Skip to main content
Top
Published in: Gut Pathogens 1/2018

Open Access 01-12-2018 | Review

The prevalence of Campylobacter spp. in vegetables, fruits, and fresh produce: a systematic review and meta-analysis

Authors: Hooriyeh Mohammadpour, Enayat Berizi, Saeid Hosseinzadeh, Majid Majlesi, Morteza Zare

Published in: Gut Pathogens | Issue 1/2018

Login to get access

Abstract

There are a number of reports indicating correlation between outbreaks of campylobacteriosis and the consumption of raw vegetables. This study is a meta-analysis on the prevalence of Campylobacter in fresh vegetables and fruits without any location limitation, which was performed through a documented review of the available resources. Relevant literature was reviewed by trained reviewers, who examined the results for the inclusion of articles in the meta-analysis. The prevalence of Campylobacter in raw vegetables, the sample source, the Campylobacter species, and the method of detection were extracted. The prevalence of Campylobacter in vegetables, fruits, and fresh produce were estimated to be 0.53%. Analysis of the various sample groups initially showed that the bean and sprouts group was the vegetable with the highest prevalence of Campylobacter (11.08%). The rate of contamination was higher when both the molecular and conventional methods were employed. The highest prevalence of Campylobacter was found in Asia (33.4%). Despite the low prevalence, consumption of raw vegetables is inherently risky because no treatment is used to inactivate the pathogens. Therefore, proper sanitation methods are recommended to treat the raw products.
Literature
2.
go back to reference Jongen W. Improving the safety of fresh fruit and vegetables. Boca Raton: CRC Press; 2005. Jongen W. Improving the safety of fresh fruit and vegetables. Boca Raton: CRC Press; 2005.
3.
go back to reference Danis K, Di Renzi M, O’Neill W, Smyth B, McKeown P, Foley B, Tohani V, Devine M. Risk factors for sporadic Campylobacter infection: an all-Ireland case-control study. Euro Surveill. 2009;14(7):19123.PubMed Danis K, Di Renzi M, O’Neill W, Smyth B, McKeown P, Foley B, Tohani V, Devine M. Risk factors for sporadic Campylobacter infection: an all-Ireland case-control study. Euro Surveill. 2009;14(7):19123.PubMed
9.
go back to reference World Health Organization. The global view of campylobacteriosis: report of an expert consultation, Utrecht. Berlin: World Health Organization; 2013. p. 2012. World Health Organization. The global view of campylobacteriosis: report of an expert consultation, Utrecht. Berlin: World Health Organization; 2013. p. 2012.
10.
go back to reference Crim SM, Iwamoto M, Huang JY, Griffin PM, Gilliss D, Cronquist AB, Cartter M, Tobin-D’Angelo M, Blythe D, Smith K. Incidence trends of infection with pathogens transmitted commonly through food. Foodborne Dis Act Surve Net US sites. 2014;10:2006–13. Crim SM, Iwamoto M, Huang JY, Griffin PM, Gilliss D, Cronquist AB, Cartter M, Tobin-D’Angelo M, Blythe D, Smith K. Incidence trends of infection with pathogens transmitted commonly through food. Foodborne Dis Act Surve Net US sites. 2014;10:2006–13.
12.
go back to reference Hall G, Kirk MD, Becker N, Gregory JE, Unicomb L, Millard G, Stafford R, Lalor K. OzFoodNet Working Group. Estimating foodborne gastroenteritis, Australia. Emerg Infect Dis. 2005;11(8):1257.CrossRef Hall G, Kirk MD, Becker N, Gregory JE, Unicomb L, Millard G, Stafford R, Lalor K. OzFoodNet Working Group. Estimating foodborne gastroenteritis, Australia. Emerg Infect Dis. 2005;11(8):1257.CrossRef
25.
go back to reference Carvalho AF, Silva DM, Azevedo SS, Piatti RM, Genovez ME, Scarcelli E. Detection of CDT toxin genes in Campylobacter spp. strains isolated from broiler carcasses and vegetables in São Paulo, Brazil. Braz J Microbiol. 2013;44(3):693–9.CrossRef Carvalho AF, Silva DM, Azevedo SS, Piatti RM, Genovez ME, Scarcelli E. Detection of CDT toxin genes in Campylobacter spp. strains isolated from broiler carcasses and vegetables in São Paulo, Brazil. Braz J Microbiol. 2013;44(3):693–9.CrossRef
26.
go back to reference Ceuppens S, Johannessen GS, Allende A, Tondo EC, El-Tahan F, Sampers I, Jacxsens L, Uyttendaele M. Risk factors for Salmonella, shiga toxin-producing Escherichia coli and Campylobacter occurrence in primary production of leafy greens and strawberries. Int J Environm Res Pub Health. 2015;12(2):9809–31. https://doi.org/10.3390/ijerph120809809.CrossRef Ceuppens S, Johannessen GS, Allende A, Tondo EC, El-Tahan F, Sampers I, Jacxsens L, Uyttendaele M. Risk factors for Salmonella, shiga toxin-producing Escherichia coli and Campylobacter occurrence in primary production of leafy greens and strawberries. Int J Environm Res Pub Health. 2015;12(2):9809–31. https://​doi.​org/​10.​3390/​ijerph120809809.CrossRef
31.
go back to reference Gómez-Govea M, Solís-Soto L, Heredia N, García S, Moreno G, Tovar O, Isunza G. Analysis of microbial contamination levels of fruits and vegetables at retail in Monterrey, Mexico. J Food Agric Environ. 2012;10(1):152–6. Gómez-Govea M, Solís-Soto L, Heredia N, García S, Moreno G, Tovar O, Isunza G. Analysis of microbial contamination levels of fruits and vegetables at retail in Monterrey, Mexico. J Food Agric Environ. 2012;10(1):152–6.
34.
go back to reference Johannessen GS, Eckner KF, Heiberg N, Monshaugen M, Begum M, Økland M, Høgåsen HR. Occurrence of Escherichia coli, Campylobcter, Salmonella and shiga-toxin producing E. coli in norwegian primary strawberry production. Int J Environ Res Pub Health. 2015;12(6):6919–32. https://doi.org/10.3390/ijerph120606919.CrossRef Johannessen GS, Eckner KF, Heiberg N, Monshaugen M, Begum M, Økland M, Høgåsen HR. Occurrence of Escherichia coli, Campylobcter, Salmonella and shiga-toxin producing E. coli in norwegian primary strawberry production. Int J Environ Res Pub Health. 2015;12(6):6919–32. https://​doi.​org/​10.​3390/​ijerph120606919.CrossRef
36.
go back to reference Little C, Roberts D, Youngs E, De Louvois J. Microbiological quality of retail imported unprepared whole lettuces: a PHLS food working group study. J Food Prot. 1999;62(4):325–8.CrossRef Little C, Roberts D, Youngs E, De Louvois J. Microbiological quality of retail imported unprepared whole lettuces: a PHLS food working group study. J Food Prot. 1999;62(4):325–8.CrossRef
37.
39.
go back to reference Medeiros DT, Sattar SA, Farber JM, Carrillo CD. Occurrence of Campylobacter spp. in raw and ready-to-eat foods and in a Canadian food service operation. J Food Prot. 2008;71(10):2087–93.CrossRef Medeiros DT, Sattar SA, Farber JM, Carrillo CD. Occurrence of Campylobacter spp. in raw and ready-to-eat foods and in a Canadian food service operation. J Food Prot. 2008;71(10):2087–93.CrossRef
40.
go back to reference Meldrum R, Ribeiro C, Smith R, Walker A, Simmons M, Worthington D, Edwards C. Microbiological quality of ready-to-eat foods: results from a long-term surveillance program (1995 through 2003). J Food Prot. 2005;68(8):1654–8.CrossRef Meldrum R, Ribeiro C, Smith R, Walker A, Simmons M, Worthington D, Edwards C. Microbiological quality of ready-to-eat foods: results from a long-term surveillance program (1995 through 2003). J Food Prot. 2005;68(8):1654–8.CrossRef
41.
go back to reference Mosupye FM, Von Holy A. Microbiological quality and safety of ready-to-eat street- vended foods in Johannesburg, South Africa. J Food Prot. 1999;62(11):1278–84.CrossRef Mosupye FM, Von Holy A. Microbiological quality and safety of ready-to-eat street- vended foods in Johannesburg, South Africa. J Food Prot. 1999;62(11):1278–84.CrossRef
43.
go back to reference Odumeru JA, Mitchell SJ, Alves DM, Lynch JA, Yee AJ, Wang SL, Styliadis S, Farber JM. Assessment of the microbiological quality of ready-to-use vegetables for health-care food services. J Food Prot. 1997;60(8):954–60.CrossRef Odumeru JA, Mitchell SJ, Alves DM, Lynch JA, Yee AJ, Wang SL, Styliadis S, Farber JM. Assessment of the microbiological quality of ready-to-use vegetables for health-care food services. J Food Prot. 1997;60(8):954–60.CrossRef
46.
go back to reference Sagoo SK, Little CL, Mitchell RT. Microbiological quality of open ready-to-eat salad vegetables: effectiveness of food hygiene training of management. J Food Prot. 2003;66(9):1581–6.CrossRef Sagoo SK, Little CL, Mitchell RT. Microbiological quality of open ready-to-eat salad vegetables: effectiveness of food hygiene training of management. J Food Prot. 2003;66(9):1581–6.CrossRef
47.
go back to reference Sagoo S, Little C, Ward L, Gillespie I, Mitchell R. Microbiological study of ready-to-eat salad vegetables from retail establishments uncovers a national outbreak of salmonellosis. J Food Prot. 2003;66(3):403–9.CrossRef Sagoo S, Little C, Ward L, Gillespie I, Mitchell R. Microbiological study of ready-to-eat salad vegetables from retail establishments uncovers a national outbreak of salmonellosis. J Food Prot. 2003;66(3):403–9.CrossRef
49.
go back to reference Söderqvist K, Lambertz ST, Vågsholm I, Boqvist S. Foodborne bacterial pathogens in retail prepacked ready-to-eat mixed ingredient salads. J Food Prot. 2016;79(6):978–85.CrossRef Söderqvist K, Lambertz ST, Vågsholm I, Boqvist S. Foodborne bacterial pathogens in retail prepacked ready-to-eat mixed ingredient salads. J Food Prot. 2016;79(6):978–85.CrossRef
51.
go back to reference Thunberg RL, Tran TT, Bennett RW, Matthews RN, Belay N. Microbial evaluation of selected fresh produce obtained at retail markets. J Food Prot. 2002;65(4):677–82.CrossRef Thunberg RL, Tran TT, Bennett RW, Matthews RN, Belay N. Microbial evaluation of selected fresh produce obtained at retail markets. J Food Prot. 2002;65(4):677–82.CrossRef
52.
go back to reference Thung TY, Siti Norshafawatie BM, Premarathne JM, Chang WS, Loo YY, Kuan CH, New CY, Ubong A, Ramzi OS, Mahyudin NA, Dayang FB. Isolation of food-borne pathogen bacteriophages from retail food and environmental sewage. Int Food Res J. 2017;24(1):450–4. Thung TY, Siti Norshafawatie BM, Premarathne JM, Chang WS, Loo YY, Kuan CH, New CY, Ubong A, Ramzi OS, Mahyudin NA, Dayang FB. Isolation of food-borne pathogen bacteriophages from retail food and environmental sewage. Int Food Res J. 2017;24(1):450–4.
55.
go back to reference Wijnands LM, Delfgou-Van Asch EHM, Beerepoot-Mensink ME, Van Der Meij-Florijn A, Fitz-James I, Van Leusden FM, Pielaat A. Prevalence and concentration of bacterial pathogens in raw produce and minimally processed packaged salads produced in and for the Netherlands. J Food Prot. 2014;77(3):388–94.CrossRef Wijnands LM, Delfgou-Van Asch EHM, Beerepoot-Mensink ME, Van Der Meij-Florijn A, Fitz-James I, Van Leusden FM, Pielaat A. Prevalence and concentration of bacterial pathogens in raw produce and minimally processed packaged salads produced in and for the Netherlands. J Food Prot. 2014;77(3):388–94.CrossRef
56.
go back to reference Christidis T, Pintar K, Butler A, Nesbitt A, Thomas M, Marshall B, Pollari F. Campylobacter spp. prevalence and levels in raw milk: a systematic review and meta-analysis. J Food Prot. 2016;79(10):1775–83.CrossRef Christidis T, Pintar K, Butler A, Nesbitt A, Thomas M, Marshall B, Pollari F. Campylobacter spp. prevalence and levels in raw milk: a systematic review and meta-analysis. J Food Prot. 2016;79(10):1775–83.CrossRef
57.
go back to reference Korsak D, Mackiw E, Rozynek E, Żylowska M. Prevalence of Campylobacter spp. in retail chicken, turkey, pork, and beef meat in Poland between 2009 and 2013. J Food Prot. 2015;78(5):1024–8.CrossRef Korsak D, Mackiw E, Rozynek E, Żylowska M. Prevalence of Campylobacter spp. in retail chicken, turkey, pork, and beef meat in Poland between 2009 and 2013. J Food Prot. 2015;78(5):1024–8.CrossRef
62.
go back to reference Centers for Disease Control and Prevention. 2013. OutbreakNet, foodborne outbreak online database. Centers for Disease Control and Prevention. 2013. OutbreakNet, foodborne outbreak online database.
Metadata
Title
The prevalence of Campylobacter spp. in vegetables, fruits, and fresh produce: a systematic review and meta-analysis
Authors
Hooriyeh Mohammadpour
Enayat Berizi
Saeid Hosseinzadeh
Majid Majlesi
Morteza Zare
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Gut Pathogens / Issue 1/2018
Electronic ISSN: 1757-4749
DOI
https://doi.org/10.1186/s13099-018-0269-2

Other articles of this Issue 1/2018

Gut Pathogens 1/2018 Go to the issue