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Increased Prevalence of Cestode Infection Associated with History of Deworming among Primary School Children in Ethiopia

Nader MohamedDepartment of Biology, Colgate University, Hamilton, New York;

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Anna MuseDepartment of Biology, Colgate University, Hamilton, New York;

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Moges WordofaDepartment of Medical Laboratory Sciences, College of Health Sciences, Addis Ababa University, Addis Ababa, Ethiopia

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Dessie AberaDepartment of Medical Laboratory Sciences, College of Health Sciences, Addis Ababa University, Addis Ababa, Ethiopia

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Abiyot MesfinDepartment of Medical Laboratory Sciences, College of Health Sciences, Addis Ababa University, Addis Ababa, Ethiopia

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Mistire WoldeDepartment of Medical Laboratory Sciences, College of Health Sciences, Addis Ababa University, Addis Ababa, Ethiopia

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Kassu DestaDepartment of Medical Laboratory Sciences, College of Health Sciences, Addis Ababa University, Addis Ababa, Ethiopia

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Aster TsegayeDepartment of Medical Laboratory Sciences, College of Health Sciences, Addis Ababa University, Addis Ababa, Ethiopia

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Bineyam TayeDepartment of Biology, Colgate University, Hamilton, New York;

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Mass deworming of school-aged children with anthelmintics has been recognized as an effective approach for reducing the burden of soil-transmitted helminth (STH) infections. However, the consequences of this intervention on nontargeted parasite populations sharing the same gastrointestinal niche are unclear. We conducted a cross-sectional survey among three primary schools in Sululta town, Ethiopia, to examine the association between students’ histories of deworming treatment in the past 6 months and the prevalence of cestode and protozoan infections. An interviewer-led questionnaire administered to parents provided information on sociodemographic factors, and deworming status was ascertained from school records. Stool samples were collected from 525 children for microscopic examination. The independent associations of “any cestode” (positive either for Hymenolepis nana or Taenia spp. eggs) and “any protozoan” (positive either for Giardia lamblia or Entamoeba histolytica/Entamoeba dispar) with history of deworming were examined using logistic regression. Overall, 25.9% of children were infected with at least one intestinal parasite of which H. nana was the most common. In multivariate analyses, deworming in the past 6 months was positively associated with increased odds of both “any protozoan” and “any cestode” infections; the latter reached statistical significance (AOR = 1.83, 95% CI: 0.69–4.86, P = 0.220, AOR = 3.82, 95% CI: 1.17–12.73, P = 0.029, respectively). If this observed association is causal, a greater understanding of interspecies interactions within the gastrointestinal niche may elucidate possible consequences of mass deworming treatments against STHs on coexisting nontargeted parasites.

INTRODUCTION

The WHO recommends controlling for soil-transmitted helminth (STH) infections in high-risk countries by implementing mass deworming programs.13 Soil-transmitted helminths comprise a number of intestinal nematodes such as Ascaris lumbricoides, hookworm (Ancylostoma duodenale and Necator americanus), Trichuris trichiura, and Strongyloides stercoralis4 (although the latter species is not recognized as STH by the WHO).3 Mass treatment ( irrespective of infection status) of all school-aged children consists of a single-dose of anthelmintics (400 mg albendazole or 500 mg mebendazole) either annually in areas with STH prevalence between 20% and 50% or biannually in areas with STH prevalence above 50%.5 This intervention has been recognized as an effective approach in reducing both the prevalence and intensity of STH infections.6 In addition, some studies show important health, nutritional, and societal benefits beyond the removal of worms.710 However, the reported advantages of mass deworming are highly disputed. The Cochrane Collaboration (2015) and Campbell Collaboration (2017), systematic reviews and meta-analyses of randomized trials, found no evidence of improved nutritional status, hemoglobin, cognition, school attendance, physical well-being, or survival.11,12 Yet, others have argued against the validity of this conclusion because most of the included studies in Cochrane’s pooled analysis lack long-term follow-up to assess the effect of periodic deworming. In addition, many of these articles use individual-level data, meaning they may fail to detect population-level health benefits from deworming solely because they lack the statistical power to do so.13 Regardless of inconsistencies in findings, school-based deworming programs promote ongoing government and policy maker investments.

Ethiopia is a country where STHs are widespread, with an estimated 79 million people living in STH-endemic areas; about 25.3 million of these are school-age children.14 In an effort to reduce STH burdens, the Ethiopian Federal Ministry of Health launched a national deworming program to treat 16.5 million school-age children in 459 woredas (districts) in 2015.15 Since the launch of the national deworming program, more than 19 million people have been treated for schistosomiasis and/or STHs with treatment a coverage of 77% and 76.5–80.5% for schistosomiasis and STHs, respectively.16

The existing deworming programs focus solely on reducing the morbidity caused by STH infections and thus fail to account for the potential effect of removing these parasites on other intestinal pathogens coinfecting the host within the same gastrointestinal niche (e.g., bacteria, viruses, protozoa, and cestodes).17,18 Because infection with STHs has been suggested to suppress non-STH pathogen populations by cross-immunity or competitive inhibition,19,20 it is possible that reducing worm burden through anthelmintic drugs could disrupt local parasite community relationships leading to unforeseen consequences.21 A study of wild mice confirmed this phenomenon showing that mice given single-dose anthelminthic contained lower nematode levels but higher numbers of other gastrointestinal parasites such as coccidial protozoans and cestodes.22 Similarly, after receiving routine anthelmintic treatment, human populations in Bolivia and Bangladesh had decreased worm burden but an increased risk of infection for Giardia lamblia.23,24 The antagonistic relationship between hookworm spp. and A. lumbricoides with G. lamblia shown to exist among the Bolivian population implies STH species may play a role in suppressing concurrent protozoa species.24 Altogether, these studies suggest deworming treatment may disrupt STH interactions with other pathogens sharing the same gastrointestinal niche, thereby unintentionally increasing the host’s susceptibility to non-STH parasite infections.

Research assessing the potential impact of STH-targeted anthelmintics on coinfecting parasites sharing the same intestinal niche is limited.23,24 We, therefore, used our data from Ethiopian schoolchildren to examine possible associations between children’s histories of deworming treatment (single dose of 500 mg mebendazole) in the past 6 months and the prevalence of cestodes and protozoan infections.

METHODS

Study setting and design.

We conducted a cross-sectional survey in three primary schools that participated in the first round of mass deworming treatments in Sululta town, Ethiopia. Sululta is located in the Oromia region, approximately 30 km north of the capital city, Addis Ababa. The altitude of this region is 2,450 m above sea level with average temperatures ranging from 15°C to 18°C. The rural town’s estimated population is 49,000. We used single-stage cluster sampling to recruit schoolchildren from April to August 2017. Of the nine governmental primary schools in Sululta town, three (Laga Dima, Wasarbi, and Abdi Boru) were selected randomly to recruit participants. The Oromia region was chosen for investigation because intestinal parasites are endemic among the population and many schools participate in mass deworming programs for treating students.16 Before conducting our fieldwork, we approached the local health department and visited each school to explain the school principals and teachers about the goal and nature of this study. These individuals were then responsible for explaining the objective of the study within their school community. The school principals contacted the randomly selected students who were instructed to bring their parents or legal guardian to the school. The investigators then provided supplemental information sheets to the parents to further explain the objective of the study. Parents were given the opportunity to discuss their participation with friends and other family members before deciding. After parents consented, schoolchildren had the autonomy to make their decision of participating. Children willing to enroll in the study provided stool specimens. This approach is valued by parents and has been shown to be feasible in previous studies in our setting. In our study, school-age children were identified as individuals in the 5–14-year age range as defined by the WHO classification of this age group.

Measurement and data collection.

After receiving a signed consent form by parents or students’ legal guardians, information about socioeconomic, environmental, and selected lifestyle variables was gathered using an interviewer-based questionnaire. Responses provided information about socioeconomic factors, including gender, place of residence, age, family size, parents’ education and occupation, family income, and use of electricity. Furthermore, the questionnaire asked about various potential confounders, including environmental factors (e.g., sanitation, water supply, and the presence of animals) and selected lifestyle factors (e.g., handwashing practices, fingernail trimming, shoe wearing, the frequency of soap use, vaccination history, and child’s use of antibiotics). The questionnaire was translated from English to local languages (Oromiffa and Amharic) for optimal understanding and accuracy of responses. Before the actual data collection, the translated version of the questionnaire was pretested among nonparticipating parents in Sululta town for purposes of clarity, validation, suitability, and logical flow of the questions.

Trained health extension workers administered the anthelmintic drugs to schoolchildren regardless of their age, size, or weight differences. In the study schools, only one round of deworming drug was distributed, and children did not receive any school-based deworming before our parasitological survey. The school principal provided the investigators with the children’s records to confirm their deworming status. Parasitological assessment was performed within 6 months following deworming.

During the survey, parents were asked to collect a fecal sample from their child using a leak-proof plastic container. The samples were processed immediately (i.e., within a maximum of 30 minutes after collection) for microscopic examination using direct wet mounts and the Kato–Katz technique at the temporary laboratory set-up at each school. The remaining stool specimens were preserved using sodium acetate–acetic acid–formalin (SAF) and transported to Department of Medical Laboratory Sciences, Addis Ababa University, for formol–ether concentration analysis. Two experienced medical laboratory technologists ran all parasitological tests.

Laboratory testing.

Direct wet mount microscopy.

Approximately 2 mg of the freshly collected stool sample was mixed with 0.85% NaCl solution using a wooden applicator stick to produce a uniform suspension of the stool under a 22 × 22-mm coverslip. Examination of the suspended sample for evidence of parasitic infection (parasitic cysts, ova, and/or mobile trophozoites) was performed using a microscope at ×100 magnification. Further analysis was conducted at ×400 magnification to identify parasite species.

Kato–Katz technique.

After performing the wet mount examination, each stool sample was analyzed using the Kato–Katz technique at the site on the same day of collection. Kato–Katz thick smears were prepared following the WHO’s protocol.25 A significant amount of fecal sample was pressed on a flat surface with a nylon screen and the surface of the screen was then scraped with a plastic spatula to sieve the fecal sample. A calibrated template of 41.7 mg was used to keep the amount of sieved fecal material consistent across samples. The fecal material was transferred to a microscope slide and covered with a cellophane strip soaked overnight in methylene blue glycerol solution. After pressing the slide on a flat surface to evenly spread the sample, the stool was examined under the microscope for evidence of parasite eggs.

Formol–ether concentration technique.

Following on-site stool examination, the samples were analyzed using the formol–ether concentration technique at Addis Ababa University. A stool sample of approximately 1 g was homogenized using an applicator stick in 8 mL of sodium acetate–SAF The emulsified feces were sieved and collected in a tube with 4 mL of diethyl ether. The tube was closed with a rubber stopper and inverted for about 30 seconds. The sample was then centrifuged for 1 minute at 3,000 rpm. The supernatant (i.e., the top three layers formed) was decanted and the remaining sediment was examined for intestinal parasite ova and larvae using microscopy.26

Exposure definition.

For this study, deworming status was defined as receiving a single dose (500 mg) of mebendazole in the past 6 months before the survey as part of the mass school-based deworming programs (as evidenced from school records). Children who did not receive mebendazole in the specified timeframe were characterized as non-dewormed.

Outcome definitions.

The primary outcomes of the study were operationally defined as follows:

Any cestode infection” was defined as being positive for at least one egg of Hymenolepis nana or Taenia species, whereas “any protozoan infection” was defined as being positive for at least one cyst and/or mobile trophozoite(s) of G. lamblia or Entamoeba histolytica/Entamoeba dispar.

“Any STH” was defined as being positive either for A. lumbricoides, T. trichiura, hookworms, or S. stercoralis.

Statistical analysis.

Data were coded and entered into Microsoft Excel and transported to SPSS Statistical software version 24 (SPSS, Inc., Chicago, IL) for analysis. Descriptive statistics were used to present the sociodemographic variables and distribution of intestinal parasites. Before investigating the association between deworming in the past 6 months and the prevalence of “any cestode” or “any protozoan” infections, univariate analysis was performed to identify the possible confounders. Variables that were associated with both exposure (history of “deworming in the past six months”) and outcome (“any cestode,” “any protozoan,” and “any STH”) variables in the crude analysis using a statistical significance of P < 0.3 were categorized as possible confounders. These variables were gender, place of residence, age, family size, maternal education and occupation, water source, toilet type, and waste disposal site. In addition, we included variables previously shown in the literature to be associated with intestinal parasite infections among Ethiopian children, such as family size,27 handwashing,28 fingernail trimming,29 and washing fruit before eating.29 Our hypothesis that deworming in past 6 months would be associated with a higher prevalence of cestode and protozoan infections was assessed using multivariate logistic regression. We estimated odds ratios (ORs) associated with deworming in past 6 months for “any cestode” and “any protozoan” infections. The ORs were adjusted for a priori and potential confounders listed in Supplemental Tables 14. The same approach was used in a separate set of analyses to assess the association between deworming in past 6 months with prevalence of individual cestodes (i.e., H. nana and Taenia species) and protozoans (i.e., G. lamblia and E. Histolytica/E. dispar) as outcome variables. Covariates were kept in the model if they changed the coefficient of exposure (deworming status) by > 10% or if they were independently associated with the outcome at P < 0.10. Probability values < 0.05 were considered statistically significant for main effects.

RESULTS

Sociodemographic characteristics of the study subjects.

Table 1 shows the distribution of sociodemographic characteristics. Of the 525 children enrolled in the study, 59.9% were females and the majority (76.6%) were urban dwellers. The mean age of children was 10.8 years (SD 2.6 years) with a range of 4 to 15 years. More than half of the mothers were illiterate (52.0%) and housewives (57.3%). Most parents reported using piped water as their primary drinking source (83.2%) and using pits as their toilets (82.4%). Furthermore, most households had at least one animal (67.8%) and never used electricity for cooking (68.1%). The majority of the children (80.4%) had a history of deworming treatment in the past 6 months.

Table 1

Sociodemographic characteristics of school-age children enrolled in three primary schools in Sululta, Ethiopia (N = 525)

VariablesFrequencyPercentage
Gender
 Female31359.6
 Male21240.4
Place of residence
 Urban40276.6
 Rural12323.4
Age (years)
 5–915529.6
 10–1436870.4
Weight (kg), mean (SD)30.3 (9.87)
Height (m), mean (SD)1.47 (1.53)
Family size
 0–38416.3
 4–525449.2
 > 517834.5
Family income (ETB)*
 < 2000 ETB23862.2
 ≥ 2000 ETB11131.8
Maternal education†
 Illiterate27352.0
 Informal education8816.8
 Formal education16431.2
Maternal occupation
 Housewife30157.3
 Farmer101.9
 Office-related jobs6612.6
 Others‡14828.2
Paternal education†
 Illiterate9017.1
 Informal education16130.7
 Formal education27452.2
Paternal occupation
 Office-related jobs15529.5
 Farmer489.1
 Merchant17833.9
 Others‡11722.3
 Unemployed275.1
Drinking water source
 Pipe43583.2
 Well7013.4
 River/pond/dam183.4
Any animal§
 Yes35667.8
 No16932.2
Type of toilet
 Flushed toilet224.2
 Pit43182.4
 Open field7013.4
Handwashing after toilet
 Always35167.5
 Sometimes14628.1
 Never234.4
Consumption of raw meat
 Yes24947.7
 No27352.3
Washing fruit before eating
 Always11021.8
 Sometimes35470.2
 Never407.9
Fingernail trimming
 Yes34869.3
 No15430.7
Waste disposal
 Pit7414.7
 Open field18035.9
 Burning17033.9
 Garbage bin7815.5
Frequency of soap use
 Always11225.6
 Sometimes32173.3
 Never51.1
Cooking with electricity
 Always8616.4
 Sometimes8115.5
 Never35668.1
Deworming in the past 6 months∥
 Yes42280.4
 No10319.6

* Family income is given as Ethiopian birr (ETB) per month; 1 Ethiopian birr = 0.036 US dollars.

† Parental education: Formal if they had primary or secondary schooling or higher education. Informal if they do not fit in the formal category but can read and write. Illiterate was defined as those who cannot read and write.

‡ Others include daily laborer and trading-related occupations.

§ Any animal includes presence of cat, dog, hen, cow/ox, sheep, or horse/mule in the household.

∥ Deworming status was defined, received single dose (500 mg of mebendazole) as part of the mass school-based deworming programs in the past 6 months as evidenced form school records.

Distribution of intestinal parasites.

Table 2 provides the distribution of intestinal parasites. Overall, 25.9% (136/525) of the children were infected with at least one intestinal parasite. H. nana was the most prevalent parasite (6.9%) followed by E. histolytica/E. dispar (5.5%) and then G. lamblia (3.0%). In a separate analysis, after creating new outcome variables by grouping parasites in three categories, infection with “any cestode” was the highest (9.8%) followed by “any protozoan” (8.6%) and then “any STH” (6.1%).

Table 2

Distribution of intestinal parasites among schoolchildren enrolled in three primary schools in Sululta, Ethiopia (N = 525)

VariablesFrequencyPercentage
Individual parasite infections
H. nana366.9
E. histolytica/E. dispar295.5
G. lamblia163.0
A. lumbricoides152.9
Taenia spp.112.1
T. trichiura91.7
 Hookworms71.3
Enterobius vermicuralis30.6
S. stercoralis10.2
 Multiple infections*91.7
Any parasite†
 Yes13625.9
 No38974.1
Any cestode‡
 Yes479.8
 No47890.2
Any protozoan§
 Yes458.6
 No48091.4
Any STH∥
 Yes326.1
 No49393.9

STH = soil-transmitted helminth.

* Multiple infections defined as concurrent infection with at least two parasite species.

† Any parasite was defined as being positive for at least one intestinal parasite (include both helminths and protozoan).

‡ Any cestode was defined as being positive for at least one egg of H. nana or Taenia species.

§ Any protozoan infection was defined as being positive for at least cyst and/or mobile trophozoites of G. lamblia or E. histolytica/E. dispar.

∥ Any STH was defined as being positive either for A. lumbricoides, T. trichiura, Hookworms, or S. stercoralis.

Effects of demographic and potential confounders on outcome and exposure variables.

We ran a series of independent univariate analyses to examine the impact of demographic and potential confounders on the primary outcomes and exposure variables (Supplementa1 Tables 14). We found no statistically significant association between the outcome variables (infection with “any cestode” and “any protozoan”) and most demographic and lifestyle variables including child’s gender, age group, place of residence, eating raw meat, and figure nail trimming. Certain family characteristics (i.e., family income, maternal education, maternal occupation, and paternal occupation.) and common environmental factors (i.e., type of toilet, source of drinking water, waste disposal, and presence of animal in household) were not significantly associated with either “any cestode” or “any protozoan” infections (Supplemental Tables 1 and 2). However, children who never/sometimes washed their hands after toilet use or had illiterate fathers were more likely to be infected with “any cestode”, meanwhile, households that used open fields for waste disposal and sometimes used electricity for cooking were significantly associated with “any protozoan” infection (Supplemental Tables 1 and 2). Furthermore, our main exposure variable (history of deworming in the past 6 months) was significantly associated with a few demographic and confounding variables, such as age group, type of toilet, and sometimes handwashing after toilet use (Supplemental Table 3). We also found no significant association between infections with “any STH” and most demographic and potential confounders except for the paternal occupation as a farmer and waste disposal using garbage bins (Supplemental Table 4).

Association between history of deworming in the past 6 months and cestode infections.

The prevalence of “any cestode” (positive either for H. nana or Taenia spp. eggs) infections were higher among children who had a history of deworming treatment in the past 6 months (10.4%) than the non-dewormed children (2.9%). In multivariate analysis adjusted for a priori and potential confounders, deworming in the past 6 months was significantly associated with increased odds of “any cestode” infections (AOR = 3.82, 95% CI: 1.17–12.73, P = 0.029) (Table 3). When the analysis was restricted to the individual cestode parasite infections, a higher prevalence of H. nana infection was significantly associated with a history of deworming in the past 6 months (AOR = 4.61, 95% CI: 1.07–19.87, P = 0.040) (Table 4). A broadly similar trend of association was observed between infections with Taenia species and history of deworming in the past 6 months, but this did not achieve statistical significance (Unadjusted OR = 2.47, 95% CI: 0.31–19.56, P = 0.390) (Table 5).

Table 3

Multivariate logistic regression of “any cestode” infection in relation to history of deworming treatment in the past 6 months among school-age children enrolled in three primary schools in Sululta, Ethiopia

VariablesAny cestode,* N (%)Crude OR (95% CI)P valueAdjusted OR† (95% CI)P value
YesNo
Deworming status‡
 Dewormed44 (10.4)380 (89.6)3.88 (1.18–12.75)0.0263.82 (1.17–12.73)0.029
 Non-dewormed3 (2.9)100 (97.1)11

* Any cestode defined as being positive for at least one egg of H. nana or Taenia species.

† Adjusted for gender, place of residence, type of toilet, maternal education, and use of electricity for cooking.

‡ Deworming status was defined, received single dose (500 mg of mebendazole) as part of the mass school-based deworming programs in the past 6 months as evidenced form school records.

Table 4

Multivariate logistic regression of H. nana infection in relation to history of deworming treatment in the past 6 months among school-age children enrolled in three primary schools in Sululta, Ethiopia

VariablesH. nana, N (%)Crude OR (95% CI)P valueAdjusted OR* (95% CI)P value
YesNo
Deworming status†
 Dewormed34 (8.1)388 (91.9)4.42 (1.05–18.7)0.0434.61 (1.07–19.87)0.040
 Non-dewormed2 (1.9)101 (98.1)11

* Adjusted for paternal education, habit of fingernails trimming, use of electricity for cooking, and type of toilet.

† Deworming status was defined, received single dose (500 mg of mebendazole) as part of the mass school-based deworming programs in the past 6 months as evidenced form school records.

Table 5

Univariate logistic regression of Taenia species infection in relation to history of deworming treatment in the past 6 months among school-age children enrolled in three primary schools in Sululta, Ethiopia

VariablesTaenia species, N (%)Crude OR* (95% CI)P valueAdjusted OR (95% CI)P value
YesNo
Deworming status†
 Dewormed10 (2.4)412 (97.6)2.47 (0.31–19.56)0.390NANA
 Non-dewormed1 (1.0)100 (99.0)11

* We reported crude analysis because the number of children infected with Taenia spp. was low to fit multivariate logistics regression analysis, which could result in bias standard errors of the logit coefficients.

† Deworming status was defined, received single dose (500 mg of mebendazole) as part of the mass school-based deworming programs in the past 6 months as evidenced form school records.

Association between history of deworming in the past 6 months and protozoan infections.

We ran separate logistic regression models relating “any protozoan” (positive either for G. lamblia or E. histolytica/E. dispar) infection (outcome) to a child’s history of deworming treatment in the past 6 months. These showed a nonsignificant increase in the odds of “any protozoan” infections among dewormed children (AOR = 1.83, 95% CI: 0.69–4.86, P = 0.220) compared with non-dewormed children (Table 6). Analyzing each protozoa species separately revealed a relatively analogous trend of nonsignificant, positive association between a history of receiving deworming treatment in the past 6 months and infection with G. lamblia (AOR = 1.64, 95% CI: 0.36–7.52, P = 0.519) (Table 7) or E. histolytica/E. dispar (AOR = 1.88, 95% CI: 0.54–6.53, P = 0.318), respectively (Table 8).

Table 6

Multivariate logistic regression of any protozoan infection in relation to history of deworming treatment in the past 6 months among school-age children enrolled in three primary schools in Sululta, Ethiopia

VariablesAny protozoan*, N (%)Crude OR (95% CI)P valueAdjusted OR† (95% CI)P value
YesNo
Deworming status‡
 Dewormed39 (9.2)383 (90.8)1.65 (0.67–4.10)0.2711.83 (0.69–4.86)0.220
 Non-dewormed6 (5.8)97 (94.2)11

* Any protozoan was defined as being positive for at least cyst and/or mobile trophozoites of G. lamblia or E. histolytica/E. dispar.

† Adjusted for gender, age group, place of residence, presence of any animal in the house, habit of fingernails trimming, maternal education, source of water, and use of electricity for cooking.

‡ Deworming status was defined, received single dose (500 mg of mebendazole) as part of the mass school-based deworming programs in the past 6 months as evidenced form school records.

Table 7

Multivariate logistic regression of G. lamblia infection in relation to history of deworming treatment in the past 6 months among school-age children enrolled in three primary schools in Sululta, Ethiopia

VariablesG. lamblia, N (%)Crude OR (95% CI)P valueAdjusted OR* (95% CI)P value
YesNo
Deworming status†
 Dewormed14 (3.3)408 (96.7)1.73 (0.38–7.74)0.4721.64 (0.36–7.52)0.519
 Non-dewormed2 (1.9)101 (98.1)11

* Adjusted for paternal education, source of water, habit of washing had after toilet, and use of electricity for cooking.

† Deworming status was defined, received single dose (500 mg of mebendazole) as part of the mass school-based deworming programs in the past 6 months as evidenced form school records.

Table 8

Multivariate logistic regression of E. Histolytica/E. dispar infection in relation to history of deworming treatment in the past 6 months among school-age children enrolled in three primary schools in Sululta, Ethiopia

VariablesE. histolytica/E. dispar, N (%)Crude OR (95% CI)P valueAdjusted OR* (95% CI)P value
YesNo
Deworming status†
 Dewormed25 (5.9)397 (94.1)1.56 (0.53–4.58)0.4201.88 (0.54–6.53)0.318
 Non-dewormed4 (3.9)99 (96.1)11

* Adjusted for gender, age, habit of washing hand before eating, total white blood cell count, habit of washing fruit before eating, and use of electricity for cooking.

† Deworming status was defined, received single dose (500 mg of mebendazole) as part of the mass school-based deworming programs in the past 6 months as evidenced form school records.

Association between history of deworming in the past 6 months and STH infections.

Table 9 presents the results of multivariate logistic regression analysis for an association between history of deworming treatment in the past 6 months and infection with “any STH” (defined as positive for either A. lumbricoides, T. trichiura, hookworms, or S. stercoralis). These showed a nonsignificant reduction in the odds of “any STH” infection among children who had a history of deworming treatment in the past 6 months (AOR = 0.67, 95% CI: 0.28–1.71, P = 0.420) compared with non-dewormed children.

Table 9

Multivariate logistic regression of any STH infection in relation to history of deworming treatment in the past 6 months among school-age children enrolled in three primary schools in Sululta, Ethiopia

VariablesAny STH*, N (%)Crude OR (95% CI)P valueAdjusted OR† (95% CI)P value
YesNo
Deworming status‡
 Dewormed22 (5.2)400 (94.8)0.51 (0.23–1.12)0.0920.67 (0.28–1.71)0.420
 Non-dewormed10 (9.7)93 (90.3)11

STH = soil-transmitted helminth.

* Any STH was defined as being positive either for A. lumbricoides, T. trichiura, hookworms, or S. stercoralis.

† Adjusted for age, paternal education, type of toilet, place of waste disposal, and family size.

‡ Deworming status was defined, received single dose (500 mg of mebendazole) as part of the mass school-based deworming programs in the past 6 months as evidenced form school records.

DISCUSSION

This observational study provides evidence for the association between children’s history of deworming treatments (i.e., with a single dose of 500 mg mebendazole) in the past 6 months and prevalence of cestodes and protozoan infections. We found a higher prevalence of “any cestode” infections among children who had a history of deworming treatment in the past 6 months compared with those non-dewormed. More specifically, we found that children who had received deworming treatment in the past 6 months had significantly higher odds of H. nana infection.

Most studies of mass deworming focus solely on anticipated health benefits of deworming treatments against STHs710 and consequently ignore the possible consequence of such treatment on other intestinal parasites sharing the same gastrointestinal niche (protozoan and cestodes). Our analyses suggest that deworming treatment in the past 6 months may increase the odds of cestode infections among schoolchildren. Although we could not find studies specifically assessing the association between deworming and cestode infections, one cluster-randomized study evaluating effects of deworming with 400 mg albendazole on child mortality reported a similar positive association between deworming and cestode infections.30 Dewormed children had a higher prevalence of Hymenolepis spp. infection (5.7%) than the placebo group (4.9%); however, this observation was restricted to younger children (1.0–2.9 years) and failed to reach statistical significance.30 Another study evaluating the deworming campaign in Egypt reported a significantly higher prevalence of H. nana among schoolchildren treated with 400 mg albendazole compared with untreated children (1.4% and 1.2%, P < 0.05, respectively).31 On trend with these findings, general surveys of intestinal parasites among children in Ethiopia and Peru reported a higher prevalence of H. nana infections in the areas where mass deworming is widely administered to treat soil-transmitted nematodes.32,33 Unfortunately, both studies lack data on individual deworming status to further categorize the observed higher prevalence of H. nana based on deworming status. Even though it is difficult to compare data from a general survey with our findings, the higher prevalence of H. nana following a decreased burden of STHs after mass chemotherapy deserves closer investigation. Despite the paucity of literature assessing the association between cestodes and deworming in the human population, a study by Pedersen and Antonovics22 in experimental animals found a significant increase in cestode and coccidial parasite infections following the removal of nematodes with single-dose anthelmintic treatments. These authors suggested the possibility of a strong and unexpected antagonistic force exerted by nematodes on nontarget parasites and highlighted some of the consequences anthelmintics may have on the parasite community composition, dynamics, and host health.22

In this study, the outcome variables representing “any protozoan” infection and separate protozoan species (i.e., G. lamblia or E. histolytica/E. dispar) were positively, although not significantly, related to children’s history of deworming treatment in the past 6 months. To the best of our knowledge, only two studies have assessed the association between deworming and protozoan infections among human populations.23,24 Studies in the Bolivian lowlands and Bangladesh reported treatment with albendazole or mebendazole increased odds of G. lamblia infection.23,24 Among the Bolivian individuals, G. lamblia infection was associated with significantly lower odds of both hookworm infection (OR = 0.60, P < 0.001) and A. lumbricoides infection (OR = 0.63, P < 0.001).24 Similarly, comparison of Bangladeshi children treated for STHs with controls showed a significant difference in G. lamblia prevalence, with the mebendazole group exhibiting a lower prevalence of A. lumbricoides (6%) but higher prevalence of G. lamblia (38%) than the placebo group (P < 0.005).23 These reports are broadly in agreement with our finding of increased G. lamblia among children with a history of deworming in the past 6 months but differ in the magnitude of effect estimate and level of significance. The difference in size of the effect estimate (ORs) between studies may be due to variation in age, method of parasite detection, differences in the study design, and environmental factors. In addition, the wider confidence interval in our study could be due to our relatively small sample size and fewer cases of protozoan infection.

Our results also show a nonsignificant reduction in the odds of “any STH” infection among children with a history of deworming treatment (i.e., a single dose of 500 mg mebendazole) in the past 6 months. A recent randomized double-blind trial in Tanzania also showed a nonsignificant reduction in Hookworm and T. trichiura infection among children treated with a single dose of 500 mg mebendazole.34 However, other studies have demonstrated a significant reduction in odds of STH infections among children treated with a single dose of 500 mg mebendazole compared with those nontreated.3537 In this study, failure to detect a significant reduction in the odds of “any STH” infections among dewormed children could be due to either the low efficacy of mebendazole as shown in previous studies38,39 or the small number of outcome variables (“any STH”), resulting in insufficient power to detect a statistical significant difference between the two groups.

Our findings should be interpreted in light of several limitations. First, we used a cross-sectional study design because we did not have baseline data of the children’s parasite infection status before receiving deworming treatment. The observational aspect of this study makes it difficult to attribute a causal relationship between mass deworming and the increase in prevalence of cestode and protozoa infections. A more controlled longitudinal design would be crucial in confirming our findings and minimizing the possibility of reverse causation. Second, infectious status among the study subjects was determined using only a single stool sample, which may underestimate the true prevalence of both single and multiple species of parasite infections in this population. However, we used multiple diagnostic approaches (i.e., direct microscopy, Kato–Katz technique, and formol–ether concentration technique) as recommended by the literature to increase the sensitivity parasite detection.40 Third, deworming status in our study was ascertained historically from school records because of logistical issues, which prevented us from ruling out the possibility that children may have received similar or other forms of anthelminthic drugs from other providers. However, our study population is from a low-income country with limited access to standard treatment, making this an unlikely source of bias. Furthermore, we found comparable socioeconomic distribution between dewormed and non-dewormed children, suggesting that selection biases due to social advantage is unlikely to play a major role in this study. Fourth, residual confounding by unmeasured factors is difficult to exclude, although a large number of potential confounders that might have been linked with either deworming or parasite infection were included in our analysis. Fifth, we did not assess the rate of reinfection of STHs because of one-time stool collection following deworming. However, previous pooled analyses of epidemiological studies report a high recovery of STH prevalence to levels close to the initial pretreatment at 6 and 12 months posttreatment follow-up.41

Despite these limitations, our study is the first to examine the possible association between the history of deworming in the past 6 months and prevalence of cestode and protozoa infections using data from resource-limited settings. Although we cannot fully explain the exact reasons for the apparent increase in cestodes and protozoan infection among dewormed children, low efficacy of single-dose mebendazole could be part of the explanation. A previous study indicated that mebendazole administration at doses higher than those commonly used to treat STH infections is sufficiently effective on some protozoa and cestodes.42 Other researchers, however, provided an alternative plausible explanation using ecological perspectives in which deworming treatment may disrupt STH interactions with other pathogens sharing the same gastrointestinal niche, thereby unintentionally increasing a population’s susceptibility to non-STH parasites infections.21 This may be due to a “bottom-up” process (via competition for space/resources) in which deworming treatment against STHs reduces nematodes’ ability to compete for the available resource/space resulting in increased density of nontargeted parasites such as protozoa and cestodes.19 Another explanation for this phenomenon may be due to the changes in behavior or dietary habits of nontargeted parasites following deworming treatment against STHs. Further experiments are needed to elucidate the specific mechanisms.

In conclusion, our data from a low-income setting provide evidence of higher prevalence of “any cestode” infections among children who had a history of deworming treatment in the past 6 months compared with those non-dewormed. We believe this study sheds light on the importance of considering coinfection when administering mass deworming programs that target only STHs. However, the question of whether treatment for STHs increases susceptibility to cestodes and protozoa infections must be confirmed using a more controlled longitudinal design.

Supplemental materials

Acknowledgments:

We gratefully thank the parents/guardians and children at each school, who generously provided their information and thank the school administrators for facilitating stool collection and their commitment during the fieldwork. Colgate University Research Council funded the study. The views expressed are those of the author(s) and not necessarily those of Colgate University or the Department of Medical Laboratory Sciences, College of Health Sciences, Addis Ababa University.

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Author Notes

Address correspondence to Bineyam Taye, Department of Biology, Colgate University, 214 Olin Hall, 13 Oak Dr., Hamilton, NY 13346. E-mail: btaye@colgate.edu

Ethics approval: Departmental Research and Ethics Review Committee (DRERC) of Addis Ababa University College of Health Sciences, Department of Medical Laboratory Sciences, approved the study. We obtained written or fingerprint consent from children’s parents or their legal guardians after informing them of the study procedures. To ensure participant privacy, confidential numerical identifiers were assigned to each child and all participant information remains password-protected in electronic files. The children were also informed about their ability to withdraw from this study at any time without jeopardizing their right to receive any services at their school. Children who were found to have intestinal parasites were treated with antiparasitic drugs in local health centers.

Authors’ addresses: Nader Mohamed, Anna Muse, and Bineyam Taye, Department of Biology, Colgate University, Hamilton, NY, E-mails: nmohamed1@colgate.edu, amuse@colgate.edu, and btaye@colgate.edu. Moges Wordofa, Dessie Abera, Abiyot Mesfin, Mistire Wolde, Kassu Desta, and Aster Tsegaye, Department of Medical Laboratory Sciences, College of Health Sciences, Addis Ababa University, Addis Ababa, Ethiopia, E-mails: heranmakmow@gmail.com, dessabera@gmail.com, abiyot2012@gmail.com, mistire08@gmail.com, kassudesta2020@gmail.com, and tsegayeaster@yahoo.com.

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