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Licensed Unlicensed Requires Authentication Published by De Gruyter January 17, 2018

Changes in the incidence of intestinal giardiosis in Mexican population during five years (2011-2015)

Gabriela Ibáñez-Cervantes, Gloria León-Ávila, Juan Manuel Bello-López, Armando Pérez-Rangel, Gregorio León-García, Benjamín Nogueda-Torres and José Manuel Hernández
From the journal Acta Parasitologica

Abstract

Giardiosis is a parasitic disease caused by the protozoan Giardia intestinalis, which is distributed worldwide. Most of the data on the prevalence of giardiosis in Mexico comes from research, but it is also necessary to study the data provided by the Mexican Health Ministry and issued by the General Directorate of Epidemiology. The aim of this work was analyse the national surveillance data for human giardiosis in order to update the epidemiological data of this disease in Mexico. A retrospective observational analysis of giardiosis (from January 2011 to December 2015) was performed in the annual reports emitted by the GDE in Mexico. The cases were classified by year, state, age group, gender and seasons of the year. During the period of 2011–2015, a reduction of 38.51% was observed in the total number of new cases of giardiosis reported in the whole country The states of Sinaloa, Yucatan, and Chiapas presented the highest number of new cases reported during the analysed period. Giardiosis rates were always higher among women in all age groups, but the maximum incidence was observed in both sexes in the age group of 1–4 years old (the most susceptible group). On the other hand, the number of cases increased dramatically in southern states during warmer months. Giardiosis is influenced by ambient temperature changes along the year, although this study suggests that tends to decrease in all the analysed states and could be related to the overall improvement of hygienic practices within the Mexican population,

  1. Authors’ contributions: GIC, APR, JMBL, GLA, GLG, BNT and JMHH designed the study; GIC, APR, JMBL, GLA, GLG, BNT and JMHH analysed and interpreted the data and results; GIC, GLA, JMBL and JMHH gave a major contribution to the writing. All authors read and approved the final manuscript. GIC, GLA, JMBL, and JMHH are guarantors of the paper.

  2. Competing interests: the authors reported no potential conflict of interest.

  3. Ethical approval: Not required.

  4. Funding: This work was supported by the Consejo Nacional de Ciencia y Tecnología, México [grants 167376 (GLA), 180016 (JMHH), postdoctoral position 205977 (GIC)] and SIP20160735, SIP20170589 (GLA).

Acknowledgements

The authors thank Miss Jimena Hernández León for the critical review of the manuscript.

References

Ali S.A., Hill D.R. 2003. Giardia intestinalis. Current Opinion in Infectious Diseases, 16, 453–460. 10.1097/01.qco.0000092817.64370.abSearch in Google Scholar PubMed

Balderrama-Carmona A.P., Gortáres-Moroyoqui P., Álvarez-Valencia L.H., Castro-Espinoza L., Balderas-Cortés J de J., Mondaca-Fernández I., et al. 2015. Quantitative microbial risk assessment of Cryptosporidium and Giardia in well water from a native community of Mexico. International Journal of Environmental Health Research, 25, 570–582. 10.1080/09603123.2014.989492Search in Google Scholar PubMed

Berkman D.S., Lescano A.G., Gilman R.H., Lopez S.L., Black M.M. 2002. Effects of stunting, diarrhoeal disease, and parasitic infection during infancy on cognition in late childhood: a follow-up study. Lancet. 16, 564–571. 10.1016/S0140-6736(02)07744-9Search in Google Scholar

Bonadonna L., Briancesco R., Magini V., Orsini M., Romano-Spica V. 2004. A preliminary investigation on the occurrence of protozoa in swimming pools in Italy. Annali di igiene: medicina preventiva e di comunita, 16,709–19Search in Google Scholar PubMed

Castro–Espinoza L., Gortáres–Moroyoqui P., Mondaca–Fernández I. 2009. Emerging pathogens as restriction to the reuse of treated municipal wastewaters from Ciudad Obregon, Sonora, Mexico. Revista Latinoamericana de Recursos Naturales, 5, 9–21Search in Google Scholar

Cedillo-Rivera R., Leal Y.A., Yépez-Mulia L., Gómez-Delgado A., Ortega-Pierres G., Tapia-Conyer R., et al. 2009. Seroepidemiology of giardiosis in Mexico. American Journal of Tropical Medicine and Hygiene, 80, 6–1010.4269/ajtmh.2009.80.6Search in Google Scholar

Chaidez C., Soto M., Gortares P., Mena K. 2005. Occurrence of Cryptosporidium and Giardia in irrigation water and its impact on the fresh produce industry. International Journal of Environmental Health Research, 155, 339–345. 10.1080/09603120500289010Search in Google Scholar PubMed

Children’s health and environment in North America. A first report on indicators and Measures, National Report: Mexico. Ministry of Health, 2005. MexicoSearch in Google Scholar

Cifuentes E., Suárez L., Espinosa M., Juárez-Figueroa L., Martínez-Palomo A. 2004. Risk of Giardia intestinalis infection in children from an artificially recharged groundwater area in Mexico City. American Journal of Tropical Medicine and Hygiene, 71,65–7010.4269/ajtmh.2004.71.65Search in Google Scholar

Diagnosis and Treatment of Giardiasis in Children and Adolescents aged 1 to 18 years in the First and Second Level of Care. In Spanish. 2012. México, Secretaría de SaludSearch in Google Scholar

Dawson D. 2005. Foodborne protozoan parasites. International Journal of Food Microbiology, 103, 207–227. doi.org/10.1016/j.ijfoodmicro.2004.12.032Search in Google Scholar PubMed

Efstratiou A., Ongerth J., Karanis P. 2017. Evolution of monitoring for Giardia and Cryptosporidium in water. Water Research, 123, 96–112. 10.1016/j.watres.2017.06.042Search in Google Scholar PubMed

Fletcher S., Caprarelli G., Merif J., Andresen D., Hal S.V., Stark D., et al. 2014. Epidemiology and geographical distribution of enteric protozoan infections in Sydney, Australia. Journal of Public Health Research, 3, 298. 10.4081/jphr.2014.298Search in Google Scholar PubMed PubMed Central

Gautret P., Cramer J.P., Field V., Caumes E., Jensenius M., Gkrania-Klotsas E., et al. 2012. Infectious diseases among travellers and migrants in Europe. Eurosourveillance, 17. pii:2020510.2807/ese.17.26.20205-enSearch in Google Scholar

Guerrant DI., Moore SR., Lima AA., Patrick PD., Schorling JB., Guerrant RL. 1999. Association of early childhood diarrhea and cryptosporidiosis with impaired physical fitness and cognitive function four-seven years later in a poor urban community in northeast Brazil. American Journal of Tropical Medicine and Hygiene, 61, 707–71310.4269/ajtmh.1999.61.707Search in Google Scholar

Graczyk T.K., Kacprzak M., Neczaj E., Tamang L., Graczyk H., Lucy F.E., et al. 2008. Occurrence of Cryptosporidium and Giardia in sewage sludge and solid waste landfill leachate and quantitative comparative analysis of sanitization treatments on pathogen inactivation. Environmental Research, 106, 27–33. 10.1016/j.envres.2007.05.005Search in Google Scholar PubMed

Heimer J., Staudacher O., Steiner F., Kayonga Y., Havugimana J.M., Musemakweri A., et al. 2015. Age–dependent decline and association with stunting of Giardia duodenalis infection among schoolchildren in rural Huye district, Rwanda. Acta Tropica, 145, 17–22. 10.1016/j.actatropica.2015.01.01110.1016/j.actatropica.2015.01.011Search in Google Scholar PubMed

Hoque M.E., Hope V.T., Scragg R., Kjellstróm T., Lay-Yee R. 2001. Nappy handling and risk of giardiasis. Lancet, 37, S13–19. 10.1016/S0140-6736(00)04251-3Search in Google Scholar

Ignatius R., Gahutu J.B., Klotz C., Steininger C., Shyirambere C., Lyng M., et al. 2012. High prevalence of Giardia duodenalis Assemblage B infection and association with underweight in Rwandan children. PLoS Negl Trop Dis, 6, e1677. 10.1371/journal.pntd.0001677Search in Google Scholar PubMed

Karanis P., Kourenti C., Smith H. 2007. Waterborne transmission of protozoan parasites: a worldwide review of outbreaks and lessons learnt. Journal of Water and Health, 5, 1–3810.2166/wh.2006.002Search in Google Scholar PubMed

Lim Y.A., Ahmad R.A., Smith H.V. 2008. Current status and future trends in Cryptosporidium and Giardia epidemiology in Malaysia. Journal of Water and Health, 6, 239–254. 10.2166/wh.2008.023Search in Google Scholar PubMed

Linnane E., Roberts R., Looker N. 2001. Nappies and transmission of Giardia lamblia between children. Lancet, 358, 50710.1016/S0140-6736(01)05646-XSearch in Google Scholar PubMed

Mukherjee A.K., Chowdhury P., Rajendran K., Nozaki T., Ganguly S. 2014. Association between Giardia duodenalis and coinfection with other diarrhea–causing pathogens in India Biomed Research International, 2014, ID786480. 10.1155/2014/786480Search in Google Scholar PubMed PubMed Central

Monzingo D.L., Hibler C.P. 1987. Prevalence of Giardia sp. in a beaver colony and the resulting environmental contamination. Journal of Wild life Diseases, 23, 576–58510.7589/0090-3558-23.4.576Search in Google Scholar PubMed

Morales-Espinoza E.M., Sánchez-Pérez H.J., García-Gil M. del M, Vargas-Morales G., Méndez-Sánchez J.D., Pérez-Ramírez M. 2003. Intestinal parasites in children, in highly deprived areas in the border region of Chiapas, Mexico. Salud Publica de México, 45, 379–38810.1590/S0036-36342003000500008Search in Google Scholar PubMed

National Development Plan 2013–2018. Government of México. National Water Program. http://www.conagua.gob.mx/CONAGUA07/Contenido/documentos/PROGRAMA_Na-cional_Hidrico_2014_2018_ingles.pdfSearch in Google Scholar

Neghina R., Dumitrascu V., Neghina A.M., Vlad D.C., Petrica L., Vermesan D., et al. 2013. Epidemiology of ascariasis, enterobiasis and giardiosis in a Romanian western county (Timis), 1993–2006. Acta Tropica, 125, 98–101. 10.1016/j.acta-tropica.2012.10.005Search in Google Scholar

NORMA Oficial Mexicana NOM–017–SSA2–2012, Para la vigilancia epidemiológica. In spanishSearch in Google Scholar

NORMA OFICIAL MEXICANA NOM–127–SSA1–1994, “Salud ambiental, agua para uso y consumo humano–límites permisibles de calidad y tratamientos a que debe someterse el agua para su potabilizacion”. http://www.salud.gob.mx/unidades/cdi/nom/127ssa14.html. (In Spanish)Search in Google Scholar

NORMA OFICIAL MEXICANA. NOM–014–SSA1–1993 “Procedimientos sanitarios para el muestreo de agua para uso y consumo humano en sistemas de abastecimiento de agua públicos y privados”. http://www.salud.gob.mx/unidades/cdi/nom/014ssa13.html. (In Spanish)Search in Google Scholar

Ortega Y, Adam R.D. 1997. Giardia: overview and update. Clinical infectious diseases 25, 545–549. 10.1086/513745Search in Google Scholar PubMed

Painter J.E., Gargano J.W., Collier S.A., Yoder J.S., Centers for Disease Control and Prevention. 2015. Giardiasis surveillance. United States, 2011–2012. Morbidity and mortality weekly report Recommendations and reports, Surveillance summaries, 64, 15–25Search in Google Scholar

Paniagua G.L., Monroy E., García-González O., Alonso J., Negrete E., Vaca S. 2007. Two or more enteropathogens are associated with diarrhoea in Mexican children. Annals of clinical microbiology and antimicrobials, 28, 6–17. 10.1186/1476-0711-6-17Search in Google Scholar PubMed PubMed Central

Quihui L., Valencia M.E., Crompton D.W., Phillips S., Hagan P., Morales G., et al. 2006. Role of the employment status and education of mothers in the prevalence of intestinal parasitic infections in Mexican rural schoolchildren. BMC Public Health, 6,225–232. 10.1186/1471-2458-6-225Search in Google Scholar PubMed PubMed Central

Quihui–Cota L., Morales–Figueroa G.G. 2012. Persistence of intestinal parasitic infections during the national de–worming campaign in schoolchildren of northwestern Mexico: a cross–sectional study. Annals of Gastroenterology, 25, 57–60Search in Google Scholar PubMed

Rickard LG., Siefker C., Boyle CR., Gentz. 1999. The prevalence of Cryptosporidium and Giardia spp. in fecal samples from free-ranging white-tailed deer (Odocoileus virginianus) in the southeastern United States. Journal of Veterinary Diagnostic Investigation, 11, 65–72. 10.1177/104063879901100111Search in Google Scholar PubMed

Rodríguez-Morales A.J., Granados-Álvarez S., Escudero-Quintero H., Vera-Polania F., Mondragon-Cardona A., Díaz-Quijano F.A. 2016. Estimating and mapping the incidence of giardiasis in Colombia, 2009–2013. International Journal of Infectious Diseases, 49, 204–209. 10.1016/j.ijid.2016.06.005Search in Google Scholar PubMed

Rosado-García F. M., Guerrero-Flórez M., Karanis G., Hinojosa M.D.C., Karanis P. 2017. Water-borne protozoa parasites: The Latin American perspective. International Journal of Hygiene and Environmental Health, 220, 783–798 10.1016/j.ijheh.2017.03.008Search in Google Scholar PubMed

Ryu H., Abbaszadegan M. 2008. Long–term study of Cryptosporidium and Giardia occurrence and quantitative microbial risk assessment in surface waters of Arizona in the US. Journal of Water and Health, 62, 263–273. 10.2166/wh.2008.030Search in Google Scholar PubMed

Sánchez-Vega J.T., Tay-Zavala J., Aguilar-Chiu A., Ruiz-Sánchez D., Malagón F., Rodríguez-Covarrubias J.A., et al. 2006. Cryptosporidiosis and other intestinal protozoan infections in children less than one year of age in Mexico City. American Journal of Tropical Medicine and Hygiene, 75, 1095–109810.4269/ajtmh.2006.75.1095Search in Google Scholar

Shields J.M., Gleim E. R., Beach M. J. 2008. Prevalence of Cryptosporidium spp. and Giardia intestinalis in swimming pools, Atlanta, Georgia. Emerging Infectious Diseases, 14, 948–950. 10.3201/eid1406.071495Search in Google Scholar PubMed

Steiner T.S., Thielman N.M., Guerrant R.L. 1997. Protozoal agents: what are the dangers for the public water supply? Annual Review of Medicine. 48, 329–40. doi.org/10.1146/annurev.med.48.1.329Search in Google Scholar PubMed

Tay J., Ruiz A., Schenone H., Robert L., Sánchez-Vega J.T., Uribarren T. 1994. Frequency of intestinal protozoosis in the Mexican Republic. Boletín de Informaciones parasitarias Chilenas, 49, 9–15Search in Google Scholar

Thompson R.C.A. 2000. Giardiasis as a re-emerging infectious disease and its zoonotic potential. International Journal of Parasitology, 30, 1259–1267. 10.1016/S0020-7519(00)00127–2Search in Google Scholar

Vázquez T.O., Campos R.T. Giardiasis. 2009. Giardiasis. La parasitosis más frecuente a nivel mundial. Revista del Centro de Investigación de la Universidad La Salle, 8, 75–90. (In Spanish)Search in Google Scholar

Wallis P.M., Buchanan-Mappin J.M., Faubert G.M., Belosevic M. 1984. Reservoirs of Giardia spp. in southwestern Alberta. Journal of Wild Life Diseases, 20, 279–28310.7589/0090-3558-20.4.279Search in Google Scholar PubMed

World Health Organization (WHO). 2007. Combating waterborne disease at the household level/International Network to Promote Household Water Treatment and Safe Storage, World Health OrganizationSearch in Google Scholar

Yoder J.S., Harral C., Beach M.J. Centers for Disease Control and Prevention (CDC). Giardiasis surveillance – United States, 2006-2008. Morbidity and mortality weekly report Recommendations and reports Surveillance summaries, 2010, 59, 15–25Search in Google Scholar

Received: 2017-7-7
Revised: 2017-10-5
Accepted: 2017-10-9
Published Online: 2018-1-17
Published in Print: 2018-3-26

© 2018 W. Stefański Institute of Parasitology, PAS