Causes and Characteristics of Helminth Infections

Emphasis is placed on the four most common STH infections and the three most common schistosome infections. Together, these infections account for most of the global helminth disease burden.

Soil-transmitted Helminths

The four most common STHs are roundworm (Ascaris lumbricoides), whipworm (Trichuris trichiura), and the anthropophilic hookworms (Necator americanus and Ancylostoma duodenale). Recent estimates suggest that A. lumbricoides infects 1.221 billion people, T. trichiura 795 million, and hookworms 740 million (de Silva and others 2003) (table 24.1). The greatest numbers of STH infections occur in the Americas, China and East Asia, and Sub-Saharan Africa. Strongyloides stercoralis is also a common STH in some of these regions, although detailed information on the prevalence of strongyloidiasis is lacking because of the difficulties in diagnosing human infection. The life cycles of Ascaris, Trichuris, and hookworm follow a general pattern. The adult parasite stages inhabit the gastrointestinal tract (Ascaris and hookworm in the small intestine; Trichuris in the colon), reproduce sexually, and produce eggs, which are passed in human feces and deposited in the external environment.

Table 24.1

Global Prevalence and Distribution of Helminth Infections.

STH infections rarely cause death. Instead, the burden of disease is related less to mortality than to the chronic and insidious effects on the hosts' health and nutritional status (Stephenson, Latham, and Ottesen 2000; Stoltzfus and others 1997). Hookworms have long been recognized as an important cause of intestinal blood loss leading to iron deficiency and protein malnutrition. The iron deficiency anemia that accompanies moderate and heavy hookworm burdens is sometimes referred to as hookworm disease (Hotez and others 2004). When host iron stores are depleted, the extent of iron deficiency anemia is linearly related to the intensity of hookworm infection (Stoltzfus and others 1997). Because of their underlying poor iron status, children, women of reproductive age, and pregnant women are frequently the ones most susceptible to developing hookworm anemia (Brooker, Bethony, and Hotez 2004). Iron deficiency anemia during pregnancy has been linked to adverse maternal-fetal consequences, including prematurity, low birth-weight, and impaired lactation (WHO 2002).

Chronic STH infections resulting from Ascaris, Trichuris, and hookworm can dramatically affect physical and mental development in children (WHO 2002). Studies have also shown that the growth and physical fitness deficits caused by chronic STH infections are sometimes reversible following treatment with anthelmintic drugs (Stephenson, Latham, and Ottesen 2000). The effects on growth are most pronounced in children with the heaviest infections, but light infections may also contribute to growth deficits if the nutritional status of the community is poor (Stephenson, Latham, and Ottesen 2000).

Epidemiology of STH Infections and Schistosomiasis

The most striking epidemiological features of human helminth infections are aggregated distributions in human communities, predisposition of individuals to heavy (or light) infection, rapid reinfection following chemotherapy, and age-intensity profiles that are typically convex (with the exception of hookworm).

For all the major human STH and schistosome infections studied to date, worm burdens exhibit a highly aggregated (overdispersed) distribution so that most individuals harbor just a few worms in their intestines, although a few hosts harbor disproportionately large worm burdens (Anderson and May 1991). As a rule, 20 percent of the host population harbors approximately 80 percent of the worm population. This overdispersion has many consequences, both with regard to the population biology of the helminths and the public health consequence for the host, because heavily infected individuals are simultaneously at highest risk of disease and the major source of environmental contamination. One feature that may help explain overdispersion is that individuals tend to be predisposed to heavy (or light) infections. Predisposition has been demonstrated for all four major STHs and the schistosomes. The underlying cause of such predisposition remains poorly understood. However, a combination of heterogeneity in exposure to infection or differences in susceptibility to infection and the ability to mount effective immunity (genetic and nutritional factors) is likely to be important.

People of all ages rapidly reacquire infection following treatment, but in schistosomiasis, older people reacquire infection at slower rates than younger ones (Kabatereine and others 1999). The rate of reinfection is specific to certain species of helminths and depends on the life expectancy of that species (short-lived helminths reinfect more rapidly), on the intensity of transmission within a given community, and on the treatment efficacy and coverage. The basic reproductive rate (R_o)describes the transmission potential of a parasite (and thus its ability to reinfect the host). It defines the average number of female offspring produced during the life span of the parasite that survive to reproductive maturity in the absence of density dependence.R_o is determined by parasite immigration anddeath rates as well as by host density (and, in schistosomiasis, also snail density). A parasite will fail to become established unless R_o is greater than unity (Anderson and May 1991). Adult worms usually survive between one and four years, whereas eggs can sometimes remain viable for several more years in the environment. Therefore, reinfection rates will remain high until adults are removed with chemotherapy and until infective stages, through time, become uninfective. In reality, density-dependent processes regulate parasite populations; at endemic equilibrium, the effective reproductive ratio equals unity (that is, each female replaces herself). Control programs rely on reducing the effective reproductive ratio long enough for the parasite population to be driven to local elimination. Theoretically,R_o provides useful insights, and it is helpful to think of control programs attempting to break the transmission cycle by reducing to less than unity. Therefore,R_o estimates can be made about how long and how many rounds of chemotherapy are required to treat intestinal helminths. For example, A. lumbricoides with an of three and a life R_oexpectancy of one year will need to be treated annually with a drug that is 95 percent efficacious and with coverage of more than 91 percent of the population. Where R_o is five—that is,in areas where transmission is higher—treatment must be given more frequently than once a year (Anderson and May 1991).

The age-dependent patterns of infection prevalence are generally similar among the major helminth species, exhibiting a rise in childhood to a relatively stable asymptote in adulthood (figure 24.1). Maximum prevalence of A. lumbricoides and T. trichiura is usually attained before five years of age, and the maximum prevalence of hookworm and schistosome infections is usually attained in adolescence or in early adulthood. The nonlinear relationship between prevalence and intensity has the consequence that the observed age-prevalence profiles provide little indication of the underlying profiles of age intensity (age in relation to worm burden). Because intensity is linked to morbidity, the age-intensity profiles provide a clearer understanding of which populations are vulnerable to the different helminths (figure 24.1). For A. lumbricoides and T. trichiura infections, the age-intensity profiles are typically convex in form, with the highest intensities in children 5 to 15 years of age (Bundy 1995). For schistosomiasis, a convex pattern is also observed, with a similar peak but with a plateau in adolescents and young adults 15 to 29 years of age (Kabatereine and others 1999). In contrast, the age-intensity profile for hookworm exhibits considerable variation, although intensity typically increases with age until adulthood and then plateaus (Brooker, Bethony, and Hotez 2004). In East Asia it is also common to find the highest intensities among the elderly. However, more generally, children and young adults are at higher risk of both harboring higher levels of infection (thus greater levels of morbidity) and becoming reinfected more quickly. Both may occur at vital stages in a child's intellectual and physical development.

Figure 24.1

Age-associated Prevalence and Intensity Profiles of STH and Schistosome Infections: Typical Age Profiles of Prevalence and Intensity of STH Infections and Schistosomiasis

Burden of the Disease

The revised estimates in 2003 (de Silva and others 2003) use the methodology developed by Chan and others (1994) and build on recent applications of geographical information systems to derive updated atlases of helminth infections. To reflect recent changes in the epidemiology of infection, de Silva and others used data from only 1990 onward. These data confirm that STH infections are the most prevalent infections of humans and that a large proportion of the population in developing countries is at risk. Of the 187 million cases of schistosomiasis estimated to occur worldwide, most are caused by S. haematobium in Sub-Saharan Africa (table 24.1).

WHO (2002) estimates that 27,000 people die annually from STH infections and schistosomiasis (case fatality rate of 0.0014 percent). Many investigators, however, believe that this figure is an underestimate. Crompton (1999) estimated that 155,000 deaths annually occur from these infections (case fatality rate of 0.08 percent), whereas Van der Werf and others (2003), using the limited data available from Africa, estimated the schistosomiasis mortality alone at 280,000 per year (case fatality rate of 0.014 percent) because of nonfunctioning kidneys (from S. haematobium) and hematemesis (from S. mansoni). Therefore, the difference between estimates for helminth-associated mortality is more than 10-fold.

Because it is uncommon for STHs and schistosomes to kill their human host, citing mortality figures provides only a small window on their health impact. Instead, measurements of disease burden using disability-adjusted life years (DALYs) and similar tools portray a more accurate picture for helminthic disease burden. WHO estimates the global burden of disease from STH infections and schistosomiasis on the basis of the enormous number of infected individuals, together with an associated low disability weight (Van der Werf and others 2003). However, because an estimated 2 billion people are infected with STHs and schistosomes, even minor adjustments to the disability weights produce enormous variations in DALYs or other measurements of disease burden. This helps to explain why, for instance, in 1990 the disease burden for the STH infections and schistosomiasis was almost 18 million DALYs, whereas the 2001 estimate was only 4.7 million DALYs. In the intervening 11 years, the DALYs were as low as 2.6 million. Such disparities are substantial when one considers that the 1990 estimate ranks helminths close to major disease entities such as tuberculosis, measles, and malaria, whereas the lowest estimate during the 1990s ranks helminth infections on a par with gonorrhea, otitis media, and iodine deficiency. The Disease Control Priorities Project helminth working group has determined that the WHO global burden of disease estimates are low because they do not incorporate the full clinical spectrum of helminth-associated morbidity and chronic disability, including anemia, chronic pain, diarrhea, exercise intolerance, and undernutrition (King, Dickman, and Tisch 2005). However, for this chapter, the average disability weights estimated by WHO are used throughout. Some of the specific controversies are described below.

Cost-Effectiveness Analysis of Interventions

Classifying Interventions

The three major interventions are anthelmintic drug treatment, sanitation, and health education.

Anthelmintic Drug Treatment

Anthelmintic drug treatment ("deworming") is aimed at reducing morbidity by decreasing the worm burden. Repeated chemotherapy at regular intervals (periodic deworming) in high-risk groups can ensure that the levels of infection are kept below those associated with morbidity (figure 24.2) and will frequently result in immediate improvement in child health and development. Anthelmintic drug treatment can prevent the development of irreversible consequences of schistosomiasis in adulthood. For ascariasis and trichuriasis, for which intensity peaks among school-age children, frequent and periodic deworming may reduce transmission over time. Obstacles that diminish the effectiveness of periodic deworming are the low efficacy of single-dose mebendazole and albendazole for the treatment of hookworm and trichuriasis, respectively (Adams and others 2004; Albonico and others 1994); high rates of posttreatment reinfection for STHs in areas of high endemicity (Albonico and others 1995); and diminished efficacy with frequent and repeated use (Albonico and others 2003), possibly because of anthelmintic resistance (see the section "Research and Development").

Figure 24.2

Predicted Effect on Ascaris and Trichuris Prevalence following Frequent and Periodic Dewormings with Benzimidazole Anthelmintics

Improved Sanitation

Improved sanitation is aimed at controlling transmission by reducing soil and water contamina tion. Sanitation is the only definitive intervention to eliminate STH infections, but to be effective it should cover a high percentage of the population. Therefore, because of the high costs involved, implementing this strategy is difficult where resources are limited (Asaolu and Ofoezie 2003). Moreover, when used as the primary means of control, it can take years or even decades for sanitation to be effective (Brooker, Bethony, and Hotez 2004).

Health Education

Health education is aimed at reducing transmission and reinfection by encouraging healthy behaviors. For STH infections and schistosomiasis, the aim is to reduce contamination of soil and water by promoting the use of latrines and hygienic behavior. Without a change in defecation habits, periodic deworming cannot attain a stable reduction in transmission. Health education can be provided simply and economically and presents no contraindications or risks. Furthermore, its benefits go beyond the control of helminth infections. In this perspective, it is reasonable to include this component in all helminth control programs.

Other Control Measures

In specific epidemiological conditions, environmental or chemical control of snails can be useful tools for reducing the transmission of schistosomiasis. Research to develop new tools for control is in progress, including vaccine development programs for hookworm infection and schistosomiasis (see "Research and Development").

Choosing Interventions

Periodic deworming stands out as the most cost-effective means to reduce the morbidity of STH and schistosome infections.

Periodic Anthelmintic Therapy

Periodic anthelmintic therapy, or periodic deworming, represents the main measure in areas where infections are intensely transmitted, resources for disease control are limited, and funding for sanitation is lacking. Drug treatment can be administered in the community using different strategies:

• Universal treatment. The entire community is treated, irrespective of age, sex, infection status, and other characteristics.
• Targeted treatment. Treatment targets population groups, which may be defined by age, sex, or other social characteristics, irrespective of the infectious status.
• Selective treatment. Treatment targets individual-level application of anthelmintic drugs, which is selected on the basis of either diagnosis or a suspicion of current infection.

Recommended drugs for use in public health interventions to control STH infection are the benzimidazole anthelmintics (BZAs), albendazole (single dose: 400 mg, reduced to 200 mg for children between 12 and 24 months), or mebendazole (single dose: 500 mg), as well as levamisole or pyrantel pamoate (WHO 2002). Praziquantel (PZQ) (single dose: 40–60 mg/kg) is the major drug used for the treatment of schistosomiasis. However, therapy with oxamniquine has been the cornerstone for treatment of S. mansoni infection in South American national control programs over the past 20 years. The efficacy of oxamniquine and PZQ is comparable, although that of PZQ is slightly better. The BZAs and PZQ are inexpensive; they have undergone extensive safety testing and have been used by millions of individuals with only a few minor side effects. Drugs that do not need dosage according to weight, such as BZAs (in school-age children), are considered easier to use for population-based interventions; however, the use of proxy indicators—for example, substituting height for weight—has proved a successful implementation strategy for PZQ (Hall and others 1999).

Distribution Strategy and Frequency of Treatment

The selection of the distribution strategy and the frequency of treatment is based on epidemiological data. The recommended strategy for helminth control is a population-based approach, in which individuals in targeted communities are treated irrespective of their infection status (WHO 2002). This strategy is justified for several reasons, including the simplicity and safety of delivering treatment. Individual diagnosis is difficult and expensive and offers no safety benefit.

The intrinsic transmission potential of the parasite species determines the frequency of treatment (see "Epidemiology of STH Infections and Schistosomiasis," earlier in this chapter). To control morbidity in areas of intense transmission (prevalence greater than 70 percent and more than 10 percent of moderate-and heavy-intensity infection), WHO (2002) recommends treatment two or three times a year for STH infections. In areas with a lower intensity of transmission (prevalence between 40 and 60 percent and less than 10 percent of moderate- and heavy-intensity infection), intervention once a year is recommended (WHO 2002).

School-Age Children as a High-Risk Population

School-age children typically have the highest intensity of worm infection of any age group, and chronic infection negatively affects all aspects of children's health, nutrition, cognitive development, learning, and educational access and achievement (World Bank 2003). Regular deworming can cost-effectively reverse and prevent much of this morbidity. Furthermore, schools offer a readily available, extensive, and sustained infrastructure with a skilled workforce that is in close contact with the community. With support from the local health system, teachers can deliver the drugs safely. Teachers need only a few hours of training to understand the rationale for deworming and to learn how to give out the pills and keep a record of their distribution. School-based deworming also has major externalities for untreated children and the whole community. By reducing transmission in the community of Ascaris and Trichuris infections, deworming substantially improves the health and school participation of both treated and untreated children, both in treatment schools and in neighboring schools (Bundy and others 1990; Miguel and Kremers 2003).

These observations provided a basis for the adoption of resolution 54.19 at the 2001 World Health Assembly, which urged member states to ensure access to essential drugs for STH and schistosome infections in endemic areas for the treatment of clinical cases and groups at high risk for morbidity (box 24.1). To achieve this goal, WHO has developed a broad partnership that promotes the incorporation of deworming into existing institutions and programs, for both the education sectors and the health sectors. The Partnership for Parasite Control was launched in 2001 with the aim of mobilizing resources and promoting synergy among public and private efforts for the control of soil-transmitted helminths and schistosomiasis at global and national levels. School-based deworming has its full effect when delivered within an integrated school health program that includes elements of the Focusing Resources on Effective School Health (FRESH) framework.

Box 24.1

The 54th World Health Assembly. The 54th World Health Assembly, which met in May 2001, urged member states to ensure access to essential drugs for schistosomiasis and STH infections in endemic areas for the treatment of clinical cases and groups at high (more...)

Other At-Risk Populations

Not only school-age children can benefit from treatment. Preschool children (one to five years of age) are vulnerable to the developmental and behavioral deficits caused by iron deficiency anemia, and recent analyses by Brooker, Bethony, and Hotez (2004) indicate that hookworm is an important contributor to anemia in that age group (see "Estimating Intervention Effectiveness"). Women of reproductive age (15 to 49 years of age) are particularly susceptible to iron deficiency anemia because of iron loss during menstruation and because of increased needs during pregnancy (Bundy, Chan, and Savioli 1995). In certain circumstances, male worker populations can also be at increased risk (Guyatt 2000).

Intervention Costs

Several studies have evaluated the costs of school-based periodic deworming in several different settings, whereas comparable studies on other interventions are still lacking.

Periodic Deworming

The advantage of periodic deworming lies in its simplicity (one tablet per child) and safety. Teachers and other personnel without medical training can easily apply the simple measures, which can be incorporated without difficulty in existing health and nonhealth activities that reach the high-risk group. Several organizations, including nongovernmental organizations, include an STH and schistosome infection-control package within their routine activities and, with very limited budgets, relieve the burden of helminth infections in the population covered. The costs of albendazole and PZQ are available through the International Drug Price Indicator Guide (http://www.msh.org). Delivery systems for deworming have often depended on vertical programs, in which mobile teams visit schools or communities to carry out treatment (WHO 2002). Estimated costs for this approach are outlined in table 24.2. For STH infections in Tanzania, Nigeria, and Montserrat, the costs range from US$0.21 to US$0.51 per treatment. However, by training teachers and other school officials to administer anthelmintic drugs, the system could achieve low-cost delivery by "piggy-backing" on existing programs in the educational sector (WHO 2002). Specific examples of such programs conducted in Ghana and Tanzania are summarized in the section "Implementation of Control Strategies: Lessons of Experience," later in this chapter. It was found that delivery of school-based targeted anthelmintic treatment could cost as little as US$0.03 per child, which may be as low as one-tenth of the estimated costs for vertical delivery (WHO 2002). Thus, at current drug prices, the total cost (drug plus delivery) of a single treatment with albendazole or mebendazole may be as low as US$0.05, and that of a combined treatment with PZQ may be as low as US$0.25 per child (WHO 2002).

Table 24.2

Recent Examples of Delivery Costs for a Single Mass Treatment.

Integrating drug distribution through the school system rather than using mobile teams, along with a marked decline in the price of BZAs and PZQ, has resulted in a 10-fold reduction in delivery costs. However, those costs are artificially low because they do not include the external costs for the coordinating center responsible for supporting those approaches (Guyatt 2003). It has been estimated, for instance, that mass albendazole treatment of school-age children in Kenya could cost more than US$3 million each year, equivalent to some 4 percent of current national public expenditure on health care (Guyatt 2003). This analysis has not been evaluated against actual operations, however, and current estimates from the parasite control authorities in Kenya suggest that the actual cost is likely to be far less. Large-scale chemotherapy programs for helminth control continue to rely heavily on donor support, suggesting that some affected countries may be unable to support the costs of deworming.

Monitoring of control programs is an important part of the managerial process, and it should be carried out at minimum cost so as not to divert resources from the intervention (Brooker and others 2004). It is recommended that, at the planning stage, approximately 5 to 10 percent of the program budget be reserved for monitoring activities (Montresor and others 2002).

Improved Sanitation

When sanitation improvements are made alongside deworming, the results obtained last longer. However, the investment needed to reach the level required to interfere with STH transmission could be high. To correctly evaluate the advantage of such investments, one must take into account the consequences for other health indicators and for economic development. An efficient sanitation infrastructure removes the underlying cause of most poverty-related communicable diseases and can boost the economic development of a country. The resources needed to improve hygienic standards can be huge and require the cooperation of several sectors of society (Asaolu and Ofoezie 2003). Currently, these are qualitative judgments, and no cost-effectiveness analysis (CEA) estimates exist for sanitation in this context.

Health Education and Communication

Measures to increase the health awareness of the population are included as an essential component of any population-based activity aimed at controlling morbidity attributable to helminth infections. However, the effectiveness of those activities in reducing transmission of infection varies according to different reports. In some cases, health education can decrease costs, increase levels of knowledge, and decrease reinfection rates (Lansdown and others 2002). Health education efforts can build trust and engage communities, aspects that are crucial to the success of public health initiatives. No CEA estimates exist for health education in this context.

Linking Costs and Effects of Interventions

Interventions to reduce morbidity from helminth infections fall into two categories: targeting the transmission mechanisms and treating individuals directly. The former encompasses improvements in infrastructure, including water supply and sanitation, and health education. The latter entails the periodic drug treatment of the population. Substantial improvements through prevention may be a long-term outcome of economic growth in general, because wealthier households have improved sanitation facilities and practices, but those improvements are not an option in the short term without large investments in infrastructure. As shown in the previous section, deworming options dominate on both effectiveness and cost-effectiveness criteria. Costs continue to fall as drug costs decrease. With better data and detailed mapping of disease distribution within communities, targeting individuals at high risk becomes more feasible, thus improving the cost-effectiveness of control programs (Michaud, Gordon, and Reich 2003).

Evidence from existing programs that narrow the intervention to school-age children (a high-risk group) shows that the treatment costs of chemotherapy for helminth infections are quite low—well below US$1 per school-age child. This finding is in part due to the accessibility of the target group and the cost savings of incorporating delivery into existing school and health programs. Moreover, as discussed in the following sections, the economic benefits of targeting this group may be substantial. Still other targeted groups may also have low cost per treatment when treatment is merged into existing programs. For example, interventions through prenatal care programs for pregnant women may be cost-effective. Likewise, evidence on costs of treatment through existing integrated management of infant and childhood illness (IMCI) programs for small children and health campaigns (such as vaccination and micronutrient programs) find low cost per case treated (Montresor and others 2002).

Several factors can potentially alter the ranking of interventions in regard to cost-effectiveness, although there are no existing studies to evaluate this. Previous analysis may underestimate the effectiveness and overestimate the cost-benefit ratios of mass treatment of school-age children if the externalities of treatment are not considered (Miguel and Kremer 2003). The cost-effectiveness of school-based deworming programs will change as the programs are extended to cover children who are not enrolled in school. Such program extensions are likely to have greater costs because they entail additional staff and outreach efforts per case treated. However, the effectiveness of mass treatment of school-age children (both enrolled and not enrolled) may be greater. Children who are not enrolled in school come from households with lower income levels. Lower income, which leads to poorer sanitation conditions, is associated with greater incidence and intensity of infections. Expanding mass treatment to children not enrolled in school will result in treating populations that have higher incidence and intensity, thus raising effectiveness (box 24.2).

Box 24.2

The High Cost-Effectiveness of Mass Treatment for Helminth Infection. The combination of low-cost treatment and high prevalence rates suggests that the cost per DALY averted from treating helminth infections will be quite low. Following the consistent (more...)

Averted, Avertable, and Nonavertable Burden

In the short run, deworming can avert helminth infections. In the long run, it is assumed that as income levels grow and infrastructure improves, the number of infections averted by reducing transmission will increase. However, given the slow rate of poverty reduction in the 1990s for the poorest regions, such as Sub-Saharan Africa, waiting for economic development to lead to a reduction in infections is only, at best, a slow-paced solution for the majority of the infected population. It is more likely that most averted infections will depend on periodic deworming. Thus, the question remains as to what portion of existing infections is potentially avertable through recommended interventions and what portion is currently averted with existing programs. For schistosomiasis, successful programs in several countries, including Brazil, China, and the Arab Republic of Egypt, and the issues related to the sustainability of these successes have been described (see "Implementation of Control Strategies: Lessons of Experience" later in this chapter). However, the number of averted schistosomiasis infections in Sub-Saharan Africa is likely to be small, because few serious attempts at widespread control have been made in recent years, and not much of the burden of STH and schistosome infections is currently averted through private treatment. In part, the low number of averted infections may be due to the lack of information on the part of infected individuals, the insidious nature of the condition, and the lack of drugs in the public or private health delivery system.

Economic Benefits of Intervention

The characteristics of helminth infections make a compelling case for public sector intervention if based only on the evidence related to the intervention's effect on health. From an economic perspective, the public sector has several reasons to become involved in improving health outcomes. First, other benefits may be gained, in addition to the benefit for the treated individual. Second, some forms of intervention are almost pure public goods; that is, no one can be excluded from using the goods or services the interventions deliver, and the private sector is thus unlikely to deliver them. Finally, preventive measures, such as information on the value of washing hands,may not be delivered through the private sector. The lack of knowledge about infections and subclinical symptoms may make individuals less likely to seek treatment. In analyzing the gains of interventions for worm control, one should account for the burden of helminth infections, which extends well beyond the health impacts and DALYs. The economic implications may be quite large.

The negative correlation between helminth infections and income level is clearly demonstrated both within and between countries (de Silva and others 2003). However, causality cannot be inferred from this established relationship; poverty promotes higher worm burdens, yet poor health induced by helminths can lead to lower income. There may also be opportunity costs to uninfected household members residing with infected persons. Few studies have been designed to evaluate, either directly or indirectly, the magnitude of the effect of deworming on economic productivity. The indirect evidence at the micro level suggests that helminth infection has a significant impact on adult productivity and, subsequently, on earnings. More direct evidence for children shows that helminth infection has long-term implications for educational attainment and economic status.

Studies are increasingly documenting a causal impact of adult health (broadly defined) on labor force participation, wages, and productivity in developing countries (Thomas and Strauss 1997). Moreover, helminth infection is known to affect some of the health conditions related to productivity—namely, iron deficiency anemia and wasting. Guyatt (2000) reviews numerous studies relating these conditions to physical fitness and productivity; Haas and Brownlie (2001) review studies on the effect of iron supplementation on work. The studies generally show productivity gains linked to better health along the various health dimensions studied. However, although some evidence points to the indirect impact of STHs on income earnings, these relationships have not been adequately studied, either directly or indirectly.

More compelling links between helminth infection and economic well-being may exist for children. The strong association between worm burden and poor health outcomes for children suggests that infections may affect school enrollment, attendance, grade repetition, and grade attainment. In turn, the potential impact on educational outcomes has implications for the assessment of the economic benefits of intervention. Numerous studies have demonstrated the benefits of schooling, showing that the return on education is quite high. Increased education is associated with, among other things, higher worker productivity and generally higher productivity in nonmarket production activities, including greater farmer efficiency and productivity (Psacharopoulos and Patrinos 2002).

Although observational studies show that lower levels of learning and schooling are linked to helminth infection (World Bank 2003), establishing a causal relationship requires adequately controlling for all unobserved or confounding factors. Miguel and Kremer (2003) note that several methodological issues hamper many existing randomized treatment-control evaluations. First, externalities associated with interventions can lead to underestimating impacts among the untreated population. Second, sample selection and attrition issues can affect the validity of findings, although the direction of this effect is ambiguous. Third, existing studies typically evaluate the impact of deworming on cognitive skills, likely the culmination of several years of health and education investments, as assessed by tests administered to treated and untreated children. Although studies find an effect on cognitive skills for those with the heaviest worm burden, they do not focus on other important education outcomes, which are likely to be more affected in the short run by health improvements, such as school enrollment and school attendance.

The study by Miguel and Kremer (2003) in Kenya attempts to address those shortcomings through improved study design and analytical methods. In addition to providing health gains, deworming reduced total primary school absenteeism by at least one-quarter in the first two years of the project. The gains were largest for the youngest children, who suffered from more intense worm infections. Externalities would cause a substantial underestimation of this effect. In terms of cost-effectiveness as an educational intervention, deworming proved to be far more effective at improving school attendance than other educational interventions implemented in a study in Kenya. Deworming offers a high rate of return, increasing the net present value of discounted wages by more than US$30 per treated child compared with per treatment costs of under US$1. For realistic estimates of returns to schooling, these results show in general that the net present discounted value of lifetime earnings is high compared with the costs of treatment even for small gains in school participation (figure 24.3).

Figure 24.3

Returns to School Participation

Bleakley (2003) examined the effect of a hookworm control program undertaken about 1910 in the southern part of the United States. Hookworm infection was estimated to cause a 23 percent drop in the probability of school attendance, and children with greater exposure to the hookworm eradication campaign were more likely to be literate. Moreover, the long-term follow-up of affected cohorts showed that hookworm infection in childhood led to significantly lower wages in adulthood.

Helminth infections in preschool-age children can have consequences for subsequent schooling, such as delaying primary school enrollment and school attainment, thereby affecting future labor market outcomes. Bobonis, Miguel, and Sharma (2003) conducted a study of preschool-age children, using iron supplementation and deworming drugs administered to children two to six years of age. Preliminary results indicate that, in addition to the weight gain associated with treatment, average preschool participation rates increased sharply by 6.3 percentage points among assisted children older than two, reducing preschool absenteeism by roughly one-fifth.

Beyond the current impacts on schooling and implications for cognition, helminth infection in children can have long-term implications for economic outcomes in adulthood through its effect on physical growth. Height has been shown to affect wage-earning capacity as well as participation in the labor force for men and women (Thomas and Strauss 1997). This relationship may be strongest in settings where infection rates are highest—that is, low-income areas, where physical endurance yields high returns in the labor market.

Implementation of Control Strategies: Lessons of Experience

Two case studies illustrate the profound health effects of periodic deworming.

Research and Development

Among the important tasks to be done to control helminth infections are collection of better data on helminth disease burden, research on the health and economic effects (and safety) of periodic deworming, monitoring of the emergence of anthelmintic drug resistance, and development of new tools to supplement or complement existing control strategies.

Conclusions: Promises and Pitfalls

Fulfilling the mandate of World Health Assembly resolution 54.19 will require the regular treatment of hundreds of millions of children over decades. The obstacles in this undertaking are formidable, and success will depend on the ability of countries to identify or create reliable and sustained infrastructures for this purpose. A focus on using preexisting school systems may be key to achieving this goal. The treatment of schoolchildren for A. lumbricoides, T. trichiura, and schistosome infections achieves large externalities that reduce infection in other vulnerable age groups. However, the different epidemiology of hookworm raises concerns about the risks to preschool children and women of reproductive age who remain untreated. Providing regular treatment to these populations appears to be a less cost-effective option, largely because of the absence of a preexisting infrastructure. This situation presents a strong argument for developing a hookworm vaccine that could be used to protect these vulnerable groups. It has yet to be seen whether the emergence of BZA drug resistance is a genuine concern that could derail global deworming efforts in much the same way that resistance to DDT and chloroquine has affected the ambitions for global malaria control. It is possible that the specific dynamics of helminth populations will provide sufficient genetic flow to maintain susceptibility in much the same way that insecticides remain the effective staple of global agribusiness. Until new technologies become available, anthelmintic chemotherapy for school-age children remains the most practical and substantive means to control STH and schistosome infections in the developing world.

References

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