Introduction
Neglected tropical diseases (NTDs) exist and persist for social and economic reasons
that enable the vectors and pathogens to take advantage of changes in the behavioral
and physical environment. Persistent poverty at household, community, and national
levels, and inequalities within and between sectors, contribute to the perpetuation
and re-emergence of NTDs. Changes in production and habitat affect the physical environment,
so that agricultural development, mining and forestry, rapid industrialization, and
urbanization all result in changes in human uses of the environment, exposure to vectors,
and vulnerability to infection. Concurrently, political instability and lack of resources
limit the capacity of governments to manage environments, control disease transmission,
and ensure an effective health system. Social, cultural, economic, and political factors
interact and influence government capacity and individual willingness to reduce the
risks of infection and transmission, and to recognize and treat disease. Understanding
the dynamic interaction of diverse factors in varying contexts is a complex task,
yet critical for successful health promotion, disease prevention, and disease control.
Many of the research techniques and tools needed for this purpose are available in
the applied social sciences. In this article we use this term broadly, and so include
behavioral, population and economic social sciences, social and cultural epidemiology,
and the multiple disciplines of public health, health services, and health policy
and planning. These latter fields, informed by foundational social science theory
and methods, include health promotion, health communication, and heath education.
Social science health researchers have attended particularly to HIV/AIDS, and more
recently to malaria and tuberculosis (TB), reflecting the prevalence and resistance
to control of these diseases and their emphasis in the United Nations Millenium Development
Goals. Other infectious diseases, by default, have slipped into a “neglected” category.
These include most “tropical” diseases, such as Chagas disease, dengue, human African
trypanosomiasis, leishmaniasis, leprosy, lymphatic filariasis, schistosomiasis, and
onchocerciasis. The inclusion of these diverse diseases as “neglected” refers not
only to their status relative to HIV, TB, and malaria. Their neglect reflects their
epidemiology: they are prevalent among the poorest and most marginalized of the world's
population. More than 70% of countries and territories affected by NTDs are low-income
and lower middle-income countries, and 100% of low-income countries are affected by
at least five NTDs [1]. This is due to multiple factors, including the focality of
most NTDs and hence the localization of vulnerability, morbidity, and mortality. Various
social determinants (e.g., poverty, gender, education, and migration) interact to
establish local patterns of co-morbidity of NTDs and other pertinent public health
problems (e.g., malnutrition, malaria, diarrheal diseases, and violence). These vulnerable
populations tend to lack the power to draw attention from decision makers to their
problems and to attract resources, and national resources tend to be directed to high
prevalence, epidemic conditions at the expense of endemic diseases. NTDs also attract
little research nationally or internationally, and virtually no investment or commercially
based research and development in wealthy research settings [2].
In recent years, however, NTDs have received increasing international interest, partly
in response to promising advances in drug development. Concerted efforts are being
made also to promote innovative public health approaches such as integrated delivery
of multiple interventions [3]–[5], which require research effort into effective public
health interventions. This article was stimulated by the renewed interest in populations
affected by NTDs and in feasible ways to prevent and control NTDs. Rather than focusing
on specific medically defined NTDs, in this article, we focus on neglected diseases
of poverty, i.e., diseases that disproportionately affect poor and marginalized or,
in other words, diseases of “neglected” populations. We begin with a summary of the
history of social research activities supported by the Special Programme for Research
and Training in Tropical Diseases (TDR) at the World Health Organization (WHO). We
then highlight the ongoing and emerging challenges to sustain and extend research
to improve the control of NTDs, all of which are also neglected diseases of poverty.
We identify emerging research priorities and reflect on the challenges in mainstreaming
these issues in research and disease control programs, drawing attention to the urgency
of particular research questions.
Methods
The focus of this review was established at an expert consultation in which we participated,
hosted by TDR on April 23–24, 2007. The experts convened to examine the current status
of applied social science research in tropical disease control, identify ongoing challenges,
and develop a strategy to mainstream gender and the social sciences within TDR. Priority
areas for the review were based on consensus panel discussion. Literature reviewed
was identified through MeSH heading searches in Web of Science, PubMed, and Scopus
using various combinations of terms including social science, tropical diseases, neglected
diseases, gender, and poverty. The review also drew on research funded by TDR and
work conducted by TDR-trained scientists, represented both in peer-reviewed journals
and in grey literature. Our aim was to inform developments in the identified key areas,
and reflecting this aim, we have not sought to cover comprehensively all social science
research in tropical and neglected diseases. In addition, we do not necessarily reflect
the views of WHO, nor specifically those of TDR.
The Evolution of Themes in Social Research on NTDs
The research themes and priorities for social research on NTDs reflect evolving approaches
and discourses in international public health and the specific public health challenges
of the era. In the early 1950s, well before the international health community would
coin the term “neglected tropical diseases,” public health practitioners involved
in infectious disease control programs had developed a keen interest in applied social
science research. Considerable work began to focus on understanding reasons for adverse
reactions to vertical infectious disease control efforts [6]. Later, notable advances
in medical anthropology led to health social science applications in health education
and community participation [7]–[9].
In the 1970s, primary health care, community participation, and support for horizontal
health care systems emerged as important concepts and tools to address health inequalities.
TDR was established as a joint special program of the United Nations Development Programme
(UNDP), the World Bank, and WHO (now with the partnership also of the United Nations
Children's Fund [UNICEF]) to counteract the neglect in research and development efforts
for tools to combat infectious diseases among the poor [10],[11]. The program recognized
not only the impact of infectious diseases in undermining people's health but also
the links between economic development, poverty alleviation, and good health. In 1976,
anticipating the emphasis on community and society iterated at the Alma Ata Conference
(1978), the then Director-General of the WHO, Dr. Halfdan Mahler, emphasized that
the “(TDR) Programme was not designed simply to advance medical technology but rather
as a contribution to the promotion of human welfare in the widest sense, in the context
of a new international order in economic and social affairs.” The first technical
review group called for “a commitment to long-term continuity of (such) research,
which had been lacking from most previous efforts in the field.” Preparations to do
this took two years because of the absence of a social research community and significant
relevant research tradition on which to build; the first TDR Steering Committee on
Social and Economic Research became operational in late 1979.
TDR funded a significant number of young scholars for higher degrees as well as an
expanding number of research projects through the Research Strengthening Group and
the Steering Committee on Social and Economic Research, and after 1994, through various
initiatives and task forces on applied field research [12]. These committees oversaw
the development of methods and basic research to describe the effects of poverty,
gender, quality of care, and other socio-cultural contexts on exposure, experience,
health-seeking behaviors, and sequelae of disease. They included projects concerned
with interventions, with particular attention to the potential merit of social science
information to national control programs and nongovernmental organization and private
sector interventions. This work included the development of rapid assessment tools
for malaria [13]–[16], the use of school-based surveys to assess community prevalence
of schistosomiasis [17]–[22], the establishment of economic analyses of tropical disease
research and interventions [19], [23]–[26], the development of gender-sensitive health
services interventions [27]–[31], and the implementation of collaborative work on
the household management of fever to support the early diagnosis and treatment of
malaria and pneumonia [32]–[34]. Important social research breakthroughs resulting
from field research initiatives included the development of the concept of community-directed
treatment for onchocerciasis, insecticide-treated bednets, and development of unit
dose packaging (blister packs) for easy distribution of anti-malarials to communities
and homes — interventions that empowered community members to take simple measures
on their own to prevent disease and protect their health. The research programs developed
from 1979 to the mid 1990s highlighted a commitment by collaborating researchers in
the concerted and systematic application of trans-disciplinary social sciences in
tropical disease research and control programs [35]–[38].
Over the decades, a considerable sub-literature on social sciences in infectious diseases
and their control has emerged, including chapters in textbooks of tropical medicine
[39]–[41], resulting in significant bodies of evidence in health economics, health
policy research, and (medical) anthropology of infectious diseases [42]. A missing
and critically needed perspective in research was the foregrounding of gender [27],
[38], [43]–[53]. The link between gender and exposure, risk, susceptibility, disease
experience, and outcome was established through a number of studies, based on secondary
analyses of quantitative data and new qualitative studies explicitly concerned with
gender and its impact on vulnerability and outcome. These studies highlighted differences
in rates of infection tightly correlated with economic activities and social status,
and drew attention to significant disparities in access to treatment. This work resulted
in the increased collection and reporting of sex disaggregated data, and increased
attention to the effects of both sex and gender on disease. Research on female genital
schistosomiasis, relationships for women between stigma and treatment, and gender
inequalities in access to resources and presentation for care provide powerful examples
of developments in this area [47], [52], [54]–[62].
In the mid 1990s, “upstream” issues such as globalization, equity, gender, and human
rights gained increasing prominence in international health. In 2000, a new TDR Steering
Committee on Social, Economic, and Behavioural Research (SEB) was established with
the mandate to build on, promote, and support social research identifying constraints
in, and opportunities for, infectious disease control and prevention in resource-poor
settings. Emphasis was placed on elucidating social, cultural, economic, health-systems,
and policy-related factors, and proposing strategic solutions to barriers in disease
control and public health. In contrast to the work of the earlier committees, attention
now was placed on social research that would address large-scale, “transnational”
issues and challenges in relation to infectious diseases and their control. Researchers
were encouraged, in this context, to attend to the societal and economic impact of
globalization as well as specific disease and health-systems factors [12]. A clearer
elucidation of globalization led to research on the impact of widening social inequalities
on disease persistence, emergence, and resurgence [63]; the effects of political conflict
and other forms of violence on NTDs; the role of community resilience; the ethical,
legal, and social implications of biotechnology use and transfer into resource-poor
settings [64]; and a human rights analysis of NTDs [65]. Research with a sharper focus
on public health systems in endemic countries focused on equity effects of health
sector reforms [66], research ethics [67], and inequalities of access to proven therapies,
prevention, and information. Research in health economics focused on human resources,
including difficulties in sustaining the health research workforce and retaining both
volunteers and health system staff [68]. While some research was also conducted on
private sector collaboration and emerging interest in public–private partnerships
(PPPs) [69], this has been generally limited because of poorer investment in research
[70]. TDR's social research activities address both basic social science and implementation
research issues, including most recently research on community-directed interventions
for major health problems in Africa [71].
The research programs and related training of social scientists have consolidated
the role of social sciences in the tropical disease agenda, particularly with respect
to a stronger evidence base on the social determinants of health, on potential areas
for interventions, and on preliminary developments in the area of implementation research.
However, major challenges remain in understanding the complex interactions of community,
household, personal, and governmental factors that maintain health and produce disease,
and in finding effective ways to address these issues at various political levels.
Continuing and Emerging Themes
As reflected in the bibliography, the social science and applied health literature
on infectious diseases of poverty is substantial, but uneven across diseases, themes,
regions, and institutions. There is, for example, greater attention to communities
who are vulnerable to disease, and less to institutions involved in disease prevention
and control. Below, we draw attention to what we regard now as the most urgent and
emerging research questions.
Government, Community, and Environmental Change
Continued research is needed on the implementation of interventions and control programs
to ensure a critical evidence base to inform the effective, sustained, and embedded
adoption of interventions by communities [72]. This involves a more critical understanding
of government decision-making and individual choices related to disease prevention,
and a better understanding of how the relationships of people to their governments
influence adherence, shared commitment and community participation in control programs
[73],[74]. Since the Alma Ata Declaration of 1978, there has been considerable interest
in community involvement, volunteer activities, relationships between local governments
and communities, and decentralization. Early work focused on the ways in which these
approaches might work to control infectious disease in rural areas, where there were
almost always limited resources, poor infrastructure, and lack of services. But the
prevalence of infectious diseases in urban areas has become an increasing concern,
reflecting global trends in urbanization and the inability of urban as well as rural
governments to manage infrastructure and meet the health and welfare needs of their
populations. Conflict usually results in or contributes to a breakdown of health services
infrastructure and migration of vulnerable populations, often with a negative impact
on the control of NTDs.
Increased urbanization is partly driven by economic changes, but also by environmental
and climate change, resulting in changed patterns of land use and residence, and changes
in vector habitat and behavior. Global warming has both direct and indirect effects
on the distribution and prevalence of NTDs, highlighting the need for further research
on the links between society, environment, agriculture, and human health, and the
relationship of these factors to the control of neglected vector-borne diseases such
as dengue [46],[75]. Water resource development schemes often lead to new exposure
of vulnerable populations, and health impact assessments based on social science approaches
are critical. Further research is also needed on community participation in the prevention
and control of disease in urban and peri-urban slums; on the social organization of
urban areas to establish mechanisms for the implementation of community-directed treatment
approaches in cities; and on vertical versus horizontal approaches and effective implementation
of interventions under decentralization.
Notwithstanding growing attention to health programs, health services, and access
to care, research is still required to explore how access to health services is conditioned
by poverty and inequality, as shaped by structural and political-economic factors
(gender, ethnicity, migration patterns, etc.). In an emerging research agenda, there
is a need to move to explore practical ways to disrupt disease transmission and enhance
accessibility of care. Because of changes in land use, climate, and population demographics,
and subsequent changes in the distribution of NTDs and continuing risk of drug resistance,
there is a need too for ongoing research on the maintenance of disease control in
areas of low prevalence. This will enable monitoring and prevent resurgence, without
the need for resource-intensive programs. The various roles of the not-for-profit
sector, industries, and civil society need further exploration. There are also continuing
questions regarding government and population interactions, governance and government
institutions [73],[76].
The research on gender has almost without exception focused on issues affecting women
with a disregard for how gender affects the disease experience of men. The fluid nature
of the concept of gender and its dynamic interaction with other determinants of vulnerability,
such as socioeconomic status, ethnicity, and age, also remain poorly understood. Our
understanding of the significance of and interactions between gender differences and
other social and economic variables is sparse, and little work has been conducted
to apply our current knowledge from gender studies to the development of gendered
policy and practice across all aspects of the health sector, including human resources
and capacity building. These issues need to be understood within a broader political
and environmental context that takes into account issues such as inequality, political
instability and violence, displacement, and globalization [77].
Biomedicine and Innovation
New biomedical priority areas need to be enhanced by social science research. Innovative
vector control interventions and new drugs and diagnostics need to be considered in
terms of their introduction, acceptability, and adherence, and the integration of
such innovations as a component of community-based interventions. Research needs to
be undertaken on the acceptability and utilization of drugs in multi-intervention
approaches for disease control (e.g., combined use of praziquantel and oxamniquine),
including in relation to the acceptability and affordability of new approaches and
new drug regimes. People in endemic areas frequently have multiple infections; however,
limited work has been undertaken on the social implications of this. Other areas requiring
greater attention include decision-making regarding treatment, the impact of complex
treatments, particularly when a person has more than one communicable and/or non-communicable
disease, willingness to carry the cost of treatment for recurrent infections, and
attitudes towards side effects.
Research needs to be continued on the supply and distribution of drugs, including
in relation to the proliferation of counterfeit drugs, the failure or inability to
adhere to prescribed treatment regimes, the illegal circulation of drugs, and other
questions on the use of pharmaceuticals and the roles of the private sector [78].
With the increase in large-scale drug-based, multi-disease control programs, it is
necessary not only to monitor pharmacological side effects (“pharmaco-vigilance”),
but also to understand evolving attitudes in the target populations (“socio-vigilance”).
A number of NTDs, particularly helminthic infections, leprosy, and in India, Nepal,
and Bangladesh, visceral leishmaniasis, have the potential to be eliminated. To support
this effort, further work is needed on cost-effective strategies using optimal interventions
that include both treatment of disease and where applicable, vector control.
TDR's social research activities address both basic social science and implementation
research issues, including most recently research on community-directed interventions
for major health problems in Africa [71]. Political and economic changes, with or
without violence as a backdrop, influence the willingness of populations to trust
in and collaborate with disease control agencies, and their preparedness to develop
common goals for disease prevention. Again, the relationship between communities,
householders, and the public and private sectors, and the optimal ways of bringing
these together, needs to be explored. Strategies are required to extend integrated
disease control programs for NTDs and malaria in areas where community-directed treatment
programs are established, as in onchocerciasis control areas.
Capacity Building and Managerial Issues
The hierarchical structure of personnel within the health sector in many disease-endemic
countries stems from a colonial legacy that privileges the knowledge and contributions
of biomedically trained personnel, and fails to appreciate fully the importance of
engaging with a range of health professionals, such as lay providers, volunteer workers,
and traditional specialists, to enhance the effectiveness of behavioral, household,
and community-based interventions [72]. There is a need to pursue the integration
of NTD control and routine primary health services [79] and to analyze the reasons
why NTD prevention activities and outreach receive low priority [80],[81]. It is clear,
for instance, that health sector reform has not produced a uniform community gain,
and those who are most vulnerable to NTDs are often hardest hit [82]. PPPs have been
proposed as an alternative. However, the relationships between public and private
providers, and the viability of this approach in different settings, is complex, partly
because of different interests and commitments to disease control [83]. Reflecting
this, there has been limited investment in social science and health systems research
on private sector collaboration with disease control programs [70].
While social scientists need to engage in research related to health policy, administration,
and management, in countries where NTDs are endemic, there are still few applied social
scientists working on health-related questions, and a limited understanding within
the health sector of the contributions that they might make. Further, for non-medically
trained health service personnel engaged in research and in the design and delivery
of programs, there is usually a limited career trajectory: social scientists are typically
employed at levels not commensurate with their qualifications, without opportunities
to utilize their specialized skills. This lack of recognition serves as a disincentive
for those with the capacity to return to or remain within the health sector, contributes
to their dissatisfaction in improving health services, limits the quality of applied
social science research, and inhibits the translation of relevant social science findings
into practice.
Conclusion
The research themes that we believe to be of key importance in the years to come fall
into two broad areas. One relates to globalization and its impacts: global warming
and changes in the epidemiology of disease, urbanization, anthropogenic environmental
change, and the availability, cost, and distribution of drugs. The other area relates
to the control of disease, and in this context, to community participation, government–community
partnerships, PPPs, health services research, and strategies for control of both single
diseases and multiple infectious diseases. It will take time to nurture and strengthen
new areas of research, not least if they are breaking new ground and are conceptually
difficult; it will also take time, and is always complex, to sustain the small group
of researchers working in these fields in endemic countries. Strategies and resource
allocation need to be based on long-term outcomes.
NTDs are referred to often as diseases of poverty, but implicit in the use of the
term poverty is the tight inter-relationship of poverty and inequality. This reference
to poverty extends to include individuals, households, communities, and countries.
It refers to the individuals and households affected by infectious diseases, the effects
of continuing, untreated infection, and the impoverishment that occurs as a direct
result of disease and the high costs of health care. It refers to the material circumstances
of communities at risk—in poor, isolated, and ill-served rural areas and in the sub-standard
conditions of urban slums and squatter settlements. It acknowledges, too, the difficulties
faced by countries too poor to provide the infrastructure, human resources, and services
that reduce the toll of such infections, and that are crippled by international debt
and economic disadvantage in ways that are echoed in the incidence and prevalence
of diseases. A social science perspective on diseases of poverty is critical to ensure
that equity remains an underlying principle in policy development, research, advocacy/dialogue,
legislation, resource allocation, planning, implementation, and monitoring of programs
and projects.
Box 1. Key Learning Points
Social research has drawn attention to the difficulties in ensuring effective and
sustained interventions for NTDs in both urban and rural communities, and in environments
that have been disrupted by war, resettlement, and migration.
Gender has a major impact on the distribution of disease, risks of transmission, and
diagnosis and patterns of care. However, the links between gender differences and
other social and economic variables, such as socioeconomic status, ethnicity, and
age, are poorly understood.
Social research on community diagnosis, treatment, and control highlights the importance
of community participation for the successful introduction, acceptability, and adherence
of innovative vector control interventions and new drugs and diagnostics.