In an editorial published in PLOS Neglected Tropical Diseases in August 2009, Peter
Hotez [1] wrote:
“Given the extremely modest costs, the rapid health impact, and the resulting high
rates of economic return, we cannot afford further delays in implementing large-scale
NTD [neglected tropical disease] control measures.”
Our report, which describes success in preventing soil-transmitted helminth (STH)
infections in Chinese schoolchildren through the use of a health education package
that includes a 12-minute cartoon, “The Magic Glasses,” may thus prove timely. The
results from the cluster randomized intervention trial, conducted in 38 rural Chinese
schools and involving 1,718 children, showed that the video-based health education
package had 50% efficacy in preventing new STH infections after treatment [2]. This
study established proof of principle that health education can indeed increase knowledge
and change behavior, resulting in fewer intestinal worm infections. However, we have
a ways to go before we can show broad application, and we appreciate that these findings
will require further validation in other epidemiological and cultural settings.
With a third of the world's population infected [3], STHs are the most widespread
and disabling chronic infections globally and the most common of the neglected tropical
diseases (NTDs). The most recent estimate (2010) of the worldwide burden of infection
with STHs is 5.2 million disability-adjusted life years (DALYs) [4]. Children have
the greatest risk of morbidity due to STHs [5], which have a particularly debilitating
effect on their health and cognitive development, causing anemia, malnutrition, stunted
growth, and learning delays [3]. Almost half of the global disease burden due to these
worm infections is borne by children 5 to 14 years of age [5]. A recent study has
shown that this age group can contribute up to 50% of the Ascaris lumbricoides burden
in the community [6].
In 2012, the announcement of the World Health Organization (WHO) roadmap [7] galvanized
public and private support in the fight against the NTDs. Major pharmaceutical companies;
the Bill & Melinda Gates Foundation; the governments of the United States, United
Kingdom, and United Arab Emirates; and the World Bank have announced substantial funding
to accelerate the control, elimination, and possibly the eradication of the NTDs.
Measures mainly include sustaining or expanding current mass drug administration (MDA)
programs to meet the United Nations (UN) Millennium Development Goals by 2020 and
promoting research and development of new drugs and drug targets by sharing expertise
and compounds. All partners endorsed the “London Declaration on Neglected Tropical
Diseases,” through which they pledged new levels of collaborative effort and tracking
of progress in tackling ten of the 17 NTDs currently on WHO's list [8]. The WHO strategy
for STH control is to treat all preschool- and school-age children and women of childbearing
age living in endemic areas. Treatment frequency depends on the STH prevalence in
a particular community. When the prevalence of intestinal worm infection exceeds 20%,
mass treatment should be given to major risk groups once a year; two treatments per
year are recommended when the prevalence is greater than 50%. In addition to MDA,
WHO recommends health education and the provision of clean water and adequate sanitation
to reduce reinfection [9].
Significant progress has been made in controlling STH infections over the past 10
years, with over 300 million preschool-age and school-age children dewormed in 2011
(representing 30% of all children in the world at risk of STH infection due to living
in endemic areas) [10]. However, the UN Millennium Development Goal of treating 75%
of school-age children at risk of STH infection by 2010 was not achieved. In the WHO
roadmap to overcome the global impact of NTDs, released in January 2012, the goal
for STH was reset to 75% treatment coverage for children in endemic areas by 2020
[7]. Even if this ambitious goal is achieved by 2020, concerns regarding the effectiveness
and sustainability of MDA remain. The efficacy of the available drugs, albendazole
and mebendazole, is high for A. lumbricoides, moderate to high for hookworm, but low
for Trichuris trichiura
[11]–[13]. For the last 20 years, rapid reinfection rates after treatment cessation
have been reported repeatedly for intestinal helminths [14]. For example, in a high-prevalence
setting in Pemba Island, Tanzania, in 1995, pretreatment infection levels were reached
only 6 months after treatment was stopped [15]. In another, more recent study from
Sri Lanka, even after 10 years of mass chemotherapy, the STH prevalence rebounded
to pretreatment levels after MDA was terminated [16].
There is also growing concern about the potential development of parasite resistance
to albendazole and other anthelminthics as a result of continued treatment pressure
[13]. It is considered inevitable that drug resistance will develop in human nematodes,
given the many examples of drug-resistant nematode species infecting sheep and other
livestock due to extensive drug use [17]–[19]. Furthermore, community enthusiasm for
MDA often wanes, especially when the community is not engaged in the program [20].
This can result in poor compliance and donor fatigue in areas where treatment needs
to be repeated regularly [21]–[25]. In addition, maintaining a supply of anthelminthic
drugs in remote areas can be difficult, and this may distract from other priorities
in resource-poor areas, weakening the local health care system [26].
The benefit of MDA has been intensely debated after the recent publication of a second
edition of a Cochrane review by Taylor-Robinson and colleagues in 2012, which summarized
the effects of deworming on nutritional indicators, hemoglobin, and school performance
in 42 randomized controlled trials (RCTs) comprising a total of 65,000 participants
[27]. The review concluded that there is insufficient reliable information to determine
whether deworming has an effect on nutritional indicators, hemoglobin, and school
performance and, hence, the justification for programs consisting of only deworming
is questionable [27]. Whether this perceived limited benefit of MDA is due to lack
of sustainability, poor compliance, variable efficacy of the deworming drugs used
in mass treatment programs, or a combination thereof was not discussed in the review,
and these issues require addressing in the future. The report has stimulated intense
debate within the NTD community, although its methods of analysis and study selection
criteria have been criticized by MDA advocates. This debate is ongoing and being continually
updated in a PLOS Medicine blog that can be visited at http://blogs.plos.org/speakingofmedicine/2012/07/18/should-deworming-policies-in-the-developing-world-be-reconsidered.
Taking all this information into account, interventions preventing STH reinfection,
such as improvements in hygiene through health education, are urgently required to
augment the effect of chemotherapy as part of an integrated multicomponent approach
to control. Chemotherapy temporarily reduces morbidity and infection prevalence, whereas
preventive interventions, such as health education or improved sanitation, prevent
reinfection, thereby reducing incidence. In the long term, a combination of the two
approaches will lead to a reduction in the number of treatment cycles required for
effective control, thereby reducing the treatment pressure and resulting in a more
sustainable approach to control [20], [28].
China is in an ideal position to undertake an integrated public health strategy that
combines MDA with health education and improved water, sanitation, and hygiene (WASH)
for the control of STHs. It has already successfully pioneered multicomponent integrated
control strategies, which include health education, for other NTDs such as lymphatic
filariasis [29] and schistosomiasis [30], [31]. Due to the intense economic development,
improved sanitation, and raised living standards, STH prevalence has decreased considerably
in eastern China, whereas endemic hot spots remain in remote rural areas of Yunnan,
Sichuan, and Guizhou provinces [32]. Worldwide, China's economic and political influence
is increasing rapidly, and expectations have already been raised for China to take
the lead in transferring its NTD control and elimination know-how and to provide support
for NTD control in sub-Saharan Africa [33].
We concur with others [34], [35] that the only way to achieve sustainable control
of STH infections and, more generally, to achieve the UN Millennium Development Goals
is through integrated control efforts in a multicomponent strategy, including chemotherapy,
improved WASH, and health education, that addresses the social and ecological causes
of STH, and not stand-alone treatment-based control of a number of different NTDs.
Treatment-based control, or targeting multiple diseases with one MDA program, is also
often referred to as integrated control [36], [37] but is not to be confused with
the multicomponent integrated control strategy as described above and by Utzinger
and colleagues [35]. The need for health education and additional public health measures,
including novel, effective, and easy-to-use educational control tools, has repeatedly
been advanced [35], [37]–[44]. The literature indicates that strategies involving
health education inducing behavior change have been poorly implemented in practice
[45], and evidence-based control strategies that address the social, cultural, and
behavioral dimensions of disease are urgently required [45]. Furthermore, their cost
effectiveness and the cost per DALY averted need to be determined. The effective video-based
educational package we have developed and tested [2] complements the current strategy
for the control of STHs as advocated by the WHO. With culturally sensitive adaptation
and appropriate resourcing, this tool has the potential to be incorporated into current
ongoing deworming programs, not only in China [46] and other parts of Southeast Asia
but also in sub-Saharan Africa, with implications for the future control of STHs globally.