Trichuris trichiura: a problematic parasite for deworming programs?

Gabrie JA1., Sanchez A1., Rueda MM2., Canales M2., Gyorkos TW3. aDept. Community Health Sciences, Brock University, Canada; bSchool of Microbiology, National University of Honduras; cDept. Epidemiology, Biostatistics and Occupational Health, McGill University, Canada

Jose Gabrie, jgabrie@brocku.ca, Tel. (905) 688-5550 ext. 4388

Three intestinal helminths: roundworms (Ascaris lumbricoides), whipworms (Trichuris trichiura), and hookworms (Ancylostoma duodenale and Necator americanus) are collectively known as soil-transmitted helminths (STH) due to their ability to survive in the environment and be transmitted by fecally-contaminated soil1,2.

In endemic countries, STH are major causes of childhood malnutrition, anemia, diarrhea, stunted growth and decreased school performance. Hookworms and Trichuris infections are those STH directly implicated in causing anemia. T. trichiura has a direct life cycle as depicted below. Mass school-based preventive chemotherapy is recommended by the World Health Organization (WHO) as the main intervention strategy for reducing the occurrence of STH in children living in highly endemic areas1. Typically, deworming programs administer single-dose tablets of either Albendazole (ALB) or Mebendazole (MBZ)3.

This regimen of treatment against Trichuris infection may not be optimal. Several studies have demonstrated that both drugs have low efficacy against this parasite4,5. As seen in Table 1, a recent meta-analysis found an overall cure rate of 43.6 % and 23.0 % for ALB and MBZ, respectively. In Honduras, deworming campaigns have been in place for several years but a structured nation-wide program for school-age children (single-dose ALB or MBZ/twice a year) only started in 19986. National prevalence studies in Honduras have been conducted in 2001, 2005 and 2011. As the graph below shows there is a decrease in STH infections; however, this decrease is likely not solely attributable to the chemotherapy.

Funding for this study was provided by grants awarded by GHRI (AS) and CIHR (TWG). We also acknowledge the cooperation of Honduras’ National University of Agriculture in Catacamas and the field work done by the graduate students in the Master’s degree program in Zoonotic and Infectious Diseases (MEIZ-UNAH).

•Despite previous deworming treatment, the prevalence of STH remained high in the study population.

•A single-dose ALB/MBZ regimen twice a year seems to be more effective against Ascaris and hookworms but not Trichuris infections.

•Honduras’ deworming program would benefit from monitoring not only nation-wide STH prevalence but also from assessing parasite-specific response as well as community-specific risk factors in order to adjust control strategies aimed at reducing STH burden in the country.

•Studies are needed in Honduras to determine the long-term impact of deworming programs.

Introduction

Methods

• To study gender-specific determinants of STH in school-age children in rural Honduras.

• To determine risk factors for STH infection.

• To indirectly evaluate deworming effectiveness by comparing the occurrence of STH in children who had previously been dewormed with children who had not.

• To assess deworming effectiveness at school level.

The study was conducted between February and March 2011 in eight schools in three rural areas of Catacamas, Department of Olancho, Honduras. Enrolled students in grades three to five were asked to provide one stool specimen and answer a standardized questionnaire for retrieving epidemiological data. Anthropometric measurements were taken to evaluate children’s nutritional status and growth.

Stool specimens were examined using the Kato-Katz thick smear technique. Infection intensity was measured in eggs per gram of feces (epg) and classified according the thresholds defined by the WHO7.

Statistical analyses including univariate Chi square, t-test, correlation and multiple logistic regression were performed using SPSS (v.20; SPSS Inc., Chicago, IL)

Objectives

Results A total sample of 320 children (aged 7-14, Mean= 9.8) enrolled in grades 3 to 5 completed the study; 48 % were girls.

The overall STH prevalence was 72.5 %, with 67 %, 30 % and 16 % for Trichuris, Ascaris and hookworm infections, respectively (Figure 3).

Results (cont’d)

Conclusions

Acknowledgements

Figure 1. Life Cycle of Trichuris trichiura

About 86% of the children (275) reported previous deworming.

Previous deworming was not found to be significantly associated with STH prevalence. Moreover, children in schools with either no deworming or deworming once a year were 3 times more likely to have Ascaris infections (OR = 3.4, 95% CI: 1.6-7.5) and hookworm infections (OR = 3.0, 95% CI: 1.1-8.1) than those in schools where deworming was given twice a year. Conversely, this analysis showed no significant difference for Trichuris infections (p = .148).

Risk factors associated with STH were evaluated through multiple logistic regression; adjusted p-values obtained are shown below. Figure 5 depicts risk factor analyses specifically for Trichuris showing that open defecation was more strongly associated with trichuriasis than deworming alone.

The prevalence of STH by sex is described below. Infection intensity is shown in Figure 4. About 73 % of Trichuris infections were light (Mean= 806.9 ± 4269.8 epg) as were 94 % of hookworms infections (Mean= 102.9 ± 593.4 epg); whereas 54 % of Ascaris infections were moderate (Mean= 4592.7 ± 12585.5 epg).

30%

67% 16%

Ascaris Trichuris Hookworms

Figure 3. Prevalence of STH in school-age children

Drug Parasite

Studies

Identified and

Included, No.

Individuals

No.

Overall

Cure Rate, %

Albendazole (400 mg) A. lumbricoides 66 5126 93.9

T. trichiura 64 5147 43.6

Hookworm 64 6334 78.4

Mebendazole (500 mg) A. lumbricoides 12 2036 96.5

T. trichiura 12 3112 23.0

Hookworm 14 3192 22.9

Table 1. Summary of observational and case studies reporting the use of single-dose oral

Albendazole and Mebendazole against Ascaris lumbricoides, Trichuris trichiura , and Hookworm

Infection (Modified from Keiser and Utzinger, 2008)

Figure 2. Prevalence of STH by Kato-Katz technique reported in school-age children in Honduras from 2001 to 2011

In 1998, National Deworming Program started in school-age children

0

15

30

45

60

1998 2000 2002 2004 2006 2008 2010 2012

Pre

vale

nce

(%

)

Year of report

Ascaris lumbricoides Trichuris trichiura Hookworms

Figure 4. Infection intensity of STH by Kato-Katz technique

40%

73%

94%

54%

25%

2%

6%

2%

4%

0% 20% 40% 60% 80% 100%

Ascaris

Trichuris

Hookworms

Percentage

Light Moderate Heavy

Hookworms

Ascaris Trichuris Hookworms

Girls 25% 66% 11%

Boys 34% 67% 20%

Parasite

Sex

Table 2. Prevalence of STH in school-age children by sex

Figure 5. Adjusted Odds ratios of risk factors for Trichuris infections

Factor Ascaris Trichuris Hookworms

0-1 per year treatment at school 0.002** 0.148 0.028**

Previous deworming 0.446 0.537 0.656

Go out without shoes 0.148 0.390 0.887

Play with dirt 0.598 0.061* 0.332

Defecation at open 0.002** 0.001** 0.087*

Absence of potable water 0.577 0.209 0.316

Dirty nails 0.095* 0.290 0.233

Had worms before 0.002** 0.081* 0.050*

Sex (female) 0.145 0.880 0.058*

* p < .10 ** p < .05

Table 3. p- values obtained in multiple logistic regression of factors

associated with STH infection