001). In this study, illiterate food handlers who comprised 17.3% of the total subjects under study, showed the highest rate of bacterial infestation (86.8%). Stool cultures revealed the isolation of Shigella boydii from two food handlers (0.9%). No other enteropathogenic bacteria were isolated from stools specimens.
Discussion Several authors have emphasized the importance of food handlers with poor personal hygiene as threats in the transmission of bacterial diseases [9—14]. In this survey of 220 food handlers examined, 62.2% (n = 137) were carrier of some pathogenic bacteria mainly S.aureus, P.aeroginosa and S.boydii in their fingernails and 65.4% (n = 144) were found to be harboring S.aureus in their nostrils. Our results are in agreement with previous studies reported from other parts of the country [15] and are similar to findings of Humodi et al. from
Please cite this article in press as: Nasrolahei M, et al. Bacterial assessment of food handlers in Sari City, Mazandaran Province, north of Iran. J Infect Public Health (2016), http://dx.doi.org/10.1016/j.jiph.2016.03.006
JIPH-575; No. of Pages 6
ARTICLE IN PRESS
4
M. Nasrolahei et al. Table 2 Frequency and type of bacteria isolated from fingernail contents of food handlers in Sari, northern Iran, 2013—2014. Variable
Gender Male Female Occupation Fast food workers Butchers Chicken store workers Restaurant workers Bakers School cafeterias staff Fruit/vegetables sellers Educational status Illiterate Grade 1—6 Grade 7—12 University educated Economic status ≤ 200 US $ >200 US $ Hand washing practice after toilet use Yes No Total
Bacteria frequency (%)
Total positive (%)
S.aureus
E.coli
35(40.7) 28(55)
30(34.9) 16(18.6) 10(19.6) 9(17.6)
Coliform
p value
P.aeroginosa 5(5.8) 4(7.8)
86(57.3) 51(72.8)
0.31
5(38.5) 2(15.3) 4(14.8) 3(9.4) 6(23) 2(12.5) 3(17.6)
— 1(8) 1(9) — 3(11.5) 1(6.2) 3(17.6)
13(76.5) 13(86.6) 27(73) 15(46.9) 36(73.5) 16(53.3) 17(42.5)
0.04*
20(60.6) 17(68) 25(34.2) 1(16.6)
4(12.1) 5(15.1) 5(20) 3(12) 30(41) 13(17.9) 1(16.6) 4(66.6)
4(12.1) — 5(6.8) —
33(86.8) 25(75.7) 73(55.7) 6(33.3)
0.005*
39(41.9) 24(54.5)
29(31.2) 19(20.4) 11(25) 6(13.6)
6(6.5) 3(6.8)
93(67.9) 44(32.1)
0.001*
11(36.7) 52(49) 63(46)
9(30) 6(20) 31(28.80 19(17.7) 40(29.2) 25(18.2)
4(13.3) 5(4.5) 9(6.6)
30(33.30 107(82.3) 137(62.2)
0.001*
3(23) 8(61.5) 13(20.6) 7(21.8) 20(55.5) 8(50) 4(23.5)
5(38.5) 2(15.3) 9(22.5) 5(15.6) 7(26.9) 5(31.2) 7(41.2)
*Statistically significant at p < 0.05.
Sudan who reported S. aureus as the most common pathogen isolated from food handlers [16]. However, some studies have reported a lower rate of infestation [17]. High prevalence of S. aureus in this study was because it is the true pathogenic bacteria included in the resident micro-flora of the skin and 40—50% of healthy peoples carry S .aureus in the anterior nostrils of the nose [18]. Food handlers
can easily contaminate food with S aureus (common cause of food poisoning), if they sneeze or cough during food preparation and if they do not wash their hands properly after making contact with their nose or after using toilet [19,20]. Our findings showed a significant difference in the rate of bacterial infestation between different occupational categories (Fisher exact p = 0.04) and
Table 3 The rate of nasal carrier for Staphylococcus aureus among seven occupational categories of 220 food handlers in Sari, northern Iran, 2013—2014. Variable Gender Male Female Occupation Bakers Chicken store workers School cafeterias staff Butchers Fruits/vegetables sellers Restaurant workers Fast food workers Total
Total examined n (%)
Positive (%)
150(68.2) 70(31.8)
95(63.3) 49(70)
49(22.3) 37(16.8) 30(13.6) 15(6.8) 40(18.2) 32(14.5) 17(7.8) 220(100)
27(55.1) 30(81) 20(66.6) 9(60) 24(60) 20(62.5) 14(82.3) 144(65.4)
p value 0.45
>0.05
Please cite this article in press as: Nasrolahei M, et al. Bacterial assessment of food handlers in Sari City, Mazandaran Province, north of Iran. J Infect Public Health (2016), http://dx.doi.org/10.1016/j.jiph.2016.03.006
JIPH-575; No. of Pages 6
ARTICLE IN PRESS
Bacterial assessment of food handlers in Sari City, Mazandaran Province, north of Iran the level of education (p = 0.005). Taking continuous training and health education, have good knowledge on food safety, presence of running water, access to toilet facilities and operate in clean area could lead to the difference in the rate of bacterial infestation between different categories of food handlers in this study as was shown by AbdulMutalib et al [21]. The presence of P. aeruginosa in the fingernails of the subjects may be as a result of contact with contaminated raw products such as raw meat, poultry, fish, unwashed fruits and vegetables as reported earlier [22]. In this study, subjects were supposed to be more health conscious than usual practice which was one of our survey limitations. Despite the awareness of annual check -up, the rate of bacterial infestation was high in food handlers, which reflects poor personal hygiene practice and environmental sanitation, lack of supply of safe water and ignorance of health promotion practices. According to our findings, food handlers, hand washing practices after toilet use, were lower (90/220, 41%) than those reported by others [23,24] and significantly increased the rate of bacterial infestation (p = 0.001). Reduced hand washing practice after using toilet in our investigation, might have been confounded by the fact that most food handlers were individuals from the lower socioeconomic class with a low income level. In this survey, the highest rate of bacterial infestation were identified among individuals with low income level (p = 0.001); hence, it is estimated that the better the living conditions, the lower the prevalence rates. In this study, no significant difference in the rate of bacterial infestation was identified between two sexes (p > 0.05). Stool cultures of two food handlers were positive for S.boydii. The low frequency of S.boydii recorded in this study, is in line with that previously reported by Alwia [25], who found that only 10 of 400 (2.5%) patients with diarrhea tested positive for the pathogen. However, these carriers may spread the pathogen via food to consumers and may lead to outbreaks of bacillary dysentery. One limitation of our study was that, although all food handlers were included in the study, the sample size was small, and it was thus unable to use advanced analysis to make associations.
5
bacterial infestation in food handlers was high in this survey. An effective means of preventing the transmission of pathogens from food handling personnel via food consumers is strict adherence to good personal hygiene and to hygienic food handling practices. These findings indicate the need for protective enforcement including rising awareness about foodborne diseases, intensive training/retraining and health education of all food service employees and strengthening the existing screening methods to control the problem of bacterial infestation in food handlers.
Funding source Research deputy of Mazandaran University of Medical Sciences, provided financial support for the conduct of the research but had no involvement in study design, in the collection of data, in the writing of the report and etc.
Competing interests None declared.
Ethical approval Annual check-up of food handlers is Public Health Center policy in the country. It is to notify that this survey is supported by the research deputy of Mazandaran University of Medical Sciences which attends Public Health Center and supervises annual check-up of food handlers in Sari city, so there was no need for approval ethics to be issued for this study.
Acknowledgments The authors acknowledge the research deputy and laboratory staff who helped us while performing this study. Sincere thanks also to the participating food handlers in Sari city and its suburb, for their kind cooperation during the study.
References Conclusions Although educational and legal efforts to promote food safety are active in this area, still the rate of
[1] Schlundt J, Toyofuku H, Jansen J. Emerging food-borne zoonoses. Rev Sci Tech 2004;23:513—5. [2] Fendler EJ, Dolan MJ, Williams RA. Hand washing and gloving for food protection: Part I. Examination of the evidence. Dairy Food Environ Sanit 1998;18:814—23.
Please cite this article in press as: Nasrolahei M, et al. Bacterial assessment of food handlers in Sari City, Mazandaran Province, north of Iran. J Infect Public Health (2016), http://dx.doi.org/10.1016/j.jiph.2016.03.006
JIPH-575; No. of Pages 6
ARTICLE IN PRESS
6
M. Nasrolahei et al.
[3] WHO- Prevention and control of intestinal parasitic infections. World Health Organization, Geneva.1987; pp. 7—18. (Technical report series no.749). [4] Bas M, Ersun AS, Kivanc G. The evaluation of food hygiene knowledge, attitudes and practices of food handlers in food business in Turkey. Food Control 2006;17(4):317—22. [5] Shinkawa N, Noda M, Yoshizumi S, Tokutake Y, Shiraishi T, Arita-Nishida T. Molecular epidemiology of noro viruses detected in food handler associated outbreaks of gastroenteritis in Japan. Intervirology 2008;51:422—6. [6] Stein-Zamir C, Tallen-Gozani E, Abramson N, Shoob H, Yishai R, Among V, et al. Salmonella enterica outbreak in a banqueting hall in Jerusalem: the unseen hand of the epidemiological triangle. Israel Med Assoc J 2008;11:94—6. [7] WHO- Health surveillace and management procedures of food-handling personnel. World Health Organization, Geneva 1989. pp. 1—46. (Technical Report Series no.785). [8] Barrow GI, Feltham RKA. Characters of gram- negative bacteria. In: Cowans, Steels, editors. Manual for identification of medical bacteria. UK: Cambridge University Press; 2003. p. 6, 130—1. [9] Al-Lahham AB, Abu-Saud M, Shehabi AA. Prevalence of Salmonella, Shigella and intestinal parasites in food handlers in Irbid, Jordan. J Diarrhoeal Dis Res 1990;8(4):160—2. [10] Oteri T, Ekanem EE. Food hygiene behavior among hospital food handlers. Public Health 1989;103(3):153—9. [11] Yamada S, Matushita S, Kudoh Y. Recovery and its evaluation of Shigella bacilli or Salmonella from healthy food handlers in Tokyo (1961—1997). Kansenshogaku Zasshi 1999;73:758—65. [12] Wiwanitkit V, Assawawitoontip S. High prevalence of positive culture and parasites in stool samples of food handlers in a Thai hospital setting. Med Gen Med 2002;4:8. [13] Hundy RL, Cameron S. An outbreak of infections with a new Salmonella phage type linked to a symptomatic food handler. Commun Dis Intell 2002;26:562—7. [14] Feglo PK, Frimpong EH, Essel-Ahun M. Salmonellae carrier status of food vendors in Kumasi, Ghana. East Afr Med J 2004;81:358—61. [15] Fallah M, Sadeghian S, Taherkhani H, Habibi F, Barghi ZH. Study of parasitic and bacterial infections in the
[16]
[17]
[18]
[19]
[20]
[21]
[22]
[23]
[24]
[25]
food-handling personnel, Hamadan, Iran. J Res Health Sci 2004;4:3—10. Humodi AS, Hatim HH. Bacteriological and parasitological assessment of food handlers in the Omdurman area of Sudan. J Micbiol Immunol Infect 2010;43(1):70—3. Soto A, Saldias ME, Oviedo P, Fernandez M. Prevalence of Staphylococcus aureus among food handlers from a metropolitan university in Chile. Rev Med Chile 1996;124:1142—6. Redway K, Knights B, Bozoky Z, Theobald A, Hardcastle S. Hand drying: a study of bacterial types associated with different hand drying methods and with hot air dryers. Applied Ecology Research Group, University of Westminster. London, UK. 14. Brodie, J 1965. Hand hygiene. Scot Med J 1994;10(1):115—25. Brooks GF, Butel JS, Morse SA. Medical microbiology. 21st ed. New York: Lange Medical Books/McGraw-Hill Medical publishing Division; 1998. p. 466. Isara AR, Isah EC, Lofor PVO, Ojide CK. Food contamination in fast food restaurants in Benin city, Edo state, Nigeria. Implication for food hygiene and safety. J Pub Health 2010:471. Abdul-Mutalib NA, Abdul-Rashid MF, Mustafa S, Amin-Nordin S, Hamat RA, Osman M. Knowledge, attitude and practices regarding food hygiene and sanitation of food handlers in Kuala Pilah, Malaysia. Food Control 2012:289—93. Larson EKJ, McGinley GL, Grove JJL, Talbot GH. Physiologic, microbiologic, and seasonal effects of hand washing on the skin of health care personnel. Am J Infect Control 1986;14(2):51—9. Nassiri V, Esmailnia K, Karimi G, Nasiri M, Akhavan O. Intestinal parasitic infections among inhabitants of Karaj city, Tehran province, Iran in 2006—2008. Korean J Parasitol 2009;47:265—8. Abera B, Biadegelgen F, Bezabih B. Prevalence of Salmonella typhi and intestinal parasites among food handlers in Bahir Dar town, Northwest Ethiopia. Ethiop J Health Dev 2010;24:46—50. Alwia M. Bacterial cause of diarrhea in children. University of Khartoum: Thesis submitted in partial fulfillment of MD in Clinical Pathology; 1994.
Available online at www.sciencedirect.com
ScienceDirect
Please cite this article in press as: Nasrolahei M, et al. Bacterial assessment of food handlers in Sari City, Mazandaran Province, north of Iran. J Infect Public Health (2016), http://dx.doi.org/10.1016/j.jiph.2016.03.006