Article:Soil-transmitted helminth reinfection after drug treatment: a systematic review and meta-analysis (3348161)

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This page is the ScienceSource HTML version of the scholarly article described at Its title is Soil-transmitted helminth reinfection after drug treatment: a systematic review and meta-analysis and the publication date was 2012-05-08. The initial author is Tie-Wu Jia.

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Journal Information

Title: PLoS Neglected Tropical Diseases

Soil-Transmitted Helminth Reinfection after Drug Treatment: A Systematic Review and Meta-Analysis

Alternative Title: Soil-Transmitted Helminth Reinfection

  • Tie-Wu Jia
  • Sara Melville
  • Jürg Utzinger
  • Charles H. King
  • Xiao-Nong Zhou

[1]Key Laboratory on Biology of Parasites and Vectors, MOH, WHO Collaborating Center on Malaria, Schistosomiasis and Filariasis, National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Shanghai, People's Republic of China

[2]Hughes Hall College, Cambridge University, Cambridge, United Kingdom

[3]Department of Epidemiology and Public Health, Swiss Tropical and Public Health Institute, Basel, Switzerland

[4]University of Basel, Basel, Switzerland

[5]Center for Global Health and Diseases, Case Western Reserve University School of Medicine, Cleveland, Ohio, United States of America

  • Philip J. Cooper (Editor)

Universidad San Francisco de Quito, Ecuador

Publication date (collection): 5/2012

Publication date (epub): 5/2012



Soil-transmitted helminth (STH) infections (i.e., Ascaris lumbricoides, hookworm, and Trichuris trichiura) affect more than a billion people. Preventive chemotherapy (i.e., repeated administration of anthelmintic drugs to at-risk populations), is the mainstay of control. This strategy, however, does not prevent reinfection. We performed a systematic review and meta-analysis to assess patterns and dynamics of STH reinfection after drug treatment.


We systematically searched PubMed, ISI Web of Science, EMBASE, Cochrane Database of Systematic Reviews, China National Knowledge Infrastructure, WanFang Database, Chinese Scientific Journal Database, and Google Scholar. Information on study year, country, sample size, age of participants, diagnostic method, drug administration strategy, prevalence and intensity of infection pre- and posttreatment, cure and egg reduction rate, evaluation period posttreatment, and adherence was extracted. Pooled risk ratios from random-effects models were used to assess the risk of STH reinfection after treatment. Our protocol is available on PROSPERO, registration number: CRD42011001678.

Principal Findings

From 154 studies identified, 51 were included and 24 provided STH infection rates pre- and posttreatment, whereas 42 reported determinants of predisposition to reinfection. At 3, 6, and 12 months posttreatment, A. lumbricoides prevalence reached 26% (95% confidence interval (CI): 16–43%), 68% (95% CI: 60–76%) and 94% (95% CI: 88–100%) of pretreatment levels, respectively. For T. trichiura, respective reinfection prevalence were 36% (95% CI: 28–47%), 67% (95% CI: 42–100%), and 82% (95% CI: 62–100%), and for hookworm, 30% (95% CI: 26–34%), 55% (95% CI: 34–87%), and 57% (95% CI: 49–67%). Prevalence and intensity of reinfection were positively correlated with pretreatment infection status.


STH reinfections occur rapidly after treatment, particularly for A. lumbricoides and T. trichiura. Hence, there is a need for frequent anthelmintic drug administrations to maximize the benefit of preventive chemotherapy. Integrated control approaches emphasizing health education and environmental sanitation are needed to interrupt transmission of STH.


Author Summary

Infections with soil-transmitted helminths (the roundworm Ascaris lumbricoides, the whipworm Trichuris trichiura, and hookworm) affect over 1 billion people, particularly rural communities in the developing world. The global strategy to control soil-transmitted helminth infections is ‘preventive chemotherapy’, which means large-scale administration of anthelmintic drugs to at-risk populations. However, because reinfection occurs after treatment, ‘preventive chemotherapy’ must be repeated regularly. Our systematic review and meta-analysis found that at 3, 6, and 12 months after treatment, A. lumbricoides prevalence reached 26% (95% confidence interval (CI): 16–43%), 68% (95% CI: 60–76%) and 94% (95% CI: 88–100%) of pretreatment levels, respectively. For T. trichiura, respective reinfection prevalence at these time points were 36% (95% CI: 28–47%), 67% (95% CI: 42–100%), and 82% (95% CI: 62–100%); and for hookworm, 30% (95% CI: 26–34%), 55% (95% CI: 34–87%), and 57% (95% CI: 49–67%). Prevalence and intensity of reinfection were positively correlated with pretreatment infection status. Our results suggest a frequent anthelmintic drug administration to maximize the benefit of preventive chemotherapy. Moreover, an integrated control strategy, consisting of preventive chemotherapy combined with health education and environmental sanitation is needed to interrupt transmission of soil-transmitted helminths.



Infections with soil-transmitted helminths (STHs) affect more than 1 billion people, particularly the rural poor of the developing world [1], [2]. The four most common STHs are the roundworm (Ascaris lumbricoides), the whipworm (Trichuris trichiura), and two hookworm species (Ancylostoma duodenale and Necator americanus) [2]. The greatest number of STH infections occur in Central and South America, People's Republic of China (P.R. China), Southeast Asia, and sub-Saharan Africa [2], [3]. Warm climates and adequate moisture are essential for the hatching or embryonation of STH eggs in the environment or development of larvae.

Important contextual determinants for human infection are poverty, lack of sanitation, and inadequate hygiene (e.g., absence of hand washing with soap after defecation and before eating, and walking barefoot) [4][6]. In such social-ecological systems, multiple species STH infections are common [7].

Transmission of STHs occurs via contact with contaminated soil (hookworm) or consumption of egg-contaminated foods (A. lumbricoides and T. trichiura) [4]. An important epidemiological feature is their highly aggregated distribution: the majority of patients harbor low intensity infections, while only few individuals harbor very heavy infections [8]. People infected with STHs may suffer from anemia, growth stunting, diminished physical fitness, and impaired cognitive development [7], representing a persistent drain on social and economic development of low-income countries [9], [10]. The current global strategy to control STH infections is preventive chemotherapy, that is the repeated large-scale administration of anthelmintic drugs to at-risk populations, most importantly school-aged children [11], [12]. A shortcoming of this strategy is failure to prevent reinfection after effective deworming [6], [7], [13], [14]. Hence, identifying factors that determine reinfection risk is crucial to improving the effectiveness of this strategy [15].

To foster the design of more effective integrated control strategies, the objectives of this systematic review and meta-analysis were to assess available evidence on global patterns of STH reinfection after drug treatment, and to identify, through pooled risk estimates, the frequency and leading determinants of STH reinfection.


This systematic review was developed in line with the PRISMA guidelines (see Checklist S1) [16]. A protocol was prospectively registered in PROSPERO [17], registration number: CRD42011001678; available from

Selection Criteria

We aimed to include all published studies in English or Chinese in which reinfection with STH was measured, for the period January 1, 1900 to December 31, 2010. Both observational studies and trials were eligible for inclusion. We excluded the following studies: (i) data without rate of infection after preventive chemotherapy; (ii) where time of follow-up was less than 2 months or more than 3 years; (iii) hospital-based or case studies in which the representativeness of the sample for the general population was unknown; and (iv) duplicate publication or extended analysis of previously published studies (see Figure 1 for selection flow of included studies). Additional exclusion criteria were: low adherence (loss rate of subjects at follow-up >30%), low initial prevalence (<10%), and poor cure rate (CR; i.e., <80% for A. lumbricoides, <20% for T. trichiura, or <20% for hookworm) unless cure was boosted by repeated treatment [18]. In our review, CR is defined as the percentage of STH-positive individuals who became egg-negative posttreatment, as assessed within 7 to 60 days after treatment [18], [19]. Adherence was defined as the percentage of individuals who were followed-up, and hence included in a per-protocol analysis.

10.1371/journal.pntd.0001621.g001Figure 1

Flowchart visualizing the procedure for identifying relevant publications.

aThe original article or full text could not be obtained. b14 parasitology: 9 dynamics and structure of population, 4 immunology, 1 quantitative measure method of reinfection. cExtended analysis of previously published study. d2 on enteroparasite (intestinal parasites including Enterobius vermicularis, Hymenolepis nana, Giardia intestinalis, Entamoeba coli, Entamoeba histolytica, and others), 1 on bancroftian filariasis.

Search Strategy

We identified published studies using the National Library of Medicine's PubMed (1900 to December 2010), ISI Web of Science (1900 to December 2010), EMBASE (1947 to December 2010), China National Knowledge Infrastructure (CNKI; 1979 to December 2010), WanFang Database (1980 to December 2010), and Chinese Scientific Journal Database (VIP; 1989 to December 2010). We employed the following terms (phoneticism (Pinyin) of Chinese keywords given in parenthesis): helminth (ruchong), or nematode (xianchong), or Ascaris (huichong), or hookworm (gouchong), or whipworm, or Trichuris (bianchong) and reinfection (zaiganran), or chemotherapy (hualiao), or albendazole (abendazuo or bingliumizuo), or mebendazole (jiabendazuo), or levamisole (zuoxuanmizuo), or pyrantel pamoate (saimiding) and longitudinal study (zongxiang), or cohort study (duilie), or trial (shiyan).

Automated database searches covered the period from when earliest electronic records were available (e.g., 1900 in the case of ISI Web of Science) to the end of December 2010. Additional studies published before and during this period were identified by hand-searching reference lists of obtained articles or published abstracts of older literature from the Cochrane Database of Systematic Reviews (CDSR), and by searching Google Scholar using the terms helminth and reinfection. Identified reports were imported into EndNote X2 (Thomson Reuters) for management. Two experienced, independent reviewers (TWJ, SM) assessed studies against inclusion and exclusion criteria according to a pre-established study protocol. Tables S1 and S2 give details of 139 retrievable studies recovered by our search, which were ultimately included (n = 51, Table S1) or excluded in our meta-analyses (n = 88, Table S2).

Outcome Assessments

We abstracted and compared the following components associated with STH reinfection: rate and intensity of infection before and after treatment, CR, time between evaluations before and after treatment, and adherence to follow-up. Additional study characteristics included year and country where the trial was implemented, sample size, age of study participants, diagnostic method and number of stool samples examined, and strategy of drug administration (universal, targeted, or selective treatment).

In the first phase of assessment, outcomes related to STH reinfection of different cohorts or subgroups were analyzed separately, and only one cohort was included per study. Those cohorts without statistically significant differences in infection rates both before and after treatment were combined and analyzed as one, but those with significant differences were selected according to adherence rate first, then CR or initial prevalence. If multiple rounds of chemotherapy were administered within 1 year, expecting a relatively higher CR, we conservatively selected the prevalence after the latest treatment as the main outcome. Finally, data were stratified by species of STH, subgroup, and time interval of follow-up after treatment, categorized as ‘3 months’ (3–4 months), ‘6 months’ (6–8 months) or ‘12 months’ (10–12 months).

Data Analysis

Review Manager software 5.0.23, provided by the Cochrane Collaboration group, was used for meta-analysis. Risk ratios (RR) were listed by study and compared for the risk or predisposition to reinfection after preventive chemotherapy. The primary analysis was performed according to helminth species-specific infection and length of follow-up intervals. Additional analysis was performed for specific population subgroups. Prevalence risk ratio (PRR) was utilized as indicator for estimating the risk of reinfection after treatment according to the following formula: [20]. Hence, PRR reflects the re-acquired level of infection after treatment, in comparison with the pretreatment level. In some studies, this indicator was directly used as the reinfection rate [21], [22].

Subgroup analysis was based on initial infection status, age, sex, and selected socioeconomic factors (Table 1). We calculated pooled estimates with a random-effects model, unless heterogeneity level determined by Moran's I2 was less than 50% [23]. Of note, I2 represents the proportion of the between-study variance of the total variance in a pooled estimate. An I2 of 0% indicates that all variability in effect estimates is due to sampling error within studies, and that none is due to heterogeneity [24], [25]. Publication bias was visually examined using funnel plots [26]. Results are presented by means of forest plots, including 95% confidence intervals (CI). In the figures and tables presented, RR not equal to 1 indicates that reinfection rate is associated with the key variable underlying the subgroup analysis (e.g., age and sex).

10.1371/journal.pntd.0001621.t001Table 1

Summary of 51 included studies reporting on posttreatment reinfection by soil-transmitted helminths (STHs), stratified by parasite species.

Number of studies by species*
A. lumbricoides T. trichiura Hookworm Number of studies [reference(s)]
1. Prevalence of STH infection after treatment 21 12 14 24 [13], [19], [22], [27][47]
2. Predisposition factors
Initial infection (present or absent) 8 5 3 9 [31], [44], [48][54]
Initial infection intensity (light or heavy) 9 8 6 16 [32], [35], [49], [50], [52], [53], [55][64]
Age 8 5 5 11 [32][34], [44], [49], [51], [54], [57], [62], [65], [66]
Sex 8 4 4 9 [21], [32][34], [44], [51], [54], [65], [67]
3. Other factors
Nutrient supplementation 4 3 3 4 [19], [22], [68], [69]
Malnutrition or growth-retarded 2 2 1 2 [21], [39]
Health promotion 2 2 2 2 [37], [70]
Hand washing with soap 1 0 0 1 [71]
Geophagy 1 1 1 1 [72]
Education or occupation of mother 2 1 1 2 [21], [50]
Crowded housing 2 0 0 2 [50], [64]
Type of floor or yard 3 1 0 3 [13], [61], [65]
Sanitary latrine 3 1 3 4 [21], [27], [50], [73]
Vegetable plantation area 1 0 1 1 [41]
Seasonal fluctuation 3 0 0 3 [13], [29], [48]
Total 43 27 27 51


Studies Identified and Characteristics

Of the 154 studies identified through our systematic database searches, complemented with hand searches, 51 studies carried out in 26 countries met inclusion criteria for subsequent meta-analysis (Figure 1). Twenty-four studies presented STH infection rates of populations or mixed cohorts, including information on the numbers infected and uninfected before and after treatment that could be used to assess the re-acquired prevalence of STH infections at specified time intervals posttreatment. Forty-two studies provided reinfection data by subgroups and evaluated their relative predisposition to reinfection. Table 1 summarizes the number of studies related to reinfection and its potential determinants, stratified by species of STH.

Of the 51 studies included, 84% provided data on A. lumbricoides after treatment, 53% on T. trichiura, and 53% on hookworm. Twenty-five studies investigated single-species infection after treatment: 17 for A. lumbricoides alone, five for hookworm alone, and three for T. trichiura alone, 20 assessed all three STH species concurrently, four assessed A. lumbricoides and T. trichiura, and two assessed A. lumbricoides and hookworm.

Dynamics of Reinfection

Twenty-four studies provided STH infection rates before and after treatment, including sample sizes. Most of these focused on A. lumbricoides and on reinfection in the 6–12 months follow-up period (Table S3). We performed nine pooled estimates (3 species×3 time points) of reinfection level in total, but were unable to pool the RRs of T. trichiura and hookworm at 3 months after treatment due to an insufficient number of studies. Heterogeneity was high for all pooled estimates (I2>80%) [24], even after exclusion of five studies due to poor quality (three with low adherence rates [32], [36], [39], two with poor CR [13], [28]; for details, see Table S3). Publication and selection bias were not detected visually using funnel plots in eight pooled estimates with the exception of A. lumbricoides at the 3 months posttreatment follow-up time point.

Re-Acquired Prevalence of STH at 3 Months Posttreatment

For A. lumbricoides, we found a random pooled RR of reinfection, based on five studies, of 0.26 (95% CI: 0.16–0.43) [29], [31], [42][44]. The estimates from the individual studies are listed in Figure 2. CRs ranged from 89.7% to 97.7% for three studies [31], [42], [43]. The remaining two studies applied an excluding or retreatment procedure to the uncured [29], [44]. The study carried out by Liu et al. (2006) [44] showed that even after four rounds of treatment with pyrantel pamoate (10 mg/kg per dose given at 3 months interval for a year), the prevalence of A. lumbricoides reached 47% of the original prevalence at 3 months after the final treatment. We also performed a subgroup analysis of school-aged children (6–15 years) after excluding one population-based study [44]. Their pooled RR from four studies was 0.22 (95% CI: 0.13–0.39) [29], [31], [42], [43], slightly less than the value obtained using all age groups. We performed another pooled estimate in view of the detected publication bias caused by one large study (n = 1017) [42]. After excluding this study, the pooled RR changed slightly, rising from 0.26 to 0.29 (95% CI: 0.17–0.51) [29], [31], [43], [44].

10.1371/journal.pntd.0001621.g002Figure 2

Forest plot of prevalence of Ascaris lumbricoides 3, 6, and 12 months posttreatment.

A random relative risk (RR) value of less than 1 indicates a lower infection rate after treatment compared to the initial level. Diamonds represent the pooled estimate across studies. See Table S1 for full references. *The infection rate 3 or 6 months after the last round of treatment was abstracted (Table S3).

Due to low CR, only a few studies were included in our evaluation of reinfection with T. trichiura or hookworm at the 3 months posttreatment follow-up. In this review only two studies of T. trichiura and hookworm were included, which is insufficient for pooling [31], [42]. If the threshold of CR was set at 50%, then the resulting RR 3 months after treatment was 0.36 (95% CI: 0.28–0.47) for T. trichiura[31], and 0.30 (95% CI: 0.26–0.34) for hookworm (Table S3) [42].

Re-Acquired Prevalence of STH 6 Months Posttreatment

For A. lumbricoides, the random pooled RR derived from nine studies was 0.68 (95% CI: 0.60–0.76) [29], [34], [40][44], [46], [47]. Estimates of the individual studies are given in Figure 2. CRs ranged from 92% to 100% in four studies [34], [40], [41], [43], while the remaining five studies applied an excluding or retreatment procedure to the uncured, and hence resulted in a higher CR [29], [42], [44], [46], [47]. We also performed a subgroup analysis of children aged 2–15 years after excluding two population-based studies and obtained a pooled estimate of 0.69 (95% CI: 0.60–0.79) [34], [44]. After three outlier studies were removed [40], [42], [43], the fixed RR was estimated to be 0.71 (95% CI: 0.68–0.75) (I2 = 0%; χ2 = 3.22, P = 0.67) [29], [34], [41], [44], [46], [47].

For T. trichiura, four studies were included in the pooled estimate, two with moderate CRs (>67%) [34], [47], and two with poor CRs (30–40%), even after two rounds of treatment at 6-month intervals in 1 year (Table S3) [40], [42]. Poor CRs caused two outlier results and a higher pooled estimate without a significant difference from 1 (RR = 0.67; 95% CI: 0.42–1.08) (Figure 3) [34], [40], [42], [47]. When these two outlier studies were excluded [40], [42], the random RR dropped to 0.54 (95% CI: 0.41–0.71) [34], [47]. For hookworm, there were only two studies included with high CR (>90%) [41], [42], and the random RR was 0.55 (95% CI: 0.34–0.87).

10.1371/journal.pntd.0001621.g003Figure 3

Forest plot of prevalence of Trichuris trichiura or hookworm after treatment.

A random relative risk (RR) value of less than 1 indicates a lower infection rate after treatment compared to the initial level. Diamonds represent the pooled estimate across studies. See Table S1 for full references. *The infection rate 6 months after the last round of treatment was abstracted (Table S3).

Re-Acquired Prevalence of STH 12 Months Posttreatment

Generally, the heterogeneity effect caused by CR, treatment regimen, subpopulation, and variability in study design decreased gradually over the posttreatment follow-up time and became non-significant. STH prevalence tended to regress to the pretreatment level in A. lumbricoides and T. trichiura, and persisted at approximately half the level in the case of hookworm. However, poor adherence in some studies was a major source of heterogeneity, which could introduce an influential outlier. This effect was evaluated for a study in which the adherence rate for A. lumbricoides was relatively high (74%; 724/977), but considerably lower for T. trichiura (56%; 548/977) and hookworm (60%; 588/977) (Table S3) [22].

For A. lumbricoides, eight studies were included, resulting in a random RR of 0.94 (95% CI: 0.88–1.01) (Figure 2 and Table S3) [19], [22], [30], [33], [37], [44], [46], [47]. Removal of two outlier studies [19], [37], resulted in a fixed RR of 0.96 (95% CI: 0.93–0.98) (I2 = 49%; χ2 = 9.85, P = 0.08).

For T. trichiura, there were three studies included with a random RR of 0.82 (95% CI: 0.62–1.07) (Figure 3 and Table S3) [19], [37], [47]. One study was excluded from this pooling due to poor adherence of the T. trichiura cohort (56%; 548/977), of which the individual RR was 0.42 (95% CI: 0.35–0.51) [22]. If combined into the random-effects model, the pooled estimate dropped to 0.69 (95% CI: 0.45–1.05). We ultimately removed this cohort of T. trichiura from the pooled estimate based on our exclusion criteria (Table S3) [22].

For hookworm, there were five studies included with a random RR of 0.57 (95% CI: 0.49–0.67) (Figure 3 and Table S3) [19], [27], [35], [37], [45]. After removing two outlier studies [35], [45], we obtained a fixed RR of 0.57 (95% CI: 0.52–0.62) from three studies (I2 = 0%; χ2 = 0.32, P = 0.85) [19], [27], [37]. In contrast to A. lumbricoides and T. trichiura, the re-acquired prevalence of hookworm returned to only about half of the initial level. We also removed a cohort of hookworm from the pooled estimate due to poor adherence (Table S3) [22]. Including that study would have resulted in a slightly lower pooled estimate (RR = 0.53; 95% CI: 0.44–0.64).

Figure 4 shows the rapidity of re-acquiring soil-transmitted helminth (STH) infections at the 3, 6, and 12 months posttreatment follow-up time points.

10.1371/journal.pntd.0001621.g004Figure 4

Summary of the rapidity of re-acquiring soil-transmitted helminth (STH) infections after treatment.

Determinants of Predisposition to Reinfection

Most studies focused on the risk of A. lumbricoides reinfection, particularly reinfection predisposition relating to the initial infection status, age, and sex. Seven studies were included into the pooled estimate of effect of initial infection status on A. lumbricoides reinfection, with a fixed RR of 1.95 (95% CI: 1.62–2.34) (I2 = 0%, χ2 = 3.63, P = 0.73) (Figure S1) [31], [44], [48], [50], [51], [53], [54]. This means that 6 months after treatment, risk of reinfection in the pretreatment-positive group was almost twice as high than that of the pretreatment-negative group (P<0.001). The pooled estimates of the risk ratios of STH reinfection between subgroups are summarized in Table 2. Overall, males had a significantly lower risk of A. lumbricoides reinfection (P<0.001), and those with heavy intensity pretreatment infection with hookworm predisposed to re-acquiring high numbers of worm after therapy (P = 0.04) [63].

10.1371/journal.pntd.0001621.t002Table 2

Summary estimates of the risk of soil-transmitted helminth (STH) reinfection by determinants of predisposition.*

Subgroups in comparison Risk ratios (RR) of reinfection, stratified by STH species (95% CI) (number of studies) [Reference]
A. lumbricoides T. trichiura Hookworm
Initial infection (present vs. absent) 1.95 (1.62–2.34) (n = 7)F[31], [44], [48], [50], [51], [53], [54] 1.07 (0.41–2.80) (n = 4)R[31], [51], [53], [54] 1.57 (0.74–3.37) (n = 3)F[31], [51], [54]
Initial intensity (heavy vs. light) 3.65 (1.03–12.96, P = 0·05) (n = 2)R[52], [63] 2.82 (0.62–12.75) (n = 1) [63] 2.55 (1.02,6.37) (n = 1) [63]
Age (adults vs. children) 0.76 (0.52–1.12) (n = 5)R[44], [51], [54], [57], [65] 0.93 (0.31–2.81) (n = 2)R[51], [54] 1.15 (0.58–2.28) (n = 2)F[51], [54]
Sex (male vs. female) 0.71 (0.61–0.83) (n = 4)F[44], [51], [54], [65] 1.06 (0.67–1.68) (n = 2)F[51], [54] 1.42 (0.91–2.19) (n = 2)F[51], [54]

*: Meta-analysis of nutrient supplementation, malnutrition, health promotion, individual behavior, and family and community environment was restricted because of small sample size (i.e., number of available studies for inclusion), or because of inconsistent measures used to assess infection and/or reinfection.


Pooled estimate of fixed-effects model.


Pooled estimate of random-effects model.

For some important outcome measures, it was not possible to perform meta-analyses because of the low number of studies addressing such outcomes and the broad differences in the measures and statistical methods used to assess them [79]. Of 16 studies reporting the predisposition to heavy or light intensity of infection after treatment, 15 provided significant statistics and one was depicted by column chart without any statistics [49]. Only two provided data of subgroups categorized by intensity level and could be pooled (Table 2) [52], [63]. Statistical tests in 15 studies consistently found a positive relationship between the intensity of infection pre- and posttreatment. Eleven were tested by Kendall's correlation [32], [35], [49], [52], [55][59], [62], [64], two by Pearson's [50], [53], one by Spearman [61], and one by χ2[63]. Among nine studies reporting reinfection risk of infected individuals, two could not be combined due to discordant or absent statistics [49], [52]. Two studies indicated that growth-retarded children were more susceptible to STH reinfection in comparison to children with normal development [21], [39]. One randomized controlled trial indicated that multi-micronutrient fortification significantly enhanced deworming efficacy [69]. However, two randomized controlled trials separately demonstrated that supplementation of iron or multi-micronutrients in children had no significant effect, neither on prevalence nor on intensity of reinfection [19], [22], and one cross-sectional cohort study in 1- to 5-year-old children identified possible transitory benefit of vitamin A supplementation [68]. One longitudinal study in Kenyan women during pregnancy reported a positive relationship between earth-eating and STH reinfection [72]. One controlled trial in Chinese pupils assessed and quantified the impact of hand washing with soap on A. lumbricoides infection [71]. Four studies assessed the effect of sanitation to control STH reinfection [21], [27], [50], [73]. Three studies observed the seasonal fluctuations of A. lumbricoides reinfection, indicating transmission is highest when rainfall is minimal and lowest when rainfall is at its highest [29], [48].


Investigation of STH reinfection patterns following drug therapy dates back to the early 1920s [27]. However, nearly 90% (45/51) of studies included in the meta-analysis reported here were pursued in the past 30 years, suggesting their relevance to current deworming strategies and programs. Our broad-based meta-analysis shows that after targeted or mass drug administration, the prevalence of STH infections recovers rapidly in most endemic areas. Indeed, 6 months posttreatment, the prevalence of all three species reached or exceeded half the initial level; and at 12 months posttreatment follow-up, the prevalence of A. lumbricoides and T. trichiura usually returned to levels close to the initial pretreatment, while levels of hookworm reinfection continued to fluctuate at about half pretreatment level (Figure 4). The rate and intensity of initial pretreatment infection status were positively correlated with reinfection, although such predisposing effects were not as clear-cut for T. trichiura and hookworm due to limited data or discordant statistics.

Publication and Selection Bias

We report relatively conservative pooled effect sizes, as demonstrated through sensitivity analysis. Had case studies with poor CR, low adherence with follow-up, or low coverage for treatment been included, the projected prevalence at around 6 months posttreatment would be higher than the presented pooled estimates (Table S3) [13], [28], [32], [36], [39]. One study included in our review, but not included in pooled estimates due to the difference in follow-up interval, showed that by 9 months posttreatment, re-acquired prevalence of A. lumbricoides and T. trichiura almost reached pre-intervention levels [38]. We acknowledge that some potentially relevant studies reported in Thai, Korean, Japanese, and Portuguese, identified by hand searching reference lists of included studies, were omitted. However, we are confident that excluding these studies and unpublished studies (‘grey literature’) would not impact our conservative pooled estimates (Figure 1). Our claim is substantiated by only a modest publication bias detected by funnel plots.

Assessment of Quality of Included Studies

For our analysis, it was important to include the broadest range of data (i.e., covering a large time period and multiple locations) from field-based studies to develop a more general and inclusive assessment of the risk of STH reinfection after treatment. There was potential heterogeneity of individual study inclusion criteria, initial prevalence and intensity levels, CR, drug administration strategies, adherence, and coverage rates, as well as sanitation and risk behavior. During the process of heterogeneity testing and sensitivity analysis, it was found that a low adherence rate created outliers with a large effect on the pooled estimate. For this reason, the final exclusion threshold for adherence was set conservatively at 70%. A low initial prevalence of STH infections (<10%) also created outliers (but with little influence on estimates), while a low CR could directly limit effective measurement of reinfection rates within 6 months after drug administration. We therefore removed such cohorts from our final pooled estimates.

Most studies on reinfection of STH are based on the infected cohort (sometimes along with the uninfected cohort). Restricted by the methods of pooled analysis, the reinfection rate of such a cohort could not be combined and compared among studies. We therefore selected PRR between posttreatment and pretreatment as the indicator for estimating risk of reinfection after drug administration, which balanced the heterogeneity of studies and made them comparable. For some pooled estimates (Figure 2), we removed several outlier studies to compare the difference between fixed- and random-effects models. We found that the random estimate was similar to that of the fixed model, with wider 95% CIs than the fixed-effects model.

Main Outcomes

In May 2001, at the 54th World Health Assembly, member states were urged to pursue preventive chemotherapy to control morbidity due to STH infections and schistosomiasis, mainly among school-aged children [9], [80][82]. Our study indicates that in endemic areas where the prevalence of STH infections is above 10%, biannual treatment might be indicated against A. lumbricoides and T. trichiura and at least one treatment per year against hookworm. The seasonality of transmission of STHs is an important factor to consider in planning and timing of preventive chemotherapy, so that the effectiveness of this control strategy can be enhanced [13], [29], [40], [48], [83].

Our study shows that the rate and intensity of reinfection are positively correlated with the initial pretreatment infection status (Table 2). Although the dynamics of STH transmission may be intricate, reinfection levels should be expected to be similar over repeated treatments if the factors responsible for predisposition to light or heavy infection are stable through time [84]. For example, in view of PRR, there was only a modest decrease after a second-round treatment compared to the initial treatment (50.6% vs. 61.8% of the initial level of pretreatment for A. lumbricoides, 33.5% vs. 46.0% for T. trichiura[34] (for details, see Table S3). Overall, the ultimate objective of preventive chemotherapy is to control morbidity rather than to interrupt transmission of STH infections [15], [52], [81].


There are limitations to this systematic review and meta-analysis, which are offered for consideration. First, epidemiological and statistical heterogeneity between studies allows possible confounding of the observed results. For example, differences in age, sex, socioeconomic and nutritional status could modify the risk of STH reinfection, which could then confound estimation of the effects of these determinants. However, details of these potentially modifying factors were not available in most of the studies included in our analysis, so adjustment was not attempted in the summary statistics. Other factors, such as diagnostic method, the frequency, approach, and efficacy of anthelmintic drugs, and length and adherence of follow-up, also varied between studies. Second, for continuous distributions, relatively large changes in average worm load could have been related to only small changes in overall prevalence such that prevalence, and hence CR, may not be the best indicator to monitor the impact of anthelmintic treatment in highly endemic areas [33], [40], [52], [76]. Indeed, it has been argued that egg reduction rate (ERR) rather than CR should be used for anthelmintic drug efficacy evaluations [85][87], and perhaps for studying patterns of reinfection after treatment. Intensity of infection is an important aspect of all helminthiases, but could not be well addressed in our pooled estimates. Similarly, the significant relationships between STH reinfection and socioeconomic factors could not be definitively assessed [4]. Finally, the generalized estimates from our study will probably not apply to low endemicity areas, characterized by prevalence estimates below 10%.

Concluding, preventive chemotherapy with the current drugs of choice against STHs, while showing good results on morbidity reduction, does not prevent rapid reinfection [88]. Decision-makers have to make tradeoffs between benefits, cost (selected vs. mass treatment), acceptability, and harms (e.g., drug resistance) of preventive chemotherapy according the local settings [89][92]. Our results therefore support recommendations for integrated control approaches, complementing preventive chemotherapy with information, education, and communication (IEC) strategies, and sanitation improvement, in order to control STH infections more durably [6], [93][95]. The experience from the southern parts of the United States of America almost 100 years ago, as well as the Republic of Korea, P.R. China, and some parts of sub-Saharan Africa indicates that control strategies must be adapted to the prevailing social-ecological setting, and require long-term political commitment [95], [96]. In resource-limited settings, regular deworming of school-aged children is considered to be a cost-effective intervention for control of morbidity due to STH infections [9], [80], [96]. More intense treatment (e.g., twice yearly) is likely to further impact on morbidity, as seen for schistosomiasis [90], but might bear the risk of drug resistance development [91], [97]. If resources allow, efforts should be made to promote clean water, improved sanitation, health promotion in schools, and these efforts should ultimately aim at behavioral change [6], [98][101]. Communities living in newly industrialized countries such as P.R. China, should benefit from an integrated treatment and sanitation strategy. Hence, rather than solely being restricted to preventive chemotherapy targeting STHs and other neglected tropical diseases [102], comprehensive control requires inter-programmatic and intersectoral action for health and development [103], [104].

Supporting Information

Figure S1

Forest plot of reinfection risk of individuals initially infected with Ascaris lumbricoides, 6–12 months posttreatment. Notes: A random relative risk (RR) of less than 1 indicates a lower infection rate after treatment compared to the initial level. Diamonds represent the pooled estimate across studies. See Table S1 for full references.


Click here for additional data file.

Table S1

Included studies.


Click here for additional data file.

Table S2

Excluded studies.


Click here for additional data file.

Table S3

Studies included in our meta-analysis pertaining to reinfection patterns of soil-transmitted helminths (STHs) 3–12 months posttreatment.*


Click here for additional data file.

Checklist S1

PRISMA checklist.


Click here for additional data file.


The authors thank Helen Wakeford (BA Oxon) from Cambridge University for editorial assistance in drafting the manuscript, Wei Li (BA) from Jiangsu Institute of Parasitic Diseases for obtaining relevant articles in Chinese, and Prof. Long-Qi Xu and Prof. Ming-Gang Chen, from National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, for assistance with study design. We also thank Paul Chinnock (MSc) from Hughes Hall for helpful comments and suggestions after reviewing the study protocol and early drafts of this manuscript.


  1. PJ HotezDH MolyneuxA FenwickJ KumaresanSE Sachs2007Control of neglected tropical diseases.N Engl J Med3571018102717804846
  2. PJ HotezPJ BrindleyJM BethonyCH KingEJ Pearce2008Helminth infections: the great neglected tropical diseases.J Clin Invest1181311132118382743
  3. NR de SilvaS BrookerPJ HotezA MontresorD Engels2003Soil-transmitted helminth infections: updating the global picture.Trends Parasitol1954755114642761
  4. LM VandemarkTW JiaXN Zhou2010Social science implications for control of helminth infections in Southeast Asia.Adv Parasitol7313717020627142
  5. A AlemuA AtnafuZ AddisY ShiferawT Teklu2011Soil transmitted helminths and schistosoma mansoni infections among school children in Zarima town, northwest Ethiopia.BMC Infect Dis1118921740589
  6. K ZiegelbauerB SpeichD MausezahlR BosJ Keiser2012Effect of sanitation on soil-transmitted helminth infection: systematic review and meta-analysis.PLoS Med9e100116222291577
  7. J BethonyS BrookerM AlbonicoSM GeigerA Loukas2006Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm.Lancet3671521153216679166
  8. CV Holland2009Predisposition to ascariasis: patterns, mechanisms and implications.Parasitology1361537154719450374
  9. WHO2005Deworming for health and development. Report of the third global meeting of the Partners for Parasite ControlGenevaWorld Health Organization
  10. CH King2010Parasites and poverty: the case of schistosomiasis.Acta Trop1139510419962954
  11. WHO2006Preventive chemotherapy in human helminthiasis: coordinated use of anthelminthic drugs in control interventions: a manual for health professionals and programme managersGenevaWorld Health Organization
  12. WHO2010First WHO report on neglected tropical diseases 2010: working to overcome the global impact of neglected tropical diseasesGenevaWorld Health Organization
  13. GF Otto1930Ascaris lumbricoides: treatment, loss of worms and reinfestation.JAMA95194196
  14. BH SingerMC de Castro2007Bridges to sustainable tropical health.Proc Natl Acad Sci U S A104160381604317913894
  15. RM AndersonGF Medley1985Community control of helminth infections of man by mass and selective chemotherapy.Parasitology906296603892436
  16. D MoherA LiberatiJ TetzlaffDG Altman2009Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement.PLoS Med6e100009719621072
  17. The PLoS Medicine Editors2011Best practice in systematic reviews: the importance of protocols and registration.PLoS Med8e100100921364968
  18. J KeiserJ Utzinger2008Efficacy of current drugs against soil-transmitted helminth infections: systematic review and meta-analysis.JAMA2991937194818430913
  19. A OlsenJ NawiriH Friis2000The impact of iron supplementation on reinfection with intestinal helminths and Schistosoma mansoni in western Kenya.Trans R Soc Trop Med Hyg9449349911132373
  20. T SkovJ DeddensMR PetersenL Endahl1998Prevalence proportion ratios: estimation and hypothesis testing.Int J Epidemiol2791959563700
  21. M Hesham Al-MekhlafiJ SurinAS AtiyaWA AriffinAK Mohammed Mahdy2008Pattern and predictors of soil-transmitted helminth reinfection among aboriginal schoolchildren in rural Peninsular Malaysia.Acta Trop10720020418582430
  22. A OlsenFW Thiong'oJH OumaD MwanikiP Magnussen2003Effects of multimicronutrient supplementation on helminth reinfection: a randomized, controlled trial in Kenyan schoolchildren.Trans R Soc Trop Med Hyg9710911412886816
  23. M BorensteinLV HedgesJPT HigginsHR Rothstein2010A basic introduction to fixed effect and random effects models for meta-analysis.Research Synthesis Methods19711126061376
  24. JP HigginsSG Thompson2002Quantifying heterogeneity in a meta-analysis.Stat Med211539155812111919
  25. JP Higgins2008Commentary: Heterogeneity in meta-analysis should be expected and appropriately quantified.Int J Epidemiol371158116018832388
  26. K KnoblochU YoonPM Vogt2011Preferred reporting items for systematic reviews and meta-analyses (PRISMA) statement and publication bias.J Craniomaxillofac Surg39919221145753
  27. RB Hill1925Hookworm reinfestation in sanitated and unsanitated areas.Southern Med J18665668
  28. GF OttoWW Cort1934Further studies on post-treatment reinfection with Ascaris in the United States.J Parasitol20245247
  29. CT PanLS RitchieGW Hunter 3rd1954Reinfection and seasonal fluctuations of Ascaris lumbricoides among a group of children in an area where night soil is used.J Parasitol4060360813202020
  30. F ArfaaE Ghadirian1977Epidemiology and mass-treatment of ascariasis in six rural communities in central Iran.Am J Trop Med Hyg26866871907049
  31. B Sinniah1984Prevalence, treatment and reinfection of intestinal helminths among schoolchildren in Kuala Lumpur, Malaysia.Public Health9838426709819
  32. MR Haswell-ElkinsDB ElkinsK ManjulaE MichaelRM Anderson1988An investigation of hookworm infection and reinfection following mass anthelmintic treatment in the south Indian fishing community of Vairavankuppam.Parasitology965655773405641
  33. DB ElkinsM Haswell-ElkinsRM Anderson1988The importance of host age and sex to patterns of reinfection with Ascaris lumbricoides following mass anthelmintic treatment in a South Indian fishing community.Parasitology961711843362574
  34. L ChanSP KanDA Bundy1992The effect of repeated chemotherapy on the prevalence and intensity of Ascaris lumbricoides and Trichuris trichiura infection.Southeast Asian J Trop Med Public Health232282341439974
  35. RJ QuinnellAF SlaterP TigheEA WalshAE Keymer1993Reinfection with hookworm after chemotherapy in Papua New Guinea.Parasitology1063793858316435
  36. M AlbonicoPG SmithE ErcoleA HallHM Chwaya1995Rate of reinfection with intestinal nematodes after treatment of children with mebendazole or albendazole in a highly endemic area.Trans R Soc Trop Med Hyg895385418560535
  37. C MuennooW AchwanichkulS Sa-nguankiatS PubampenW Maipanich1997The impact of primary health care intervention on reinfection of soil-transmitted helminths in the community.Southeast Asian J Trop Med Public Health288168199656407
  38. I PaulG GnanamaniNR Nallam1999Intestinal helminth infections among school children in Visakhapatnam.Indian J Pediatr6666967310798127
  39. I HagelNR LynchMC Di PriscoM PerezJE Sanchez1999Helminthic infection and anthropometric indicators in children from a tropical slum: Ascaris reinfection after anthelmintic treatment.J Trop Pediatr4521522010467832
  40. M AlbonicoRJ StoltzfusL SavioliHM ChwayaE d'Harcourt1999A controlled evaluation of two school-based anthelminthic chemotherapy regimens on intensity of intestinal helminth infections.Int J Epidemiol2859159610405869
  41. GT HanN HanL QiaoY Li2003Infection status of intestinal helminths after chemotherapy in school children living in the vegetable planting area of Shenqiu county.Chin J School Health24358(in Chinese)
  42. E SaathoffA OlsenJD KvalsvigCC Appleton2004Patterns of geohelminth infection, impact of albendazole treatment and re-infection after treatment in schoolchildren from rural KwaZulu-Natal/South-Africa.BMC Infect Dis42715310401
  43. YL FeiF XuZP Wang2006Longitudinal study on Ascaris infection in town or village pupils in Fengxian.Chin J School Doctor20522523(in Chinese)
  44. CY LiuXJ ZengWS JiangHG ChenXL Hong2006Reinfection after different chemotherapy measures carried out in heavy epidemic areas with Ascaris lumbricoides.J Pathog Biol1449451(in Chinese)
  45. Y ZhangA KoukounariN KabatereineF FlemingF Kazibwe2007Parasitological impact of 2-year preventive chemotherapy on schistosomiasis and soil-transmitted helminthiasis in Uganda.BMC Med52717767713
  46. M NchitoPW GeisslerL MubilaH FriisA Olsen2009The effect of iron and multi-micronutrient supplementation on Ascaris lumbricoides reinfection among Zambian schoolchildren.Trans R Soc Trop Med Hyg10322923618937957
  47. CC AppletonTI MosalaJ LevinA Olsen2009Geohelminth infection and re-infection after chemotherapy among slum-dwelling children in Durban, South Africa.Ann Trop Med Parasitol10324926119341539
  48. BD Cabrera1984Reinfection and infection rates of ascariasis in relation to seasonal variation in the Philippines.Southeast Asian J Trop Med Public Health153944016523175
  49. DAP BundyES CooperDE ThompsonJM DidierI Simmons1988Effect of age and initial infection intensity on the rate of reinfection with Trichuris trichiura after treatment.Parasitology974694763217141
  50. FJ Henry1988Reinfection with Ascaris lumbricoides after chemotherapy: a comparative study in three villages with varying sanitation.Trans R Soc Trop Med Hyg824604643232186
  51. N Soeripto1991Reinfection and infection rates of soil-transmitted-helminths in Kemiri Sewu, Yogyakarta, Indonesia.Southeast Asian J Trop Med Public Health222162211948282
  52. A HallKS AnwarAM Tomkins1992Intensity of reinfection with Ascaris lumbricoides and its implications for parasite control.Lancet339125312571349668
  53. FJ HenrySR HuttlyMU AhmedA Alam1993Effect of chemotherapy on helminth reinfection in slums and villages in Bangladesh.Southeast Asian J Trop Med Public Health243073128266234
  54. K NarainGK MedhiSK RajguruJ Mahanta2004Cure and reinfection patterns of geohelminthic infections after treatment in communities inhabiting the tropical rainforest of Assam, India.Southeast Asian J Trop Med Public Health3551251715689058
  55. GA SchadRM Anderson1985Predisposition to hookworm infection in humans.Science228153715404012307
  56. MR Haswell-ElkinsDB ElkinsRM Anderson1987Evidence for predisposition in humans to infection with Ascaris, hookworm, Enterobius and Trichuris in a South Indian fishing community.Parasitology953233373696767
  57. T HlaingT SawM Lwin1987Reinfection of people with Ascaris lumbricoides following single, 6-month and 12-month interval mass chemotherapy in Okpo village, rural Burma.Trans R Soc Trop Med Hyg811401462965438
  58. DAP BundyES CooperDE ThompsonJM DidierI Simmons1987Epidemiology and population dynamics of Ascaris lumbricoides and Trichuris trichiura infection in the same community.Trans R Soc Trop Med Hyg819879933503421
  59. DAP BundyES CooperDE ThompsonJM DidierRM Anderson1987Predisposition to Trichuris trichiura infection in humans.Epidemiol Infect9865713556438
  60. DAP BundyES Cooper1988The evidence for predisposition to trichuriasis in humans: comparison of institutional and community studies.Ann Trop Med Parasitol822512563250338
  61. JE ForresterME ScottDAP BundyMHN Golden1990Predisposition of individuals and families in Mexico to heavy infection with Ascaris lumbricoides and Trichuris trichiura.Trans R Soc Trop Med Hyg842722762389320
  62. M BradleySK Chandiwana1990Age-dependency in predisposition to hookworm infection in the Burma valley area of Zimbabwe.Trans R Soc Trop Med Hyg848268282136254
  63. ES UpathamV ViyanantWY BrockelmanS KurathongP Ardsungnoen1992Predisposition to reinfection by intestinal helminths after chemotherapy in south Thailand.Int J Parasitol228018061428513
  64. M Haswell-ElkinsD ElkinsRM Anderson1989The influence of individual, social group and household factors on the distribution of Ascaris lumbricoides within a community and implications for control strategies.Parasitology981251342717212
  65. JY ChaiBS SeoSH LeeSY Cho1983Epidemiological studies on Ascaris lumbricoides reinfection in rural communities in Korea II. Age-specific reinfection rates and familial aggregation of the reinfected cases.Korean J Parasitol21142149
  66. J ImaiO SakamotoFE MuntheS Sinulingga1985Survey for soil-transmitted helminths in Asahan Regency, North Sumatra, Indonesia.Southeast Asian J Trop Med Public Health164414464095609
  67. YK Peng2001Rate of reinfection with Ascaris after combination chemotherapy of albendazole and mebendazole.Chin J of Schisto Contr13156(in Chinese)
  68. LG PayneKG KoskiE Ortega-BarriaME Scott2007Benefit of vitamin A supplementation on Ascaris reinfection is less evident in stunted children.J Nutr1371455145917513406
  69. TT NgaP WinichagoonMA DijkhuizenNC KhanE Wasantwisut2009Multi-micronutrient-fortified biscuits decreased prevalence of anemia and improved micronutrient status and effectiveness of deworming in rural Vietnamese school children.J Nutr1391013102119321576
  70. XP FengXH WangJF NiFX WuFH Zhang2000Observations on the effect of some measures for preventing intestinal helminth infection in soldiers.J Prev Med Chin PLA (People's Libration Army)18210211(in Chinese)
  71. LQ XuDH XiaoCH ZhouXQ ZhangSG Lan2001On cleanliness of hands in diminution of Ascaris lumbricoides infection in children.Chin J Parasit Dis Contr19294297(in Chinese)
  72. AI LoubaPW GeisslerB EstambaleJ OumaD Alusala2005Earth-eating and reinfection with intestinal helminths among pregnant and lactating women in western Kenya.Trop Med Int Health1022022715730505
  73. WW CortL SchapiroNR Stoll1929A study of reinfection after treatment with hookworm and Ascaris in two villages in Panama.Am J Epidemiol10614625
  74. M AlbonicoPG SmithA HallHM ChwayaKS Alawi1994A randomized controlled trial comparing mebendazole and albendazole against Ascaris, Trichuris and hookworm infections.Trans R Soc Trop Med Hyg885855897992348
  75. DI PritchardRJ QuinnellAF SlaterPG McKeanDD Dale1990Epidemiology and immunology of Necator americanus infection in a community in Papua New Guinea: humoral responses to excretory-secretory and cuticular collagen antigens.Parasitology1003173262345664
  76. DB ElkinsM Haswell-ElkinsRM Anderson1986The epidemiology and control of intestinal helminths in the Pulicat Lake region of Southern India. I. Study design and pre- and post-treatment observations on Ascaris lumbricoides infection.Trans R Soc Trop Med Hyg807747923603617
  77. GW Hunter 3rdEP Hodges1948Studies of Schistosomiasis: II Summary of further studies on methods of recovering eggs of S. japonicum from stools.Bull U S Army Med Dep812813118909930
  78. RB Hill1923Investigations on the control of hookworm disease. XXV. The use of the egg-counting method in an intensive campaign.Am J Epidemiol33760
  79. CH KingK DickmanDJ Tisch2005Reassessment of the cost of chronic helmintic infection: a meta-analysis of disability-related outcomes in endemic schistosomiasis.Lancet3651561156915866310
  80. DH MolyneuxPJ HotezA Fenwick2005“Rapid-impact interventions”: how a policy of integrated control for Africa's neglected tropical diseases could benefit the poor.PLoS Med2e33616212468
  81. WHO2002Prevention and control of schistosomiasis and soil-transmitted helminthiasis: report of a WHO expert committeeGenevaWorld Health Organization
  82. L SavioliAF GabrielliA MontresorL ChitsuloD Engels2009Schistosomiasis control in Africa: 8 years after World Health Assembly Resolution 54.19.Parasitology1361677168119765347
  83. B GungorenR LatipovG RegalletE Musabaev2007Effect of hygiene promotion on the risk of reinfection rate of intestinal parasites in children in rural Uzbekistan.Trans R Soc Trop Med Hyg10156456917418321
  84. RM Anderson1986The population dynamics and epidemiology of intestinal nematode infections.Trans R Soc Trop Med Hyg806866963299886
  85. B LeveckeN SpeybroeckRJ DobsonJ VercruysseJ Charlier2011Novel insights in the fecal egg count reduction test for monitoring drug efficacy against soil-transmitted helminths in large-scale treatment programs.PLoS Negl Trop Dis5e142722180801
  86. A Montresor2011Cure rate is not a valid indicator for assessing drug efficacy and impact of preventive chemotherapy interventions against schistosomiasis and soil-transmitted helminthiasis.Trans R Soc Trop Med Hyg10536136321612808
  87. J VercruysseJM BehnkeM AlbonicoSM AmeC Angebault2011Assessment of the anthelmintic efficacy of albendazole in school children in seven countries where soil-transmitted helminths are endemic.PLoS Negl Trop Dis5e94821468309
  88. SO AsaoluIE Ofoezie2003The role of health education and sanitation in the control of helminth infections.Acta Trop8628329412745145
  89. JM SpiegelS DharamsiKM WasanA YassiB Singer2010Which new approaches to tackling neglected tropical diseases show promise?PLoS Med7e100025520502599
  90. CH KingSK OlbrychM SoonME SingerJ Carter2011Utility of repeated praziquantel dosing in the treatment of schistosomiasis in high-risk communities in Africa: a systematic review.PLoS Negl Trop Dis5e132121949893
  91. J VercruysseM AlbonicoJM BehnkeAC KotzeRK Prichard2011Is anthelmintic resistance a concern for the control of human soil-transmitted helminths?International J for Parasitology: Drugs and Drug Resistance11427
  92. M ParkerT Allen2011Does mass drug administration for the integrated treatment of neglected tropical diseases really work? Assessing evidence for the control of schistosomiasis and soil-transmitted helminths in Uganda.Health Res Policy Syst9321211001
  93. WHO1998Guildelines for the evaluation of soil-transmitted helminthiasis and schistosomiasis at community level. WHO/CTD/SIP/98.1GenevaWorld Health Organization
  94. WHO1999Monitoring helminth control programmes aimed at reducing morbidity caused by soil-transmitted helminths and schistosomes, with particular reference to school-age children. WHO/CDS/CPC/SIP/99.3GenevaWorld Health Organization
  95. A MontresorDT CongM SinuonR TsuyuokaC Chanthavisouk2008Large-scale preventive chemotherapy for the control of helminth infection in Western Pacific countries: six years later.PLoS Negl Trop Dis2e27818846234
  96. C UrbaniK Palmer2001Drug-based helminth control in Western Pacific countries: a general perspective.Trop Med Int Health693594411703849
  97. S GeertsB Gryseels2000Drug resistance in human helminths: current situation and lessons from livestock.Clin Microbiol Rev1320722210755998
  98. DWT CromptonL Savioli2007Handbook of helminth for public healthBoca Ration, USACRC Press
  99. J KobayashiM JimbaH OkabayashiP SinghasivanonJ Waikagul2007Beyond deworming: the promotion of school-health-based interventions by Japan.Trends Parasitol23252917134943
  100. IH NockT Aken'ovaM Galadima2006Deworming: adding public health education to the equation.Trends Parasitol227816303331
  101. T AllenM Parker2012Will increased funding for neglected tropical diseases really make poverty history?Lancet(in press). DOI: 10.1016/S0140-6736(12)60159-7
  102. PJ LammieA FenwickJ Utzinger2006A blueprint for success: integration of neglected tropical disease control programmes.Trends Parasitol2231332116713738
  103. ST HongJY ChaiMH ChoiS HuhHJ Rim2006A successful experience of soil-transmitted helminth control in the Republic of Korea.Korean J Parasitol4417718516969055
  104. JC HolveckJP EhrenbergSK AultR RojasJ Vasquez2007Prevention, control, and elimination of neglected diseases in the Americas: pathways to integrated, inter-programmatic, inter-sectoral action for health and development.BMC Public Health7617229324
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