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Keywords:

  • helminths;
  • protozoa;
  • Peru

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgement
  8. References

Objective

To compare prevalences of intestinal helminths and waterborne protozoa in indigenous and settler populations in a remote area of Peru. These populations live in adjacent but segregated small urban villages.

Methods

Stool samples were collected from representative members of these two populations and analysed for geohelminths and protozoa.

Results

The risk of soil-transmitted helminths is significantly higher in the settler than the indigenous population in the same isolated region of Peru (OR 5.18; 95% CI 3.44–7.81; < 0.001). In contrast, the rates of protozoa presence were similar in both populations (OR 1.28; 95% CI 0.77–2.14; P = 0.336).

Conclusions

Potential explanations for unexpected finding of a lower prevalence of helminths in indigenous relative to the settler population could include housing design in flood – prone areas and the use of local medicinal plants that possibly have antihelmintic properties.

Objectif

Comparer les prévalences des helminthiases intestinales et des protozoaires aquatiques dans les populations autochtones et récentes dans une zone reculée du Pérou. Ces populations vivent en voisinage mais séparées dans de petits villages urbains.

Méthodes

Des échantillons de selles ont été recueillis auprès des membres représentatifs de ces deux populations et analysés pour les géohelminthes et les protozoaires.

Résultats

Le risque de géohelminthiases est significativement plus élevé chez les populations récentes que chez les autochtones dans la même région isolée du Pérou (OR: 5,18; IC95%: 3,44 à 7,81, P < 0,001). En revanche, les taux de présence des protozoaires étaient similaires dans les deux populations (OR: 1,28; IC95%: 0,77 à 2,14, P = 0,336).

Conclusions

Les raisons de ces résultats inattendus pourraient être la conception des logements dans les zones inondables et l'utilisation de plantes médicinales locales ayant peut-être des propriétés vermifuges.

Objetivo

Comparar las prevalencias de helmintos intestinales y protozoos acuáticos en poblaciones indígenas y de colonos en áreas remotas del Perú. Estas poblaciones viven en pequeñas poblaciones urbanas, adyacentes pero segregadas.

Métodos

Se recolectaron muestras de heces de miembros representativos de estas dos poblaciones y se analizaron en busca de geohelmintos y protozoos.

Resultados

El riesgo de helmintiasis transmitida por tierra es significativamente mayor entre las poblaciones de colonos que entre los indígenas de la misma región aislada del Perú (OR 5.18; IC 95% 3.44–7.81; P < .001). En contraste, las tasas de presencia de protozoos eran similares en ambas poblaciones (OR 1.28; IC 95% 0.77–2.14; = 0.336).

Conclusiones

Las razones de estos hallazgos inesperados podrían ser el diseño de las casas en áreas con tendencia a las inundaciones y el uso de plantas medicinales locales que podrían tener propiedades antihelmínticas.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgement
  8. References

Soil-transmitted helminths (geohelminths) are a major global cause of morbidity and malnutrition. The highest prevalence of geohelminth infection is found in impoverished communities lacking basic sanitation and access to clean drinking water (Bethony et al. 2006). Waterborne protozoa thrive under these similar conditions.

In Peru, parasitoses and other intestinal infections account for 7.7% of deaths (OMS/OPS 1998). It has been estimated that one of every three Peruvians carries one or more species of intestinal parasites (Náquira 1997). The prevalence of helminths is highest in the jungles of Peru; protozoa are more common on the coast and in the mountains. This study of the prevalence of intestinal infection, conducted in a remote jungle region of Peru, compared the prevalences of intestinal parasites (geohelminths and protozoa) in two adjacent but distinct populations.

Methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgement
  8. References

The prevalences of intestinal parasites (geohelminths and protozoa) were measured in two adjacent but distinct populations in a remote jungle region of Peru. The first population consisted of 10 indigenous villages of native people from the four ethnic groups Allahuis, Chapras, Chawis and Huambisa. The people of these villages speak their own native language and their children do not attend schools. They have no access to tap water, sewers, electricity or a hospital. They do not wear shoes. The second population consisted of seven settler (non-indigenous Mestizos) villages. The settlers speak Spanish and their children do attend schools. They have no access to tap water or a hospital, but do have sewers and electricity, and they wear shoes.

The indigenous population lives in houses on stilts (approximately three feet above the ground, Figure 1); the settler population lives in houses at ground level. Both types of villages are situated along a tributary of the Amazon River.

image

Figure 1. Raised dwelling of indigenous people.

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The study and its informed consent procedure were approved by the Institutional Ethics Committee of Universidad Peruana Cayetano Heredia. People of the indigenous and settler villages were randomly chosen to be in the study and consented. A local district leader functioned as the mediator and interpreter between the study team and indigenous village leaders and a mediator to the leaders of the settlers. One stool sample per participant was collected. Stool samples were preserved in 5% formaldehyde and brought to the Parasitology Laboratory at the Institute of Tropical Medicine Alexander von Humboldt for processing with the spontaneous sedimentation in tube laboratory technique (SSTT). This test is inexpensive and commonly used in Peru (Tello & Canales 2000; Terashima et al. 2009). Standard agar plate culturing (Lau et al. 2005) was not performed in the field due to the intense heat of the jungle and the inability to maintain the agar. Samples collected were coded to conceal the participant's identity.

Data were analysed by chi-square test or Fisher's exact test for the analysis for categorical variables and Student's t-test was used for continuous variables. Univariable logistic regression models were used to estimate the odds ratios (OR) and 95% confidence intervals (CI) for the risk of helminths and protozoa between Indigenous and Settler populations. Age and gender were evaluated as risk factors for helminths and protozoa. Multivariable logistic regression model was used to evaluate adjusted OR for helminths. All statistical analyses were performed using SAS version 9.3. Two-sided P-values <0.05 were considered statistically significant.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgement
  8. References

The indigenous population was younger than the settler population (21.7 ± 15.1 vs. 29.2 ± 15.0 years., < 0.001, Table 1). As shown in Table 2, the prevalence of soil-transmitted helminths was higher in the settler than the indigenous villages (69.9% vs. 31.0%, < 0.0001, chi-square). In contrast, the rates of protozoal/flagellate infections were similar in both populations (85.1% vs. 81.7%, = 0.35, chi-square). Univariable logistic regression revealed that settlers were 5.18 times more likely to have helminths than the indigenous communities (odds ratio of 5.18, Table 3). The correlation between being indigenous and presence of helminths was highly significant (< 0.001). Multiple logistic regression was applied to control for age in the two populations (Table 4). Settler communities remained more likely to have helminths (< 0.001) than indigenous populations even when controlling for age. The correlation between protozoa and indigenous and settler communities was not significant with a = 0.336 (Table 5). Table 6 shows the prevalences of individual helminths. Ascaris lumbricoides (< 0.001), Trichuris trichiura, (< 0.001) and Ancylostoma duodenale/Necator americanus (= 0.007) infections were more common in the population of settlers than in the indigenous population, using chi-square. Prevalence of Strongyloides stercoralis was low and did not differ significantly between the two populations ([= 0.455], Fisher's exact test).

Table 1. Demographics
 IndigenousSettlers P
N197236 
Age (years)
Range2–975–73 
Mean ± SD21.7 ± 15.129.2 ± 15.1<0.0001
Male105 (53.3%)113 (47.9%)0.806
Female92 (46.7%)123 (52.1%)
Table 2. Parasitism by the type of parasite (helminths, protozoa or both)
TypeIndigenous% (n)Settlers% (n)
Helminths and protozoa24.9 (49)57.6 (136)
Helminths only6.1 (12)12.3 (29)
Protozoa only56.9 (112)27.5 (65)
Negative12.2 (24)2.5 (6)
Total100.0 (197)100.0 (236)
Table 3. Univariable logistic regression analysis for helminths
CovariatesOdds ratio (95% CI)P-value
Age group
(10–20 vs. 0–10)1.09 (0.56–2.12)0.792
(20–40 vs. 0–10)2.84 (1.45–5.55)0.002
(40–60 vs. 0–10)0.84 (0.39–1.83)0.659
(60+ vs. 0–10)1.62 (0.58–4.49)0.354
Indigenous (settlers vs. indigenous)5.18 (3.44–7.81)<0.001
Gender (female vs. male)1.20 (0.83–1.76)0.336
Table 4. Multivariable Logistic regression for outcome: helminths
CovariatesOdds ratio (95% CI)P-value
Age group
(10–20 vs. 0–10)0.86 (0.42–1.75)0.678
(40–60 vs. 0–10)0.51 (0.22–1.18)0.117
(60+ vs. 0–10)0.80 (0.27–2.41)0.691
Indigenous (settlers vs. indigenous)4.82 (3.12–7.44)<0.001
Table 5. Univariable logistic regression analysis for protozoa
CovariatesOdds ratio (95% CI)P-value
Age group
(10–20 vs. 0–10)1.00 (0.44–2.31)0.991
(20–40 vs. 0–10)1.26 (0.54–2.95)0.589
(40–60 vs. 0–10)3.31 (0.95–11.5)0.06
(60+ vs. 0–10)0.81 (0.23–2.77)0.731
Indigenous (settlers vs. indigenous)1.28 (0.77–2.14)0.336
Gender (female vs. male)1.17 (0.71–1.95)0.535
Table 6. Prevalence of helminths for indigenous and settler populations
Pathogenic parasites (helminths)Indigenous% (n)Settlers% (n) P
  1. a

    Fisher's exact test was used.

Ascaris lumbricoides 21.83 (43)54.66 (129)<0.001
Ancylostoma duodenale/Necator americanus 7.61 (15)16.10 (38)0.007
Trichuris trichiura 4.06 (8)19.07 (45)<0.001
Strongyloides stercoralis 0.51 (1)0 (0)0.455a

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgement
  8. References

Understanding the epidemiology of intestinal geohelminth infection in poor isolated communities is important in designing effective strategies to combat this neglected tropical disease. We found that the prevalences of soil-transmitted helminth infections (Ascaris lumbricoides, Trichuris trichiura, Ancylostoma duodenale/Necator americanus) were higher in settler than in indigenous villages in the same isolated region of Peru. In contrast, the rates of waterborne protozoa infections were similar in both populations. Infections with the geohelminth Strongyloides stercoralis did not differ significantly between the two populations, but the SSTT diagnostic technique used is not the gold standard (Lau et al. 2005) for testing this type of organism.

Common risk factors for intestinal helminths are poverty, poor sanitation, lack of shoes and lack of education (Bethony et al. 2006; Ziegelbauer et al. 2012). As these risk factors are less marked in the settler villages relative to the indigenous villages, they do not explain the findings. Urbanisation may be associated with higher rates of geohelminth infection than rural regions (Brooker et al. 2006), but the two types of village were of similar size and located in a rural setting. A prior study from Peru showed higher rates of intestinal helminths in a large Spanish-speaking town than in smaller villages with indigenous populations. The authors speculated that indigenous populations had better hygiene practices (Kroeger et al. 1992). In our study, there was no significant difference in prevalence of waterborne protozoa infections between the two types of villages, which suggests that the standards of hygiene or sanitation may be comparable between the two groups. Evaluation of food sources did not explain differences in helminth prevalence. One potential explanation for the findings may be that use of local medicinal plants (for example, the ojé plant) by indigenous people may be effective against helminths, but not against protozoa. Use of local plant-based medicines for anthelmintic properties is commonly used throughout the world (Athanasiadou et al. 2007; Koné et al. 2012).

Future research should consider the hypothesis that a difference in housing design may have contributed to the infection pattern seen between the two populations in this study. The indigenous population tends to live in houses on average three feet above the ground on stilts, while the settler population tends to live in houses at ground level. In the rainy season, the settlers' houses are more susceptible to flooding. Geohelminth eggs may enter these homes in soil sediments during floods and remain behind after the flood receded. The eggs are drought resistant and may remain in the domestic environment for months. They could be ingested by children through pica or contaminate food stores. In reviews of epidemiological data in areas with wet climates and frequent flooding, increased prevalence of Ascaris lumbricoides and Trichuris trichiura infections has been associated with flooding (Mboera et al. 2011). If future studies validated the hypothesis that elevated housing in wet tropical climates can reduce the risk of helminth infection, it would have implications for public health strategy.

Our study measured the presence or absence of helminths infection in individuals. There was no attempt to quantify the burden of infection in individuals or assess individual propensity to infection or domestic clustering (Walker et al. 2011) or to use statistical modelling of sample collection to distinguish between household and communal risk factors for geohelminth infection (Barreto et al. 2010). These issues will be addressed once deworming and follow-up monitoring programs are established in these communities.

In conclusion, we found that the indigenous communities have a lower prevalence of intestinal helminths than settler communities in a remote region of Peru; waterborne protozoa had similar prevalences in both communities. Future studies are required to further explain this finding and should include evaluating both the protective effects of elevated traditional housing, and the use of local medicinal plants which may have anthelmintic properties.

Acknowledgement

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgement
  8. References

We would like to acknowledge Hu Xie, MS, of the Fred Hutchinson Cancer Research Center for her help and guidance with the statistical analysis in this manuscript. We are grateful to Mr Robert Alarcón, District Counselor (2008) of Morona District who made this work possible, and to Henry Anchante, Parasitology Laboratory, at Instituto de Medicina Tropical Alexander von Humboldt, UPCH.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgement
  8. References
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