Regional, household and individual factors that influence soil transmitted helminth reinfection dynamics in preschool children from rural indigenous Panamá

PLoS Negl Trop Dis. 2013;7(2):e2070.

Carli M. Halpenny1, Claire Paller1, Kristine G. Koski2, Victoria E. Valdés3 and Marilyn E. Scott1

1Institute of Parasitology and McGill School of Environment Macdonald Campus of McGill University, Ste-Anne de Bellevue, Quebec, Canada, 2School of Dietetics and Human Nutrition Macdonald Campus of McGill University, Ste-Anne de Bellevue, Quebec, Canada, 3Escuela de Nutrición y Dietética, Facultad de Medicina, Universidad de Panamá, Ciudad de Panamá, Panamá



BACKGROUND: Few studies have investigated the relative influence of individual susceptibility versus household exposure factors versus regional clustering of infection on soil transmitted helminth (STH) transmission.  The present study examined reinfection dynamics and spatial clustering of Ascaris lumbricoides, Trichuris trichiura and hookworm in an extremely impoverished indigenous setting in rural Panamá over a 16 month period that included 2 treatment and reinfection cycles in preschool children.

METHODOLOGY/PRINCIPLE FINDINGS: Spatial cluster analyses were used to identify high prevalence clusters for each nematode.   Multivariate models were then used (1) to identify factors that differentiated households within and outside the cluster, and (2) to examine the relative contribution of regional (presence in a high prevalence cluster), household (household density, asset-based household wealth, household crowding, maternal education) and individual (age, sex, pre-treatment eggs per gram (epg) feces, height-for-age, latrine use) factors on preschool child reinfection epgs for each STH.  High prevalence spatial clusters were detected for Trichuris and hookworm but not for Ascaris.  These clusters were characterized by low household density and low household wealth indices (HWI).  Reinfection epg of both hookworm and Ascaris was positively associated with pre-treatment epg and was higher in stunted children.  Additional individual (latrine use) as well as household variables (HWI, maternal education) entered the reinfection models for Ascaris but not for hookworm.

CONCLUSIONS/SIGNIFICANCE: Even within the context of extreme poverty in this remote rural setting, the distinct transmission patterns for hookworm, Trichuris and Ascaris highlight the need for multi-pronged intervention strategies.  In addition to poverty reduction, improved sanitation and attention to chronic malnutrition will be key to reducing Ascaris and hookworm transmission.



Currently, control programs for soil transmitted helminth (STH) infections focus on delivering chemotherapy to school age children in high risk populations living in endemic areas [1,2].  However, ensuring control of infections in preschool children is particularly important given the fact that STH infection has negative consequences for early growth and cognitive development [3,4].  Children become infected with STH infections when they are exposed to the egg or larvae of the parasite.  Exposure to infection is determined by factors at the individual level, for example, not wearing shoes [5], geophagy [6,7]; at the household level, for example, poverty [8], household crowding [9,10] and limited latrine access [8,11,12]; and the regional level, for example, coverage of sanitation and hygiene infrastructure [13], soil type [14,15] and vegetation cover [14,16].  Studies that examined the influence of biophysical versus socioeconomic (SES) factors on the distribution of STH infection have demonstrated that SES played a greater role than biophysical factors such as rainfall, soil type and vegetation cover [17-19].  Individual susceptibility to infection can relate to genetics and/or nutritional status because both genetic factors [20] and nutritional deficiencies [4,11,21,22] result in impaired immune function.

Longitudinal studies of STH reinfection are rare and of those studies, few have the necessary individual data to examine the influence of nutritional status on reinfection burdens [11,21,22].  Our longitudinal study in indigenous Ngäbe preschool children in rural western Panama aimed to better understand the exposure and susceptibility variables that influenced the transmission of STH infections in this region.  Specifically, we monitored reinfection dynamics of 3 STH infections (Ascaris, Trichuris and hookworm) over two reinfection cycles to gain an understanding of regional (presence in a high prevalence cluster), household (household density, asset-based household wealth (Figure 1), household crowding, maternal education) and individual (age, sex, pre-treatment eggs per gram (epg) feces, height-for-age, latrine use) factors that influenced transmission of these infections among preschool children.

Although the relationship between poor SES and STH infection has been established [17-19], we demonstrated that even in an area of extreme poverty there were heterogeneities in this relationship and that the scale of this relationship varied among the STH species.   Specifically, despite the rural setting where virtually all preschool children in our study live under conditions of extreme poverty, we found that Trichuris and hookworm infection clustered in the more impoverished regions (Figure 2) whereas Ascaris was present throughout the study area, indicating the importance of regional scale clustering for two, but not the third, STH.  At the household level, traits related to household poverty such as low maternal education and low household wealth were indicative of higher Ascaris reinfection burdens but not hookworm (Table 1).

Furthermore, within this context of regional clustering of infection and household poverty, we were able to examine the importance of chronic undernutrition (low height-for-age) as a factor influencing individual-level susceptibility to STH transmission.  Specifically, we were able to control for the regional clustering of infection and the poverty related factors (maternal education, HWI, latrine use) that may influence child height-for-age to investigate the hypothesis that nutritional deficiencies may make children more susceptible to reinfection.  We found that preschool children who were chronically malnourished (low height-for-age) had a higher reinfection burden of Ascaris and hookworm (Table 2).  This finding is particularly important given that STH infection further degrades nutritional status thus perpetuating a negative cycle of poor health during a critical period in their physical and cognitive development [3,4].  In our study we also noted a lower treatment efficacy of Albendazole for Trichuris which was followed by high infection levels during the second reinfection cycle. The lower treatment efficacy in our study area may be due to genetic polymorphisms associated with benzimidazole resistance [23].  This calls attention to the importance of monitoring drug efficacy, especially against Trichuris, as well as the possibility of using multiple treatments or an alternative anthelmintic.

This cross-disciplinary analysis of preschool child STH transmission emphasizes the importance of multi-pronged intervention strategies to break the cycle of poverty and infection in impoverished rural areas. First, improving both the regional and household level sanitation and hygiene environment will ensure the reduction of the transmission of multiple STH infections.  Second, nutrition interventions are needed to reduce the long term developmental consequences of infection for the most vulnerable children.  Third, sanitation and nutrition interventions need to be combined with monitoring of drug efficacy and targeted anthelmintic delivery to ensure that infections with all species of STH are controlled.   Taken together, comprehensive control programs that combine short term morbidity control with the development of long term economic capacity, sanitation infrastructure and improved food security are necessary to make lasting improvements for child health in poor rural areas.     


Carli Halpenny-1

Figure 1. Assets included in Principal Components Analysis of Household Wealth Index (HWI)

(a) Scoring factors for the assets included in Principal Components Analysis to determine HWI  and (b) distribution of select assets in the low (lowest 40% of households), medium (middle 40% of households) and high (top 20% of households) “wealth” groups. 


Carli Halpenny-2

Figure 2.  Spatial clusters of households with high prevalence of hookworm and Trichuris infection.

High prevalence clusters (dotted line) for hookworm (A) and Trichuris (B) infection detected at Baseline of Cycle 2.   Uninfected (small grey dots) and infected households (large dark dots) based on data from Cycle 2 at 6 mo (hookworm and Trichuris).



Table 1. Comparison of characteristics between households within and outside the high prevalence clusters.1

Carli Halpenny-3

1 Summary statistics presented are mean ±SEM or % (95% CL).

 2 Asset based index, weights derived from the first component of Principle Components Analysis.

*p<0.05; **p<0.001

# remained significant in final multiple logistic regression models predicting household presence within Cycle 2 high prevalence clusters.


Table 2. Negative binomial regression models of Ascaris and hookworm reinfection intensity in Panamanian preschool children during two reinfection cycles (Cycle 1 – 9 mo reinfection period, Cycle 2 – 6 mo reinfection period).

Carli Halpenny-41Incidence Rate Ratio.

2Household within identified high prevalence cluster of infection by SaTScan Spatial Scan (0=no, 1=yes).

3 NA = Not applicable

4NE = Variable was excluded during the stepwise process (p>0.10).

50=boy, 1=girl

60=no, 1=yes

71/Alpha statistic indicates the degree of overdispersion in the data.

*p<0.05, **p<0.001

Variables that did not enter any model: Household crowding.



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ACKNOWLEDGEMENTS: This study was part of a collaborative effort between McGill University, the Panamanian Ministry of Health (MINSA) and the Instituto Conmemorativo Gorgas de Estudios de la Salud .  The study was supported by grants from the International Development Research Centre (IDRC) and the “Science versus Poverty” grant from Secretaria Nacional de Ciencia , Tecnología y Inovación (SENACYT).  FLOTAC fecal analysis equipment was kindly donated by The Regional Center for Monitoring Parasites (CREMOPAR), Department of Pathology and Animal Health, Faculty of Veterinary Medicine, University of Naples Federico II, Naples, Italy.

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