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A call to strengthen the global strategy against and soil-transmitted : the time is now

Nathan C Lo, David G Addiss, Peter J Hotez, Charles H King, J Russell Stothard, Darin S Evans, Daniel G Colley, William Lin, Jean T Coulibaly, Amaya L Bustinduy, Giovanna Raso, Eran Bendavid, Isaac I Bogoch, Alan Fenwick, Lorenzo Savioli, David Molyneux, Jürg Utzinger, Jason R Andrews Lancet Infect Dis 2016 In 2001, the World Health Assembly (WHA) passed the landmark WHA 54.19 resolution for global scale-up of mass Published Online administration of drugs for morbidity control of schistosomiasis and soil-transmitted helminthiasis, which November 29, 2016 affect more than 1·5 billion of the world’s poorest people. Since then, more than a decade of research and experience has http://dx.doi.org/10.1016/ S1473-3099(16)30535-7 yielded crucial knowledge on the control and elimination of these helminthiases. However, the global strategy has Division of Infectious remained largely unchanged since the original 2001 WHA resolution and associated WHO guidelines on preventive and Geographic Medicine chemotherapy. In this Personal View, we highlight recent advances that, taken together, support a call to revise the global (N C Lo BS, J R Andrews MD), strategy and guidelines for preventive chemotherapy and complementary interventions against schistosomiasis and soil- and Division of Epidemiology, transmitted helminthiasis. These advances include the development of guidance that is specific to goals of morbidity Stanford University School of Medicine, Stanford, CA, USA control and elimination of transmission. We quantify the result of forgoing this opportunity by computing the yearly (N C Lo); Children Without burden, mortality, and lost economic productivity associated with maintaining the status quo. Without change, , Task Force for Global we estimate that the population of sub-Saharan Africa will probably lose 2·3 million disability-adjusted life-years and Health, Decatur, GA, USA US$3·5 billion of economic productivity every year, which is comparable to recent acute epidemics, including the (D G Addiss MD); Sabin Institute and Texas Children’s 2014 Ebola and 2015 Zika epidemics. We propose that the time is now to strengthen the global strategy to address the Hospital Center for Vaccine substantial disease burden of schistosomiasis and soil-transmitted helminthiasis. Development, National School of at Baylor Introduction people using (against schistosomiasis) and College of Medicine, Houston, TX, USA (Prof P J Hotez MD); More than 15 years ago, the World Health Assembly 565 million people using or Department of Biology, Baylor (WHA) passed the landmark WHA 54.19 resolution to (against soil-transmitted helminthiasis) throughout Africa, University, Waco, TX, USA address the 1·5 billion people affected by schistosomiasis Asia, Latin America, and the .5,6 During this (Prof P J Hotez); James A Baker and soil-transmitted helminthiasis (including , period, the number of and global disease burden III Institute for Public Policy, Rice University, Houston, TX, 1,2 1,2,7 disease, and ). WHO sub­ estimates have been correspondingly reduced. This USA (Prof P J Hotez); Center for sequently created a Department of Neglected Tropical strategy of morbidity control has defined a goal of and Diseases, Diseases (NTDs), and produced guidelines that set a new eliminating helminths as a public health problem. For soil- Case Western Reserve framework for a public health approach against many transmitted helminthiasis, this goal is defined as less than University, Cleveland, OH, USA (Prof C H King MD); NTDs, including schistosomiasis and soil-transmitted 1% prevalence of moderate-to-heavy intensity in Department of Parasitology, helminthiasis, through a strategy of preventive chemo­ at-risk populations, as determined by egg counts on Liverpool School of Tropical therapy (via ).­ 3 This strategy microscopic examination; for schistosomiasis, the goal has Medicine, Liverpool, UK involves large-scale, periodic (eg, yearly) empirical been expressed as less than 1% prevalence of heavy- (Prof J R Stothard PhD, Prof D Molyneux DSc); treatment of entire populations and typically focuses on intensity infections based on egg counts in stools or urine. United States Agency for groups assumed to have the greatest disease morbidity, Although this commendable morbidity control International Development, such as school-aged children (aged 5–15 years) for strategy has certainly led to success, mainly by averting Global Health, Washington, DC, USA (D S Evans DPH); schistosomiasis and preschool and school-aged children long-term sequelae in school-aged children, the Center for Tropical and 3,4 8,9 (aged 1–15 years) for soil-transmitted helminthiasis. reinfection rate has been high in most settings. Emerging Global Diseases and These helminthiases are characterised by mostly chronic, Unfortunately, even countries that have successfully the Department of often insidious helminth-specific sequelae ranging from implemented the recommended preventive chemo­ Microbiology, University of Georgia, Athens, GA, USA mild to severe morbidities. These sequelae include therapy strategy for schistosomiasis and soil-transmitted (Prof D G Colley PhD); Global anaemia, chronic , and , and helminthiasis—ie, WHO recommends repeated Public Health, Johnson & also more rare and serious complications including treatment of school-aged children with at least Johnson, New Brunswick, NJ, , ,­ and death for 75% coverage—have met challenges in achieving USA (W Lin PhD); Unité de Formation et de Recherche schistosomiasis, and small and rectal optimal morbidity control or the more ambitious goal of Biosciences, Université Félix 8,10,11 prolapse for soil-transmitted helminthiasis. transmission elimination. This finding is consistent Houphouët-Boigny, Abidjan, Today, under the auspices of the WHO Department of with estimates by the Global Burden of Disease (GBD) Côte d’Ivoire NTDs—catalysed by the 2012 London Declaration for study12 and others5 that have documented how progress (J T Coulibaly PhD); Centre Suisse de Recherches NTDs, and with large-scale support from governments, has lagged behind for schistosomiasis and soil- Scientifiques en Côte d’Ivoire, pharmaceutical companies, and non-governmental transmitted helminthiasis relative to many other NTDs. Abidjan, Côte d’Ivoire organisations (NGOs)—preventive chemotherapy pro­ To address this challenge, in light of the past decade (J T Coulibaly); Swiss Tropical grammes have achieved impressive gains. In 2015 alone, of data and experience from the field, we re-visit and Public Health Institute, Basel, Switzerland these programmes delivered treatment to 65 million the global strategy for preventive chemotherapy and www.thelancet.com/infection Published online November 29, 2016 http://dx.doi.org/10.1016/S1473-3099(16)30535-7 1 Personal View

studies.16 Furthermore, expanded community-wide Strength of evidence treatment can be highly cost-effective because of this Step 1: Update strategy for preventive chemotherapy averted morbidity, even if transmission is not Expanded treatment across broader age groups Modelling and cost-effectiveness studies,10,13–15 with eliminated.10,14 To achieve community-wide coverage, (ie, community-wide treatment) support from systematic review and meta-analysis of settings could use distribution networks from other observational studies16 community-based health platforms for feasibility and 14 Lower prevalence thresholds for treatment, Modelling and cost-effectiveness studies, with cost-efficiency, including integration with especially for schistosomiasis support from observational studies programmes, Demographic and Health Surveys (DHS), Formal guidelines for integration of praziquantel Cost-effectiveness modelling studies, with support and programming from feasibility studies10,14,17,18 or through continued use of lymphatic or drug distributors who have delivered Validated strategy with trial data Trials underway community-wide (eg, and 19 Rigorous monitoring and evaluation strategies to Statistical models with field validation 33,34 detect emergence of drug resistance albendazole) at scale. Guidelines currently provide prevalence thresholds, Step 2: Incorporate complementary interventions in the global strategy above which a preventive chemotherapy strategy is Water, , and programming Systematic review and meta-analysis with mixed (eg, community-led total sanitation) findings, including mostly observational studies20–28 recommended, but these guidelines might be too restrictive to achieve optimal averted disability and cost- Information, education, and communication Trial data26 14 programmes effectiveness even under a goal of morbidity control. control (for spp) Systematic review and meta-analysis, including These prevalence thresholds are based on expert opinion mostly observational studies; modelling studies29,30 and a historically more limited drug supply, and have 3,4 Step 3: Create distinct guidelines based on epidemiology, programmatic goals, and resource constraints remained largely unchanged for more than a decade. Guidelines for a goal of morbidity control Expert opinion Although these thresholds have guided efforts in vs elimination of transmission preventive chemotherapy, analysis of new data suggests they can be improved by considering transmission Table 1: Key steps for strengthening of the global strategy for schistosomiasis and soil-transmitted 10,14 helminthiasis dynamics and health economics. A study that rigorously assessed these prevalence thresholds found them to often be too restrictive on the basis of morbidity control (J T Coulibaly, G Raso PhD, complementary interventions against schistosomiasis (measured in disability-adjusted life-years [DALYs]) and Prof J Utzinger PhD); University and soil-transmitted helminthiasis. cost-effectiveness, especially for schistosomiasis.14 For of Basel, Basel, Switzerland (J T Coulibaly, G Raso, example, annual school-based treatment of schisto­ Prof J Utzinger); Clinical Preventive chemotherapy somiasis was cost-effective at 5% prevalence rather than Research Department, London As the post-2020 agenda for NTDs is considered, interest the currently recommended 50% prevalence, and new School of Hygiene & Tropical is growing in improving the morbidity control strategy, prevalence thresholds were defined for community-wide Medicine, London, UK 14 (A L Bustinduy MD); Division of and when appropriate, shifting towards a more ambitious coverage for both sets of helminthiases. General Medical Disciplines, goal of elimination of transmission, which is defined Although expanded treatment would have great (E Bendavid MD), and Center for as interruption of transmission. The critical, policy- potential to avert disease morbidity, reduce overall Health Policy and the Center relevant question to be asked is how we can use new reinfection, and prevent chronic sequelae in young for Primary Care and Outcomes Research, Stanford University, evidence to strengthen current strategies and guidelines children, the potential emergence of drug resistance from Stanford, CA, USA (E Bendavid); for preventive chemotherapy to achieve these goals increased treatment pressure is a concern. Therefore, Department of Medicine, (table 1). The current strategy of morbidity control rigorous methods to monitor drug efficacy will be University of Toronto, Toronto, emphasises treatment of school-aged children alone essential, although community-wide treatment at ON, Canada (I I Bogoch MD); Division of Internal Medicine (with extension to preschool-aged children for soil- 75% coverage still falls under the best practices according and Infectious Diseases, transmitted helminthiasis); however, adolescents and to conservative estimates from veterinary literature.35 This Toronto General Hospital, adults (15 years and older, including pregnant women) concern can further be addressed by a longer-term but University Health Network, and younger children (<5 years) in the case of schisto­ necessary research and development agenda to create Toronto, ON, Canada (I I Bogoch); Schistosomiasis somiasis, are often infected and are not sufficiently improved drug regimens with greater efficacies against Control Initiative, Imperial addressed in exisiting global strategy or in parasitological schistosomiasis and soil-transmitted helminthiasis College London, London, UK monitoring.3,4,31 If left untreated, these groups can (particularly trichuriasis), for which drug efficacy might (Prof A Fenwick PhD); and serve as a hidden reservoir and potential source of be lower than expected, or even anthelmintic to Global Schistosomiasis 36–38 Alliance, Chavannes de Bogis, reinfection for all age groups. Modelling studies prevent reinfection. New diagnostics for helminths Switzerland (L Savioli MD) indicate that expanding treatment from school-aged (eg, point-of-care circulating cathodic antigen urine Correspondence to: children alone to entire communities could substantially cassette test for ) can also be applied Nathan C Lo, Stanford University reduce reinfection across all age groups, and avert to guide new treatment thresholds.39 School of Medicine, Division of accumulated morbidity in these populations, especially Re-examination of the preventive chemotherapy Infectious Diseases and Geographic Medicine, schistosomiasis-related chronic sequelae in preschool- strategy should also consider evidence from the Cochrane 300 Pasteur Drive, Lane L-134, aged children.10,13,29,31,32 The relative advantage of comm­ Collaboration40 and Campbell Collaboration41 systematic Stanford, CA 94305, USA unity-based treatment has been further supported by a reviews and meta-analyses of trial data that suggest [email protected] systematic review and meta-analysis of observational limited benefit of school-based preventive chemotherapy

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for soil-transmitted helminth­iasis, although such evidence for the association between various components findings should be considered within the limitations of of WASH (including improved water, sanitation, and the data and substantial debate surrounding potential hygiene and health behaviour) and helminth prevalence methodological challenges ().42–44 For example, and mean intensity.21–25 However, experimental evidence See Online for appendix studies might be underpowered­ to detect a meaningful from trials implementing WASH interventions is effect and relevant health outcomes might not be realised mixed, and studies are ongoing to validate the data within the short timeframe of most trials. Furthermore, from observational studies.23,25–28 Nonetheless, these children could have high rates of reinfection in school- programmes are likely to have substantial spillover based programmes that limit improvements to health, benefit by reducing the incidence of other infectious but this could be overcome with community-wide diseases improving country-level cost-effectiveness.25 treatment strategies.10,16,32 The importance of snail control in schistosomiasis The updated global strategy for preventive chemo­ control and elimination has been supported by a meta- therapy should increase attention to country-level analysis,29 empirical analyses of historical data,30 and coordination of integrated programmatic delivery (ie, modelling studies.46 The inclusion of multiple means of giving multiple medicines in the same programme) that snail control within a coordinated strategy alongside would yield substantial cost-savings and biological preventive chemotherapy for schistosomiasis is an synergies within the constraints of proven feasibility.10,14,17,18 important step forward to eliminate transmission in low Although integrated preventive chemotherapy guide­ endemicity settings and also to control disease morbidity lines do exist, improving country-level coordination of in high endemicity settings. these programmes would benefit cost-efficiency.14,45 The prevalence threshold itself is lower for adding another Guidelines for morbidity control versus medicine in addition to an existing treatment elimination of transmission programme compared with a standalone programme Distinct programmatic guidance is urgently needed that due to reduced delivery cost, and because the majority of is specific to the different goals of morbidity control or cost is from delivery and not the drugs themselves.10,17 elimination of transmission, and is informed by the For example, programmatic delivery of praziquantel setting’s local helminthiases epidemiology and health should include albendazole or meben­dazole, as done by priorities of the country. Decisions about strategy should the Schistosomiasis Control Initiative, because soil- further be made on a sub-national basis with transmitted helminthiasis is most often co-endemic and consideration of the focal nature of schistosomiasis. co-administration is safe.18 The integration of these Disease burden differs considerably among settings, and programmes should work within the constraints of the elimination of transmission might not be possible in all drug supply and the relevant ecological zone locations with existing tools and resources. High-burden (eg, national, sub-national, community) to address the settings could set a near-term goal of morbidity control, focal nature of schistosomiasis, which is in contrast with while low-burden settings could target elimination of the more homogeneous nature of soil-transmitted transmission. In all cases, settings should first aim to helminthiasis. achieve effective morbidity control before expanding to a goal of elimination of transmission. Complementary interventions To achieve these goals, settings targeting the goal of The global strategy should include water, sanitation, and morbidity control should focus on ensuring high drug hygiene (WASH) interventions, information, education, coverage in all risk groups, including preschool-aged and communication (IEC) programmes, and focal snail children and adults. By contrast, settings with low control (for schistosomiasis), especially when elimination prevalence might set a goal of eliminating transmission of transmission is the goal. Coordinated guidelines are and could prioritise non-drug interventions such as needed that define the conditions (eg, prevalence WASH programming, snail control, and intensive threshold, programmatic goals) where each complemen­ surveillance.47 In all cases, the country’s goals and tary intervention should be implemented alongside resource constraints will inform this choice, and preventive chemotherapy within the broad framework of distinct strategic recommendations should be available local health needs. While WASH programming, IEC, to reflect these different scenarios. Programmatic goals and snail control are not the focus of current global should be established with full country ownership of efforts, growing evidence supports the need for greater these programmes, especially in regions with an inclusion within the updated strategy, especially where improving economy and health systems. In developed disease dynamics are recalcitrant to preventive countries, particular attention should be given to “blue chemotherapy alone or elimination of transmission is marble health”, which recognises that the sizable the goal. proportion of the global burden of helminthiasis that Implementation of the WHO WASH–NTD global occurs in the poorer populations of wealthy countries strategy will probably be essential to eliminate will require distinct strategies and political support transmission.20 Observational studies have provided structures.48 www.thelancet.com/infection Published online November 29, 2016 http://dx.doi.org/10.1016/S1473-3099(16)30535-7 3 Personal View

Disease burden Mortality Economic losses* Avertable Avertable mortality Avertable (DALYs) (DALYs) (2015 US$, disease burden (DALYs)† economic losses* thousands) (DALYs)† (2015 US$, thousands)† No treatment 4 156 306 176 393 6 482 613 2 481 755 87 516 3 766 679 Current global strategy‡ 3 957 325 176 392 6 182 450 2 282 774 87 515 3 466 516 Idealised WHO guidelines§ 3 474 731 159 921 5 462 829 1 800 180 71 044 2 746 895 Cost-effective guidelines14 1 674 551 88 877 2 715 934 Ref Ref Ref

DALYs=disability-adjusted life-years. *Economic losses are estimated as the product of disability (DALYs) and country GDP per capita (appendix). †Cost-effective guidelines14 relative to each strategy. ‡Estimation based on WHO guidelines with current global coverage for preventive chemotherapy. §Estimation based on WHO guidelines with 75% coverage and uses school-based preventive chemotherapy programmes, except for inclusion of preschool-aged children in soil-transmitted helminthiasis treatment. Results are annualised over a 5-year simulation and are intended to give a broad estimate of the magnitude of avertable health and economic loss. Methodological details, limitations, and discussions of uncertainty are provided in the appendix.

Table 2: Annual disease burden, mortality, and economic burden of current global strategy and avertable loss estimations

The proposed revision to the global strategy could guidelines for schistosomiasis and soil-transmitted substantially expand the target population for preventive helminthiasis to incorporate new knowledge and chemotherapy and resources needed for complementary experience gained over the past 15 years. If we miss this interventions. In countries that have yet to achieve the opportunity, then we fail to do all we can to help the 2020 goal of at least 75% drug coverage of all at-risk populations who suffer the greatest burden of populations, development of an updated strategy will helminthiases and other NTDs. serve to clarify resource, drug supply, and programmatic Contributors needs to attain the 2020 goal and beyond. In settings that NCL conceived the article and did the data analysis. NCL had full access have reached 75% drug coverage targets, strengthened to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. All authors contributed guidance should provide an evidence-based strategy intellectual material and approved the final draft. towards a post-2020 era through a more ambitious and Declaration of interests well defined goal of optimal morbidity control or DM acknowledges support from GlaxoSmithKline. All other authors elimination of transmission without allowing for declare no competing interests. infection rebound. Acknowledgments The historic creation of many aspirational targets in NCL dedicates this article to the inspirational memory of Vicki Mosley. global health, including the 3 by 5 initiative for HIV/ We received financial support from the National Institutes of Health AIDS, the Millennium Development Goals, and the Medical Scientist Training Program (MSTP), Doris Duke Charitable Foundation, University of Georgia Research Foundation, Bill & London Declaration on NTDs, illustrates the potential of Melinda Gates Foundation, and Schistosomiasis Consortium for setting a higher bar to improve human health. The Operational Research and Evaluation (SCORE). DM and JRS receive inclusion of NTDs as a specific target within the UN support from the UK Department for International Development as Sustainable Development Goals further signifies the part of the COUNTDOWN Implementation research award. importance of addressing NTDs to achieve universal References 49 1 Karagiannis-Voules DA, Biedermann P, Ekpo UF, et al. Spatial and health coverage. temporal distribution of soil-transmitted helminth infection in To quantify the potential gains of strengthening the sub-Saharan Africa: a systematic review and geostatistical global strategy for schistosomiasis and soil-transmitted meta-analysis. Lancet Infect Dis 2015; 15: 74–84. 2 Lai YS, Biedermann P, Ekpo UF, et al. Spatial distribution of helminthiasis, we compared evidence-based strategies schistosomiasis and treatment needs in sub-Saharan Africa: for preventive chemotherapy relative to the current a systematic review and geostatistical analysis. Lancet Infect Dis global strategy and idealised WHO guidelines. Without 2015; 15: 927–40. change, we estimate that the population of sub- 3 WHO. Preventive chemotherapy in human helminthiasis. Coordinated use of anthelminthic drugs in control interventions: Saharan Africa will probably lose 2·3 million DALYs a manual for health professionals and programme managers. and US$3·5 billion of economic productivity every Geneva: World Health Organization, 2006. year, which is similar to the impact of recent acute 4 WHO. Helminth control in school-age children: a guide for managers of control programmes. Geneva: World Health Organization, 2011. epidemics, including the 2014 Ebola and 2015 Zika 5 WHO. Accelerating work to overcome the global impact of epidemics (table 2, appendix). neglected tropical diseases: a roadmap for implementation. Geneva: World Health Organization, 2012. 6 WHO. Summary of global update on preventive chemotherapy Conclusions implementation in 2015. Wkly Epidemiol Rec 2016; 91: 456–59. With a shared goal of reducing the burden of NTDs on 7 GBD 2013 DALYs and HALE Collaborators, Murray CJL, the world’s poorest people, and following the leadership Barber RM, et al. Global, regional, and national disability-adjusted life years (DALYs) for 306 diseases and injuries of WHO Director-General Margaret Chan and colleagues and healthy life expectancy (HALE) for 188 countries, 1990–2013: around the world for NTDs, we respectfully advocate for quantifying the epidemiological transition. Lancet 2015; revision of the global strategy and associated WHO 386: 2145–91.

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