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. 1–3
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. 3,7–9 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.
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
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
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
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
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
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
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. 18–20 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.
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