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ORIGINAL ARTICLE  
Year : 2017  |  Volume : 10  |  Issue : 5  |  Page : 1195-1198
Gastrointestinal carriage of Salmonella species and intestinal parasites, and nasal and hand carriage of Staphylococcus aureus among asymptomatic food handlers


Department of Microbiology, Topiwala National Medical College and BYL Nair Charitable Hospital, Mumbai, Maharashtra, India

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Date of Web Publication6-Nov-2017
 

   Abstract 


Background: Food borne diseases continue to be a public health problem globally. Food handlers (FHs) have been implicated in food borne outbreaks. Asymptomatic carriers go unnoticed and are thus an important source of pathogens. Aims and Objectives: This study was conducted to detect intestinal carriage of Salmonella species and parasites as well as nasal and hand carriage of Staphylococcus aureus (S. aureus) among asymptomatic FHs. Personal hygiene practices followed by them were recorded. Materials and Methods: A total of 300 asymptomatic FHs were studied. A semi-structured questionnaire was filled. Nasal swabs and finger impressions were taken on mannitol salt agar plates which were incubated overnight at 37°C; colonies suggestive of S. aureus were identified and confirmed by standard biochemical tests. Stool culture for Salmonella species was done on MacConkey agar, Xylose Lysine Deoxycholate agar and simultaneously inoculated in Selenite F broth for further processing; colonies suggestive of Salmonella species were identified by standard biochemical tests and Salmonella antisera (Denka Seiken, Japan). Stool-routine/microscopy for parasites was done by gross examination, direct saline, and iodine mount followed by concentration method (saturated salt solution). An arbitrary 10-point scale used in earlier studies was utilized for classifying the level of personal hygiene of FHs. Results: Salmonella Typhi was detected in stool culture of two FHs. Intestinal parasites detected in 10 (3.3%) subjects, included Ascaris lumbricoides (5;1.7%), Entamoeba histolytica (3;1.0%), and Giardia intestinalis (2;0.66%). S. aureus carriage was noted in anterior nares (116;38.7%) and hand (83;27.7%). A total of 149 (50%) FHs were S. aureus carriers. Conclusion: This study indicates that FHs may be a potential source of food borne pathogens.

Keywords: Asymptomatic carriers, intestinal parasites, Salmonella Typhi

How to cite this article:
Dash L, Khaparde A, Vivek K, Shastri JS. Gastrointestinal carriage of Salmonella species and intestinal parasites, and nasal and hand carriage of Staphylococcus aureus among asymptomatic food handlers. Ann Trop Med Public Health 2017;10:1195-8

How to cite this URL:
Dash L, Khaparde A, Vivek K, Shastri JS. Gastrointestinal carriage of Salmonella species and intestinal parasites, and nasal and hand carriage of Staphylococcus aureus among asymptomatic food handlers. Ann Trop Med Public Health [serial online] 2017 [cited 2019 Dec 15];10:1195-8. Available from: http://www.atmph.org/text.asp?2017/10/5/1195/217502



   Introduction Top


Food borne diseases continue to be a public health problem globally as highlighted by the World Health Organization slogan “From Farm to Table, make Food Safe” declared on World Health Day 2015.[1] Food Handlers (FHs) are implicated in 18% of food borne outbreaks.[2] Asymptomatic carriers among FHs go unnoticed and thus are an important source of pathogens. Here, we have assessed intestinal carriage of  Salmonella More Details species and parasites as well as nasal and hand carriage of Staphylococcus aureus (S. aureus) among asymptomatic FHs and recorded their personal hygiene practices.


   Materials and Methods Top


Study population

A cross-sectional study was conducted among 300 asymptomatic FHs working in different licensed eateries and restaurants from South and Central Mumbai Municipal wards (A, B, C, and D) in Mumbai, India. They presented to our institute as part of the periodic clinical and laboratory check-up under the FHs program of the Municipal Corporation of the city. Institutional Ethics Committee approval and written informed consent were obtained. A pretested semi-structured questionnaire was used to collect data on age, sex, nature of the occupation, and place of employment. Asymptomatic adult FHs of either gender were included in the study. Symptomatic FHs with gastrointestinal disorders, jaundice, or skin diseases and those who had taken antibiotics or anthelminthics 3 weeks before the study were excluded from the study.

Methodology

An arbitrary 10-point scale used in earlier studies was utilized for classifying the level of personal hygiene of FHs. The scale included hygiene and sanitation components that evaluated the wearing of clean clothes, use of gloves, wearing of cap, cutting of hair, washing of hands, cutting of nails, use of towels, bathing frequency, brushing of teeth, and use of footwear. The practices were classified as good (≥7 score), fair (4–6 score), and poor (≤3 score).[3]

Sample collection and processing

A single nasal swab and finger impression of both the hands were taken on Mannitol salt agar (MSA) from each subject. A freshly passed stool sample was collected in a sterile wide-mouthed container from all the FHs included in the study. The MSA plates were incubated overnight aerobically at 37°C. Colonies suggestive of S. aureus were identified by Gram staining and standard biochemical tests.[4] Stool routine microscopy for parasites included gross examination, direct microscopy, and microscopic examination after concentration method (saturated salt solution) by saline and iodine mount. Stool culture for Salmonella was done on MacConkey agar, Xylose Lysine Deoxycholate agar and in Selenite F broth and processed further as per the WHO protocol.[5] Colonies suggestive of Salmonella species were identified using standard biochemical tests and Salmonella antisera (Denka Seiken, Japan). Antimicrobial testing was done on Mueller-Hinton agar by Kirby-Bauer disc diffusion method as per CLSI guidelines 2012. The antimicrobial agents tested were ampicillin (10 μg), cotrimoxazole (1.25/23.75 μg), chloramphenicol (30 μg), ciprofloxacin (5 μg), ceftriaxone (30 μg), and nalidixic acid (30 μg).[6]

Statistical analysis

Data were analyzed using Microsoft Excel version 2007. Categorical data were analyzed as frequency and percentages.

Reporting of results

Results of stool-routine/microscopy were conveyed to the FHs through proper channels.


   Results Top


Out of the total 300 asymptomatic FHs studied, 262 (87.3%) were in the age group of 20–39 years and 38 (11.7%) were above 40 years. Incidentally, all were employed as chefs with males comprising of 286 (95.3%) and females 14 (4.7%). A total of 268 (89.3%) respondents were noted to have fair to good personal hygiene [Table 1]. Laboratory investigations [Table 2] revealed Salmonella Typhi(S. Typhi) isolation from the stool culture of 2 (0.7%) FHs. The S. Typhi isolates were sensitive to ampicillin, cotrimoxazole, chloramphenicol, ciprofloxacin, and ceftriaxone but resistant to nalidixic acid. The intestinal parasitic rate was found to be 3.3% (10/300). The most common parasite detected was Ascaris lumbricoides (5; 1.7%), followed by Entamoeba histolytica (3; 1%), and Giardia intestinalis (2; 0.7%). Among the FHs, nasal carriage of S. aureus was found in 116 (38.7%) while finger impression yielded S. aureus in 83 (27.7%). A total of 149 (50%) FHs were S. aureus carriers with 50 (16.7%) showing carriage at both sites.
Table 1: Sociodemographic data and personal hygiene assessment of food handlers


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Table 2: Results of laboratory investigations


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   Discussion Top


Food borne illnesses are important public health problems worldwide, affecting both developed as well as developing countries leading to substantial costs in public health terms and serious losses in morbidity and mortality. Salmonella species and S. aureus in particular are the most commonly implicated organisms.[7] Intestinal parasitic infections pose a significant problem in developing countries.[8] FHs infected with these pathogens may transfer them to food through the feco-oral route, due to poor personal hygiene, and inappropriate handling of food. S. aureus, present as normal nasal/hand flora may also be transmitted from a FH to ready-to-eat foods.

In the present study, maximum FHs were in the age group of 20–39 years (262; 87.3%) with a smaller proportion above 40 years (38; 11.7%). In comparison, Udgiri and Masalihad maximum respondents (73.1%) below 30 years of age.[9] Among the FHs in our study, 268 (89.3%) were noted to have fair to good practice of personal hygiene with the remaining 32 (10.7%) assessed to have poor practice. Bobhate et al. had found poor personal hygiene in 34.3% among the 137 FHs studied.[3] Isolation of Salmonella from stool is a recommended method for the detection of carriers as corroborated by Mohan et al.[10] In the present study, S. Typhi was isolated from stool culture of two (0.7%) FHs. Results from a study by Mohan et al. conformed to our findings. However, Parikh and Murti from Mumbai (formerly Bombay), in their study (1987) had detected Salmonella spp. in 16/450 (3.5%) FHs.[11]

In our study, intestinal parasites were detected in 3.3% (10/300) of the asymptomatic FHs with the most common parasite being A. lumbricoides (5; 1.7%), followed by E. histolytica (3; 1%) and G. intestinalis (2; 0.7%). Khurana et al. observed nil to 6.8% parasitic infection rate in their study between years 2001 and 2006 with G. lamblia being the commonest.[12] Bobhate et al. who have included both symptomatic and asymptomatic FHs found a parasitic rate of 9.5% among 137 FHs in their study.[3] Gunduz et al. from Turkey have reported intestinal parasites in 8.8% of 8895 FHs.[13] High rates of parasitic infections have been reported from African countries including 23% by Zaglool et al. from Saudi Arabia,[14] 24.3% by Al-Hindi et al. from Palestine,[15] and 41.1% by Abera et al. from Ethiopia.[16] The lower rate of isolation in the present study may be attributed to the inclusion of only asymptomatic study subjects and their practice of fair to good personal hygiene, and periodic medical check-up among the respondents. Moreover, the stool concentration was done using saturated salt solution instead of the commonly used formol ether sedimentation technique.

In the present study, a total of 50 (16.7%) FHs were noted to have both nasal and hand carriage of S. aureus with nasal carriage in 116 (38.7%) and hand carriage in 83 (27.7%). A total of 149 (50%) FHs were S. aureus carriers. These figures are higher compared to reports by Dagnew et al. from NW Ethiopia, who found nasal S. aureus in 20.5% of 200 FHs [17] and Zaglool et al. from Egypt who detected 17.5% S. aureus carriage in fingernails among 200 FHs. S. aureus strains that produce staphylococcal enterotoxins (SEs) are the causative agents of staphylococcal food poisoning. It is recognized that FHs are the major source of contamination of food with staphylococci. FHs must be considered a potential source of enterotoxigenic staphylococci, and the identification of the enterotoxin produced by strains isolated from both FH and incriminated food will help trace the agent's profile. Carmo et al., who investigated an outbreak of staphylococcal food poisoning involving 42 people at a restaurant in MG, Brazil noted that four of five FHs were nasal carriers of enterotoxigenic staphylococci with one additionally having throat colonization.[18]


   Conclusion Top


Asymptomatic carriage of bacterial and parasitic pathogens and the varying levels of personal hygiene practices noted in this study indicate that FHs may be a potential source of food borne pathogens.

Recommendations

As asymptomatic carriers can unknowingly transmit infection and pose a danger to the consumer, we recommend periodic educational programs for food handlers for safe food handling, food sanitation, and personal hygiene. Besides this, periodic inspection of practices and food premises where food is prepared and handled should be conducted.

Acknowledgment

The authors wish to thank the Dean of TNMC and BYL Nair Ch. Hospital, Mumbai, for permission to conduct the study and the staff of the Department of Microbiology, for general support throughout the study.

Financial support and sponsorship

The Research Society, Topiwala National Medical College and BYL Nair Ch. Hospital, Mumbai, provided support in the form of financial grant for the study.

Conflicts of interest

There are no conflicts of interest.



 
   References Top

1.
World Health Organization. World Health Day 2015: Food Safety. Geneva. Available from: http://www.who.int/campaigns/world-health-day/2015/en/. [Last accessed on 2016 Apr 02].  Back to cited text no. 1
    
2.
Bryan FL. Risks of practices, procedures and processes that lead to outbreaks of foodborne diseases. J Food Prot 1988;51:663-73.  Back to cited text no. 2
    
3.
Bobhate PS, Shrivastava SR, Gupta P. Profile of catering staff at a Tertiary care hospital in Mumbai. Australas Med J 2011;4:148-54.  Back to cited text no. 3
    
4.
Washington CW Jr., Stephen DA, William MJ, Elmer WK, Gary WP, Paul CS, et al., editors. Staphylococci and related Gram Positive Cocci. In: Koneman's Color Atlas and Textbook of Diagnostic Microbiology. 6th ed. PA: Lippincott Williams and Wilkins; 2006. p. 623-71.  Back to cited text no. 4
    
5.
WHO Laboratory Protocol for Isolation of Salmonella and Shigella from Faecal Specimens; 2010.  Back to cited text no. 5
    
6.
Clinical Laboratory Standards Institute. Performance standards for Antimicrobial Susceptibility Testing; Twenty – Second Informational Supplement. M100-S22. PA: CLSI; 2012.  Back to cited text no. 6
    
7.
An outbreak of of Acute Gastroenteritis due to Staph aureus following a Funeral ceremony- Alwar, Rajasthan. NCDC Newsletter. 2013;2:1-12. Available from: www.ncdc.gov.in. [Last accessed on 2017 Sep 30].  Back to cited text no. 7
    
8.
Murry CJ, Lopenz AD. The Global Burden of Diseases: A Comprehensive Assessment of Mortality and Disability from Diseases, Injuries and Risk Factors in 1990 and Projected to 2020. Cambridge (MA): Harvard University Press; 1996. p. 990-1.  Back to cited text no. 8
    
9.
Udgiri RS, Masali KA. A study on the Health Status of Food Handlers employed in Food Establishments in Bijapur City. Ind J Comm Med 2006;31;60-1.  Back to cited text no. 9
    
10.
Mohan U, Mohan V, Raj K. A study of Carrier state of S. Typhi, Intestinal Parasites and personal hygiene amongst Food handlers in Amritsar City. Ind J Comm Med 2006;31:60-1.  Back to cited text no. 10
    
11.
Parikh UN, Murti P. Salmonella carriers in foodhandlers in Bombay. Indian J Public Health 1987;31:217-20.  Back to cited text no. 11
[PUBMED]    
12.
Khurana S, Taneja N, Thapar R, Sharma M, Malla N. Intestinal bacterial and parasitic infections among food handlers in a tertiary care hospital of North India. Trop Gastroenterol 2008;29:207-9.  Back to cited text no. 12
[PUBMED]    
13.
Gündüz T, Limoncu ME, Cümen S, Ari A, Serdaǧ E, Tay Z, et al. The prevalence of intestinal parasites and nasal S. aureus carriage among food handlers. J Environ Health 2008;70:64-5, 67.  Back to cited text no. 13
    
14.
Zaglool DA, Khodari YA, Othman RA, Farooq MU. Prevalence of intestinal parasites and bacteria among food handlers in a tertiary care hospital. Niger Med J 2011;52:266-70.  Back to cited text no. 14
  [Full text]  
15.
Al-Hindi A, Elmanama AA, Ashour N, Hassan I, Salamah Al-Shimaa. Occurrence of intestinal parasites and hygiene characters among food handlers in Gaza Strip, Palestine. Ann Alquds Med 2012;8:2-13.  Back to cited text no. 15
    
16.
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.  Back to cited text no. 16
    
17.
Dagnew M, Tiruneh M, Moges F, Tekeste Z. Survey of nasal carriage of Staphylococcus aureus and intestinal parasites among food handlers working at Gondar University, Northwest Ethiopia. BMC Public Health 2012;12:837.  Back to cited text no. 17
[PUBMED]    
18.
Carmo LS, Dias RS, Linardi VR, Sena MJ, Santos DA. An outbreak of staphylococcal food poisoning in the municipality of Passos, MG, Brazil. Braz Arch Biol Technol 2003;46:581-6.  Back to cited text no. 18
    

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Correspondence Address:
Lona Dash
Department of Microbiology, Topiwala National Medical College and BYL Nair Charitable Hospital, Dr. AL Nair Road, Mumbai - 400 008, Maharashtra
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ATMPH.ATMPH_200_16

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