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Diversity and Prevalence of Helminths and Protozoa Among Pregnant Women in Tropical Ecuador: Implications for Chemotherapy
Manuel Calvopina
manuelcalvopina@gmail.com
Manuel Calvopina
One Health Research Group, Facultad de Medicina, Universidad de las Américas (UDLA), Quito, Ecuador;
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Jesse Contreras
Jesse Contreras
Department of Epidemiology, University of Michigan, Ann Arbor, Michigan;
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William Cevallos
William Cevallos
Instituto de Biomedicina, Facultad de Ciencias Médicas, Universidad Central del Ecuador, Quito, Ecuador;
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Gwenyth Lee
Gwenyth Lee
Rutgers Global Health Institute and Department of Biostatistics and Epidemiology, Rutgers University, New Brunswick, New Jersey;
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Karen Levy
Karen Levy
Department of Environmental and Occupational Health Sciences, University of Washington, Seattle, Washington
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Joseph N. S. Eisenberg
jnse@umich.edu
Joseph N. S. Eisenberg
Department of Epidemiology, University of Michigan, Ann Arbor, Michigan;
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ABSTRACT.
Deworming for pregnant women using a single dose of albendazole or mebendazole is recommended by the WHO in areas where the baseline prevalence of hookworm and/or trichuriasis is >20%. However, other helminths and protozoa infecting pregnant women are not affected by these drugs and dosages. To assess the prevalence and diversity of intestinal helminth and protozoan infections, we analyzed stool samples from pregnant women recently enrolled into a birth cohort, along a rural-urban gradient in northern coastal Ecuador from 2019 to 2022. Participants provided a stool sample in their third trimester (n = 444). Samples were concentrated by the Ritchie method and observed microscopically for the detection of cysts, eggs, and larvae. The overall prevalence of infection with one or more parasites was 69% (95% CI: 67–74%), ranging from 52% in urban participants to 76% in rural participants (percentile rank = 1.39, 95% CI: 1.07–1.87). This differential between urban and rural communities persisted when data were disaggregated into helminth and protozoan infections (prevalence = 19% and 46%, respectively, in urban participants compared with 42% and 58% among rural participants). The most prevalent helminth was Ascaris lumbricoides (27%), followed by Trichuris trichiura (13%) and hookworm (7.4%). Hymenolepis nana, Strongyloides stercoralis, and Enterobius vermicularis were also observed. Six protozoan pathogens were detected, including Entamoeba histolytica/dispar (23%), Giardia intestinalis (5%), and Balantidium coli, along with nine protozoa that are nonpathogenic or of debated pathogenicity. The high infection burden and diversity of intestinal parasites found in this study highlight a need to revise strategies for preventing and treating intestinal parasitic infections in pregnant women.
Author Notes
Financial support: This work was partially supported by an award from the
Disclosure: The study protocol was approved by the ethics committee of the Universidad San Francisco-Quito (2018-022M), Emory University (IRB00101202), and the Ministerio de Salud Pública del Ecuador (MSP-DIS-2019-0002-O).
Current contact information: Manuel Calvopina, One Health Research Group, Facultad de Medicina, Universidad de las Américas (UDLA), Quito, Ecuador, E-mail: manuel.calvopina@udla.edu.ec. Jesse Contreras and Joseph N. S. Eisenberg, Department of Epidemiology, University of Michigan, Ann Arbor, MI, E-mails: jdcon@umich.edu and jnse@umich.edu. William Cevallos, Instituto de Biomedicina, Facultad de Ciencias Médicas, Universidad Central del Ecuador, Quito, Ecuador, E-mail: wcevallos@uce.edu.ec. Gwenyth Lee, Rutgers Global Health Institute, Department of Biostatistics and Epidemiology, School of Public Health, Rutgers, The State University of New Jersey, New Brunswick, NJ, E-mail: gwenyth.lee@globalhealth.rutgers.edu. Karen Levy, Department of Environmental and Occupational Health Sciences, University of Washington, Seattle, WA, E-mail: klevyx@uw.edu.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
de Silva NR, Brooker S, Hotez PJ, Montresor A, Engels D, Savioli L, 2003. Soil-transmitted helminth infections: Updating the global picture. Trends Parasitol 19: 547–551.
-
2.
World Health Organization, 2017. Guideline: Preventive Chemotherapy to Control Soil-Transmitted Helminth Infections in At-Risk Population Groups. Geneva, Switzerland: WHO.
-
3.
Taghipour A, Ghodsian S, Jabbari M, Olfatifar M, Abdoli A, Ghaffarifar F, 2021. Global prevalence of intestinal parasitic infections and associated risk factors in pregnant women: A systematic review and meta-analysis. Trans R Soc Trop Med Hyg 115: 457–470.
-
4.
Espinosa Aranzales AF, Radon K, Froeschl G, Pinzón Rondón ÁM, Delius M, 2018. Prevalence and risk factors for intestinal parasitic infections in pregnant women residing in three districts of Bogotá, Colombia. BMC Public Health 18: 1071.
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5.
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6.
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7.
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8.
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9.
Abdoli A, Pirestani M, 2014. Are pregnant women with chronic helminth infections more susceptible to congenital infections? Front Immunol 5: 53.
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10.
Saboyá MI, Catalá L, Nicholls RS, Ault SK, 2013. Update on the mapping of prevalence and intensity of infection for soil-transmitted helminth infections in Latin America and the Caribbean: A call for action. PLoS Negl Trop Dis 7: e2419.
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11.
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14.
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-
15.
Camacho-Alvarez I, Goyens P, Luizaga-López JM, Jacobs F, 2021. Geographic differences in the distribution of parasitic infections in children of Bolivia. Parasite Epidemiol Control 14: e00217.
-
16.
Riesel JN, Ochieng’ FO, Wright P, Vermund SH, Davidson M, 2009. High prevalence of soil-transmitted helminths in western Kenya: Failure to implement deworming guidelines in rural Nyanza Province. J Trop Pediatr 56: 60–62.
-
17.
Bryan PE, Romero M, Sánchez M, Torres G, Gómez W, Restrepo M, Restrepo A, Mejia R, 2021. Urban versus rural prevalence of intestinal parasites using multi-parallel qPCR in Colombia. Am J Trop Med Hyg 104: 907–909.
-
18.
Langbang D, Dhodapkar R, Parija S, Premarajan K, Rajkumari N, 2019. Prevalence of intestinal parasites among rural and urban population in Puducherry, South India—A community-based study. J Family Med Prim Care 8: 1607–1612.
-
19.
Chelkeba L, Mekonnen Z, Alemu Y, Emana D, 2020. Epidemiology of intestinal parasitic infections in preschool and school-aged Ethiopian children: A systematic review and meta-analysis. BMC Public Health 20: 117.
-
20.
Phiri K, Whitty CJM, Graham SM, Ssembatya-Lule G, 2000. Urban/rural differences in prevalence and risk factors for intestinal helminth infection in southern Malawi. Ann Trop Med Parasitol 94: 381–387.
-
21.
Nolan LB, 2015. Slum definitions in urban India: Implications for the measurement of health inequalities. Popul Dev Rev 41: 59–84.
-
22.
Montresor A, Comprton DW, Hall A, Bundy DA, Savioli L, 1998. Guidelines for the Evaluation of Soil-Transmitted Helminthiasis and Schistosomiasis at Community Level. Geneva, Switzerland: WHO.
-
23.
Sangaré I, Guiguemdé KT, Zida A, Sirima C, Sawadogo PM, Cissé M, Assogba SB, Guiguemdé TR, Bamba S, 2021. Prevalence of intestinal parasitic infections among pregnant women in Bobo-Dioulasso (Burkina Faso). Ann Parasitol 67: 489–497.
-
24.
Steinmann P, Du Z-W, Wang L-B, Wang X-Z, Jiang J-Y, Li L-H, Marti H, Zhou X-N, Utzinger J, 2008. Extensive multiparasitism in a village of Yunnan province, People’s Republic of China, revealed by a suite of diagnostic methods. Am J Trop Med Hyg 78: 760–769.
-
25.
Centers for Disease Control and Prevention, 2020. Resources for Health Professionals: Parasites, Blastocystis Spp. Infection. Available at: https://www.cdc.gov/parasites/blastocystis/health_professionals/index.html. Accessed January 25, 2024.
-
26.
Durán Pincay Y, Rivero De Rodríguez Z, Quimis Cantos Y, García Figueroa M, 2023. Parasitosis intestinales en el ecuador. Revisión Sistemática. Kasmera [Internet]. 19 de abril de 2023 [citado 11 de octubre de 2024];51:e5137705.
-
27.
Tapia-Veloz E, Gozalbo M, Guillén M, Dashti A, Bailo B, Köster PC, Santín M, Carmena D, Trelis M, 2023. Prevalence and associated risk factors of intestinal parasites among schoolchildren in Ecuador, with emphasis on the molecular diversity of Giardia duodenalis, Blastocystis sp. and Enterocytozoon bieneusi. PLoS Negl Trop Dis 17: e0011339.
-
28.
Palacios T-E, 2017. Prevalencia de Cryptosporidium spp. y Giardia spp. en terneros, y su presencia en agua y en niños con problemas digestivos en el cantón San Fernando, Ecuador. MASKANA 8: 111–119.
-
29.
Vasco K, Graham JP, Trueba G, 2016. Detection of zoonotic enteropathogens in children and domestic animals in a semirural community in Ecuador. Appl Environ Microbiol 82: 4218–4224.
-
30.
Weatherhead J, Cortés AA, Sandoval C, Vaca M, Chico M, Loor S, Cooper PJ, Mejia R, 2017. Comparison of cytokine responses in Ecuadorian children infected with Giardia, Ascaris, or both parasites. Am J Trop Med Hyg 96: 1394–1399.
-
31.
Calvopina M, Atherton R, Romero-Álvarez D, Castaneda B, Valverde-Muñoz G, Cevallos W, Izurieta R, 2019. Identification of intestinal parasite infections and associated risk factors in indigenous Tsáchilas communities of Ecuador. Int J Acad Med 5: 171.
-
32.
González-Ramírez LC, Robalino-Flores X, De la Torre E, Parra-Mayorga P, Prato JG, Trelis M, Fuentes MV, 2022. Influence of environmental pollution and living conditions on parasite transmission among indigenous Ecuadorians. Int J Environ Res Public Health 19: 6901.
-
33.
Romero-Sandoval N, Cifuentes L, León G, Lecaro P, Ortiz-Rico C, Cooper P, Martín M, 2019. High rates of exposures to waterborne pathogens in indigenous communities in the Amazon region of Ecuador. Am J Trop Med Hyg 101: 45–50.
-
34.
Cepon-Robins TJ et al., 2019. Soil-transmitted helminth infection and intestinal inflammation among the Shuar of Amazonian Ecuador. Am J Phys Anthropol 170: 65–74.
-
35.
Cooper PJ, Chico ME, Platts-Mills TAE, Rodrigues LC, Strachan DP, Barreto ML, 2015. Cohort profile: The Ecuador Life (ECUAVIDA) study in Esmeraldas Province, Ecuador. Int J Epidemiol 44: 1517–1527.
-
36.
Ster IC, Niaz HF, Chico ME, Oviedo Y, Vaca M, Cooper PJ, 2021. The epidemiology of soil-transmitted helminth infections in children up to 8 years of age: Findings from an Ecuadorian birth cohort. PLoS Negl Trop Dis 15: e0009972.
-
37.
Lee GO et al., 2021. Gut microbiome, enteric infections and child growth across a rural-urban gradient: Protocol for the ECoMiD prospective cohort study. BMJ Open 11: e046241.
-
38.
Steinitz-Kannan M, López C, Jacobsen D, Guerra MdL, 2020. History of limnology in Ecuador: A foundation for a growing field in the country. Hydrobiologia 847: 4191–4206.
-
39.
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