Review
Neglected tropical diseases: progress towards addressing the
Lancet 2017; 389: 312–25
Published Online
September 14, 2016
http://dx.doi.org/10.1016/
S0140-6736(16)30171-4
Department of Parasitology,
Liverpool School of Tropical
Medicine, Liverpool, UK
(Prof D H Molyneux DSc); Global
Schistosomiasis Alliance,
Chavannes de Bogis,
Switzerland (L Savioli MD); and
Department of Control of
Neglected Tropical Diseases,
World Health Organization,
Geneva, Switzerland
(D Engels MD)
Correspondence to:
Prof David H Molyneux,
Department of Parasitology,
Liverpool School of Tropical
Medicine, Pembroke Place,
Liverpool, L3 5QA, UK
david.molyneux@lstmed.ac.uk
312
chronic pandemic
David H Molyneux, Lorenzo Savioli, Dirk Engels
The concept of neglected tropical diseases (NTDs) emerged more than a decade ago and has been recognised as a
valid way to categorise diseases that affect the poorest individuals. Substantial progress in control and elimination has
been achieved and policy momentum has been generated through continued bilateral, philanthropic, and non-
governmental development organisation (NGDO) support, and donations of drugs from pharmaceutical companies.
WHO has defined a Roadmap to reach 2020 targets, which was endorsed by member states in a World Health
Assembly Resolution in 2013. NTDs have been included within the Sustainable Development Goal targets and are a
crucial component of universal health coverage, conceptualised as “leaving no one behind”. WHO reported that more
than 1 billion people in 88 countries have benefited from preventive chemotherapy in 2014. The research agenda has
defined the need for affordable products (diagnostics, drugs and insecticides). However challenges such as insecurity
and weak health systems continue to prevail in the poorest countries, inhibiting progress in scaling up and also in
achieving Roadmap goals.
Introduction Momentum for further investment came in 2015
NTDs and the global heath agenda with the inclusion of NTDs within the health targets of
In this Review, we will present progress since the 2010 the Sustainable Development Goals (SDGs)11 when the
Lancet Series on neglected tropical diseases (NTDs).1–4 Global Fund Board12 agreed to support interventions
NTDs have been defined as a group of infections strongly that addressed co-infection and co-morbidities and the
associated with poverty in tropical and subtropical G7 Heads of State recognised NTDs as a major
environments. NTDs are diverse in biological and challenge emphasising the need to support research
transmission characteristics; they predominantly infect and interventions.13 An agreed SDG target was to
populations in low-income and middle-income countries reduce the number of people accessing NTD
with limited access to health services.5 During the past interventions by 90% by 2030. However, the burden of
decade, the momentum to address NTDs has been driven NTDs is heavy on the poorest people in G20 countries
by pledges from pharmaceutical companies to provide (together with Nigeria) and if these countries
free medicines (all on the WHO Essential Medicines list implemented NTD programmes then a high proportion
and valued in billions of US$), NGDOs’ commitments to of the NTD burden could be resolved.14
assist implementation of programmes in endemic Increased investment for NTDs will improve the
countries, bilateral support from the US and UK Govern- wellbeing of vulnerable groups, which together with
ments, and an increase in commitment from endemic improvements in water, sanitation, hygiene, and
countries.6 However, despite evidence that interventions education, are appropriate links to many of the SDGs.
to address NTDs are one of the best health investments, NTDs define poverty in many settings and have been
only 0·6% of official development assistance for health is described as litmus tests of progress in poverty
provided to NTDs affecting more than 1 billion people. alleviation, or are described as markers of poverty.15
This underinvestment reflects a persistent and continuing
inequity in global health financing.7 NTD partnerships: evolution and expansion
The London Declaration of 20128 recorded increased from disease-specific to a wider context
commitments of donated drugs for visceral leishmaniasis, Disease-specific partnerships represent the diversity
lymphatic filariasis, and schistosomiasis, while earlier of communities involved in NTDs and have made a
commitments to provide drugs for fascioliasis, leprosy, major contribution to scaling up of programmes.
leishmaniasis, lymphatic filariasis, onchocerciasis, NGDO commitment was pioneered by NGDOs that
trypanosomiasis, and soil-transmitted helminthiases at supported the delivery of ivermectin for onchocerciasis
no cost to endemic countries were reinforced. In 2013, control and multidrug therapy for leprosy elimination
the World Health Assembly approved Resolution WHA programmes.16 Since 2010, new partnerships have
66.12, which defined strategies for NTDs with clear emerged to coordinate and advocate for particular
targets and milestones for 17 NTDs, and endorsed the conditions (table). Disease-specific alliances generate
WHO NTD Roadmap goals linking NTDs to universal opportunities for advocacy and increased resources
health coverage. NTDs are addressed through five from non-traditional donors, and reflect the need to
strategies: preventive chemotherapy, intensified disease facilitate interaction between endemic countries,
management, vector control, veterinary public health international organisations, non-governmental
measures for zoonotic neglected diseases, and through organisations, pharmaceutical donors, philanthropic
improved water and sanitation.9,10 foundations, and academia.
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 Latest WHO Global burden* WHO Roadmap targets Partnerships and alliances Endemic Treatment progress Research and operational
resolutions, countries needs
year
DALYS (million) Deaths per year 2015/2017 2020
18
All NTDs WHA66.12, 47·90 152 000 WHO Roadmap .. .. .. .. ..
2013
Viruses
Dengue and WHA.55.17, 0·83 3000–4200 Sustainable vector Dengue control and Dengue Vaccine Initiative; 100 50–390 million infections per year; Improve availability of vaccine;
dengue 2002 control interventions surveillance systems Paediatric Dengue Vaccine 96 million cases manifest clinically diagnostics; epidemiological
haemorr- established in 10 high established in all Initiative; Innovative Vector situation of dengue in Africa;
hagic fever priority countries regions; number of Control Consortium (IVCC) capacity for case management
cases reduced by 25% and vector control

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(2009–10 baseline) and
deaths by 50%
Rabies WHA3.20, 1·46 26 000 (other Eliminate human Eliminate human rabies Global Alliance for Rabies 150 Reduced number of cases in the Implementation and
1950 sources 55 000) rabies transmitted by transmission by dogs Control Americas—40% reported of all cases resourcing of dog vaccination
dogs and dog-to-dog and dog-to-dog from Haiti; progress in selected strategy and improved access
transmission in all transmission in all countries (Philippines, South Africa, to post-exposure vaccine
endemic areas in Latin affected countries in Tanzania) with introduction of dog
America; intensified WHO’s South-East Asia vaccination programmes; Bangladesh
control and enhanced and Western Pacific reported 50% reduction in rabies
surveillance should regions deaths between 2010 and 2013, with
lead to 50% reduction increased availability of free post-
in number of human exposure vaccine
rabies deaths by 2015
Protozoa
Chagas’ WHA51.14, 0·55 10 300 Interrupt transmission Global Chagas’ Coalition; 21 in 20 endemic countries have achieved Improved diagnostic and
disease 1998 via intradomiciliary Drugs for Neglected Americas 100% blood screening to reduce therapeutics to treat chronic
vectors in Latin America Diseases Initiative (DNDi) transfusion risk disease; implementation of
and transmission via intradomiciliary vector control
blood transfusion in
Latin America, Europe
and the western Pacific
Human WHA57.2, 0·56 9100 2000–3000 cases per Elimination in 100% of Pan-African Programme for 36 Reduced number of reported cases Improved diagnostics; oral
African 2004 year reported; foci Trypanosomiasis over 2010–15 period to less than 3000 therapy for both early and late
trypano- enhance wider patient Eradication and Control; in 2015, compared with 10 000 cases stage disease; scale-up of use
somiasis accessibility; Drugs for Neglected in 2009; enhanced support for of tiny targets for vector
elimination of disease Diseases Initiative (DNDi); surveillance of endemic foci now control; for acute disease in
in 80% of foci Fund for Initiative defined by accurate maps Uganda, implement
Diagnostics (FIND) chemotherapy of cattle and
selective application of
insecticide to cattle
Leish- WHA60.13, 3·32 .. .. .. .. .. .. ..
maniases 2007
Visceral .. .. 51 600 .. 100% case-detection Drugs for Neglected 19 in Reduced incidence reported between Implement defined stategy;
Indian sub- and treatment, with Diseases Initiative (DNDi) Americas, 2011 and 2013; number of reported increase access to liposomal
continent <1 case per 10 000 east Africa, cases declined from 38 007 in 2011 to amphotericin B and
population at district and Asia 15 609 in 2013 in India, Bangladesh implement vector control
and sub-district levels and Nepal, through increased case based on documented status
detection, better access to drugs and of resistance of vector
enhanced surveillance; improved populations
strategy for vector control now defined
and availability of liposomal
amphotericin B as single dose
treatment
Review

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Latest WHO Global burden* WHO Roadmap targets Partnerships and alliances Endemic Treatment progress Research and operational
resolutions, countries needs
year
DALYS (millions) Deaths per year 2015/2017 2020
(Continued from previous page)
Cutaneous .. .. No deaths 70% of all cases .. Drugs for Neglected .. No data available, although increased Continue search for improved
attributed detected and at least Diseases Initiative (DNDi) incidence reported throughout area of drugs to treat cutaneous and
90% of all detected conflict in Middle Eastern region muco-cutaneous disease;
cases treated in the improve if possible access of
Eastern populations to therapy in
Mediterranean Region conflict areas; in stable political
areas, implement reservoir
control programmes to reduce
animal reservoir
Helminth
Cysticer- .. 0·50 1200; however, .. Interventions scaled up .. .. Taenia infections can be treated with Implement pilot projects to
cosis/ estimated that in selected countries for praziquanetl but no standard evaluate strategy; engage
Taeniasis 30% epilepsy Taenia solium taeniasis/ treatment exists for NCC; individual veterinary, sanitation and
cases due to cysticercosis control and case treatment with praziquantel or food safety sectors to reduce
neuro- elimination albendazole or both, antiepileptic disease burden— will require
cysticercosis drugs, or corticosteroids combination of tools-
(NCC) in oxfendazole treatment or
endemic vaccination of pigs to prevent
countries; deaths or cure porcine cysticercosis;
from epilepsy pig vaccine expected to
related to NCC receive regulatory approval in
estimated as India
6·9% in
Cameroon and
0·5% in Mexico
Dracu- WHA64.16, 22 human cases No deaths .. Certified Global Partnership of endemic 4: Chad, 16 countries previously endemic Understand the role of dogs as
nculiasis 2011 reported in 2015 attributed Eradication countries, WHO, Carter Ethiopia, certified free of transmission since the impediment to eradication;
in 4 endemic Center, UNICEF Mali, and eradication programme began in access in areas of insecurity;
countries (Chad, South 1986. 4 countries remain endemic enhanced surveillance in
9; Ethiopia, 3; Sudan (Chad, Ethiopia, Mali and South remaining endemic villages;
Mali, 5; and Sudan). Kenya and Sudan are in pre- maintain control of cyclops
South Sudan, 5), certification stage following more than where cases not contained
down from 126 3 years without a confirmed case.
cases reported in Angola and Democratic Republic of
2014 Congo require to be certified by the
WHO International Commission for
the Certification of Dracunculiasis
Eradication (ICCDE) as free of guinea
worm disease as no verified cases
reported from these countries since
the eradication programme began in
1986
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 Latest WHO Global burden* WHO Roadmap targets Partnerships and alliances Endemic Treatment progress Research and operational
resolutions, countries needs
year
DALYS (millions) Deaths per year 2015/2017 2020
(Continued from previous page)
Echino- .. 0·14 1200 Pilot projects to Validated strategy .. .. Limited data available, but no change in Implement pilot strategy in
coccosis validate effective available for global distribution since 2010; high areas of high risk
strategies where echinococcosis/ prevalence (5–10%) of cystic disease in
disease is a public hydatidosis and parts of Latin America, China, Central
health problem (eg, interventions scaled up Asia, and Africa; alveolar disease has high
major burden in in selected countries for prevalence in Tibetan Plateau with
China) their control and incidence of 16 000 cases; cross-sector
elimination coordination with authorities to

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implement known control measures —
carcass condemnation; deworming of
dogs and reduction of access to offal;
introduction of diagnostic ultrasound;
and promotion of PAIR (puncture,
aspiration, injection and respiration)
surgery strategy
Foodborne .. 1·88 7000 deaths .. 75% of population at .. 17 Reduced numbers of cases reported in Define extent of endemic
trematodes reported in 2005 risk of infection reached Egypt of fascioliasis; increased areas; develop serological and
but not by GBD by preventive treatments for fascioliasis in Peru and molecular methods for
study; 7·9 million chemotherapy; Bolivia since 2009; increased improved diagnosis; increase
cases with severe morbidity controlled in treatment programme for access to praziquantel (or
sequelae all endemic countries opisthorchiasis in Laos and in Vietnam triclabendazole for
for clonorchis; mapping of areas of fascioliasis); engage with
endemicity in Cambodia and initiation other sectors to reduce risk via
of treatment programme health education and
improved sanitation
Lymphatic WHA50.29, 2·78 .. By 2017, 70% of all 81 100% of all endemic Global Alliance to Eliminate In 2014, Continued maintenance of Implement albendazole
filariasis 1997 endemic countries will countries will have been Lymphatic Filariasis (GAELF) 73 treatments—peak of 559 million 2 times per year in Loa loa
have met the criteria verified as free of countries achieved in 2014; 11 countries have co-endemic areas with vector
to stop interventions transmission or will not commenced MDA programmes; control via impregnated
and entered the post- have entered post- 23 countries have implemented bednets; scale-up
intervention intervention limited MDA but not reached 100% interventions in newly defined
surveillance phase surveillance geographical coverage—insufficient to endemic areas; assess impact
reach 2020 target of elimination; of onchocerciasis programmes
18 countries moved into surveillance on filariasis endemicity and
phase following Transmission impact of lymphatic filariasis
Assessment Surveys; programmes on soil-
diethylcarbamazine available as transmitted helminthiases;
donated product since 2013–14 develop a short duration
macrofilaricide based on anti-
wolbachia antibiotics as a
substitute for doxycycline;
complete triple therapy trials;
increase efforts to address
morbidity
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Latest WHO Global burden* WHO Roadmap targets Partnerships and alliances Endemic Treatment progress Research and operational
resolutions, countries needs
year
DALYS (millions) Deaths per year 2015/2017 2020
(Continued from previous page)
Oncho- WHA62.1 0·49 No deaths Elimination in Latin Elimination in selected Organization for 37 30 countries previously had varying Develop a short duration
cerciasis 2009; attributed America and Yemen countries in Africa Elimination of levels of endemicity post-control. macrofilaricide based on
WHA47.32, Onchocerciasis in the Colombia, Ecuador, and Mexico now anti-wolbachia antibiotics as a
1994 Americas (OEPA); African verified as free of transmission; substitute for doxyclycine;
Project for Onchocerciasis Guatemala has submitted documents to implement ivermectin 2 times
Control APOC (closed end of verify absence of transmission; overall, per year strategy for control or
2015) and now Expanded 112 million/172 million total population elimination in Africa; define
Special Project for estimated to require treatment (65·3% areas of low transmission;
Elimination of NTDs) Africa global coverage); progress towards define areas where
nationwide elimination in Burundi, transmission has been
Chad, Guinea Bissau, Kenya, Malawi, arrested by implementation of
Mali, Niger, and Senegal; focal new WHO guidelines
elimination in 6 countries (Cameroon,
Ethiopia, Nigeria, Sudan, Tanzania,
Uganda) has been achieved but in
Cameroon difficulties exist in area of high
transmission zones co-endemic with
Loa loa; Northern focus in Venezuela
under surveillance while southern focus
cross border Brazil/Venezuela using
ivermectin 4 times per year or
doxycycline to reduce transmission; new
infected Yanomami communities found
Schisto- WHA.65.21, 3·31 11 700 Regional elimination Regional elimination in Global Schistosomiasis .. In 2013, 47 million individuals of 261 Develop paediatric
somiasis 2012 as a public health Americas, Pacific and Alliance million requiring treatment reached; in praziquantel formulation;
problem in eastern nationally in selected 2014, 61·6 million school age define link between HIV and
Mediterranean, countries in Africa; 75% (5–14 year-olds) and adult individuals urogenital schistosomiasis to
Caribbean and of school-aged children treated—20% of that needed; evaluate risk of HIV
Indonesia and regularly treated in all Praziquantel available as donated drug transmission
Mekong basin endemic countries with 250 million donated tablets being
available in 2016; donors purchasing
additional praziquantel
Soil- WHA54.19, 5·19 2700 50% of people in need 75% of preschool-aged STH Coalition managed by .. Number of school-age children treated Evaluate value of treating
transmitted 2001 of preventive and school-aged Children Without Worms has increased from 200 million in 2010 adults if transmission to be
helmin- chemotherapy, children in need of to 271 million in 2014 (47% of interupted; develop drug
thiases including children treatment are regularly estimated 576 million children at risk); efficacy monitoring at scale;
(preschool-aged and treated in all endemic in 2014, 138 million of 269 million evaluate new products or
school-aged children) countries pre-school children estimated to be in combinations; improve
are regularly treated in need of treatment were treated (global diagnostic tools
100% of endemic coverage of 51·4%); in 2016, India
countries treated 140 million children through a
school-based deworming programme
in a single day, and in 2014 Egypt
treated 2 million school-age children
over a 4 week period
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 Latest WHO Global burden* WHO Roadmap targets Partnerships and alliances Endemic Treatment progress Research and operational
resolutions, countries needs
year
DALYS (millions) Deaths per year 2015/2017 2020
(Continued from previous page)
Bacteria
Buruli ulcer WHA57.1, 5000–6000 Oral antibiotic therapy 70% of cases detected Global Buruli Ulcer Initiative 33 12/15 countries that report regularly Rapid point of care diagnostic
2004 cases per year incorporated into early and cured with reported 2200 new cases in 2014
control and treatment antibiotics in all compared with 5000 in 2009
endemic countries
Leprosy WHA44.9, 0·006 No deaths .. Global elimination of International Leprosy .. See text Focus on countries with
1991 attributed the public health Elimination Programme continuing high prevalence

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problem
Trachoma WHA62.1, 0·33 No deaths 10% of endemic All countries will have International Trachoma .. Global Trachoma mapping Project Implement expanded
(avoidable 2009 attributed countries were achieved the UIG and be Initiative and GET 2020 completed enabling scale up of SAFE trichiasis surgery
blindness) expected to have free from blinding strategy; Number of individuals
achieved the UIG by trachoma as a public- receiving azithromycin increased from
2013; by 2016, 40% health problem 45 million in 2010 to 54·7 million in
of endemic countries 2014, with increased number of districts
achieved this goal and treated; trichiasis surgery delivered in
entered post-endemic 43% of districts where it was defined as a
surveillance public health problem with target to
exceed 50% by 2015
Yaws/ WHA2.6, Not calculated .. .. Global eradication .. .. Pilot studies show success of ..
endemic 1949 azithromycin treatment strategy
trepone-
matoses
Non-infectious NTDs
Snake bite .. .. 96 000 per year .. .. Global Snake Bite Initiative .. Production of antivenom stopped by Develop polyvalent
manufacturers and no quality antivenom not needing cold
alternatives available for common chain; advocate for greater
snakebite in Africa attention to snake bite as
cause of mortality
Podo- .. .. No deaths .. .. International Podoconiosis .. Increased recognition of problem over Implement morbidity
coniosis attributed Initiative (Footwork) recent years; definition of areas of management
endemicity

Data are derived from various sources.6,8,46,52,53,57 MDA=mass drug administration. UIG=ultimate intervention goal. *Global Burden of Diseases, Injuries, and Risk Factors Study 2010 data.

Table: Neglected tropical diseases and the associated global burden, targets, partnerships, endemic countries, treatment progress, and research needs
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Science underpinning the NTD case
The burden of NTDs
The Global Burden of Disease study of 201017 attributed
some 27 million disability-adjusted life years (DALYs) to
NTDs. A 2014 study18 included other conditions not
included within the WHO official NTD list of 17 diseases,
and attributed 47·9 million DALYs to all NTDs; another
study5 in 2009 estimated the burden for NTDs was
56 million DALYs. The global annual mortality from
NTDs was reported as around 150 000 deaths per year by
the Global Burden of Disease study.17 However, this
estimate excluded deaths from rabies (55 000 deaths),
snakebite (up to 94 000 deaths), cancers associated with
trematode infections (60 000 deaths), and neurological
NTD conditions such as neurocysticercosis-related
epilepsy (60 000 deaths)—these deaths are also included
in other categories. These figures suggest the total
annual mortality from NTDs is actually around 350 000.
In 2010, WHO reported that schistosomiasis mortality
alone could be as high as 280 000 per year in Africa—a
20-fold difference from the official GBD data.19 Morbidity
from permanent blindness, debilitating skin disease,
disability and disfigurement with long term psychological
and social and economic consequences will elevate the
total DALY burden but are not included in Global Burden
of Disease metrics.20
NTD comorbidities: HIV, epilepsy, and cancer
A possible association between HIV and urogenital
schistosomiasis has been recognised. Ndeffo Mbah and
colleagues21 showed increased HIV positivity in females
infected with Schistosoma haematobium. The opportunity
to reduce the risk of HIV in young females (5–15 years)
associated with S haematobium urogenital pathology by
annual praziquantel has yet to be recognised by the HIV
community, despite the need to achieve high coverage of
this at-risk group irrespective of a direct link to HIV. The
safety of praziquantel has been reconfirmed during
pregnancy and lactation.22 The longstanding policy to
assure coverage of young females with praziquantel
treatment should be implemented by both the NTD and
HIV constituencies. Neurocysticercosis infection caused
by Taenia solium cysts has been associated with epilepsy
and estimates suggest some 30% of global epilepsy is
associated with neurocysticercosis.23 Bladder cancer
associated with S haematobium and food-borne trematode
infections that cause cholioangiocarcinoma are estimated
to cause 60 000 deaths annually.24 The successful
schistosomiasis control programme in Egypt has seen a
rapid decline in bladder cancer during the past
2 decades.25 Comorbidities associated with hookworm
and schistosomiasis also exacerbate malaria pathology,
particularly in pregnancy, which reduces birthweight and
increases risk of neonatal and infant mortality. Further,
the mental health comorbidity of many NTDs and the
impact these conditions have on the psycho-social status
of individuals and families, particularly depressive illness
318
and anxiety of patients with NTDs as well as caregivers
has only recently been highlighted as a problem with
significant additional burden.20
Definition of research priorities
Research priorities for NTDs have been published in a
series of reports by WHO and the Special Programme
for Research and Training in Tropical Diseases, outlining
priorities for kinetoplastid parasites (trypanosomes and
leishmanias), helminth infections, zoonoses and viral
infections (dengue, and other arboviruses).26 A consensus
has been reached that new drugs, insecticides, and
diagnostics are required, which will offer improved
and cost-effective therapies, vector-control tools, and
diagnostics. Attempts to develop vaccines for multi-
cellular parasites are yet to develop a product for large-
scale use. However, progress to address the expanding
dengue threat has been made with the development of a
vaccine for dengue (Dengvaxia, Sanofi Pasteur, Lyon,
France). Dengvaxia has been licenced in Mexico for use
in highly endemic areas, after results of safety and
efficacy studies in clinical trials showed reduced
incidence of hospitalisation in vaccinated children
aged 2–16 years old in three clinical trials involving
35 000 children.27
Research to improve delivery of existing products and
evaluate efficacy of existing therapeutics will be necessary,
as will exploration of combinations of products known to
be effective. Specific research priorities are improved oral
therapy for human African trypanosomiasis that is
effective in both early and late stage disease; and
improved chemotherapy for leishmaniases, Chagas’
disease, and buruli ulcer—current therapies are not ideal
owing to the duration of required treatment, mode of
administration, and toxicity. A short-duration macro-
filaricidal treatment to kill or permanently sterilise adult
filarial worms is still needed, because despite the efficacy
of the anti-Wolbachia antibiotic, doxycycline, the duration
of treatment and eligibility criteria currently restrict its
widespread use. Praziquantel has been donated for mass
drug administration in school-aged children for
schistosomiasis; however, it needs to be reformulated for
paediatric use given that pre-school children are
frequently infected. The combination of praziquantel
with artesunate for treatment of both adults and juvenile
forms of schistosomes might be considered.28
Research linked to implementation of programmes and
challenges that programmes face as they mature require
social science involvement to improve coverage and
adherence, and improved methodologies to evaluate
impact and address problems identified in acceptability
adherence and coverage.29 Research to understand
interactions between social networks within communities
could help ensure optimum understanding and uptake of
drugs.30 Increasingly complex and diverse research
questions have emerged as programmes dependent on
mass drug administration have progressed. Such questions
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relate to the duration and frequency of mass drug
administration for different diseases, the broad spectrum
effectiveness of the anthelminthics used and the impact of
vector control on transmission of filariasis.31
Mapping disease distribution
Accurate mapping of disease distribution is a prerequisite
for effective implementation. Onchocerciasis pro-
grammes have shown the importance of defining
endemicity; in these programmes, levels of endemicity
were defined by rapid epidemiological assessment and
mapping.32 The serious adverse events associated with
Loa loa co-endemicity with onchocerciasis meant a rapid
mapping methodology was required to define areas of
highest risk.33 Similar rapid mapping using antigen
detection methods are used to identify where lymphatic
filariasis mass drug administration should be instituted.34
The need to know the distribution of NTDs that can be
controlled or eliminated by preventive chemotherapy led
to the development of online resources to ensure all
requisite data are available and updated. The Global
Trachoma Mapping Project is an example of how mobile
phone and geographic information system technologies
can be used: population-based prevalence surveys are
done in all districts where trachoma is suspected to
acquire data on burden and risk, thus enabling
prioritisation of interventions and policy determination
for implementation of the surgery, antibiotics, facial
cleanliness, and environmental improvement (SAFE)
strategy.35 Detailed mapping of foci of human African
trypanosomiasis due to Trypanasoma brucei gambiense
infection has defined areas of highest risk for active
surveillance.36
Use of remote sensing technologies to produce datasets
that precisely define zones of climate (rainfall indices, cloud
cover), physical parameters (altitude, soil type), and
ecological parameters (forest cover, vegetation type) is
increasingly important, as predictors of disease ecology
reflecting drivers of transmission of vector borne infections.
Definable physical characteristics such as soil type are
associated with podoconiosis distribution.37 The NTD global
mapping tool provides an interactive means to assist the
planning and implementation of preventive chemotherapy
for NTDs, enabling visualisation of geographical
distribution of diseases and the priority areas requiring
mass drug administration where co-implementation should
be initiated. The global mapping tool also complements the
Global Atlas of Helminth Infections, provides information
on water and sanitation, and allows progress of interventions
to be tracked.
The need for alternative strategies— the operational
research agenda
Some preventive chemotherapy programmes require
alternative strategies to reach elimination targets, which
need to be piloted and implemented. These alternative
strategies include: ivermectin twice a year for filariasis
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Review
in Africa; albendazole twice a year for lymphatic
filariasis in L loa co-endemic areas; bednet coverage to
eliminate lymphatic filariasis; and the use of doxycycline
as a macrofilaricide or ivermectin four times per year in
some areas of onchocerciasis endemicity, such as in
Brazil and Venezuela.31,38 Thomsen and colleagues39
examined a triple combination of diethylcarbamazine,
albendazole, and ivermectin for filariasis and showed
that microfilaria levels remain suppressed for a
24 month period thus providing an opportunity to
reduce the frequency of mass drug administration in
areas where onchocerciasis is not co-endemic.
Additionally, to reduce the problem of the limited effect
of albendazole on trichuris infections, ivermectin
should be considered; however, ivermectin is not
donated for trichuris infections or for scabies. Because
extensive insecticide resistance exists in Africa, the
value of bednets to eliminate Wuchereria bancrofti
transmission needs to be reassessed.40
Cochrane systematic reviews: the deworming debate
In 2015, the Cochrane Collaboration challenged the
benefits of deworming for the control of soil-transmitted
helminthiases after their analysis41 of randomised
controlled trials (RCTs). This finding provoked robust
debate42 about whether RCTs are an appropriate way to
measure the nutritional and educational benefits of
preventive anthelminthic chemotherapy. Most RCTs do
not take into account that recovery from nutritional
deficits is a process that takes much longer than 1 year,
especially if the quality and quantity of the nutrients
assumed in the diet are limited.
Furthermore, a significant proportion of individuals
treated with preventive chemotherapy are uninfected but
are nevertheless treated for logistical reasons and thus no
nutritional benefits are expected to accrue in this group.
RCTs normally calculate the mean benefit of preventive
chemotherapy on the entire treated group but the true
benefits are obtained only by those infected and are
therefore greatly diluted.
Additionally, different worm species have different For the NTD global mapping tool
pathological effects—hookworm causes anaemia, see http://www.NTDMap.org)
ascariasis retards growth43—hence when the results of
preventive chemotherapy are evaluated it is important
to recognise which species of soil-transmitted
helminthiases are removed. For example, an
improvement in haemoglobin levels should not be
expected if hookworms are not the prevalent species in For the Global Atlas of
the population treated. On the basis of the evidence Helminth Infections see http://
www.thiswormyworld.org
from all studies including RCTs, WHO issued a
consensus statement reiterating the justification of the
present policy of preventive chemotherapy.42 Provision
of deworming to infected populations reflects equity
and ethical aspects and the intervention is recognised to
reinforce the trust in the health and education
service, aspects that the Cochrane systematic review of
RCTs is unable to evaluate.
319
 Review

For Uniting to Combat NTDs
see http://unitingtocombat
ntds.org
Progress towards Roadmap goals
Progress on specific diseases
Substantial progress towards WHO Roadmap goals and
regional targets has been achieved since 2010 (table). The
Uniting to Combat NTDs initiative tracks progress on
ten NTDs towards the agreed targets against a scorecard
that is published annually.
Dracunculiasis (Guinea worm disease)
Since the introduction of the Guinea Worm Eradication
Programme in 1986, 16 countries have been certified free
of Guinea Worm transmission, including 6 countries
since 2010 (Burkina Faso, Côte d’Ivoire, Ghana, Niger,
Nigeria, and Togo). However, four countries remain
endemic—Chad, Ethiopia, Mali, and South Sudan—who
reported only 22 cases in 2015 compared with 126 cases in
2014.44 Each of these endemic countries pose different
challenges if transmission cessation is to be confirmed. A
possible cycle of transmission that involves dogs, fish, and
amphibians as paratenic hosts was discovered in Chad,
meaning a change in approach could be required because
503 dog infections were recorded in Chad in 2015; from
January, to June, 2016, 498 dogs have been reported
infected and four human cases have been identified in
Chad. Human cases were also reported in South Sudan
and Ethiopia in June, 2016.44,45 In Mali, access to endemic
areas is curtailed due to insecurity. In South Sudan, strong
progress has been made to reduce the numbers of infected
villages but problems of access, population movement,
cattle camps, and insecurity pose end-game challenges.
Human trypanosomiases
Achievement of the target to reduce the number of
chronic human African trypansomiasis cases to
between 2000–3000 cases per year by 2015 is close:
WHO reported 3796 cases in 2014 and less than 3000 in
2015. This figure was the lowest reported incidence for
75 years and was achieved by active surveillance of
defined high-risk foci and donation of products for
chronic human African trypansomiasis therapy
(pentamidine and nifurtimox–eflornithine).46 The
availability of tiny insecticide impregnated targets for
glossina control,47 new diagnostic tests, and the prospect
of an oral therapy to treat both phases of the disease—
fexnidazole, which is now in phase 2 and 3 trials calls
for optimism.
Chemotherapy for Chagas’ disease remains
problematic; less than 1% of patients have access to
benznidazole. Despite an impact on parasite serological
parameters, a randomised trial of benznidazole did not
significantly reduce levels of cardiac clinical deterioration
through 5 years of follow-up.48
Leprosy
215 656 new cases of leprosy were reported in 2013 in
103 countries. During the past 20 years, more than
14 million patients have been cured of the disease,
4 million since 2000. The prevalence of leprosy has
dropped by 90%: from 21·1 per 10 000 people in 1983 to
less than 0·24 per 10 000 people in 2014. A substantial
decrease in the global disease burden has been achieved;
the number of leprosy cases has reduced from
5·2 million in 1985, to 180 618 cases at the end of 2013,
which has led to the suggestion that the public health
problem has been eliminated—defined by WHO as a
prevalence of less than 1 case per 10 000. However,
although the problem of leprosy has been reduced by
multidrug therapy, pockets of high endemicity remain
in several countries, including India, Brazil, and
Indonesia, therefore this ancient and stigmatising
disease should remain a priority.49
Lymphatic filariasis
In 2014, 73 countries remained endemic for lymphatic
filariasis; 18 countries are now entering the surveillance
phase but 11 countries have not yet commenced mass
drug administration programmes. Some 23 countries
have only implemented limited mass drug administration
and have not reached 100% geographical coverage.
Countries that have not achieved complete coverage will
not be able to reach the 2020 target of elimination.
However, 18 countries have moved into a surveillance
phase following transmission assessment surveys, an
evaluation which suggests transmission has been
arrested.50 However, The Gambia appears to have
eliminated transmission, without the introduction of
mass drug administration, with long-term use of
impregnated bednets for malaria control.51 A 2014
estimate of the impact of mass drug administration
during the past 13 years suggests more than 96·71 million
cases of lymphatic filariasis were prevented or cured; yet
36 million cases of hydrocoele and lymphoedema
remain.52 The economic benefits estimated to have
accrued during the first 8 years of the programme exceed
$24 billion. In 2014, 559 million people were treated for
lymphatic filariasis and the cumulative number of
treatments reported was 5·62 billion to more than
1 billion individuals.53
The filariasis test strip, which is based on the immune-
chromatographic test, has been introduced as an
improved method for use in mapping and evaluation.53
This test will be used for transmission assessment
surveys to determine the impact of mass drug
administration and allow for decision making with
regard to cessation or to evaluate any recrudescence.
Lymphatic filariasis accounts for at least 2·8 million
disability-adjusted life-years;17 this figure does not include
the substantial comorbidity of mental illness commonly
experienced by patients and their caregivers.20 For WHO’s
Global Programme to Eliminate Lymphatic Filariasis to
succeed, 100% geographical coverage of both mass drug
administration and patient care is necessary and could be
achieved through the implementation of morbidity
management and surgery.50

320 www.thelancet.com Vol 389 January 21, 2017


Onchocerciasis
Three countries have been verified as free of transmission
of Onchocerca volvulus: Colombia, Ecuador, and Mexico.
Guatemala has submitted a dossier that indicates that
transmission has stopped in all the previous endemic foci,
while the northern focus in Venezuela is under post-
control surveillance. However, the cross-border focus
straddling Brazil and Venezuela exemplifies challenges of
remote areas; migratory Yanomami groups who require
treatment characterise the difficulties of sustaining
ivermectin distribution four times per year. Some infected
individuals who remain positive have been hospitalised
for treatment with the macrofilaricide doxycycline.54
Closure of the African Programme for Onchocerciasis
Control at the end of 2015 and the creation of the
Expanded Special Project for the Elimination of NTDs in
Africa for the control of other preventive chemotherapy-
targeted NTDs will transfer the responsibility to provide
technical support to country programmes to the WHO
Regional Office for Africa. The African Programme for
Onchocerciasis Control delivered more than 1 billion
treatments between 1997 and 2014 in 19 countries, built
capacity through training or retraining of more than
148 000 health workers and 1·46 million community
directed distributors, facilitated use of community
structures for other health programmes, and empowered
more than 190 000 communities to direct their own
ivermectin treatment schedules.55
The African Programme for Onchocerciasis Control
made epidemiological progress towards nationwide
elimination in Burundi, Chad, Guinea Bissau, Kenya,
Malawi, Mali, Niger, and Senegal. Focal elimination in
six countries (Cameroon, Ethiopia, Nigeria, Sudan,
Tanzania, and Uganda) was achieved, but in Cameroon
there are difficulties in high transmission zones that are
co-endemic with L loa. In such zones, coverage and
adherence are inadequate to satisfy the expectation that
transmission can be arrested without implementation of
additional strategies.55
Scabies
Scabies is caused by the ecto-parasitic mite Sarcoptes
scabiei and is highly susceptible to ivermectin, which is
used in onchocerciasis and lymphatic filariasis
programmes. The results of a study56 in Fiji showed
efficacy of ivermectin for scabies compared with standard
treatments of topical permethrin cream. The lack of data
on the impact of ivermectin on scabies after nearly
3 decades of use in mass drug administration programmes
is a major deficit, representing a missed opportunity.
Schistosomiasis
The World Health Assembly resolution of 2012
(WHA 65.21)57 called for the elimination of schisto-
somiasis and reinforced the importance of regular
treatment of at least 75% of school age children in areas
at risk of both schistosomiasis and soil-transmitted
www.thelancet.com Vol 389 January 21, 2017
Review
helminthiasis as stated in a previous resolution
(WHA 54.19).58 Schistosomiasis programmes will now
benefit from the increased donation of praziquantel,
because from 2016, 250 million tablets equivalent to
100 million treatments will be available. The number of
school-age children treated in 2014 was 49·2 million,
equivalent to 34.6% of global coverage for this age group.
In spite of this significant progress, scale-up remains For more on scale-up of
slow in the highest burden countries where 70% of the treatment see http://www.
unitingtocombatntds.org
burden occurs. If the elimination goals for
schistosomiasis are to be met, endemic countries should
define high priority intervention areas, access the
available donated drug, implement health education
messages to emphasise the importance of safe water and
sanitation provision in reduction of transmission, and
recognise the importance of pre-school age children and
their need for treatment if possible with a paediatric
formulation of praziquantel.59 The association between
HIV and urogenital schistosomiasis requires resolution
with strong policy enforcement through the regular
treatment of school girls, women of childbearing age,
and throughout pregnancy and lactation as
recommended by WHO and the original manufacturers
of praziquantel.22
Soil-transmitted helminthiases
Between 2008 and 2013, the number of children treated
for soil-transmitted helminthiases doubled. WHO
reported that 440 million pre-school and school-age
children were treated in 2014 with anthelminthics
(albendazole and mebendazole)—rates of coverage have
increased since 2008 and a global coverage of 44–51% has
been achieved.6,60 The figures for treatment of soil-
transmitted helminthiases do not include individuals
receiving anthelminthics via filariasis and onchocerciasis
programmes that treat adults as well as younger age
groups.31 The need to treat adults is recognised, if a
permanent reduction in transmission is to be achieved,61
as well as the importance of the role of the water,
sanitation, and hygiene sector to sustain the gains regular
deworming can provide.62
Trachoma
The SAFE strategy for the elimination of trachoma with
its four components—surgery, antibiotics, face washing,
and environment—shows the multiple approaches
required if public health goals are to be achieved.46 The
Global Trachoma Mapping Project provided detailed
information for implementation of mass drug
administration using azithromycin, identified where the
burden of trichiasis is highest for prioritisation of
surgery, and identified where implementation of the face
washing and environment components of the SAFE
strategy will pose the greatest challenge.36 The
implementation of mass drug administration in all
endemic districts at 80% coverage for 3–5 years,
depending on prevalence of active trachoma, will pose a
321
 Review
significant challenge notwithstanding the estimated
backlog of 5 million cases of trichiasis surgery; Solomon63
has emphasised the benefit of improved trichiasis
surgery technique in reducing recurrence of trachoma.
Yaws
Yaws (Treponema pallidum pertenue) is a disabling skin
condition that has been identified as a potential eradication
target on the basis of oral azithromycin efficacy. WHO
developed the Morges Strategy for Yaws Eradication by
2020;64 the strategy will involve mass drug administration
of single dose azithromycin to entire endemic
communities, supported by surveillance until clinical
cases are no longer detected, and by treatment of all active
cases and their contacts. Pilot interventions have been
initiated in several countries: in Nsukka, Nigeria, mass
drug administration with oral azithromycin interrupted
transmission within 6–12 months. In India, after a 20 year
campaign using penicillin injection followed by sero-
surveillance of children for treponemal antibodies, WHO
reported65 that yaws was no longer present in India and
declared its eradication (technically elimination).
Implementation strategies requiring
collaboration with other sectors
Vector control
Vector control has been a major component of NTD
programmes over many decades. Many NTDs such as
lymphatic filariasis, visceral leishmaniasis, oncho-
cerciasis, and Chagas’ disease have benefited from vector
control.66 Additionally, new approaches to the control of
human African sleeping sickness using tiny target
technology47 or selective spraying of cattle to control the
acute zoonotic form of disease have been shown to be
effective interventions but require implementation at
scale.67 Development of novel tools and methods to curb
the spread of (day-biting and outdoor-biting) Aedes aegypti
mosquitoes that transmit dengue68 and Chikungunya69 is a
high priority, reinforced by the emergence of Zika virus.
Development of novel vector control methods will require
substantially increased investment if they are to be
implemented.6 Increasing levels of resistance to present
pyrethoid-based insecticides threaten the progress of the
lymphatic filariasis elimination programme in Africa.40
Global warming, climate change, unplanned urbanisation,
and global travel of people and goods, will have an impact
beyond the traditional populations associated with NTDs.
The establishment of schistosomiasis in Corsica
exemplifies these threats; snail populations have been
found in Corsica that are susceptible to infection with a
parasite strain from Africa, a hybrid of S haematobium and
Schistosoma bovis, therefore these strains could become
established in southern Europe.70
Neglected zoonotic diseases: the One Health concept
Neglected zoonotic diseases occur in many settings,
caused by diverse groups of organisms, hence
322
generalisations about approaches to their control is
difficult. However, progress has been made to define
strategies for control of specific diseases, which require an
approach that goes beyond the health sector.71 The vision
for One Health is a culture change that recognises the
importance of the link between humans, animals, and
ecosystems, providing added value by translation of the
One Health approach into zoonotic disease control.
Successful application of One Health strategies are the use
of dog vaccination in the control of human rabies in Latin
America, KwaZulu-Natal, the Philippines, and Bali,72 and
the control of the acute form of human sleeping sickness,
Trypansoma brucei rhodesiense, in south east Uganda. In
Uganda,67 chemotherapy of the cattle reservoir, together
with vector control by spraying of cattle to selectively kill
the tsetse fly Glossina fuscipes, has been shown to effectively
reduce the incidence of sleeping sickness cases.67 The One
Health approach can also be applied to the control of
cysticercosis and echinococcosis, globally distributed
cestode infections, in which interventions focused on
animal reservoirs (pigs and dogs) are essential components
of interventions to reduce human prevalence allied to
behaviour change and curative therapy.73,74
Water, sanitation, and hygiene
Sustained control and elimination of soil-transmitted
helminthiases and schistosomiasis, require not only
chemotherapy, but also access to clean and safe water
together with appropriate waste disposal and behaviour
changes to reduce transmission. However, provision of
clean and safe water in the more remote areas where
NTDs and other waterborne infections are most prevalent
poses a substantial challenge and the involvement of
other sectors is required. Engagement of the water,
sanitation, and hygiene sector and the inclusion of NTDs
within this framework, reflects a holistic policy approach
within the SDG goals.62
Place of NTDs in the global health context
towards 2030
During the past decade, NTDs have attracted increased
attention and investment. Availability of drugs is no
longer a barrier to achievement of universal health
coverage for most NTDs yet they remain a chronic
pandemic in the poorest sectors of society in endemic
countries who now have access to donated drugs. Further
progress will be driven by commitment of countries to
contribute to the relatively small costs of delivery—
estimated at 1–3% of national health budgets—to ensure
access to donated products with a calculated annual value
of $2–3 billion. In 2015, 1·1 billion people received
preventive chemotherapy, representing a public health
success, and 140 million children were dewormed in a
single day in February, 2016, in India.75 However, progress
towards achievement of the 2020 WHO Roadmap targets
has been patchy. The resources allocated to NTDs are not
yet adequate to address the totality of the problem. The
www.thelancet.com Vol 389 January 21, 2017

estimated requirements to achieve Roadmap goals are
double the current $300 million annual funding
provided. However if vector control is included the
estimated amount required would be ten times that
amount.6 The challenge is to persuade endemic countries
to invest national resources to develop robust and
dependable health delivery systems to ensure the gains
from NTD control or elimination are translated into
long-term human development gains.
NTDs are tracers of equity in progress toward other
SDGs and targets,15 including universal health coverage
(target 3.8), access to safe water (target 6.1), and sanitation
(target 6.2). NTD endemic populations are the least likely
to have access to such services, hence use of NTDs as an
indicator of progress is a logical step to justify these
diseases in the SDG targets. Other SDG goals upon
which NTD interventions and partnerships are relevant
are education (target 4), gender equality (target 5), decent
work and economic growth (target 8), reduced
inequalities (target 10), sustainable cities and
communities (target 11), climate action (target 13), and
partnership for the goals (target 17). The most recent
WHO and World Bank report76 on monitoring of
universal health coverage is explicit that “monitoring
preventive chemotherapy remains key to ensuring that
the diseases of the least well-off are being prioritised
from the very beginning of the path to UHC”.
However, additional challenges exist with respect to
implementation as well as the need for a new generation
of products: countries have limited human resources;
some populations are difficult to access; civil unrest and
conflict impede implementation;77 drug resistance and
insecticide resistance could develop; and environmental
change impacts on the ecology and behaviour of vectors.40
Additionally, the value of quantitative and mathematical
modelling approaches to inform policy decisions for a
group of NTDs has been emphasised through the work
of the NTD Modelling Consortium.78
A 2016 study79 on health gains from NTD programmes
has estimated that 175 million DALYs have been averted
in the 15 years of the lymphatic filariasis programme,while
if targets are met for nine NTDs 600 million DALYs would
be averted, which can be extrapolated to 2030 largely due
to the decline in morbidity of NTDs treated by preventive
chemotherapy.80 However, this figure does not estimate
for gains in subtle morbidities through improved
cognitive development and mental health and only nine
NTDs were used in the calculation. This suggests that
overall gains in DALYs from all NTD programmes would
be substantially greater than the 600 million DALY figure.
The stated commitments of donors should be translated
into resources to redress the inequities of financing, from
which NTD programmes presently suffer, to give the poor
what they deserve: access to free, high quality effective
products as they continue to be exposed to an avoidable
chronic pandemic which claimed at least ten-times more
lives than the Ebola epidemic in a single year.
www.thelancet.com Vol 389 January 21, 2017
Review
Contributors
DHM wrote the first draft and took the lead role in development of the
paper; LS and DE contributed to further development of the content and
structure of the paper, in particular the policy elements and editing, and
agreed to the final version.
Declaration of interests
DHM receives support from the UK Department for International
Development as part of the COUNTDOWN NTD Implementation
Research award to the Liverpool School of Tropical Medicine and
GlaxoSmithKline. LS is the Chair of the Executive Group of the Global
Schistosomiasis Alliance. DE declares no competing interests.
Acknowledgments
We thank Mark Bradley (GlaxoSmithKline), Antonio Montresor (WHO),
and Adrian Hopkins (Mectizan Donation Program) for constructive and
helpful comments and Joan Fahy (Liverpool School of Tropical Medicine)
for her assistance in organisation of the manuscript.
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