• View in gallery
    Figure 1.

    Estimated Giardia intestinalis cysts among children in urban (Medellín) compared with rural areas (Unguía) had a similar burden of infection. Mann–Whitney U test; P < 0.05.

  • View in gallery
    Figure 2.

    Estimated helminth burden in eggs per gram of stool using quantitative PCR among children in urban (Medellín) compared with rural areas (Unguía) had equal Ascaris but higher Trichuris burden of infection in rural areas. Mann–Whitney U test; parasite DNA (fg/µL) correlated with eggs per gram of stool; P < 0.05.

  • 1.

    Nikolay B , Brooker SJ , Pullan RL , 2014. Sensitivity of diagnostic tests for human soil-transmitted helminth infections: a meta-analysis in the absence of a true gold standard. Int J Parasitol 44: 765774.

    • Search Google Scholar
    • Export Citation
  • 2.

    Dunn JC et al. 2020. The increased sensitivity of qPCR in comparison to Kato-Katz is required for the accurate assessment of the prevalence of soil-transmitted helminth infection in settings that have received multiple rounds of mass drug administration. Parasit Vectors 13: 324.

    • Search Google Scholar
    • Export Citation
  • 3.

    Villamizar X , Higuera A , Herrera G , Vasquez-A LR , Buitron L , Muñoz LM , Gonzales-C FE , Lopez MC , Giraldo JC , Ramírez JD , 2019. Molecular and descriptive epidemiology of intestinal protozoan parasites of children and their pets in Cauca, Colombia: a cross-sectional study. BMC Infect Dis 19: 190.

    • Search Google Scholar
    • Export Citation
  • 4.

    Bouwmans MCH , Gaona MA , Chenault MN , Zuluaga C , Pinzón-Rondon ÁM , 2016. Prevalence of intestinal parasitic infections in preschool-children from vulnerable neighborhoods in Bogotá. Revista de la Universidad Ind de Santander, Salud 48: 178187.

    • Search Google Scholar
    • Export Citation
  • 5.

    García-Montoya GM , Botero-Garces JH , 2018. Giardiasis in Colombia: a review of the current knowledge. Curr Trop Med Rep 5: 154161.

  • 6.

    Carmona-Fonseca J , Botero AMC , 2014. Understanding the social determinants of health/disease: intestinal parasites and malnutrition in the families of Urabá, Colombia. Soc Med 8: 5667.

    • Search Google Scholar
    • Export Citation
  • 7.

    Salcedo-Cifuentes M , Florez O , Bermúdez A , Hernández L , Araujo C , Bolaños MV , 2012. Intestinal parasitism prevalence amongst children from six indigenous communities residing in Cali, Colombia. Rev Salud Pública 14: 156168.

    • Search Google Scholar
    • Export Citation
  • 8.

    Carmona-Fonseca J , Flórez EMA , 2017. Intestinal parasites and “progress”: a case study from Urabá Antioquia (Colombia). Soc Med 11: 3550.

    • Search Google Scholar
    • Export Citation
  • 9.

    Higuera A , Villamizar X , Herrera G , Giraldo JC , Vasquez-A LR , Urbano P , Villalobos O , Tovar C , Ramírez JD , 2020. Molecular detection and genotyping of intestinal protozoa from different biogeographical regions of Colombia. PeerJ 8: e8554.

    • Search Google Scholar
    • Export Citation
  • 10.

    Rivero MR , De Angelo C , Nuñez P , Salas M , Motta CE , Chiaretta A , Salamón OD , Liang S , 2017. Environmental and socio-demographic individual, family and neighborhood factors associated with children intestinal parasitosis at Iguazú, in the subtropical northern border of Argentina. Plos Negl Trop Dis 11: e0006098.

    • Search Google Scholar
    • Export Citation
  • 11.

    Mejia R , Vicuna Y , Broncano N , Sandoval C , Vaca M , Chico M , Cooper PJ , Nutman TB , 2013. A novel, multi-parallel, real-time polymerase chain reaction approach for eight gastrointestinal parasites provides improved diagnostic capabilities to resource-limited at-risk populations. Am J Trop Med Hyg 88: 10411047.

    • Search Google Scholar
    • Export Citation
  • 12.

    Poirier P , Wawrzyniak I , Vivares CP , Delbac F , El Alaoui H , 2012. New insights into Blastocystis spp.: a potential link with irritable bowel syndrome. PLoS Pathog 8: e1002545.

    • Search Google Scholar
    • Export Citation
  • 13.

    Lozano AM , Montoya GG , Díaz ALG , Garces JB , 2009. Prevalencia de parásitos intestinales en niños que asisten al Templo Comedor Sagrado Corazón Teresa Benedicta de la Cruz, del barrio Vallejuelos, Medellín, 2007. IATREIA 22: 227234.

    • Search Google Scholar
    • Export Citation
  • 14.

    Ministerio de Salud y Protección Social, Universidad de Antioquia , 2015. Encuesta nacional de parasitismo intestinal en población escolar 2012–2014. Medellín, Colombia: Facultad Nacional Salud Pública, Universidad de Antioquia. Available at: https://www.minsalud.gov.co/sites/rid/Lists/BibliotecaDigital/RIDE/VS/PP/ET/encuesta-nacional-de-parasitismo-2012-2014.pdf. Accessed September 15, 2020.

    • Search Google Scholar
    • Export Citation
  • 15.

    Hernández PC , Morales L , Chaparro-Olaya J , Sarmiento D , Jaramillo JF , Ordoñez GA , Cortés F , Sánchez LK , 2019. Intestinal parasitic infections and associated factors in children of three rural schools in Colombia: a cross-sectional study. PLoS One 14: e0218681.

    • Search Google Scholar
    • Export Citation
  • 16.

    World Health Organization , 2011. Department of control of neglected tropical diseases. Helminth Control in School-Age Children: a Guide for Managers of Control Programs, 2nd edition. Geneva, Switzerland: WHO. Available at: https://www.who.int/neglected_diseases/resources/9789241548267/en/. Accessed September 15, 2020.

    • Search Google Scholar
    • Export Citation
  • 17.

    Harhay MO , Horton J , Olliaro PL , 2010. Epidemiology and control of human gastrointestinal parasites in children. Expert Rev Anti Infect Ther 8: 219234.

    • Search Google Scholar
    • Export Citation
  • 18.

    Valencia S , 2016. Socio-environmental vulnerabilities in formal and informal peri-urban Bogotá and Soacha, Colombia. Doctoral dissertation, Lund University, Lund University Digital Archive, Lund, Sweden. Available at: https://portal.research.lu.se/portal/en/publications/caught-between-spaces(1ed39250-a1d9-49aa-86fb-865f24bf18d7).html. Accessed September 15, 2020.

    • Search Google Scholar
    • Export Citation
  • 19.

    Ajeagah G , Wouafo M , Ezenguele G , Nzukam J , 2013. Presence of gastrointestinal parasites in a tropical urban region (Yaoundé, Cameroon). Comp Parasitol 80: 279283.

    • Search Google Scholar
    • Export Citation
  • 20.

    Lucci P , Bhatkal T , Khan A , Berliner T , 2015. What Works in Improving the Living Conditions of Slum Dwellers: A Review of the Evidence across Four Programmes. London, UK: ODI, Overseas Development Institute, Development Progress. Available at: https://www.odi.org/publications/10222-what-works-improving-living-conditions-slum-dwellers-review-evidence-across-four-programmes. Accessed September 15, 2020.

    • Search Google Scholar
    • Export Citation
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Urban versus Rural Prevalence of Intestinal Parasites Using Multi-Parallel qPCR in Colombia

Patricia E. Bryan Laboratory of Human Parasitology, National School of Tropical Medicine, Baylor College of Medicine, Houston, Texas;

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Marcela Romero Instituto Colombiano de Medicina Tropical, Universidad CES, Medellín, Colombia

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Miryan Sánchez Instituto Colombiano de Medicina Tropical, Universidad CES, Medellín, Colombia

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Giovanny Torres Instituto Colombiano de Medicina Tropical, Universidad CES, Medellín, Colombia

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Wilber Gómez Instituto Colombiano de Medicina Tropical, Universidad CES, Medellín, Colombia

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Marcos Restrepo Instituto Colombiano de Medicina Tropical, Universidad CES, Medellín, Colombia

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Alejandro Restrepo Laboratory of Human Parasitology, National School of Tropical Medicine, Baylor College of Medicine, Houston, Texas;
Instituto Colombiano de Medicina Tropical, Universidad CES, Medellín, Colombia

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Rojelio Mejia Laboratory of Human Parasitology, National School of Tropical Medicine, Baylor College of Medicine, Houston, Texas;

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ABSTRACT

Stool samples from 122 children living in an urban slum (n = 72) and rural (n = 50) areas were analyzed using multi-parallel real-time quantitative PCR to determine intestinal prevalence parasites from two communities in Colombia. Findings indicated a prevalence of 86.1% Blastocystis spp., 62.5% Giardia intestinalis, 19.4% Cryptosporidium spp., 19.4% Ascaris lumbricoides, and 5.6% Trichuris trichiura in an urban slum; and 76% Blastocystis spp., 68% G. intestinalis, 20% Entamoeba histolytica, 50% A. lumbricoides, 46% T. trichiura, and 2% Strongyloides stercoralis in rural areas. Polyparasitism was higher in rural (58%) than urban (25%) areas (P = 0.001). Trichuris trichiura burden was higher in the rural area (P = 0.002). Over 40% of helminthic infections in rural areas had a heavy parasite burden by WHO classification. Over half of urban and rural children were infected with G. intestinalis and Blastocystis spp. Our data provide accurate epidemiologic surveillance for public health interventions.

Intestinal parasites are globally widespread infectious organisms disproportionately affecting children in resource-limited areas with associated morbidity that can have long-term child health implications. Environmental surroundings may influence exposure to these parasites. Reliable, highly sensitive, and specific diagnostic tests for intestinal parasitic infections are critical for treatment decisions in mass drug administration (MDA) programs, impact evaluation, and surveillance. 13

A multi-parallel real-time quantitative PCR (qPCR) assay was used to detect intestinal parasites commonly infecting children living in resource-limited areas, including soil-transmitted helminths (STHs) (Ascaris lumbricoides, Ancylostoma duodenale, Necator americanus, Strongyloides stercoralis, and Trichuris trichiura), protozoa (Cryptosporidium spp., Entamoeba histolytica, and Giardia intestinalis), and heterokonts (Blastocystis spp.). Data from Colombia on intestinal parasite prevalence in preschool-age children are limited. 4,5 The study population included preschool- and school-age children living in urban slums of the city of Medellín (mean age = 2 years) and rural areas of the town of Unguía (mean age = 2.5 years) located in the northwest Andean region of Colombia. Recently, protozoa detected by a molecular approach were reported among school-age children in an urban area of southwest Colombia with a prevalence of 39.2% Blastocystis spp., 10.6% G. intestinalis, and 9.8% Cryptosporidium spp. 3 Intestinal parasites were previously detected by microscopy among children younger than 15 years in a rural area of the northern coastal region of Colombia with 63% infected with protozoa and 69% infected with STHs. 6 In Colombia, comparative studies reporting molecular epidemiologic data on childhood intestinal parasitic infections between urban and rural populations within the same region are sparse. 3,79 Our study contributes to data comparing the prevalence of intestinal parasites, both STHs and protozoa, detected by qPCR among urban slum and rural children from the study sampling areas in Colombia. Accurate epidemiologic data on these parasites are critical to decision-making for treatment and public health interventions for populations of children in contrasting communities, given the interplay between socioeconomic and environmental factors. 10

Stool samples were analyzed from 122 Colombian children living in urban slums (n = 72) and rural areas (n = 50). Parasite DNA was extracted from 50 mg of stool from each stool sample using an MP FastDNA™ for Soil Kit (MP Biochemicals, Solon, OH), and species-specific primers and probes for all parasites were previously designed and tested. 11,12 Calculated G. intestinalis cysts and STH eggs were derived from spiked samples with known parasite concentrations. 11 Ethical approval for this study was granted by the Ethical Committee of the Colombian Tropical Medicine Institute and Baylor College of Medicine. Informed consent was obtained from parents/guardians. All positive cases were informed and received antiparasitic treatment.

Overall, intestinal parasites among children in this study were found to be similarly highly prevalent in both urban slum (97.2%) and rural areas (90%), with G. intestinalis and Blastocystis spp. predominantly prevalent across these sampling settings. Because urban populations generally have better access to sanitation and clean water than rural populations, 4 the high prevalence of intestinal parasites such as G. intestinalis and Blastocystis spp. in both urban and rural areas (62.5% and 86.1% versus 68% and 76%, respectively) is noteworthy. Previously reported data from Colombia on children living in urban slums (children of Medellín) indicated a significantly lower prevalence of giardiasis (25.9%) detected by microscopy, 13 and the most recent national survey reported that 15.4% of Colombian children were infected with G. intestinalis and 57.7% were infected with Blastocystis spp., also detected by microscopy-based diagnostic methods. 14 Despite the high prevalence of Blastocystis spp., the clinical importance of this parasite remains unclear. 15 However, this parasite is an important indicator of fecal contamination of food and water. 15 Giardia intestinalis represents a significant public health problem worldwide. 3,5 Giardiasis can cause acute or chronic diarrhea but is often asymptomatic and is associated with detrimental impacts to growth and development in children. 5,15 In the present study, G. intestinalis spiking studies were also conducted from which cysts per gram of stool were calculated. Subsequently, a similar G. intestinalis infection burden was found among urban slum and rural children (Figure 1), suggesting exposure to similar risk factors for giardiasis in both settings. Because fecal contamination of drinking water is the most common source of G. intestinalis cysts from domestic animal and human origins, 5,15 the inadequate or lack of access to clean water typically found in resource-deprived urban slum and rural areas of developing countries may explain the prevalence and parasite burden in the study population.

Figure 1.
Figure 1.

Estimated Giardia intestinalis cysts among children in urban (Medellín) compared with rural areas (Unguía) had a similar burden of infection. Mann–Whitney U test; P < 0.05.

Citation: The American Journal of Tropical Medicine and Hygiene 104, 3; 10.4269/ajtmh.20-1202

In this study, helminthiasis was more prevalent among rural children than the urban study population. The most prevalent STHs, A. lumbricoides and T. trichiura, were significantly highly found among rural children comparably (50% and 46% versus 19.4% and 5.6%, respectively) (Table 1). This was not unexpected because of similar transmission dynamics and greater risk of exposure to contaminated soil in rural settings combined with poor hygiene awareness and hand-to-mouth behavior characteristic of early childhood. 10 To evaluate STH parasite burden, DNA fg/µL was correlated with eggs per gram (epg) of stool-based on the WHO threshold criteria for the classification of parasite burden for A. lumbricoides (1–5,000 light; > 5,000–50,000 moderate; and > 50,000 heavy), T. trichiura (1–999 light; 1,000–9,999 moderate; ≥ 10,000 heavy), and hookworm (1–1,999 light; 2,000–3,999 moderate; ≥ 4,000 heavy). 16 Over 40% of STH infections among children in the rural setting were classified as having a heavy parasite burden. Among rural children with trichuriasis, parasite burden was higher (9,953 epg) than that in children in urban slums (325 epg) (P = 0.002), as indicated by the Mann–Whitney U test (Figure 2). Because there were only four children living in the urban slums with trichuriasis, statistical power is limited. Polyparasitism was also found in the overall study population with the highest prevalence found among rural children (58%) compared with children in urban slum areas (25%) (P = 0.001). Because morbidity is proportional to parasite burden, 2,9 polyparasitism in the study population is a significant concern, given the young age of these children. This young age-group is at increased vulnerability to the detrimental health impacts of intestinal parasites because of critical stages of growth and development occurring during early childhood. 17 Moreover, polyparasitism involving both STHs and protozoa serves as an important indicator of inadequate sanitary conditions and continual reinfection. 9

Figure 2.
Figure 2.

Estimated helminth burden in eggs per gram of stool using quantitative PCR among children in urban (Medellín) compared with rural areas (Unguía) had equal Ascaris but higher Trichuris burden of infection in rural areas. Mann–Whitney U test; parasite DNA (fg/µL) correlated with eggs per gram of stool; P < 0.05.

Citation: The American Journal of Tropical Medicine and Hygiene 104, 3; 10.4269/ajtmh.20-1202

Table 1

Urban (Medellín) and rural (Unguía) parasite prevalence and infection burden in DNA fg/µL

Parasite species Urban (Medellin) n = 72 Rural (Unguía) n = 50 P-value Urban DNA (fg/µL) geometric mean Rural DNA (fg/µL) geometric mean P-value
Any parasite 70 (97.2%) 45 (90%) 0.091
Ascaris lumbricoides 14 (19.4%) 25 (50%) 0.0004 18.20 4.764 0.478
Ancylostoma duodenale 0 0 * * * *
Necator americanus 0 0 * * * *
Strongyloides stercoralis 0 1 (2%) * * 3.122 *
Trichuris trichiura 4 (5.6%) 23 (46%) 0.0001 0.0036 0.1090 0.002
Blastocystis spp. 62 (86.1%) 38 (76%) 0.155 1.042 1.880 0.873
Cryptosporidium spp. 14 (19.4%) 0 * 5.576 * *
Entamoeba histolytica 0 10 (20%) * * 2.701 *
Giardia intestinalis 45 (62.5%) 34 (68%) 0.533 4.720 0.7736 0.114

Mann–Whitney U test; fg/µL = femtograms per microliter.

Not enough data for analysis; P < 0.05.

Findings from this study suggest that children from urban slums of Medellín and rural areas of Unguía in Colombia live in highly contaminated environments with continuous exposure to intestinal parasites in these different communities. The peripheral neighborhoods of the urban poor in cities such as Medellín typically have poor housing standards, overcrowding, and inadequate infrastructure for sanitation and access to clean water. 1820 These conditions are comparable with resource-deprived rural settings and can often lead to even greater exposure to fecal contamination in households, schools, and where children play. 14 The predominance of G. intestinalis in both urban slum and rural areas suggests the likelihood of exposure to similar contamination sources in geographically contrasting communities. 18 The high prevalence of intestinal parasites found in the study population confirms that childhood intestinal parasitic infections are a relevant health issue in both urban poor and rural communities in Colombia and serves as an important indicator of community-level socioeconomic development. 8,10 Because accurate prevalence data in a region or community are essential for identifying local vulnerabilities, 4,18,20 molecular epidemiologic data from this study provide evidence of important community needs common to both urban slum and rural communities included in this study. Accurate epidemiologic data from this study are also critical for treatment decisions in MDA programs, impact evaluation, and surveillance. This is particularly important given that MDA is not implemented in either Medellín or Unguía. 14 Furthermore, MDA programs in Colombia are not aimed at the preschool-age population and do not include treatment for intestinal protozoa. 4,5 Moreover, prevalence data generated from this study provide evidence for local decision-making for implementing resources to improve living conditions for urban and rural populations of children in Colombia. 15,20 A major limitation of this study was the lack of G. intestinalis assemblages and Blastocystis subtype identification. Future studies should include the assemblage and subtyping to allow for correlation to human disease.

REFERENCES

  • 1.

    Nikolay B , Brooker SJ , Pullan RL , 2014. Sensitivity of diagnostic tests for human soil-transmitted helminth infections: a meta-analysis in the absence of a true gold standard. Int J Parasitol 44: 765774.

    • Search Google Scholar
    • Export Citation
  • 2.

    Dunn JC et al. 2020. The increased sensitivity of qPCR in comparison to Kato-Katz is required for the accurate assessment of the prevalence of soil-transmitted helminth infection in settings that have received multiple rounds of mass drug administration. Parasit Vectors 13: 324.

    • Search Google Scholar
    • Export Citation
  • 3.

    Villamizar X , Higuera A , Herrera G , Vasquez-A LR , Buitron L , Muñoz LM , Gonzales-C FE , Lopez MC , Giraldo JC , Ramírez JD , 2019. Molecular and descriptive epidemiology of intestinal protozoan parasites of children and their pets in Cauca, Colombia: a cross-sectional study. BMC Infect Dis 19: 190.

    • Search Google Scholar
    • Export Citation
  • 4.

    Bouwmans MCH , Gaona MA , Chenault MN , Zuluaga C , Pinzón-Rondon ÁM , 2016. Prevalence of intestinal parasitic infections in preschool-children from vulnerable neighborhoods in Bogotá. Revista de la Universidad Ind de Santander, Salud 48: 178187.

    • Search Google Scholar
    • Export Citation
  • 5.

    García-Montoya GM , Botero-Garces JH , 2018. Giardiasis in Colombia: a review of the current knowledge. Curr Trop Med Rep 5: 154161.

  • 6.

    Carmona-Fonseca J , Botero AMC , 2014. Understanding the social determinants of health/disease: intestinal parasites and malnutrition in the families of Urabá, Colombia. Soc Med 8: 5667.

    • Search Google Scholar
    • Export Citation
  • 7.

    Salcedo-Cifuentes M , Florez O , Bermúdez A , Hernández L , Araujo C , Bolaños MV , 2012. Intestinal parasitism prevalence amongst children from six indigenous communities residing in Cali, Colombia. Rev Salud Pública 14: 156168.

    • Search Google Scholar
    • Export Citation
  • 8.

    Carmona-Fonseca J , Flórez EMA , 2017. Intestinal parasites and “progress”: a case study from Urabá Antioquia (Colombia). Soc Med 11: 3550.

    • Search Google Scholar
    • Export Citation
  • 9.

    Higuera A , Villamizar X , Herrera G , Giraldo JC , Vasquez-A LR , Urbano P , Villalobos O , Tovar C , Ramírez JD , 2020. Molecular detection and genotyping of intestinal protozoa from different biogeographical regions of Colombia. PeerJ 8: e8554.

    • Search Google Scholar
    • Export Citation
  • 10.

    Rivero MR , De Angelo C , Nuñez P , Salas M , Motta CE , Chiaretta A , Salamón OD , Liang S , 2017. Environmental and socio-demographic individual, family and neighborhood factors associated with children intestinal parasitosis at Iguazú, in the subtropical northern border of Argentina. Plos Negl Trop Dis 11: e0006098.

    • Search Google Scholar
    • Export Citation
  • 11.

    Mejia R , Vicuna Y , Broncano N , Sandoval C , Vaca M , Chico M , Cooper PJ , Nutman TB , 2013. A novel, multi-parallel, real-time polymerase chain reaction approach for eight gastrointestinal parasites provides improved diagnostic capabilities to resource-limited at-risk populations. Am J Trop Med Hyg 88: 10411047.

    • Search Google Scholar
    • Export Citation
  • 12.

    Poirier P , Wawrzyniak I , Vivares CP , Delbac F , El Alaoui H , 2012. New insights into Blastocystis spp.: a potential link with irritable bowel syndrome. PLoS Pathog 8: e1002545.

    • Search Google Scholar
    • Export Citation
  • 13.

    Lozano AM , Montoya GG , Díaz ALG , Garces JB , 2009. Prevalencia de parásitos intestinales en niños que asisten al Templo Comedor Sagrado Corazón Teresa Benedicta de la Cruz, del barrio Vallejuelos, Medellín, 2007. IATREIA 22: 227234.

    • Search Google Scholar
    • Export Citation
  • 14.

    Ministerio de Salud y Protección Social, Universidad de Antioquia , 2015. Encuesta nacional de parasitismo intestinal en población escolar 2012–2014. Medellín, Colombia: Facultad Nacional Salud Pública, Universidad de Antioquia. Available at: https://www.minsalud.gov.co/sites/rid/Lists/BibliotecaDigital/RIDE/VS/PP/ET/encuesta-nacional-de-parasitismo-2012-2014.pdf. Accessed September 15, 2020.

    • Search Google Scholar
    • Export Citation
  • 15.

    Hernández PC , Morales L , Chaparro-Olaya J , Sarmiento D , Jaramillo JF , Ordoñez GA , Cortés F , Sánchez LK , 2019. Intestinal parasitic infections and associated factors in children of three rural schools in Colombia: a cross-sectional study. PLoS One 14: e0218681.

    • Search Google Scholar
    • Export Citation
  • 16.

    World Health Organization , 2011. Department of control of neglected tropical diseases. Helminth Control in School-Age Children: a Guide for Managers of Control Programs, 2nd edition. Geneva, Switzerland: WHO. Available at: https://www.who.int/neglected_diseases/resources/9789241548267/en/. Accessed September 15, 2020.

    • Search Google Scholar
    • Export Citation
  • 17.

    Harhay MO , Horton J , Olliaro PL , 2010. Epidemiology and control of human gastrointestinal parasites in children. Expert Rev Anti Infect Ther 8: 219234.

    • Search Google Scholar
    • Export Citation
  • 18.

    Valencia S , 2016. Socio-environmental vulnerabilities in formal and informal peri-urban Bogotá and Soacha, Colombia. Doctoral dissertation, Lund University, Lund University Digital Archive, Lund, Sweden. Available at: https://portal.research.lu.se/portal/en/publications/caught-between-spaces(1ed39250-a1d9-49aa-86fb-865f24bf18d7).html. Accessed September 15, 2020.

    • Search Google Scholar
    • Export Citation
  • 19.

    Ajeagah G , Wouafo M , Ezenguele G , Nzukam J , 2013. Presence of gastrointestinal parasites in a tropical urban region (Yaoundé, Cameroon). Comp Parasitol 80: 279283.

    • Search Google Scholar
    • Export Citation
  • 20.

    Lucci P , Bhatkal T , Khan A , Berliner T , 2015. What Works in Improving the Living Conditions of Slum Dwellers: A Review of the Evidence across Four Programmes. London, UK: ODI, Overseas Development Institute, Development Progress. Available at: https://www.odi.org/publications/10222-what-works-improving-living-conditions-slum-dwellers-review-evidence-across-four-programmes. Accessed September 15, 2020.

    • Search Google Scholar
    • Export Citation

Author Notes

Address correspondence to Rojelio Mejia, Laboratory of Human Parasitology, National School of Tropical Medicine, Baylor College of Medicine, One Baylor Plaza, BCM 113, Houston, TX 77030. E-mail: rmejia@bcm.edu

Authors’ addresses: Patricia E. Bryan and Rojelio Mejia, Baylor College of Medicine, National School of Tropical Medicine, Houston, TX, E-mails: patricia.bryan@bcm.edu and rojelio.mejia@bcm.edu. Marcela Romero, Miryan Sánchez, Giovanny Torres, Wilber Gómez, and Marcos Restrepo, Department of Microbiology, Instituto Colombiano de Medicina tropical - Univerisidad CES, Medellín, Colombia, E-mails: iromero@ces.edu.co, msanchez@ces.edu.co, gtorres@ces.edu.co, wgomez@ces.edu.co, and mrestrepoi@gmail.com. Alejandro Restrepo, Baylor College of Medicine, National School of Tropical Medicine, Houston, TX, and Department of Microbiology, Instituto Colombiano de Medicina tropical - Univerisidad CES, Medellín, Colombia, E-mail: alejorpo75@yahoo.com.

These authors contributed equally to this work.

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