Published by Oxford University Press on behalf of the International Epidemiological Association
Ó The Author 2005; all rights reserved. Advance Access publication 8 September 2005
International Journal of Epidemiology 2005;34:961–966
doi:10.1093/ije/dyi188
EDITORIAL
Non-communicable diseases in low and
middle-income countries: a priority
or a distraction?
Shah Ebrahim1* and Liam Smeeth2
Waging a war on non-communicable
diseases?
Non-communicable diseases (NCDs) as a proportion of total
mortality inevitably rise as an epidemiological consequence of
population ageing and hazardous exposures, particularly smoking, increase. A decade ago we were told that the ‘ageing crisis’
would swamp public resources,1 and the same message
continues to be reiterated.2 Now we are being told that NCDs
in the developing world represent a ‘race against time’,3 although
over the last two decades the ‘threat’ of coronary heart disease
has been continually highlighted, without much sign of
prioritization.4–7 In the majority of countries, all-cause mortality
at ages 15–59 has shown a persistent, downward trend over the
last two decades, although these favourable trends have been
attenuated markedly in sub-Saharan Africa and some eastern
European countries as a result of deaths due to HIV and to
injuries, respectively.8 As the crisis has not materialized and the
race has not yet been lost, it is pertinent to ask who are the likely
beneficiaries of these alarmist strategies. In the former case, the
private pensions sector stood to gain considerable investment
had World Bank policies to develop mandatory ‘multi-pillar’
systems of publicly and privately managed pensions and a
voluntary pillar of personal savings been taken up. In the latter
case it is the pharmaceutical and the global health care industries
that may benefit. Of course, in both cases, there is an altruistic
element of preventing suffering and helping the sick.
Defining NCDs by what they are not is imprecise and hides the
heterogeneity within this very broad, and ultimately rather
unhelpful categorization. Too often NCDs are discussed as if they
were synonymous with cardiovascular diseases, and while
coronary heart disease and ischaemic stroke will increase in
low and middle-income countries (LMICs), it is likely that
cancers common in LMICs—liver, cervix, and stomach—in
which infectious agents play causal roles, will decrease as
populations become more affluent. Disaggregation of the major
constituents of NCDs—coronary heart disease, ischaemic stroke,
haemorrhagic stroke, cancers, chronic obstructive airways
disease, asthma—would be preferable in discussing disease
burdens and strategies for intervention.
1
2
Department of Social Medicine, University of Bristol, Bristol, UK.
Department of Epidemiology and Population Health, London School of
Hygiene and Tropical Medicine, London, UK.
* Corresponding author. E-mail: [email protected]
The use of the phrase ‘low and middle-income countries’
(LMICs) as a synonym for developing countries has grown
rapidly, emphasizing the stratification of countries in the
currently dominant dimension of economics; in the context of
NCDs, it points towards the affordability of controlling and
treating them, and the likelihood of application of different
control strategies. Unfortunately data on the costs to individuals,
families, and society of NCDs in most LMICs is scarce, making
economic appraisal of affordability and sustainability of government health programmes impossible to assess with any
reasonable certainty. Within LMICs there is marked variation
in wealth and disparity in access to relevant health services for
NCDs. The concentration of NCDs in the urban elite of many of
the LMICs provides a powerful lobby for the development of
fragmented, private sector, high-tech curative services at the
expense of a coordinated public health response. What the urban
elite has today, the aspirant populations seek for the future,
further fuelling a potentially ineffective and expensive means of
‘waging war’ on NCDs.
Burden of disease
NCDs account for the majority of the global burden of disease
and, in LMICs, are projected to increase markedly. Table 1 shows
the estimated 10 leading causes of death in 2000.9,10 Table 2
shows projections based on the Global Burden of Disease study
for the 10 leading causes of death in 2020.11 The growing
importance of NCDs as causes of death is clearly seen, in
particular, in LMICs. One important caveat to looking at such
mortality data is that disabling but less life-threatening diseases
can appear unimportant, an issue that particularly applies to
mental illness. Indeed, when looking at morbidity rather than
mortality for the same year 2020 projections, unipolar major
depression is ranked as the number one cause of disability
adjusted life years in developing regions, and is ranked 2nd
worldwide and 3rd in developed regions.11 Counting deaths is
not without its challenges, but for non-fatal conditions,
particularly mental illnesses, thresholds for defining ‘cases’
will determine the scale of burden attributable to mental illness.
The United States National Institutes of Mental Health benefit in
terms of funding from evidence that ‘the burden of psychiatric
conditions has been heavily under-estimated’,12 and in the
absence of reliable global data for most non-fatal conditions, it is
impossible to discount opportunity for lobbying by interested
parties to ensure high placing in burden of disease statistics,
which increase their profile.
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INTERNATIONAL JOURNAL OF EPIDEMIOLOGY
Table 1 Estimated 10 leading causes of death in 2000
2000
Rank
World
Causes
% Total
Developed countries
Causes
12.4
a
% Total
Developing countries
Causes
% Total
Ischaemic heart disease
22.6
Ischaemic heart disease
9.1
1
Ischaemic heart disease
2
Cerebrovascular disease
9.2
Cerebrovascular disease
13.7
Cerebrovascular disease
8.0
3
Lower respiratory infections
6.9
Trachea, bronchus, and
lung cancers
4.5
Lower respiratory infections
7.7
4
HIV/AIDS
5.3
Lower respiratory infections
3.7
HIV/AIDS
6.9
5
Chronic obstructive
pulmonary disease
4.5
Chronic obstructive pulmonary
disease
3.1
Perinatal conditions
5.6
6
Perinatal conditions
4.4
Colon and rectal cancers
2.6
Chronic obstructive pulmonary
disease
5.0
7
Diarrhoeal diseases
3.8
Stomach cancer
1.9
Diarrhoeal diseases
4.9
8
Tuberculosis
3.0
Self-inflicted injury
1.9
Tuberculosis
3.7
9
Road traffic accidents
2.3
Diabetes
1.7
Malaria
2.6
Trachea, bronchus, and lung
cancers
2.2
Breast cancer
1.6
Road traffic accidents
2.5
10
a
North America, Europe, former Soviet Union, Japan, Australia, and New Zealand.
9
10
Sources: World Health Organization, Geneva (2002) Beaglehole R and Yach D, 2003.
Table 2 Estimated 10 leading causes of death in 2020
World
1
Ischaemic heart disease
16.3
Ischaemic heart disease
24.1
Ischaemic heart disease
14.3
2
Cerebrovascular disease
11.2
Cerebrovascular disease
12.7
Cerebrovascular disease
10.9
3
Chronic obstructive pulmonary
disease
6.9
Trachea, bronchus, and lung
cancers
5.9
Chronic obstructive pulmonary
disease
7.7
4
Lower respiratory infections
3.7
Chronic obstructive pulmonary
disease
4.1
Tuberculosis
4.1
5
Trachea, bronchus, and lung cancers
3.5
Lower respiratory infections
3.2
Road traffic accidents
3.9
6
Road traffic accidents
3.4
Colon and rectal cancers
2.7
Lower respiratory infections
3.7
7
Tuberculosis
3.4
Stomach cancer
2.4
Trachea, bronchus, and lung
cancers
2.9
8
Stomach cancer
2.3
Self-inflicted injury
1.8
Stomach cancer
2.3
9
HIV/AIDS
1.8
Diabetes
1.6
Diarrhoeal diseases
2.2
10
Self-inflicted injury
1.8
Road traffic accidents
1.7
HIV/AIDS
2.1
Causes
Developed countries
a
2020
Rank
% Total
Causes
Developing countries
% Total
Causes
% Total
a
North America, Europe, former Soviet Union, Japan, Australia, and New Zealand.
11
Source: Murray CJL, Lopez AD, 1996.
Data for population surveillance of NCDs are limited in many
countries. The World Health Organization has set up a range of
projects aimed at improving the amount and quality of relevant
data. The Surveillance of Risk Factors (SuRFs) project, launched
in 2003, presents chronic disease risk factor profiles from 170
WHO member states. These data include tobacco and alcohol use,
patterns of physical inactivity, low fruit/vegetable intake,
obesity, blood pressure, cholesterol, and diabetes. The most
recent report SuRF2 came out formatted on a rectangular CDROM (Figure 1), and enables between country comparisons to be
made.13 This initiative has been made possible by investment in a
global archive of survey data—the WHO Global InfoBase—
representing a major resource that should be valuable for health
planning and policy evaluation. Figure 2 shows data on the
percentage of adults in the different countries of the Association
of Southeast Asian Nations who have a body mass index
(BMI) .30 kg/m2, pulled down from the online Global InfoBase
in a few minutes. The variation is marked. Why should two of the
poorest countries in the region, Laos and Myanmar, have severe
obesity rates comparable with some of the wealthiest? Why is
Singapore, the most developed country in the region, not
suffering an obesity epidemic? The ease of online data access
comes at the price of obscuring the source and limitations of the
data, and the extent to which they have been imputed or are real.
In this case, the differences are an artefact generated by the
estimation of BMI percentage over 30 kg/m2 for Laos and
Myanmar, which both lack real data, from a regression of log
(gross domestic product per capita) on mean BMI for countries in
the Western Pacific region. Singapore is in a different WHO
region from Laos and Myanmar, and consequently, their
estimated BMIs are not directly comparable with countries in
other regions (John Shannon and Tomoko Ono, WHO: personal
communication).
In order to improve data collection relevant to NCDs, WHO has
promoted the STEPS approach in which Step 1 relies solely on
risk factor information generated from questionnaires, Step 2
NON-COMMUNICABLE DISEASES IN LOW AND MIDDLE-INCOME COUNTRIES
963
Figure 1 Although it looks improbable, the rectangular disc really does fit into your CD-drive!
26%
14%
Brunei
Thailand
Laos
Myanmar
Malaysia
Philipines
Singapore
Female
Male
Indonesia
Cambodia
Vietnam
0
2
4
6
8
10
12
2
Percent BMI 30+kg/m
2
Figure 2 Use of WHO web Global InfoBase: check the sources carefully! Obesity (BMI > 30 kg/m ) in the Association of Southeast Asian Nations
in 2002
includes physical measurement of BMI and blood pressure, and
Step 3 adds measurement of blood cholesterol and blood glucose.
This approach to monitoring makes the assumption that the steps
are of progressive difficulty, but it is apparent that complex
exposures—alcohol intake, fruit and vegetable consumption,
and physical activity—show great between country variability in
their associations with coronary heart disease, reflecting the
intrinsic difficulty of making accurate and comparable assessments using simple questionnaires.14 Surveillance of NCD risk
factors is not an end in itself, and requires further discussion of its
purposes, particularly in relation to evaluation of intervention
strategies. WHO’s primacy in providing information of potential
value to policy makers will be challenged by the emergence of the
Ellison Institute at Harvard University and the Health Metrics
Network, the former funded by Larry Ellison of Oracle
Corporation and the latter by the Gates Foundation.15 Perhaps
the most important role for these new sources will be to give a
clear separation between provision of information and its use in
advocacy, a problem that besets WHO in its attempts to fulfil
both roles.16
A priority or a distraction?
Global and even region-specific estimates of disease burden may
not reflect the health problems faced by the world’s poorest
people who, of course, face the greatest threats to their health.
The probability of a woman aged between 15 and 60 dying from
an NCD is 12% in sub-Saharan Africa whereas it is 5% in
developed high-income countries.17 However, her risk of dying
from communicable disease or obstetric hazards is higher still at
17%. In men aged between 15 and 60, risk of dying from NCDs is
15%, from injuries and violence 13%, and 11% from communicable disease. In sub-Saharan Africa, communicable diseases,
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INTERNATIONAL JOURNAL OF EPIDEMIOLOGY
notably HIV/AIDS, malaria, tuberculosis, and diarrhoeal disease
remain the leading causes of death, and outnumber NCDs by
almost 2:1 over all ages. The world’s poor face a double jeopardy:
the highest risk of communicable disease and the highest risk of
NCDs. It has been argued that for the poorest 20% of the people
in the world, successful tackling of communicable diseases will
bring greater health gains than reducing rates of NCDs.18
However it must be recognized that the issue is not simply
replacing strategies for communicable disease by new ones
for NCDs—for example, maintaining effective vaccination
programmes and tobacco control should be priorities in all
countries.19 Differing patterns of disease risk are not just a
regional concern: they can be an important issue within
individual countries. Around half of the world’s poorest
20% of people live in India, mainly in rural areas, and NCDs
are probably not the major threat to their health. However, in
urban areas and among slightly better-off sections of the Indian
population, cardiovascular disease is emerging as a huge health
problem.20–22
In high-income countries we have witnessed the enormous
benefits of preventing and controlling many communicable
diseases. Implementing successful measures to reduce the
burden of communicable disease must remain a key priority
for the poorest populations. Research and development into
NCDs in the poorest countries must not divert resources away
from dealing with the immediate and larger threat from
communicable diseases. In the extreme scenario, worrying
about obesity and high cholesterol among people facing famine
and who are devastated by outbreaks of communicable disease is
clearly ludicrous. However, just as NCDs have emerged as the
major health threat in middle-income countries, we must face
the reality of their emergence in many of the poorest areas of the
world too. A systematic shift in the risk of NCDs to LMICs will
increase global inequalities, further exacerbated by existing
social inequalities in smoking behaviour,23 particularly in those
areas facing a persistent high burden of communicable disease.24
Causes of NCDs
Although, the biological determinants of NCDs in LMICs are
likely to be similar to those in affluent countries,25 the drivers of
these determinants are likely to differ. For example, rural–urban
migration may be an important factor in promoting the adoption
of Western dietary habits and activity patterns, leading to an
increased risk of NCDs. Socioeconomic patterns of disease risk, so
well established in affluent countries, are more complex in some
LMICs.26 Population attributable fractions for specific risk factors
will differ owing to differences in the distribution of such factors
in different settings.25,27 New opportunities to use large
demographic surveillance projects as tools to study NCDs are
emerging rapidly as part on the work of INDEPTH (International
Network of field sites with continuous Demographic Evaluation
of Populations and their Health in developing countries).28
Without studies of NCDs in LMICs, understanding of the
determinants of the rise and fall of specific NCDs will not be
possible. Understanding how rural–urban migration increases
risks of obesity, diabetes, and CVD would be useful for their
prevention. Explaining the differences in obesity prevalence in
different countries apparently exposed to very similar lifestyles
would increase our chances of modifying the rise in obesity. The
role of impaired early growth, resulting from fetal and infant
under-nutrition, as a cause of adult obesity, hypertension,
diabetes, and cardiovascular disease demonstrates that undernutrition and over-nutrition are linked, operating at different
stages of the life course.29,30
Showing, for example, that smoking causes lung cancer and
cardiovascular disease in China (or any other LMICs) is
considered by many to be a vital part of changing the policy
environment towards NCDs, putting them on the government
agenda. Peto has commented ‘the magnitude of tobacco as a
cause of death in poor countries was not understood’ and
believes that without the epidemiological results available in
Britain, the deaths from tobacco-related disease could have been
much greater. He comments ‘outside Britain, North America,
Australia, New Zealand, and Scandinavia, the medical profession
is not serious about the evidence, and the journalists are certainly
not serious—they just treat it as a joke, like saying you shouldn’t
eat cream buns.’31 Peto and Chen’s work on smoking and
mortality in China has demonstrated that even early in the
epidemic a high proportion of adult male deaths could be
attributed to smoking, and if current smokers do not stop
smoking, there are a massive number of smoking related deaths
in the pipeline.32 Although we know that cholesterol and obesity
are associated with coronary heart disease, it is mainly through
aetiological studies in China that we now know that the gradient
of risk extends from the very lowest levels of both risk
factors.33,34 Aetiological studies may also provide important
levers for necessary political action as demonstrated by the
Mauritian government’s switching of cooking oil composition
from palm to soya in the face of epidemiological evidence of
very high blood cholesterol levels.35
Control and management of NCDs
Effective forms of prevention and treatment for many NCDs are
available; should people in LMICs be denied access to them?
Although, there can be no debate on tobacco control measures as
the lynch pin of every LMICs starter-pack for NCD prevention
and control, the political will to implement the necessary fiscal
and social measures is often limited. Opportunities also vary—
the geo-political nature of Bhutan made a total ban on import,
selling, and use of tobacco products feasible (http://news.bbc.co.
uk/2/hi/south_asia/4012639.stm). The same policy could not be
successfully implemented within the porous borders of tobaccogrowing Laos, where smoking in rural malarial areas can be as
high as 90% and acts as a mosquito repellent.36
For primary prevention, we must resist exporting the failed
ideas of individually-targeted health promotion and should
concentrate on policy and fiscal measures.37 However, we can do
much better at ‘exporting success’: several secondary prevention
strategies are effective at the individual level and as drugs come
off patent could be delivered quite cheaply and affordably for
middle-income countries.38 There is a growing notion that some
form of combination pill,39 containing an anti-hypertensive, a
cholesterol-lowering statin, aspirin, and possibly folic acid and
made widely available, could be a mainstay for primary
prevention of cardiovascular disease. Although, such drugs are
clearly effective and cost-effective in some people and settings,
NON-COMMUNICABLE DISEASES IN LOW AND MIDDLE-INCOME COUNTRIES
a dual approach—both treating high-risk individuals and
population measures—is needed.9,40 In LMICs it will be
necessary to ensure that interventions focused on improving
eating habits and activity patterns are not ignored in preference
to drug treatments.41
Very little relevant cost-effectiveness data are available to aid
decision making in LMICs and virtually nothing is known of the
public’s views on resource allocation for health. In high-income
countries, the notion that rationing of publicly funded health
care is an inevitable consequence of an imbalance between
supply and demand relies more on assertion than it does on
evidence.42 In many LMICs, with regard to NCDs, the
conceptualization and operationalization of health care need
and supply is in its infancy. Without independent investigation
and evaluation it is likely that the vested interests of multinational corporate health industries will determine the rules of
what is to be treated, by whom and at what cost to individuals
and governments.43 WHO’s forthcoming report—Preventing
chronic diseases: a vital investment—may help in building
consensus and as an advocacy tool in its attempt to debunk many
of the myths surrounding chronic diseases and in providing a
guide to effective and feasible interventions that can be
implemented immediately.44
Ethical issues
An objection to conducting public health research on NCDs in
LMICs is that the investigators, institutions and governments are
seldom able to offer or identify appropriate health and social care
provision to participants in research studies who have or will
develop NCDs, raising an apparent ethical issue. This is
something of a ‘Catch 22’ as the problem can be articulated as
‘NCDs can’t be studied without effective infrastructure and
treatments, but these won’t arise without studies showing they
are needed’. Clearly, researchers of HIV/AIDS in sub-Saharan
Africa were, and still are, unable to ensure an equitable and
sufficient supply of anti-retroviral drugs to participants in their
studies or to the wider population. At the root of this perspective
on the ethics of medical research are the massive inequities in
health and wealth between countries and a trend in HIV/AIDS
drug trials to see the developing world as a passive partner or a
research laboratory in which lower ethical standards could be
applied.45 Prior agreement to apply any treatments found to be
beneficial is enshrined in the Council for International Organisation of Medical Sciences guidelines but it has been noted that
these principles are only appropriate for a very narrow range of
phase III drug trials and simply do not apply to epidemiological
research.46 However, this does not exonerate public health
researchers from considering issues posed by Bonita and
Beaglehole: what is the nature of involvement, and obligation,
to participants in research and will any benefits accrue to
participants through taking part in the research,47 be it on
chronic or communicable diseases. Much current health research
exacerbates north–south inequity and more work must be done
on creating stronger partnerships.48
Conclusion
We believe that some NCDs in most LMICs are a priority now
and it would be a serious mistake to ignore their prevention and
965
control in the coming decade. What sort of response should be
made with respect to public health research and practice? Clearly
NCDs do not lend themselves to the vertical programmes that
have been used for communicable diseases. However, drawing
out parallels with communicable disease and using them to
develop more appropriate health care systems for all patients
with long-term needs would be a valuable way forward. For
example, the needs for continuity of care, of monitoring and
long-term follow-up for HIV patients on anti-retroviral treatment
closely mirrors the clinical management of any chronic disease
control programme. What we have learnt from communicable
diseases is that without proper integration into existing health
care systems, disease control programmes often become unsustainable. It would be useful for international agencies, governments, and funding agencies to debate and produce a common
agenda for action on NCDs—in the same way as has been done
for communicable diseases—focused on their causes, prevention,
and control within the context of the broader health care
system, and including systematic review of available evidence,
needs for new research, education, training, and capacity
development.
Acknowledgements
We are grateful to Robert Beaglehole, Zulfiqar Bhutta, Pascal
Bovet, Zhenming Chen, George Davey Smith, Majid Ezzati,
Sanjay Kinra, and Debbie Lawlor, David Leon, and Salim Yusuf
for helpful comments on an earlier draft of this paper. The views
expressed in this paper are those of the authors.
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