Occurrence and Antimicrobial Susceptibility of Salmonella sp. and Escherichia coli in Minimally-processed and Frozen Fruit Pulps

Occurrence and Antimicrobial Susceptibility of Salmonella sp. and Escherichia coli in Minimally-processed and Frozen Fruit Pulps


1Departament of Food Science, UNICAMP-SP; 2Institute of Pharmaceutical Science, UNICAMP-SP; 3Departament of Food Science, UNICAMP-SP; 4Departament of Food Science, UNICAMP-SP

Fruits and fruit pulps are widely consumed worldwide due to their nutrients, flavors and varieties. However, these products become contaminated with pathogens during harvest or production, which are risks to consumers. This study analyzed the microbiological quality of frozen fruit pulps and minimally processed fruits sold in supermarkets and the presence Salmonella sp. and pathogenic Escherichia coli. Almost all frozen fruit pulps samples were adequate to consume, only one samples of unpasteurized mango pulp was positive for E. coli carrier  of est1b gene that codify thermostable toxin of Enterotoxigenic E. coli. Minimally processed fruits presented high yeast and mold counts in 36.25% (29/80) of the samples and 27.6% (22/80) had thermotolerant coliforms. In addition, one sample of grated coconut had E. coli and one sample of melon honeydew had Salmonella sp. E. coli O157:H7 was absent in all samples of minimally processed fruits. E. coli showed greater resistance to ampicillin and chloramphenicol. Multidrug resistance was observed in 14.3% (2/14) of E. coli isolates. Only one strain of Salmonella sp. was resistant to antibiotic sulfamethoxazole/trimethoprim. Therefore, the enforcement of pasteurization in the fruit pulp processing, as well hygienic-sanitary control in lead up of minimally-processed fruits and temperature control in storage are recommended to minimize the risk of foodborne disease.

Keywords: mango, melon, multidrug resistance, pathogenic E. coli.

Free Full-text PDF

How to cite this article:

SANTINI, T.P; MARQUES, J.O; NUÑES, K.V.M; KABUKI, D.Y. Occurrence and Antimicrobial Susceptibility of Salmonella sp. and Escherichia coli in Minimally-processed and Frozen Fruit Pulps. American Journal of Agricultural Research, 2020,5:83. DOI:10.28933/ajar-2019-11-2605


1. MORAES, I. V. 2006. Produção de Polpa de Fruta Congelada e Suco de Frutas. Dossiê Técnico. Brasil.
2. SILVA, C.E.F; ABUD, A.K.S . 2017. Tropical Fruit Pulps: Processing, product standardization and main control parameters for quality assurance. Brazilian Archives of Biology and Technology. http://dx.doi.org/10.1590/1678-4324-2017160209.
3. TOURNAS, V.H. 2005. Moulds and yeasts in fresh and minimally processed vegetables, and sprouts. International Journal of Food Microbiology 99:71-77. https://doi.org/10.1016/j.ijfoodmicro.2004.08.009
4. BASTOS, M.S.R. 2006. Frutas Minimamente Processadas: Aspectos da Qualidade e Segurança. Embrapa Agroindústria Tropical, Fortaleza, Brasil. v.103
5. IBARRA-SANCHEZ, L. S; ALVARADO-CASILLAS, S; RODRIGUEZ-GARCIA, M. O; MARTÍNEZ-GONZALES, N. E; CASTILLO, A. 2004. Internalization of bacterial pathogens in tomatoes and their control by selected chemicals. Journal of Food Protection 67:1353-1358. https://jfoodprotection.org/doi/pdf/10.4315/0362-028X-67.7.1353
6. FORYSTHE, S. T. 2010. The microbiology of safe foods. 2th ed. Blackweel Publishing Ltd.
7. BEUCHAT, L.R. 2002. Ecological factors influencing survival and growth of human pathogens on raw fruits and vegetables. Microbes and Infection 4:413-423. https://doi.org/10.1016/S1286-4579(02)01555-1
8. KOZAK G.K; MacDONALD,D; LANDRY, L; FARBER, J.M. (2013) Foodborne Outbreaks in Canada Linked to Produce: 2001 through 2009. Journal of Food Protection 76:173-183. https://doi.org/10.4315/0362-028X.JFP-12-126
9. GIBBS, R; NEVADA, P; MAZZUCCHELLI, T et al. 2009. An Outbreak of Salmonella enterica Serotype Litchfield Infection in Australia Linked to Consumption of Contaminated Papaya. Journal of Food Protection 72:1094-1098. https://jfoodprotection.org/doi/pdf/10.4315/0362-028X-72.5.1094
10. CENTER FOR DISEASE CONTROL AND PREVENTION (CDC) 2018. Reports of Salmonella Outbreak Investigations from 2018. Available at: https://www.cdc.gov/salmonella/outbreaks-2018.html. Accessed in: 27 mar /2018.
11. CENTER FOR DISEASE CONTROL AND PREVENTION (CDC). 2012. Multistate Outbreak of Salmonella Braenderup Infections Associated with Mangoes (Final Update). Available at: https://www.cdc.gov/salmonella/braenderup-08-12/index.html. Accessed in: 05 mar 2018.
12. LOHARIKAR, A; NEWTON, A; ROWLEY, P. et al. 2012. Typhoid Fever Outbreak Associated With Frozen Mamey Pulp Imported From Guatemala to the Western United States, 2010. Clinical Infectious Diseases 55:61-66. https://doi.org/10.1093/cid/cis296
13. DEY, M; MAYO, J.A; SAVILLE, D; WOLYNIAK, C; KLONTZ, K.C. Recalls of Foods due to Microbiological Contamination Classified by the U.S. Food and Drug Administration, Fiscal Years 2003 through 2011. 2013. Journal of Food Protection 76:932-938. https://doi.org/10.4315/0362-028X.JFP-12-464.
14. INSTITUTO ADOLFO LUTZ. 2008. Normas Analíticas do Instituto Adolfo Lutz. v. 1: Métodos químicos e físicos para análise de alimentos, 4 ed. São Paulo.
15. BEUCHAT, L.R.; COUSIN, M.A. 2001. Yeasts and Moulds. In: DOWNES, F.P.; K. ITO, Compendium of Methods for the Microbiological Examination of Foods, ed.4, American Public Heath Association, Washington, v.20, p. 209-215.
16. KORNACKI, J. L.; JOHNSON, J. L. 2001. Enterobacteriaceae, Coliforms, and Escherichia coli as quality and safety indicators. In: DOWNES, F. P.; ITO, K. Compendium of methods for the microbiological examination of foods. 4. ed. Washington: American Public Health Association, p. 69-82.
17. FENG, P.; WEAGANT, S. D.; JINNEMAN, K. 2011. Bacteriological Analytical Manual (BAM). Chapter 4: Escherichia coli Available at: http://www.fda.gov/Food/FoodScienceResearch/LaboratoryMethods/ucm070080.htm . Accepted in: 30 apr 2014
18. CHANDRA, M.; CHENG, P.; RONDEAU, G.; PORWOLLIK, S.; McCLELLAND, M. 2013. A single step multiplex PCR for identification of six diarrheagenic E. coli pathotypes and Salmonella. International Journal of Medical Microbiology 303:210-216. https://doi.org/10.1016/j.ijmm.2013.02.013
19. MÜLLER D., GREUNE L., HEUSIPP G., KARCH H., FRUTH A., TSCHÄPE H., SCHMIDT M. A. 2007. Identification of Unconventional Intestinal Pathogenic Escherichia coli Isolates Expressing Intermediate Virulence Factor Profiles by Using a Novel Single-Step Multiplex PCR. Applied and Environmental Microbiology 73:3380-3390. https://doi.org/10.1128/AEM.02855-06
20. ANDREWS, W.H; WANG, H; JACOBSON, A; HAMMACK, T. 2014. Bacteriological Analytical Manual (BAM) Chapter 5: Salmonella. Available at: https://www.fda.gov/Food/FoodScienceResearch/LaboratoryMethods/ucm070149.htm. Accepted in: 30 abr. 2014.
21. RAHN, K.; GRANDIS, S.A.; CLARKE, R.C.; MCEWEN, S.A.; GALÁN, J.E.; GINOCCHIO, C.; CURTIS, R.; GYLES, C.L. 1992. Amplification of an invA gene sequence of Salmonella typhimurium by polymerase chain reaction as a specific method of detection of Salmonella. Molecular and Cellular Probes, 6(4): 271-9.
22. Clinical and Laboratory Standards Institute/CLSI. Performance Standards for Antimicrobial Susceptibility Testing; Fifteenth Informational Supplement. 2005. CLSI/NCCLS document M100-S15 [ISBN 1-56238-556-9]. Clinical and Laboratory Standards Institute, 940 West Valley Road, Suite 1400, Wayne, Pennsylvania 19087- 1898 USA.
23. Ministério da Agricultura e do Abastecimento. Instrução Normativa Nº 1, de 7 de janeiro de 2000. Regulamento técnico geral para fixação dos padrões de identidade e qualidade para polpa de frutas. Diário Oficial da União, Nº 6, Brasília, BR
24. VALSECHI, O.A. 2006. Microbiologia dos alimentos. 1 ed, Araras, São Paulo, Brasil
25. ARMELLINI, A; THORELL, G; OLIVEIRA, O.A. 2004. Polpa de morango congelada. Disciplina de processamento de alimentos de origem vegetal, UFRGS. Available at: http://www.ufrgs.br/alimentus1/feira/prfruta/polpa_morango/cong_base.htm. Accepted in: 22 mai 2017.
26. SANTOS, J.E.F; TEIXEIRA, L.E.B; MOREIRA, I.S; SOUSA, F.C; CASTRO, D.S. 2015. Qualidade microbiológica de salada de frutas comercializadas por ambulantes na cidade de Juazeiro do Norte – Ceará. Revista Verde de Agroecologia e Desenvolvimento Sustentável, Pombal, PB,10(1):01-03.
27. NETO, J.L.F; CALOU, V.C.R; SILVA, J.R.A; MENDES, R.C. 2016. Perfil microbiológico de amostras de polpas de frutas congeladas, comercializadas na cidade de Missão Velha-CE, Brasil. Caderno de Cultura e Ciência, 15(1).
28. BRASIL. Agência Nacional de Vigilância Sanitária. Resolução RDC nº 12, de 02/01/2001. Regulamento Técnico sobre padrões microbiológicos para alimentos. Diário Oficial da República Federativa do Brasil, Brasília, BR.
29. FELLOWS, P. 1994. Tecnologia del procesado de los alimentos: principios y prácticas. Zaragoza: Acribia, 549p.
30. PINHEIRO, N.M.S.; FIGUEIREDO, E.A.T.; FIGUEIREDO, R.W.; MAIA, G.A.; SOUZA, P.H.M. 2005. Avaliação da Qualidade Microbiológica de Frutos Minimamente Processados Comercializados em Supermercados de Fortaleza. Revista Brasileira de Fruticultura, Jaboticabal-SP, Brasil, 27(1):153-6.
31. CENTERS FOR DISEASE CONTROL AND PREVENTION. 2018. Multistate outbreak of Samonella Typhimurium infections linked to dried coconut (Final update). Available at: https://www.cdc.gov/salmonella/typhimurium-03-18/index.html. Accepted in: 12 jun 2018
32. BRUNO, L.M.; QUEIROZ, A.M.M.; ANDRADE, A.P.C.; VASCONCELOS, N.M.; BORGES, M.F. 2005. Avaliação Microbiológica de Hortaliças e Frutas Minimamente Processadas Comercializadas em Fortaleza (CE). B.CEPPA, Curitiba, v.23, n.1, p.75-84.
33. WALSH, K.A; BENNETT, S.D; MAHOVIC, M; GOULD, L.H. 2014. Outbreaks associated with cantaloupe, watermelon, and honeydew in the United States, 1973–2011. Foodborne Pathog Dis 11:945-952 http://doi.org/10.1089/fpd.2014.1812
34. CENTERS FOR DISEASE CONTROL AND PREVENTION. 2018. Multistate outbreak of Salmonella Adelaide infections linked to pre-cut melon. Available at: https://www.cdc.gov/salmonella/adelaide-06-18/index.html. Accepted in: 12 jun 2018
35. MUNNOCH, S.A; WARD, K; SHERIDAN, S; FITZSIMMONS, G.J et al. 2009 A multi-state outbreak of Salmonella Saintpaul in Australia associated with cantaloupe consumption. Epidemiol Infect 137:367-374 https://doi.org/10.1017/S0950268808000861
36. PENTEADO, A. L.; LEITÃO, M. 2004. Growth of Salmonella Enteritidis in melon, watermelon and papaya pulp stored at different times and temperatures. Food Control 15:369-373. https://doi.org/10.1016/S0956-7135(03)00099-9
37. UKUKU, D.O; SAPERS, G.M. 2007. Effect of time before storage and storage temperature on survival of Salmonella inoculated on fresh-cut melons. Food Microbiology 24:288-295. https://doi.org/10.1016/j.fm.2006.04.007
38. TAN, S. L.; LEE, H. Y.; MAHYUDIN, N. A. 2014. Antimicrobial resistance of Escherichia coli and Staphylococcus aureus isolated from food handler’s hands. Food Control 44:203-207. https://doi.org/10.1016/j.foodcont.2014.04.008
39. MOURA, M.R.S.A.L; MELLO, M.J.G; CALÁBRIA, W.B; GERMANO, E.M; MAGGI, R.R.S; CORREIA, J.B. 2012. Frequência de Escherichia coli e sua sensibilidade aos antimicrobianos em menores de cinco anos hospitalizados por diarreia aguda. Revista Brasileira de Saúde Materna e Infantil, Recife, Brasil. 12:173-182.
40. MOTA, R.A; SILVA, K.P.C; FREITAS, M.F.L; PORTO, W.J.N; SILVA, L.B.G. 2005. Utilização indiscriminada de antimicrobianos e sua contribuição a multirresistência bacteriana. Brazilian Journal of Veterinary Research and Animal Science. 42(6).

Terms of Use/Privacy Policy/ Disclaimer/ Other Policies:
You agree that by using our site, you have read, understood, and agreed to be bound by all of our terms of use/privacy policy/ disclaimer/ other policies (click here for details).

This work and its PDF file(s) are licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.