From cultivation to commercialization: assessing the sanitary quality of various stages of organic vegetable production chain in southern Brazil

Vigil Sanit Debate, Rio de Janeiro, 2025, v.13: e02415 | Published on: 16/10/2025

Authors

  • Juliana da Silveira Laboratório de Parasitologia Ambiental, Departamento de Patologia Básica, Universidade Federal do Paraná (UFPR), Curitiba, PR, Brasil Author https://orcid.org/0000-0001-9659-4680
  • Jonathan Vieira dos Anjos Laboratório de Parasitologia Ambiental, Departamento de Patologia Básica, Universidade Federal do Paraná (UFPR), Curitiba, PR, Brasil Author https://orcid.org/0009-0003-9445-0730
  • Luciana Karbiak Laboratório de Parasitologia Ambiental, Departamento de Patologia Básica, Universidade Federal do Paraná (UFPR), Curitiba, PR, Brasil Author https://orcid.org/0009-0000-3462-3642
  • Gabriel Farias Souza Laboratório de Parasitologia Ambiental, Departamento de Patologia Básica, Universidade Federal do Paraná (UFPR), Curitiba, PR, Brasil Author https://orcid.org/0009-0004-9364-1188
  • Lucimara Batista Prox Laboratório de Parasitologia Ambiental, Departamento de Patologia Básica, Universidade Federal do Paraná (UFPR), Curitiba, PR, Brasil Author https://orcid.org/0009-0004-4940-7802
  • Israel Adrian Ríos Cerezo Laboratório de Parasitologia Ambiental, Departamento de Patologia Básica, Universidade Federal do Paraná (UFPR), Curitiba, PR, Brasil Author https://orcid.org/0009-0007-7789-7599
  • Alinne Petris Laboratório de Parasitologia Ambiental, Departamento de Patologia Básica, Universidade Federal do Paraná (UFPR), Curitiba, PR, Brasil Author https://orcid.org/0000-0001-9979-9243
  • Gustavo Strieder Scherer Laboratório Central do Estado do Paraná (Lacen), Unidade de Fronteira, Foz do Iguaçu, PR, Brasil Author https://orcid.org/0000-0002-6071-1651
  • Diego Averaldo Guiguet Leal Laboratório de Parasitologia Ambiental, Departamento de Patologia Básica, Universidade Federal do Paraná (UFPR), Curitiba, PR, Brasil Author https://orcid.org/0000-0001-7838-4006

DOI:

https://doi.org/10.22239/2317-269X.02415

Keywords:

Irrigation Water, Washing Water, Helminths, Protozoa, Food Safety

Abstract

Introduction: The concomitant monitoring of parasites and fecal indicator bacteria (FIB) in the organic vegetable production chain is not routinely carried out. Objective: To evaluate contamination by intestinal parasites and FIB at different stages of the organic vegetable production chain. Method: For this purpose, two groups were defined: group I – five sampling campaigns at three sites of raw water used for irrigation of vegetables, and one site of vegetable washing water (VWW) from Rio Branco do Sul/PR. Group II – curly lettuces (n = 80) from the same municipality sold at organic open-air markets in Curitiba/PR. Giardia cysts and Cryptosporidium oocysts were searched by membrane filtration and direct immunofluorescence assay and FIB by Colilert® and Enterolert®. Lettuce from group II were eluted with glycine (1M), and the entire resulting sediment was analyzed by optical microscopy to search for parasites. Results: Contamination by Cryptosporidium and Giardia (oo)cysts was detected in 20.00% (n = 4) of the samples from group I. Among these, 40.00% of the VWW samples showed contamination by both protozoa. Balantioides coli cysts were detected in 40% of the post-hygienization samples. FIB was detected in all water sites, with a higher concentration of Enterococcus sp. In open street markets, 16.25% of the samples were contaminated by parasites, with B. coli being the most frequently detected. Conclusions: The results denote a wide dispersion of parasites at different stages of the organic vegetable production chain and reinforce the need for continuous monitoring of hygienic-sanitary quality at critical points in the vegetable production chain, aiming to prevent WFD.

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Author Biographies

  • Juliana da Silveira, Laboratório de Parasitologia Ambiental, Departamento de Patologia Básica, Universidade Federal do Paraná (UFPR), Curitiba, PR, Brasil
  • Jonathan Vieira dos Anjos, Laboratório de Parasitologia Ambiental, Departamento de Patologia Básica, Universidade Federal do Paraná (UFPR), Curitiba, PR, Brasil
  • Luciana Karbiak, Laboratório de Parasitologia Ambiental, Departamento de Patologia Básica, Universidade Federal do Paraná (UFPR), Curitiba, PR, Brasil
  • Gabriel Farias Souza, Laboratório de Parasitologia Ambiental, Departamento de Patologia Básica, Universidade Federal do Paraná (UFPR), Curitiba, PR, Brasil
  • Lucimara Batista Prox, Laboratório de Parasitologia Ambiental, Departamento de Patologia Básica, Universidade Federal do Paraná (UFPR), Curitiba, PR, Brasil
  • Israel Adrian Ríos Cerezo, Laboratório de Parasitologia Ambiental, Departamento de Patologia Básica, Universidade Federal do Paraná (UFPR), Curitiba, PR, Brasil
  • Alinne Petris, Laboratório de Parasitologia Ambiental, Departamento de Patologia Básica, Universidade Federal do Paraná (UFPR), Curitiba, PR, Brasil
  • Gustavo Strieder Scherer, Laboratório Central do Estado do Paraná (Lacen), Unidade de Fronteira, Foz do Iguaçu, PR, Brasil
  • Diego Averaldo Guiguet Leal, Laboratório de Parasitologia Ambiental, Departamento de Patologia Básica, Universidade Federal do Paraná (UFPR), Curitiba, PR, Brasil

References

1. Murphy B, Martini M, Fedi A, Loera BL, Elliott CT, Dean M. Consumer trust in organic food and organic certifications in four European countries. Food Control. 2022;133(Pt.B).https://doi.org/10.1016/j.foodcont.2021.108484

2. Jabłońska-Trypuć A, Wołejko E, Wydro U, Butarewicz A. The impact of pesticides on oxidative stress level in human organism and their activity as an endocrine disruptor. J Environ Sci Health B. 2017;52(7):483-94.https://doi.org/10.1080/03601234.2017.1303322

3. Kim KH, Kabir E, Jahan SA. Exposure to pesticides and the associated human health effects. Sci Total Environ. 2017;575:525-535.https://doi.org/10.1016/j.scitotenv.2016.09.009

4. Lima SK, Galiza M, Valadares A, Alves F. Produção e consumo de produtos orgânicos no mundo e no Brasil. Brasília:Instituto de Pesquisa Econômica Aplicada; 2020 [acesso 04 nov 2024]. Disponível em: https://www.ipea.gov.br.

5. Chaidez C, Soto M, Gortares P, Mena K. Occurrence of Cryptosporidium and Giardia in irrigation water and its impact on the fresh produce industry. Int J Environ Health Res. 2005;15(5):339-45.https://doi.org/10.1080/09603120500289010

6. Moreno Y, Moreno-Mesonero L, Amorós I, Pérez R, Morillo JA, Alonso JL. Multiple identification of most important waterborne protozoa in surface water used for irrigation purposes by 18S rRNA amplicon-based metagenomics. Int J Hyg Environ Health. 2018;221(1):102-11.https://doi.org/10.1016/j.ijheh.2017.10.008

7. Rusiñol M, Hundesa A, Cárdenas-Youngs Y, Fernández-Bravo A, Pérez-Cataluña A, Moreno-Mesonero L et al. Microbiological contamination of conventional and reclaimed irrigation water: evaluation and management measures. Sci Total Environ. 2020;710.https://doi.org/10.1016/j.scitotenv.2019.136298

8. Karanis P, Kourenti C, Smith H. Waterborne transmission of protozoan parasites: a worldwide review of outbreaks and lessons learnt. J Water Health. 2007;5(1):1-38.https://doi.org/10.2166/wh.2006.002

9. Troldborg M, Duckett D, Allan R, Hastings E, Hough RL. A risk-based approach for developing standards for irrigation with reclaimed water. Water Res. 2017;126:372-84.https://doi.org/10.1016/j.watres.2017.09.041

10. Mohamed MA, Siddig EE, Elaagip AH, Edris AMM, Nasr AA. Parasitic contamination of fresh vegetables sold at central markets in Khartoum state, Sudan. Ann Clin Microbiol Antimicrob. 2016;15:17.https://doi.org/10.1186/s12941-016-0133-5

11. Javanmard E, Mirjalali H, Niyyati M, Sharifdini M, Jalilzadeh E, Seyed Tabaei SJ et al. Small-scale risk assessment of transmission of parasites from wastewater treatment plant to downstream vegetable farms. Gastroenterol Hepatol Bed Bench. 2018;11(4):352-8.

12. Dantas LMDC, Maia CMDM, Damasceno KSFSCD, Seabra LMJ, Chaves G, Assis CF et al. Prevalence of helminths in fresh vegetables: a narrative literature review. J Sci Food Agric. 2022;103(8):3761-5. https://doi.org/10.1002/jsfa.12259

13. World Health Organization – WHO. A global overview of national regulations and standards for drinking-water quality. Geneva: World Health Organization; 2018[acesso 23 maio 2019]. Disponível em:https://apps.who.int/iris/bitstream/handle/10665/272345/9789241513760-eng.pdf?ua=1

14. Conselho Nacional do Meio Ambiente – Conama. Resolução Nº 357, de 17 de março de 2005. Classificação dos corpos de água e diretrizes ambientais para seu enquadramento, condições e padrões de lançamento de efluentes. Diário Oficial União. 18 mar 2005.

15. Agência Nacional de Vigilância Sanitária – Anvisa. Resolução RDC Nº 623, de 9 de março de 2022. Dispõe sobre os limites de tolerância para matérias estranhas em alimentos, os princípios gerais para o seu estabelecimento e os métodos de análise para fins de avaliação de conformidade. Diário Oficial União. 16 mar 2022.

16. Agência Nacional de Vigilância Sanitária – Anvisa. Resolução RDC Nº 724, de 1 de julho de 2022. Dispõe sobre os padrões microbiológicos dos alimentos e sua aplicação. Diário Oficial União. 6 jul 2022.

17. Agência Nacional de Vigilância Sanitária – Anvisa. Instrução normativa Nº 161, de 1 de julho de 2022. Estabelece os padrões microbiológicos dos alimentos. Diário Oficial União. 6 jul 2022.

18. Food and Agriculture Organization of the United Nations – FAO. Multicriteria-based ranking for risk management of food-borne parasites: report of a joint FAO/WHO expert meeting. Rome: Food and Agriculture Organization of the United Nations; 2014[acesso 05 nov 2024]. Disponível em:https://iris.who.int/handle/10665/112672

19. Ministério da Saúde (BR). Surtos de doenças de transmissão hídrica e alimentar: informe 2024. Brasília: Ministério da Saúde; 2024[acesso 24 abr 2025]. Disponível em: https://www.gov.br/saude/pt-br/assuntos/saude-de-a-a-z/d/dtha/publicacoes/surtos-de-doencas-de-transmissao-hidrica-ealimentar-no-brasil-informe-2024/view

20. Dixon B, Parrington L, Cook A, Pollari F, Farber J. Detection of Cyclospora, Cryptosporidium, and Giardia in ready-to-eat packaged leafy greens in Ontario, Canada. J Food Prot. 2013;76(2):307-13.https://doi.org/10.4315/0362-028X.JFP-12-282

21. Ryan U, Hijjawi N, Feng Y, Xiao L. Giardia: an underreported foodborne parasite. Int J Parasitol. 2019;49(1):1-11.https://doi.org/10.1016/j.ijpara.2018.07.003

22. American Public Health Association – APHA. Standard methods for the examination of water and wastewater. 23rd ed. Washington: American Public Health Association; 2017.

23. Leal DAG, Souza DSM, Caumo KS, Fongaro G, Panatieri LF, Durigan M et al. Genotypic characterization and assessment of infectivity of human waterborne pathogens recovered from oysters and estuarine waters in Brazil. Water Res. 2018;137:273-80.https://doi.org/10.1016/j.watres.2018.03.024

24. US Environmental Protection Agency – US-EPA. Method 1623.1: Cryptosporidium and Giardia in water by filtration/IMS/FA. EPA-815-R-05-002. Washington: US Environmental Protection Agency; 2012[acesso 05 nov 2024]. Disponível em: https://www.epa.gov/sites/default/files/2015-08/documents/epa_1623_1.pdf

25. Matosinhos FC, Valenzuela VC, Silveira JA, Rabelo EM.Standardization of a method for the detection of helminth eggs and larvae in lettuce. Parasitol Res. 2016;115(6):1827-34. https://doi.org/10.1007/s00436-016-4922-8

26. Pineda CO, Leal DAG, Lima R, Ribeiro PP, Rodrigues A, Martini MH et al. Parasites in fresh produce: a brazilian inter-laboratory evaluation of a standardized methodology for the detection of Ascaris sp. in leafy vegetables. Food Anal Methods. 2021;14:989-96.https://doi.org/10.1007/s12161-020-01925-x.

27. Scherer GS, Leal DAG, Goulart JAG, Araújo RS, Beux MR, Moreira NM. Parasitological, microbiological, and antimicrobial resistance profiles of raw and drinking water in a tourist city in the tri-border region of South America. J Water Health. 2022;20(2):385-95.https://doi.org/10.2166/wh.2022.256

28. Waideman MA, Teixeira VP, Uemura EH, Stamford TM, Leal DAG, Stangarlin-Fiori L et al. Enterococci used as complementary indicator of fecal contamination to assess water quality from public schools in the city of Curitiba, Paraná, Brazil. Braz J Food Technol. 2020;23:1-12.https://doi.org/10.1590/1981-6723.15519

29. Yamashiro S, Leal DAG, Cantusio Neto R, Franco RMB. Assessment of pathogenic protozoa in lentic and lotic compartments of a tropical reservoir impacted by cyanobacteria blooms in Brazil. Int J Biosci. 2015;6(2):304-17. https://doi.org/10.12692/ijb/6.2.304-5

30. Nishi L, Bergamasco R, Toledo MJO, Falavigna DLM, Gomes ML, Mota LT et al. Giardia spp. and Cryptosporidium spp. in the Ivaí Indigenous land, Brazil. Vector Borne Zoonotic Dis.2009;9(5):543-7. https://doi.org/10.1089/vbz.2008.0021

31. Almeida JC, Martins FDC, Ferreira Neto JM, Santos MM, Garcia JL, Navarro IT et al. Occurrence of Cryptosporidium spp. and Giardia spp. in a public water-treatment system, Paraná, Southern Brazil. Rev Bras Parasitol Vet. 2015;24(3):303-8.https://doi.org/10.1590/S1984-29612015051

32. Leal DAG, Goulart JAG, Bonatti TR, Araújo RS, Juski Junior JA, Shimada MK et al. A two-year monitoring of Cryptosporidium spp. oocysts and Giardia spp. cysts in freshwater and seawater: a complementary strategy for measuring sanitary patterns of recreational tropical coastal areas from Brazil. Reg Stud Mar Sci. 2024;70.https://doi.org/10.1016/j.rsma.2023.103356

33. Coelho CH, Durigan M, Leal DAG, Schneider AD, Franco RMB, Singer SM. Giardiasis as a neglected disease in Brazil: systematic review of 20 years of publications. PLoS Negl Trop Dis. 2017;11(10):1-22.https://doi.org/10.1371/journal.pntd.0006005

34. Thompson RCA, Colwell DD, Shury T, Appelbee AJ, Read C, Njiru Z et al. The molecular epidemiology of Cryptosporidium and Giardia infections in coyotes from Alberta, Canada, and observations on some cohabiting parasites. Vet Parasitol. 2009;159(2):167-70.https://doi.org/10.1016/j.vetpar.2008.10.003

35. Plutzer J, Tomor B. The role of aquatic birds in the environmental dissemination of human pathogenic Giardia duodenalis cysts and Cryptosporidium oocysts in Hungary. Parasitol Int. 2009;58(3):227-31. https://doi.org/10.1016/j.parint.2009.05.004

36. Swirski AL, Pearl DL, Peregrine AS, Pintar K. A comparison of exposure to risk factors for giardiasis in non-travellers, domestic travellers and international travellers in a Canadian community, 2006–2012. Epidemiol Infect. 2016;144(5):980-99.https://doi.org/10.1017/S0950268815002186

37. LeChevallier MW, Norton WD. Examining relationships between particle counts and Giardia, Cryptosporidium, and turbidity. J Am Water Works Assoc.1992;84(12):54-60.

38. Kumar T, Abd Majid MA, Onichandran S, Jaturas N, Andiappan H, Salibay CC et al. Presence of Cryptosporidium parvum and Giardia lamblia in water samples from Southeast Asia: towards an integrated water detection system. Infect Dis Poverty. 2016;5:1-12.https://doi.org/10.1186/s40249-016-0095-z

39. Ahmed A, Ijaz M, Ayyub RM, Ghaffar A, Ghauri HN, Aziz MU et al. Balantidium coli in domestic animals: an emerging protozoan pathogen of zoonotic significance. Acta Trop. 2020;203.https://doi.org/10.1016/j.actatropica.2019.105298

40. Ponce-Gordo F, García-Rodríguez JJ. Balantioides coli. Res Vet Sci. 2021;135:424-31.https://doi.org/10.1016/j.rvsc.2020.10.028

41. Ferry T, Bouhour D, De Monbrison F, Laurent F, Dumouchel-Champagne H, Picot S et al. Severe peritonitis due to Balantidium coli acquired in France. Eur J Clin Microbiol Infect Dis. 2004;23(4):393-5.https://doi.org/10.1007/s10096-004-1126-4

42. Gomez Hinojosa P, Espinoza-Ríos J, Carlin Ronquillo A, Pinto Valdivia JL, Salas Dueñas Y, Zare Morales W. Balantidiasis colónica: reporte de un caso fatal y revisión de la literatura. Rev Gastroenterol Perú. 2019;39(3):227-234.https://doi.org/10.31403/rgp.v39i3.849

43. Panti-May JA, Servían A, Ferrari W, Zonta ML, Hernández-Mena DI, Hernández-Betancourt SF et al. Morphological and molecular identification of hymenolepidid cestodes in children and synanthropic rodents from rural Mexico. Parasitol Int. 2020;75.https://doi.org/10.1016/j.parint.2019.102042

44. Fallah AA, Pirali-Kheirabadi K, Shirvani F, Saei-Dehkordi SS. Prevalence of parasitic contamination in vegetables used for raw consumption in Shahrekord, Iran: Influence of season and washing procedure. Food Control. 2012;25(2):617-20.https://doi.org/10.1016/j.foodcont.2011.12.004

45. Hotez PJ. Human parasitology and parasitic diseases:heading towards 2050. In: Rollinson D, Stothard JR, editors. Advances in parasitology. Vol. 100. Amsterdam: Elsevier; 2018. p. 29-38.

46. Sadowska N, Tomza-Marciniak A, Juszczak M. Soil contamination with geohelminths in children’s play areas in Szczecin, Poland. Ann Parasitol. 2019;65(1):65-70.https://doi.org/10.17420/ap6501.183

Published

2025-12-12

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From cultivation to commercialization: assessing the sanitary quality of various stages of organic vegetable production chain in southern Brazil: Vigil Sanit Debate, Rio de Janeiro, 2025, v.13: e02415 | Published on: 16/10/2025. (2025). Health Surveillance under Debate: Society, Science & Technology , 13, 1-11. https://doi.org/10.22239/2317-269X.02415