Trends in prevalence of soil-transmitted helminth and major intestinal protozoan infections among school-aged children in Nepal

Authors


Abstract

Objectives

To assess the trends in prevalence of soil-transmitted helminths (STHs), Entamoeba histolytica and Giardia lamblia among school-aged children in Nepal between 1990 and 2015.

Methods

Systematic literature search in PubMed, MEDLINE, EMBASE, Google Scholar and local peer-reviewed journals for papers published between 1990 and December 2015. We conducted metaregression and meta-analyses to pool studies where applicable.

Results

Thirty-nine studies that examined a total of 14 729 stool specimens were included in the meta-analyses. The metaregression of prevalence of hookworms, roundworm, and whipworm showed a significantly decreasing trend over time. In or after 2004, the pooled prevalence of hookworm infections was 1.53% (95% CI, 0.73–2.59), of roundworm 4.31% (95% CI, 2.52–6.53) and of whipworm 2.89% (95% CI, 1.33–4.97) vs. 16.54% (95% CI, 7.64–27.97) for hookworm, 25.20% (95% CI, 13.59–38.97) for roundworm and 11.54% (95% CI 4.25–21.76) for whipworm in 1993–2003. E. histolytica and G. lamblia had stable prevalence since early 1990s, with a pooled prevalences of 4.12% (95% CI, 2.73–5.77) and 9.40% (95% CI, 7.15–11.92), respectively. The prevalence of G. lamblia was significantly higher in urban areas.

Conclusions

We observed a sharp decrease in prevalence of STHs among school-aged children in Nepal in the past decade with prevalences dropping below 5% for STHs with no variation in prevalence in rural and urban areas. However, the prevalence of E. histolytica and G. lamblia remained stable over time. These results suggest that school-based deworming programmes rolled out during the study period had an observable impact on prevalence of STHs.

Abstract

Objectifs

Evaluer les tendances de la prévalence des géàhelminthiases, Entamoeba histolytica et Giardia lamblia chez les enfants d’âge scolaire au Népal entre 1990 et 2015.

Méthodes

Recherche systématique de la littérature dans PubMed, MEDLINE, EMBASE, Google Scholar et des revues locales pour les articles publiés entre 1990 et décembre 2015. Nous avons effectué une méta-régression et une méta-analyse d’études poolées, le cas échéant.

Résultats

39 études portant sur un total de 14.729 échantillons de selles ont été incluses dans les méta-analyses. La méta-régression de la prévalence des ankylostomes, ascaris et trichures a montré une tendance à la baisse de manière significative au fil du temps. En 2004 ou après, la prévalence poolée des infections d'ankylostome était de 1,53% (IC95%: 0,73 à 2,59), des ascaris 4,31% (IC95%: 2,52 à 6,53) et des trichures 2,89% (IC95%: 1,33 à 4,97), contre 16,54% (IC95%: 7,64 à 27,97) pour l'ankylostome, 25,20% (IC95%: 13,59 à 38,97) pour l'ascaris et 11,54% (IC95%: 4,25 à 21,76) pour les trichures en 1993-2003. E. histolytica et G. lamblia ont une prévalence stable depuis le début des années 1990, avec des prévalences poolées de 4,12% (IC95%: 2,73 à 5,77) et 9,40% (IC95%: 7,15 à 11,92), respectivement. La prévalence de G. lamblia était significativement plus élevée dans les zones urbaines.

Conclusions

Nous avons observé une forte diminution de la prévalence des géohelminthiases chez les enfants d’âge scolaire au Népal dans la dernière décennie avec des prévalences chutant en dessous de 5% pour les géohelminthiases sans variation de la prévalence entre les zones rurales et urbaines. Cependant, la prévalence de E. histolytica et G. lamblia est restée stable au fil du temps. Ces résultats suggèrent que les programmes de déparasitage en milieu scolaire, déployés au cours de la période d’étude ont eu un impact observable sur la prévalence des géohelminthiases.

Abstract

Objetivos

Evaluar las tendencias en prevalencia de helmintos transmitidos por el suelo (HsTS), Entamoeba histolytica y Giardia lamblia entre niños en edad escolar en Nepal, entre 1990 y 2015.

Métodos

Revisión sistemática de la literatura en PubMed, MEDLINE, EMBASE, Google Scholar y revistas con revisión por pares, de artículos publicados entre 1990 y Diciembre del 2015. En donde era posible, realizamos meta-regresiones y meta-análisis de estudios agrupados,.

Resultados

En el meta-análisis incluimos 39 estudios que analizaban un total de 14,729 muestras coprológicas. En la meta-regresión, la prevalencia de anquilostomas, lombrices intestinales y tricocéfalos mostraba una tendencia significativa de descenso a lo largo del tiempo. En el 2004 o después de este año, la prevalencia conjunta de infecciones por anquilostomas era del 1.53% (IC 95%, 0.73-2.59), de lombrices intestinales del 4.31% (IC 95%, 2.52-6.53) y de tricocéfalos del 2.89% (IC 95%, 1.33-4.97), versus 16.54% (IC 95%, 7.64-27.97) para anquilostomas, 25.20% (IC 95%, 13.59-38.97) para lombrices intestinales y del 11.54% (IC 95% 4.25-21.76) para tricocéfalos entre 1993-2003. E. histolytica y G. lamblia tenían una prevalencia estable desde principios de la década de 1990, con una prevalencia conjunta del 4.12% (IC 95%, 2.73-5.77) y del 9.40% (IC 95%, 7.15-11.92), respectivamente. La prevalencia de G. lamblia era significativamente mayor en áreas urbanas.

Conclusiones

Hemos observado un descenso importante en la prevalencia de HsTS entre niños en edad escolar del Nepal durante la última década, con un descenso en las prevalencias por debajo del 5% para HsTS, sin variación en las prevalencias de áreas rurales y urbanas. Sin embargo, la prevalencia de E. histolytica y G. lamblia se mantuvo estable a lo largo del tiempo. Estos resultados sugieren que el despliegue de programas de desparasitación en las escuelas durante el periodo de estudio, tuvo un impacto observable sobre la prevalencia de HsTS.

Introduction

Intestinal parasitic infection is an important public health issue particularly in resource poor countries. Soil-transmitted helminths (STHs) represent one of the highest burdens of neglected tropical diseases [1, 2]. There are four important species of STHs that infect humans: Ascaris lumbricoides (roundworm), Trichuris trichiura (whipworm) and Ancyclostoma duodenale and Necator americanus (hookworms). Global estimates on prevalence of STHs report that ascariasis (roundworm infection) is the most common (819 million), followed by trichuriasis (whipworm infection) (464 million) and hookworm infection (438 million) [3].

Intestinal protozoan infections, particularly Entamoeba histolytica (E. histolytica) and Giardia lamblia (G. lamblia), also cause significant morbidity and mortality in developing countries where water quality, waste disposal, sanitation and hygiene conditions are poor. In 2010, roughly 179 million people were infected by G. lamblia [4]. Similarly, amoebic dysentery or extra-intestinal disease caused by E. histolytica affects roughly 50 million people each year, with 100000 deaths annually [5].

Heavy infections with STHs may cause malnutrition and anaemia, thus adversely affecting the mental and physical development of children [6, 7]. Effective strategies for prevention and control of STH infections are available; one such strategy is mass administration of anthelminthic drugs in schoolchildren through the school system [8]. Endemic countries with a high prevalence of STHs are urged to control morbidity through periodic administration of anthelminthic drugs [9]. In Nepal, there have been various programmes that include deworming of preschool and schoolchildren since the late 1990s. In many areas of the country, this is nested with other interventions such as midday meals for schoolchildren and vitamin A supplementation for preschool children through various international non-governmental organisations in collaboration with the Government of Nepal [10-14]. The Government of Nepal began their deworming programme in the fiscal year of 2006/2007 in public schools in 24 of 75 districts by distributing deworming tablets to school children (grade 1–5) biannually. The initial programme had a high acceptability rate, with over 90% coverage in some programme districts [15]. The programme was expanded to 43 districts in 2008/2009 [15]. Currently, the programme is nationwide and targeted to schoolchildren in both public and private schools from grade 1–10; however, precise data on current coverage and effectiveness of the programme are scarce [16]. Deworming of preschool children coupled with vitamin A supplementation has had almost complete coverage in the country since 2004 [17].

Understanding the trends in prevalence of STHs and other important intestinal parasites can be useful to assess the evolving scenario of the burden of disease and can provide evidence to better target prevention and control programmes. In the last two decades, there have been several efforts to reduce the burden of intestinal parasites, particularly in children. During the same time, there have been several prevalence studies on intestinal parasites over time; however, there is no sufficiently long-term surveillance study on either of these parasites. Thus, we conducted a systematic review and meta-analysis with an aim to understand the trends in prevalence of STHs, E. histolytica and G. lamblia in schoolchildren according to rurality, and season of sample collection in Nepal from 1990–2015 using available evidence.

Methods

Setting

Nepal is one of the world's least developed countries. It is landlocked, bordering China in the north and India in the east, west and south. The average annual precipitation rate is 1500 mm, with heavy rainfall during the monsoon season [18]. Geographically, the country is divided into three ecological regions: Himalayan region, Mid hill region and Terai (plain) region, which lie between 8848 and 60 metres above sea level and vary in temperature, precipitation, vegetation and snowfall. In 2011, the population of Nepal was 26.6 million with an estimated GDP of 642 US$ per capita. Roughly, 25% of the population live in poverty. Approximately 7.5 million children are enrolled in primary, secondary and higher secondary level of school [19]. The national sanitation coverage expressed in terms of access to a toilet increased from 6% in 1990 to 62% in 2011; however, there is a geographical variation in these coverages [20]. According to the 2010/11 Nepal Living Standard Survey (NLSS), 56% of families have toilets or latrines in their own house vs. 22% in 1995/1996. The Nepal Demographic and Health Survey 2011 (DHS) also reported that 54.4% of households had access to improved toilet/latrine facilities [21]. About 65% of schools also had functional toilets by 2010/2011 [22]. Current sanitation standards in the country are measured in terms of open-defecation-free districts (ODFs). As of the end of 2015, 27 districts (three Himalayan, 20 Mid hill and four Terai) of 75 total districts in country are ODFs [23].

Eligibility criteria

This systematic review included all identified intestinal parasitic infection surveys among school-aged children conducted in Nepal between 1990 and 2015 that reported the prevalence of each of STHs, E. histolytica and G. lamblia. These studies included children attending school regardless of any symptoms that may be related to intestinal parasite infection.

Information sources and literature search

We searched for articles in PubMed, MEDLINE, EMBASE and Google Scholar published/reported from 1990 to December 2015. An electronic search was conducted using the terms ‘parasites’, ‘intestinal’, ‘Nepal’. A manual search was conducted on all relevant references listed within articles identified after an initial screen. In addition, several researchers who had previously conducted surveys on intestinal parasites were contacted to identify more publications. According to suggestions from local experts, one author (L.A.) visited local libraries to identify publications in local peer-reviewed scientific journals whose content may not be available online. A detailed search strategy is included in Appendix I.

Study selection

The study selection process is shown in Figure 1. Studies were excluded if the study sample was an adult population, if the survey was conducted in hospital or healthcare facilities where children visited with symptomatic intestinal illness or if the study was conducted before 1990. To be included in the review, the study had to fulfil minimum criteria of information on age of participants, location of study area, date of sample collection and laboratory method of stool examination and had to be published or presented after peer review in a scientific journal.

Figure 1.

Flow chart showing study selection process.

Risk of bias in individual studies and across studies

A formal risk of bias was not assessed in individual studies; however, a systematic risk of bias is less likely as most of the studies were description of prevalence according to basic demographic variables.

Statistical methods for assessing publication/reporting bias in a meta-analysis of prevalence surveys are not well established. To assess such bias in a meta-analysis of randomised controlled trials, visual analysis by funnel plot and statistical methods are used to examine whether small studies with negative or null findings are less likely to be published. The consequence of finding extreme results in prevalence studies on their publication and reporting has not been discussed adequately in the literature. We did not conduct any conventional visual or statistical analysis of the studies included in this meta-analysis; however, we present a scatter plot of log odds of hookworm infection vs. sample size of the study which can inform the reader about the observed relationship with publication of such studies [24]. The plot of hookworm infection alone was chosen due to the relatively great importance and concern over hookworm infection vs. other intestinal parasites in the country.

Statistical analyses

We performed a metaregression of prevalence estimates over time using a sample size-weighted generalised linear models. Firstly, the proportion (p) (proportion of participants with intestinal STHs, E. histolytica and G. lamblia) values were transformed to ‘logit’ (log of the odds). Zero events of any intestinal parasite were replaced by 0.5 for continuity correction so that the studies could be included in the analyses [25]. A linear regression of ‘logit’-transformed values over time (year) was performed, giving the following relationship between the proportion ‘p’ and time’t’:

display math

The analytical weight was proportional to sample size, and we expressed the result of regression as an odds ratio. The odds ratio from our model can be interpreted as the relative change in odds (i.e. odds of infection) per year.

When the relative change in odds of infection per year was not significant, we calculated the overall pooled prevalence. Preliminary metaregression showed that prevalence of infection varied over time for STHs; thus, we pooled the prevalence of STH infection in blocks in tandem with the year when the campaign for deworming of preschool children had full coverage in the country (pre 2004 = 1990–2003, 2004 and after= 2004–2015). We pooled the prevalence using the ‘metaprop’ command in STATA 12.1 using the Freeman–Tukey double arcsine transformation and random effect model (StataCorp, College Station, TX).

Results

Study characteristics

Figure 1 shows the flowchart of study selection. Thirty-nine studies were included in the analyses [26-64]. The distribution of study variables in all 39 studies is presented in Appendix II. Altogether, 14 729 stool specimens were examined in the studies. All studies were school-based prevalence surveys, except one which included children of school-going age but recruited from a community [52]. Figure 2 shows a map of Nepal with the location of study sites mentioned in the studies included in our analyses (Figure 2). Fourteen studies used direct wet mount only, 21 studies used direct wet mount and formal ether concentration methods, and three studies used the Kato-Katz method for microscopy of the stool specimens. Figure 3 shows the scatter plot of study size plotted against log odds of hookworm infection. The graph shows no visual evidence of small studies, with lower prevalence estimates being less published.

Figure 2.

Map of Nepal showing study places (denoted by black circles).

Figure 3.

Scatter plot of log odds of hookworm infection against sample size.

Trends in prevalence of STHs

The metaregression of hookworm prevalence over time showed a significantly decreasing trend each year (odds ratio (OR) = 0.90, 95% CI 0.84–0.96) (Figure 4). The pooled prevalence of hookworms was 16.54% (95% CI, 7.64–27.97) between 1990 and 2003 and 1.53% (95% CI, 0.73–2.59) between 2004 and 2015 (Figure 5). Similarly, the prevalence of roundworm decreased significantly each year (OR 0.86, 95 CI 0.81–0.92) (Figure 4). The pooled prevalence of roundworm was 25.20% (95% CI, 13.59–38.97) between 1990 and 2003 and 4.31% (95% CI, 2.52–6.53) between 2004 and 2015 (Figure 6). Whipworm prevalence also dropped over time (OR 0.89, 0.81–0.97) (Figure 4). The pooled prevalence of whipworm was 11.54% (95% CI, 4.25–21.76) between 1990 and 2003 and 2.89% (95% CI, 1.33–4.97) between 2004 and 2015 (Figure 7).

Figure 4.

Trends in prevalence of STHs (a, b, c), E. histolytica (d) and G. lamblia (e) infections (1990–2015) (Note: Prevalence is expressed as proportions. Each grey circle indicates an individual study, and area of circle size is proportional to the sample size. The sizes of circles are comparable within individual graphs only. The trend line (dashed) is the predicted prevalence from the regression models. The prevalence scales are unique to each figure).

Figure 5.

Forest plot showing pooled prevalence of hookworm infection.

Figure 6.

Forest plot showing pooled prevalence of roundworm infection.

Figure 7.

Forest plot showing pooled prevalence of whipworm infection.

Trends in prevalence of E. histolytica and G. lamblia

The metaregression of E. histolytica and G. lamblia prevalence over time showed a stable trend (OR= 1.03, 95% CI 0.94–1.13 and OR=0.97, 95 CI 0.92–1.03, respectively). The pooled prevalence of E. histolytica (Figure 8) and G. lamblia (Figure 9) was 4.12% (95% CI, 2.73–5.77) and 9.40% (95% CI, 7.15–11.92), respectively.

Figure 8.

Forest plot showing pooled prevalence of Entamoeba histolytica infection (1990–2015).

Figure 9.

Forest plot showing pooled prevalence of Giardia lamblia infection (1990–2015).

Prevalence of STHs, E. histolytica and G. lamblia by rurality and season of sample collection

Table 1 shows the pooled prevalence of STHs (including only those studies conducted in or after 2004), E. histolytica and G. lamblia by rural vs. urban area of the study and rainy vs. non-rainy season of faecal specimen collection. In the metaregression analysis adjusted for time and season, only G. lamblia prevalence was significantly higher in urban than rural areas (OR 4.31, 95% CI 1.47–12.61, P = 0.008).

Table 1. Pooled prevalence of STHs, E. histolytica and G. lamblia infection by rurality and season
VariableHookworms, prevalence (95% CI)aRoundworm, prevalence (95% CI)aWhipworm, prevalence (95% CI)aEntamoeba histolytica, prevalence (95% CI)Giardia lamblia, prevalence (95% CI)
  1. a

    Only studies conducted after 2003 are included in these analyses; CI, confidence interval.

Rurality
Urban1.14 (0.38–2.21)4.24 (2.34–6.64)3.09 (0.55–7.34)7.08 (3.69–11.41)13.89 (8.00–21.04)
Rural2.88 (0.69–6.34)3.90 (0.92–8.66)2.99 (0.31–7.91)2.55 (0.92–4.89)6.02(3.89–8.58)
Season
Rainy0.95 (0.13–2.31)3.08 (1.30–5.52)1.75 (0.05–5.22)6.82 (3.40–11.28)12.57 (7.17–19.19)
Non-rainy2.03 (0.58–4.21)4.00 (1.42–7.71)2.93 (1.11–5.51)2.97 (1.30–5.24)7.35 (4.54–10.74)

Discussion

We observed a significant decrease in the prevalence of hookworms, roundworm and whipworm but a stable prevalence of E. histolytica and G. lamblia in Nepal over the study time period. G. lamblia infection was significantly more common in urban than rural areas. Prevalence of each type of STH was <5.0% in studies conducted on or after 2004.

Recent estimates have reported global reductions in the prevalence of STHs. Pullan et al. reported a substantial reduction in the prevalence of STHs across all endemic regions between 2010 (25.7%) and 1990 (38.6%), with the greatest reductions in countries with improving economies such as China and the Democratic People's Republic of Korea, but only modest reductions in other Asian countries [3, 65]. In our study, we observed a drastic reduction in overall prevalence of STHs in or after 2004, which coincides with the country-wide coverage of deworming in preschool children and an increase in the number of schools covered by nutrition and deworming programmes. The reason behind the substantial decrease in prevalence of STHs in the country during the study period may be due to the synergistic effect of overall improvements in sanitation, hygiene, living standards, school-based nutrition, deworming programmes and other public health achievements over the last two decades [22]. However, a decreasing prevalence of STHs but stable prevalence of intestinal protozoa such as G. lamblia and E. histolytica as observed in our study suggests that targeted interventions in schools such as deworming might be having a noticeable impact on the prevalence of STHs. Although we observed lower estimates for prevalence of STHs in school-aged children, a study conducted in 2008 among adults in five different social and geographical regions suggests that there are still communities in the country which have high prevalences of hookworm (12.8%), roundworm (39.4%) and whipworm (26.6%) infection, attributed to poor hygiene [66].

For STHs, we pooled the rural vs. urban prevalence including only the studies conducted on or after 2004. The reason for this was that there was a significantly large difference in prevalence in studies conducted before 2004 and on or after 2004, but there were not sufficient a number of studies before 2004 to pool in further categories. We observed that the prevalence of each type of STH was similar in rural and urban areas in studies conducted in or after 2004. Similar surveys in school-aged children in South Asia and Africa have reported higher prevalences of STH infections from study sites in rural areas [67-71]. However, a few studies found similar or higher prevalences of STHs in urban settings [72, 73]. According to local evidence, the prevalence of STHs in adults is more importantly determined by the general hygiene behaviour and sanitation in the community [66]. Similarly, the prevalence of STHs was similar during rainy and non-rainy seasons. A higher prevalence of intestinal helminths during and towards the end of the monsoon was reported in some studies [74, 75].

For E. histolytica and G. lamblia, we pooled the rural vs. urban prevalence, including all studies conducted between 1990 and 2015. The prevalence was higher in urban than rural areas for both, but the difference reached statistical significance only for G. lamblia. The higher prevalence of intestinal protozoan infections in urban areas may be due to poor water quality as a result of faecal contamination. In urban areas of Kathmandu, Lalitpur and Bhaktapur – where roughly one-third of the studies included in this analysis were conducted – residents only get an intermittent supply of piped water, often with heavy contamination in rainy seasons, thus people rely on shallow groundwater for drinking and cooking purposes. Such water sources (up to 90%) are contaminated with cysts of Giardia, Cryptosporidium and other indicators of faecal contamination according to several reports [76, 77]. Similarly, we observed a considerably higher but statistically not significant difference in prevalence of E. histolytica and G. lamblia in the rainy season vs. the non-rainy season. This may be due to more frequent water contamination by faecal materials during the monsoon [76].

It appears that Nepal has made significant progress in reducing the prevalence of STHs in schoolchildren in the last decade. This is an important achievement that will help to improve their physical and mental development [78-80]. However, all of the studies included in this analysis were conducted before the 7.8 magnitude scale earthquake in 2015 that killed thousands and displaced tens of thousands of people in the central and western region of Nepal. Now, Nepal faces further challenges in preventing infectious diseases, including intestinal parasitic infections, after the earthquake [81]. Studies from Haiti and Turkey reported a high prevalence of parasitic infections, particularly protozoan parasites among children, in the years after massive earthquakes [82].

Our study has some limitations. Several schools in the country had deworming programmes through government and various non-governmental organisations (NGOs) prior to the surveys. We do not know which survey sites had such programmes, and which did not. Thus, we could not stratify the results according to prior deworming status. Although we retrieved several articles, only few studies were conducted and reported from the mid-western and far-western parts of the country, which are among the least developed regions, with poorer access to toilets and sanitary systems than in other regions of the country [83]. Similarly, most of the studies were conducted in the Mid hill and Terai region, but 93% of Nepalese population also live in these regions. The majority of studies included in our analyses examined the stool specimens for many other parasites including the STHs; we do not know the diagnostic performance of such an approach compared to studies that examine solely for STHs, which may affect the detection rate and prevalence estimates of STHs. Lastly, the surveys included in our review involved basic microscopic techniques for the diagnosis of parasites which may be less sensitive than enhanced microscopic and molecular methods; however, this is not likely to affect the major results in trends of prevalence as the methods used were similar throughout the study period.

In conclusion, we observed a sharp decrease in prevalence of STHs among school-aged children in Nepal in last decade with prevalence dropping below 5% for each of STHs with no variation in prevalence in rural and urban areas, and rainy and non-rainy season of the year. However, the prevalence of E. histolytica and G. lamblia remained stable over the time, with higher prevalence of G. lamblia in urban areas of the country. These results suggest that school-based deworming programmes rolled out during the study period had an observable impact on prevalence of STHs in school-aged children.

Appendix I

Literature search

We performed an electronic search in PubMed, MEDLINE, EMBASE and Google Scholar limited to only English languages publications related to human studies published between 1990 and 2015. ‘Parasites’ and ‘Nepal’ are MeSH terms, whereas ‘Intestinal’ was used as keyword.

Search in PubMed

The search terms were ‘parasites AND nepal’. We manually scanned the abstracts of all the articles identified through search terms. We also checked the PubMed option of ‘related articles’ to see whether any relevant information was contained in such articles, and we manually checked the reference list of relevant articles identified through PubMed.

Search in MEDLINE (OVID)

1: ‘parasites’.mp.

2: nepal.mp.

3: and/1–2.

4: ‘intestinal’.mp.

5: 3 and 4.

Search in EMBASE

1: intestin*.mp.

2: nepal.mp. or Nepal/.

3: 1 and 2.

Search in Google Scholar

All documents with the following combination of words and phrases (all), but ‘in the title of the articles’ were searched.

Search 1: ‘parasites’, ‘nepal’.

Search 2: ‘parasitosis’, ‘nepal’.

Relevant titles were identified first before looking into the abstracts.

Appendix II: Table showing distribution of study variables

StudyStudy placeYearSeasonStudy sizeRuralityEHGLHWALTTLaboratory method
  1. NA, not available; EH, Entamoeba histolytica; GL, Giardia lamblia; HW, Hookworms; AL, Ascaris lumbricoides; TT, Trichuris trichiura.

Curtale et al., 1994Sarlahi1991Rainy592RuralNANA22301NAKato-katz technique
Sherchand et al., 1998Mechi1996NA219RuralNANA2532NADirect wet mount
Montressor and Celletti, 2000Parsa, Dadeldhura, Doti1996Rainy711RuralNANA460156137Kato-katz technique
Sherchand et al., 1997South-eastern region1996NA604RuralNANA70NANADirect wet mount
Yong et al., 2000Chitwan1999Non-rainy300Rural11413959Formal ether concentration
Ishiyama et al., 2001Kathmandu1999NA221Both743255577Formal ether concentration
Rai et al., 2004Dhading1999Non-rainy325Rural0123515612Direct wet mount
Rijal et al., 2001Chitwan2000NA182Rural13332751Direct wet mount
Montressor and Celletti, 2000Parsa, Dadeldhura, Doti2000Rainy426RuralNANA14111417Kato-katz technique
Rai et al., 2002Dhading2000NA423Rural0155519917Direct wet mount
Shrestha., 2001Lalitpur2001NA515BothNANANA374166Formal ether concentration
Mukhopadhya et al., 2008Western Nepal2002Both220BothNANA101910Formal ether concentration
Sharma et al., 2004Kathmandu2003NA533Both383614987218Formal ether concentration
Chandrasekhar et al., 2005Kaski2004Non-rainy2091Both3627784527Direct wet mount
Malla et al., 2004Sarlahi2004Both225Rural1421103219Direct wet mount
Shrestha et al., 2007Kathmandu2006Both188UrbanNANA23766Formal ether concentration
Adhikari et al., 2007Kathmandu2006Rainy309UrbanNANA132758Formal ether concentration
Gyawali et al., 2009Dharan2007NA182Urban1021360Formal ether concentration
Magar et al., 2011Kathmandu2008Rainy279Urban304861012Formal ether concentration
Shakya et al., 2012Birgunj2008Rainy165Rural95170Direct wet mount
Shrestha et al., 2009Bhaktapur2008Both303Urban11556198Formal ether concentration
Sherchand et al., 2010Kathmandu2008Non-rainy187Urban1639021Formal ether concentration
Bhandari et al., 2011Kavrepalanchowk2008Non-rainy360Rural021435668Direct wet mount
Vitrakoti et al., 2010Kaski2008Non-rainy366Both174251510Formal ether concentration
Tiwari et al., 2013Dadeldhura2010Non-rainy530Rural01348311Direct wet mount
Regmi et al., 2014Bara2010Rainy296Urban25271067Formal ether concentration
Khanal et al., 2011Kathmandu2011Non-rainy142UrbanNANA258Formal ether concentration
Khadka et al., 2013Kaski2011Non-rainy100Urban45141Formal ether concentration
Tandukar et al., 2013Lalitpur2011Rainy1392Both471033105Formal ether concentration
Maharjan et al., 2013Kathmandu2011Rainy101Urban3556090Direct wet mount
Mukhia et al., 2012Sindhuli2011Rainy342Rural714NANANAFormal ether concentration
Shrestha et al., 2012Baglung2011Non-rainy260Rural24157613Formal ether concentration
Bhattachan et al., 2015Chitwan2012Non-rainy296Rural812102Formal ether concentration
Sah et al., 2013Itahari2012Non-rainy200Urban1621643Direct wet mount
Jaiswal et al., 2014Kaski2012Non-rainy163Rural112115Formal ether concentration
Pradhan et al., 2013Kathmandu2012Rainy194Rural927111Direct wet mount
Shrestha and Maharjan, 2013Bhaktapur2013Non-rainy495BothNANA811230Direct wet mount
Pandey et al., 2015Kathmandu2014Both300Urban54030Formal ether concentration
Bhandari et al., 2015Kathmandu2014Rainy507Urban8530101Formal ether concentration

Ancillary