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    Schistosoma mansoni infection prevalence by stool and/or schistosome adult worm protein (SWAP) enzyme-linked immunosorbent assay (ELISA) by age.

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    Prevalence of Schistosoma mansoni, malaria, Trichuris trichiura, hookworm, and Ascaris lumbricoides infections by age.

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Schistosomiasis among Young Children in Usoma, Kenya

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  • Division of Parasitic Diseases and Malaria, Centers for Disease Control and Prevention, Atlanta, Georgia; Center for Global Health Research, Kenya Medical Research Institute, Kisumu, Kenya

Although schistosomiasis burden is greatest among school-age children (SAC) (6–15 years of age), infection among preschool-age children (PSAC) (1–5 years), may be underestimated in endemic areas. We conducted a cross-sectional study evaluating Schistosoma mansoni infection among children 1–15 years of age in a highly endemic community in Kenya. Diagnostic tests included stool exam (Kato/Katz technique), serum testing for schistosome-specific antibodies, and urine testing for circulating cathodic antigen (CCA). Overall, 268 SAC and 216 PSAC were enrolled; prevalence increased with age, with 14% of 1 year olds and more than 90% of children > 10 years of age infected. Stool exam was more sensitive among SAC than PSAC, but performance was similar after adjusting for infection intensity (based on CCA). Schistosomiasis poses a threat to PSAC in endemic areas, and stool exam may underestimate the prevalence of infection. Control programs in such areas should consider PSAC in addition to SAC.

Introduction

Chronic schistosomiasis affects more than 200 million people worldwide.1,2 Standard age prevalence curves for Schistosoma mansoni, which are based on egg excretion, show that both prevalence and intensity of infection peak between 10 and 15 years of age, after which prevalence declines gradually over years and infection intensity decreases more rapidly.3 The age distribution of infection rates and intensity is generally attributed to high levels of contact with cercariae-contaminated water among school-aged children and adolescents followed by less water contact and the development of an acquired protective immunity against infection in older adolescents and adults.46 Because of their importance in terms of the prevalence, morbidity, and transmission of schistosomiasis, along with the logistical ease of distributing praziquantel in educational settings, mass treatment of school-aged children is a cornerstone of schistosomiasis control activities.7,8

In contrast, younger children are often thought to be not infected with schistosomes or to have such low intensity infections that they do not suffer morbidity. Most mass treatment programs have not been designed to include them and younger children are often not even screened for the possibility of infection.9 However, in areas endemic for schistosomiasis, very young children are also in regular contact with water in locations where infected snails are present and infants are bathed in water where transmission is occurring.1013 Infections in young children may be missed because they are not usually examined or the testing method most commonly used for epidemiologic research (examination of a single stool specimen by Kato–Katz thick smears) may not be sufficiently sensitive, particularly in detecting light infections.14,15 Indeed, when more sensitive techniques such as multiple stool samples or serologic assays have been used to survey young children, sizeable proportions have been found to be infected.11,13,16

Immunity may also influence the ability to detect schistosome infections in young children. Previous studies on human infection with S. mansoni suggest a role for the immune response in efficient egg excretion.17 It is possible that younger children have not developed the appropriate immune responses to excrete eggs, leading to false negative results when stool examinations are used for diagnosis. We carried out a cross-sectional observational study of the prevalence of S. mansoni among children in a highly endemic area using both serologic assays and stool exams to detect infections. We tested the sensitivity of single and multiple stool exams compared with serologic diagnosis across age groups.

Materials and Methods

Study setting and population.

The study location was Usoma, a small community on the shores of Lake Victoria near Kisumu in Western Kenya. High rates of S. mansoni infection have been documented among men from the community who are self employed as sand harvesters; such work involves extensive contact with lake water. No mass drug administration with praziquantel had been carried out in Usoma before the study. We attempted to enroll all children 12 months to 15 years of age from the community in the study. On the basis of a census completed earlier in the year, we anticipated that there would be ∼680 children in Usoma in this age range. Children < 12 months of age were excluded because of potential persistence of maternal antibody that could lead to false positive serologic test results. The study protocol was approved by the Scientific Steering Committee of the Kenya Medical Research Institute (KEMRI), the Ethical Review Committee of Kenya, and the Institutional Review Board of the Centers for Disease Control and Prevention.

Data collection.

After obtaining informed consent from parents (and assent from child participants > 7 years of age), a questionnaire was administered to the parents of enrolled children to gather demographic and epidemiologic information, such as age, gender, duration of residency in the community, and variables related to S. mansoni exposure. Heights and weights were measured using standard procedures and Z-scores were calculated for height-for-age and body mass index (BMI)-for-age based on World Health Organization (WHO) growth standards.18,19

Quantitative determination of S. mansoni and soil-transmitted helminths was performed through evaluation of stool by the Kato/Katz fecal thick smear technique. The children were asked to provide fresh stool samples, one per day produced on three consecutive days, which were then used to prepare duplicate slides that were examined for the presence of eggs. Each slide was read by at least two well-trained technologists, yielding a total of 12 egg counts per child from six fecal smears. Arithmetic means of the 12 egg counts were calculated and expressed as eggs per gram (epg) of stool, and classified as light- (1–99 epg), moderate- (100–399 epg), or heavy-intensity (≥ 400 epg) S. mansoni infections.2 A finger-stick blood sample was tested using the schistosome adult worm protein (SWAP)-specific enzyme-linked immunosorbent assay (ELISA).20 A child with one or more positive stool slides or with positive SWAP ELISA results was considered infected with S. mansoni. Because Usoma has not been targeted by any preventive chemotherapy, positive serologic results were likely to represent true infections. A fresh urine sample was also requested and was tested with a commercially available circulating cathodic antigen (CCA) assay (Rapid Medical Diagnostics, Pretoria, South Africa), which includes a standard curve that allows for a gross estimate of infection intensity.20,21 Urine CCA was detected by carbon-conjugated antibody and measured as either negative or as 1-, 2-, or 3-plus. Among those children who tested positive for S. mansoni by stool and/or SWAP ELISA, infections were classified as low intensity (CCA negative or 1-plus), or high intensity (CCA 2- or 3-plus).

Blood samples were also used to test for malaria and anemia. Thick blood smears were stained with Giemsa and examined for the number of malaria parasites per 300 leukocytes. Infection status was defined by the presence of a single parasite. Hemoglobin levels were determined using a portable, battery-operated hemoglobinometer (HemoCue, Angelholm, Sweden). Anemia was defined according to Kenyan clinical guidelines: < 10.0 g/dL for children < 5 years of age, < 11.0 g/dL for children 5 to 8 years of age, and < 12.0 g/dL for children ≥ 9 years of age; anemia was classified as mild if hemoglobin was > 8.0 g/dL, moderate if 5.0–8.0 g/dL, and severe if < 5.0 g/dL.22

Treatment with praziquantel, albendazole, and Coartem (artemether-lumefantrine) was provided for schistosomiasis, other helminths, and malaria infections, respectively, as needed. Praziquantel was dosed based on weight (single dose of 40 mg/kg). The treatment of children < 4 years of age was overseen by a local pediatrician, because safety data are limited for this age group.23 For children too young to swallow pills, praziquantel pills were crushed and administered mixed with water.

Data handling and analysis.

Questionnaire data were collected on handheld computers that were programmed using Visual CE (Syware, Inc., Cambridge, MA). Laboratory results were entered using Microsoft Excel (Microsoft Corporation, Redmond, WA). Data were analyzed using SAS Enterprise Guide version 4 (SAS Institute Inc., Cary, NC). Proportions were calculated with 95% confidence intervals (CI). The sensitivities of diagnostic tests were evaluated; a child with a positive test for S. mansoni by stool and/or SWAP ELISA was considered a true positive. Comparisons across groups were done using Fisher's exact test and P values < 0.05 were considered significant.

Results

A total of 484 children were enrolled, with ages ranging from 1 to 15 years. The mean age was 6.8 and the median was 7 years. Study subjects were divided into two age groups: preschool-age children (PSAC) aged 1–5 years, of which there were 216; and school-age children (SAC) aged 6–15 years, of which there were 268. The overall prevalence of schistosomiasis for the study population was 39% (95% CI = 34–43) by stool examination, 62% (95% CI = 57–66) by SWAP ELISA, and 65% (95% CI = 61–69) by stool and/or SWAP ELISA.

Figure 1 depicts the proportion of children with S. mansoni by stool and or SWAP ELISA by age. The prevalence rate was 14% among 1 year olds and increased steadily with age. More than 90% of children over age 10 were infected. Each of three single stool exams achieved similar results, and the use of multiple stool exams did not increase the sensitivity of the test.

Figure 1.
Figure 1.

Schistosoma mansoni infection prevalence by stool and/or schistosome adult worm protein (SWAP) enzyme-linked immunosorbent assay (ELISA) by age.

Citation: The American Society of Tropical Medicine and Hygiene 84, 5; 10.4269/ajtmh.2011.10-0685

Schistosoma mansoni infection by age group (SAC versus PSAC) is presented in Table 1. By all testing modalities, a greater proportion of SAC were infected with S. mansoni compared with PSAC. Overall, 37% of PSAC and 88% of SAC were considered to have true infections (P < 0.0001). Among all infected children, a significantly greater proportion of SAC compared with PSAC had intense infections, as indicated by a urine CCA result of 2- or 3-plus. Intensity as measured by epg was also higher among SAC than PSAC. Among PSAC children with positive stool samples for S. mansoni, 24 (63%) had low-intensity infections, 9 (24%) had moderate-intensity, and 5 (13%) had heavy-intensity infections. Among SAC, the numbers (and proportions) with low-, moderate-, and heavy-intensity infections were 60 (40%), 62 (42%), and 27 (18%), respectively (P = 0.044).

Table 1

Schistosoma mansoni infection, lake water exposure, and anti-parasitic treatments by age group*

PSAC N = 216SAC N = 268P value
n%n%
Stool-positive3817.614955.6< 0.0001
Serology-positive7333.822684.3< 0.0001
Stool- and/or serology-positive7936.623587.7< 0.0001
Urine CCA ++/+++1927.110648.20.002
Ever visit lake15471.326799.6< 0.0001
Swim in lake7347.419773.8< 0.0001
Wash clothes in lake005621.0< 0.0001
Bathe in lake15198.025796.20.390
Visit lake ≥ 4×/week4026.08732.60.186
Bathe in lake water19791.225394.40.211
Ever treated for schistosomiasis0000
Ever treated for malaria216100268100
Treated in past 3 months9644.69033.80.018

PSAC = preschool-age children; SAC = school-age children.

Compared with circulating cathodic antigen (CCA) negative or “+”; denominator includes stool- or serology-positive with CCA results, N = 290.

Several well-recognized risk factors for schistosomiasis were more common among SAC than among PSAC (Table 1). All but one of the parents of SAC reported that the child ever visited the lake, compared with 71% of parents of PSAC (P < 0.0001). Swimming and washing clothes in the lake were also significantly more common among SAC compared with PSAC. However, among those children who ever visited the lake, more than 95% of both PSAC and SAC bathed in the lake, and the frequency of visiting the lake was similar across age groups. No parent reported a child having ever been treated for schistosomiasis. In contrast, all children from both age groups had received treatment of malaria; PSAC were significantly more likely to have received antimalarials within the past 3 months. No parents were able to specify whether the antimalarial received had been Coartem (which also has antischistosomal activity24).

Among PSAC (Table 2) there was no association between S. mansoni infection and related morbidities such as anemia, stunting (as indicated by the height-for-age Z-score), or wasting (as indicated by the BMI-for-age Z-score). Among SAC, S. mansoni infection was significantly associated with anemia, particularly mild anemia. Schistosomiasis did not appear to have any impact on stunting or wasting in the older age group.

Table 2

Schistosomiasis-associated morbidities by age group and infection status

PSACP valueSACP value
S. mansoni positive*N = 79S. mansoni negative N = 137S. mansoni positive*N = 235S. mansoni negative N = 33
n%n%n%n%
Anemia3341.86547.40.4799741.3721.20.035
Mild (> 8.0 g/dL)2227.84835.00.2958234.9412.10.009
Moderate (5.0–8.0 g/dL)1113.91611.70.672146.039.10.449
Severe (< 5.0 g/dL)0010.71.00010.4001.000
Height-for-age Z-score < −22430.44230.70.8835322.6515.20.821
BMI-for-age Z-score < −245.2118.40.29923.8000.708

Positive by stool exam and/or schistosome adult worm protein (SWAP) enzyme-linked immunosorbent assay (ELISA).

< 10.0 g/dL for children < 5 years, < 11.0 g/dL for children aged 5–8 years, and < 12.0 g/dL for children aged ≥ 9 years.

Excludes biologically implausible values.

PSAC = preschool-age children; SAC = school-age children; BMI = body mass index.

Table 3 summarizes the sensitivities by age group of stool and the SWAP ELISA for detecting S. mansoni infections. All stool exams—whether single or a composite of three exams—were significantly less sensitive for detecting infection in PSAC compared with SAC. In contrast, the SWAP ELISA detected similar levels of infection across both age groups. After controlling for infection intensity by stratifying the S. mansoni-positive children into those with a CCA that was negative or +, and those with ++ or +++ (Table 4), the sensitivities of single and multiple stool exams were also similar across age groups.

Table 3

Sensitivities of single stool exams, multiple stool exams, and SWAP ELISA by age group*

S. mansoni positive PSAC N = 79S. mansoni positive SAC N = 235P value
n%n%
Stool 13544.314461.30.012
Stool 23746.814561.70.025
Stool 33848.114561.70.036
Stool ×33848.114963.40.018
SWAP ELISA7392.422696.20.220

Positive by stool and/or schistosome adult worm protein (SWAP) enzyme-linked immunosorbent assay (ELISA) considered true positive.

PSAC = preschool-age children; SAC = school-age children.

Table 4

Sensitivities of single and multiple stool exams, controlling for infection intensity*

Urine CCA neg/+S. mansoni positive PSAC, N = 50S. mansoni positive SAC, N = 113P value
n%n%
Stool 11530.04338.00.377
Stool ×31752.24750.10.389
Urine CCA ++/+++S. mansoni positive PSAC, N = 19S. mansoni positive SAC, N = 106P value
n%n%
Stool 11579.09185.80.488
Stool ×31579.09286.80.475

Positive by stool and/or schistosome adult worm protein (SWAP) enzyme-linked immunosorbent assay (ELISA) considered true positive.

PSAC = preschool-age children; SAC = school-age children; CAA = circulating cathodic antigen.

The prevalences of S. mansoni, malaria, Trichuris trichiura, hookworm, and Ascaris lumbricoides infections among the study population by age are presented in Figure 2. Schistosoma mansoni was the most common parasitic infection identified across all ages. Table 5 compares the prevalence of other parasitic infections among those children infected and uninfected with S. mansoni. Trichuris trichiura and malaria infections were significantly associated with S. mansoni infection.

Figure 2.
Figure 2.

Prevalence of Schistosoma mansoni, malaria, Trichuris trichiura, hookworm, and Ascaris lumbricoides infections by age.

Citation: The American Society of Tropical Medicine and Hygiene 84, 5; 10.4269/ajtmh.2011.10-0685

Table 5

Prevalence of other parasitic infections by Schistosoma mansoni infection status

S. mansoni positive*N = 294S. mansoni negative N = 160P value
n%n%
Trichuris trichiura11436.34425.90.012
Hookworm5617.82313.50.248
Ascaris lumbricoides123.874.11.000
Malaria11137.83320.10.002

Positive by stool exam and/or schistosome adult worm protein (SWAP) enzyme-linked immunosorbent assay (ELISA).

Denominators vary because of missing values for other parasitic infections.

Malaria results unavailable for 30 children, N = 454.

Discussion

In this cross-sectional, community-wide study of children in an area that is highly-endemic for schistosomiasis where mass chemotherapy has not been used, we found high rates of infection among children of all ages. As expected, rates of infection were highest among SAC, with nearly 90% of children in this age group infected. All 14 and 15 year olds tested were positive for S. mansoni. We also found surprisingly high prevalence rates among young children, with 14% of 1 year olds infected and a prevalence that increased steadily with age. Among PSAC, more than a third of the children were infected with a disease that is not generally considered a public health problem in this age group. Our data suggest that, similar to older children, young children may be exposed to S. mansoni through bathing in lake water—whether they go to the lake to bathe or bathe at home with water carried from the lake. Other studies have reported high rates of S. mansoni11,13,16 and Schistosoma haematobium10,25,26 among young children in endemic areas. Our study findings support other authors' conclusions that schistosome infections can be common in children younger than school age in endemic areas.9,13

Despite the substantial prevalence of infection among PSAC, schistosomiasis-related morbidities were not associated with infection in this age group. Schistosoma mansoni was associated with anemia in older children—a finding consistent with numerous other studies. The association remained significant after adjusting for infection with malaria and soil-transmitted helminths (data not shown). The lack of schistosomiasis-associated morbidities in the young children in this study may reflect lower intensity infections that perhaps do not lead to measurable sequelae. Yet there is growing recognition that even low intensity infections can have important long-term consequences for the health of affected individuals,27 and it is possible that consequences of infection at a young age may take years to manifest and may not become apparent in the short term despite ongoing harm to the infected child.

The significantly higher prevalence of malaria and T. trichiura infections observed among S. mansoni-infected children suggests that children with schistosomiasis may also be at increased risk for additional parasitic infections. This association may be particularly important among PSAC, because young children suffer the greatest burden of malaria morbidity and mortality.28 However, this observation requires further investigation before firm conclusions can be drawn.

With respect to the sensitivity of stool exams for S. mansoni, in our study three stools performed no better than a single stool exam across all ages. Although other studies have found single stool exam to be less sensitive than multiple stool exams, it is possible that the relatively high intensity of infection observed in our study population may have improved the yield of a single stool exam. Nonetheless, stool exams were overall less sensitive than serology, and had particularly poor sensitivity among PSAC. However, after controlling for infection intensity using CCA as a crude marker of worm burden, the sensitivity of stool was similar across age groups.

The study had several limitations. The lack of a gold standard for diagnosing schistosomiasis based on serology meant that our results may have been affected by misclassification bias. We also had limited quality assurance of stool sample collection—containers for the second and third stool samples were left at the house and picked up the following day. Thus, it was not possible to verify that stool samples were actually produced by the child that submitted the specimen. Usoma is a single community that is highly endemic for S. mansoni. The results are therefore not directly applicable to areas with lower levels of transmission. Finally, urine CCA is a crude proxy for infection intensity and may not fully explain the difference in stool sensitivity observed between PSAC and SAC.

In conclusion, our findings show that young children are indeed at risk for schistosomiasis infection. And although PSAC are currently not targeted by schistosomiasis control activities, it may be worthwhile for programs to consider including them in preventive chemotherapy campaigns, especially where the prevalence is high among SAC.9,13 The use of praziquantel among young children has been hindered by a lack of safety data among children < 4 years of age,9,23 and no widely available liquid formulation; however, recent studies in which young children have been treated with praziquantel have reported no major adverse effects.10,11,13 We found that the sensitivity of stool exams for S. mansoni was limited, especially among PSAC; the observed difference in its performance across age groups is likely a function of infection intensity. Further investigation of the long-term effects of infection in young children is necessary to better understand how schistosomiasis impacts community health. In areas with a high prevalence of infection, the contribution of young children to transmission in the community should be considered when designing and implementing strategies to control this disease.

ACKNOWLEDGMENTS:

We thank John Adero, John Masa, Nathan Mulonga, Diana Aida, Chrispine Owaga, and Erick Livaha for their assistance with this study.

  • 1.

    Steinmann P, Keiser J, Bos R, Tanner M, Utzinger J, 2006. Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infect Dis 6: 411425.

    • Search Google Scholar
    • Export Citation
  • 2.

    WHO, 2002. Prevention and control of schistosomiasis and soil-transmitted helminthiasis. World Health Organ Tech Rep Ser 912: 157.

  • 3.

    Sleigh AC, Mott KE, 1986. Schistosomiasis. Gilles HM, ed. Epidemiology and Control of Tropical Diseases (Clinics in Tropical Medicine and Communicable Diseases, Volume 1). London, UK: W.B. Saunders Co., 643670.

    • Search Google Scholar
    • Export Citation
  • 4.

    Dalton PR, Pole D, 1978. Water-contact patterns in relation to Schistosoma haematobium infection. Bull World Health Organ 56: 417426.

  • 5.

    Butterworth AE, Capron M, Cordingley JS, Dalton PR, Dunne DW, Kariuki HC, Kimani G, Koech D, Mugambi M, Ouma JH, Prentice MA, Richardson BA, Arap Siongok TA, Sturrock RF, Taylor DW, 1985. Immunity after treatment of human schistosomiasis mansoni. II. Identification of resistant individuals, and analysis of their immune responses. Trans R Soc Trop Med Hyg 79: 393408.

    • Search Google Scholar
    • Export Citation
  • 6.

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Author Notes

*Address correspondence to W. Evan Secor, Centers for Disease Control and Prevention, 1600 Clifton Rd, Atlanta, GA 30329-4018. E-mail: WAS4@cdc.gov; wsecor@cdc.gov

Disclosure: This work is published with the permission of the Director, Kenya Medical Research Institute.

Authors' addresses: Jennifer R. Verani, Susan P. Montgomery, Sara E. Butler, and W. Evan Secor, Centers for Disease Control and Prevention, Atlanta, GA, E-mails: QZR7@cdc.gov, ZQU6@cdc.gov, CSU8@cdc.gov, and WAS4@cdc.gov. Bernard Abudho, Pauline N. M. Mwinzi, and Diana M. S. Karanja, Kenya Medical Research Institute, Kisumu, Kenya, E-mails: bernabu002@yahoo.com, PMwinzi@ke.cdc.gov, and DKaranja@ke.cdc.gov. Hillary L. Shane, Department of Cellular Biology, University of Georgia, Athens, GA, E-mail: hshane7@gmail.com.

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