Advertisement

Parasitology Research

, Volume 118, Issue 12, pp 3449–3457 | Cite as

Food safety assessment and risk for toxoplasmosis in school restaurants in Armenia, Colombia

  • Julio César Luna
  • Alejandro Zamora
  • Natalia Hernández-Arango
  • Deicy Muñoz-Sánchez
  • Magda Ivonne Pinzón
  • Jesús Alfredo Cortés-Vecino
  • Fabiana Lora-Suarez
  • Jorge Enrique Gómez-MarínEmail author
Protozoology - Original Paper

Abstract

We assessed the risk for toxoplasmosis in 10 school restaurants in Armenia (Quindio, Colombia). We analyzed the presence of Toxoplasma gondii DNA in the food, water, and living and inert surfaces of school restaurants, and we correlated these findings with the results of food safety inspection scores and with the prevalence of specific anti-T. gondii antibodies in children who ate at these restaurants. Of the 213 samples, 6.1% were positive using PCR to test for T. gondii DNA. Positive samples were found in meat, water, cucumber, guava juice, inert surfaces, and living surfaces. In 60% (6/10) of the public school restaurants, there was at least one PCR T. gondii-positive sample. In 311 serum samples from children who attended the restaurants, 101 (33%) were positive for IgG and 12 (3.9%) for IgM anti-T. gondii. The median of the compound score for the fulfillment of inspection for food safety conditions was of 60.7% (range 50–72). Higher T. gondii PCR positivity in surfaces, food, or water at each restaurant was correlated with lower inspection scores for water supply and water storage conditions. Lower scores in physical infrastructure and disinfection procedures and higher scores in furniture were correlated with a higher prevalence of IgG anti-T. gondii in children who ate at those restaurants. Inspection scores can identify restaurants with a higher risk for the presence of T. gondii.

Keywords

Toxoplasma Foodborne protozoa PCR Molecular detection 

Notes

Acknowledgments

We thank Dr. Dubey (USDA, Belstville) who kindly donated T. gondii oocysts.

Funding information

This work was funded by the Universidad del Quindio and Colciencias Grant Number: 111372553376.

Compliance with ethical standards

The protocol of this study was approved by the institutional ethical committee for the Faculty of Health Sciences of the Universidad del Quindio (Act 35 of May 14, 2012).

Conflict of interest

The authors declare they have no conflict of interest.

Supplementary material

436_2019_6473_MOESM1_ESM.docx (80 kb)
ESM 1 (DOCX 79 kb)

References

  1. Alvarez C, de-la-Torre A, Vargas M et al (2015) Striking divergence in Toxoplasma ROP16 nucleotide sequences from human and meat samples. J Infect Dis 211:1–8.  https://doi.org/10.1093/infdis/jiu833 CrossRefGoogle Scholar
  2. Bik HM, Maritz JM, Luong A et al (2016) Microbial community patterns associated with automated teller machine keypads in New York City. mSphere 1:e00226-16.  https://doi.org/10.1128/mSphere.00226-16
  3. Cañón-Franco W, López-Orozco N, Gómez-Marín J, Dubey JP (2014) An overview of seventy years of research (1944 – 2014) on toxoplasmosis in Colombia, South America. Parasit Vectors 7:427.  https://doi.org/10.1186/1756-3305-7-427 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Cook N, Nichols RAB, Wilkinson N, Paton CA, Barker K, Smith HV (2007) Development of a method for detection of Giardia duodenalis cysts on lettuce and for simultaneous analysis of salad products for the presence of Giardia cysts and Cryptosporidium oocysts. Appl Environ Microbiol 73:7388–7391.  https://doi.org/10.1128/AEM.00552-07 CrossRefPubMedPubMedCentralGoogle Scholar
  5. da Cunha DT, de Rosso VV, Stedefeldt E (2016) Should weights and risk categories be used for inspection scores to evaluate food safety in restaurants? J Food Prot 79:501–506.  https://doi.org/10.4315/0362-028X.JFP-15-292 CrossRefPubMedGoogle Scholar
  6. DANE (2018) Reloj de población. Reloj de población, In http://www.dane.gov.co/reloj/. Google Scholar
  7. De Moura L, Garcia Bahia-Oliveira LM, Wada MY et al (2006) Waterborne toxoplasmosis, Brazil, from field to gene. Emerg Infect Dis 12:326–329.  https://doi.org/10.3201/eid1202.041115 CrossRefPubMedPubMedCentralGoogle Scholar
  8. FAO/WHO (2014) Multicriteria-based ranking for risk management of food-borne parasites, First. WHO/FAO, GenevaGoogle Scholar
  9. Franco-Hernandez EN, Acosta A, Cortés-Vecino J, Gómez-Marín JE (2016) Survey for Toxoplasma gondii by PCR detection in meat for human consumption in Colombia. Parasitol Res 115:691–695.  https://doi.org/10.1007/s00436-015-4790-7 CrossRefPubMedGoogle Scholar
  10. Lee P, Hedberg CW (2016) Understanding the relationships between inspection results and risk of foodborne illness in restaurants. Foodborne Pathog Dis 13:582–586.  https://doi.org/10.1089/fpd.2016.2137 CrossRefPubMedGoogle Scholar
  11. Lora-suarez F, Aricapa J, Pérez J, et al. (2007) Detección de Toxoplasma gondii en carnes de consumo humano por la técnica de reacción en cadena de la polimerasa en tres ciudades del eje cafetero. 117–123Google Scholar
  12. Lora-Suarez F, Rivera R, Triviño-Valencia J, Gomez-Marin JE (2016) Detection of protozoa in water samples by formalin/ether concentration method. Water Res 100:377–381.  https://doi.org/10.1016/j.watres.2016.05.038 CrossRefPubMedGoogle Scholar
  13. Robertson LJ (2016) Parasitic protozoa in salad vegetables. Food hygiene and toxicology in ready-to-eat foods, In, pp 69–88Google Scholar
  14. Rousseau A, La Carbona S, Dumètre A et al (2018) Assessing viability and infectivity of foodborne and waterborne stages (cysts/oocysts) of Giardia duodenalis, Cryptosporidium spp., and Toxoplasma gondii : a review of methods. Parasite 25:14.  https://doi.org/10.1051/parasite/2018009 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Tripepi G, Jager KJ, Dekker FW, Zoccali C (2010) Stratification for confounding – part 1: the Mantel-Haenszel formula. Nephron Clin Pract 116:c317–c321.  https://doi.org/10.1159/000319590 CrossRefPubMedGoogle Scholar
  16. Triviño-Valencia J, Lora F, Zuluaga JD, Gomez-Marin JE (2016) Detection by PCR of pathogenic protozoa in raw and drinkable water samples in Colombia. Parasitol Res 115:1789–1797.  https://doi.org/10.1007/s00436-016-4917-5 CrossRefPubMedGoogle Scholar
  17. Zamora-Vélez A, Cuadrado-Ríos S, Triviño-Valencia J et al (2016) Diversidad Genética Y Filogenia De Toxoplasma Gondii a Partir De Secuencias Parciales De B1 De Colombia Y Otros Países. Rev la Asoc Colomb Ciencias Biológicas 28:8–15Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Julio César Luna
    • 1
  • Alejandro Zamora
  • Natalia Hernández-Arango
    • 1
  • Deicy Muñoz-Sánchez
    • 1
  • Magda Ivonne Pinzón
    • 2
  • Jesús Alfredo Cortés-Vecino
    • 3
  • Fabiana Lora-Suarez
    • 1
  • Jorge Enrique Gómez-Marín
    • 1
    Email author
  1. 1.Grupo Parasitología Molecular (GEPAMOL), Centro de Investigaciones Biomédicas, Facultad de Ciencias de la SaludUniversidad del QuindioArmeniaColombia
  2. 2.Facultad de Ciencias AgroindustrialesUniversidad del QuindíoArmeniaColombia
  3. 3.Laboratorio de Parasitología Veterinaria, Grupo de Parasitología Veterinaria, Departamento de Salud Animal, Facultad de Medicina Veterinaria y de ZootecniaUniversidad Nacional de ColombiaBogotáColombia

Personalised recommendations