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Vol.22 No.10
Parasites, people and policy: infectious
diseases and the Millennium
Development Goals
Robert M. May
Department of Zoology, Oxford University, Oxford, OX1 3PS, UK
Here, I briefly review past history and present patterns in
the interactions between parasites (defined broadly to
include viruses and bacteria along with protozoan, helminth and arthropod parasites) and human populations
in developed and developing countries. Against this
background, I offer thoughts on current public health
initiatives at national and international levels, with
particular reference to the Millennium Development
Goals. The news is both good and bad: mortality and
morbidity from infectious diseases in the developing
world are significantly lower than they were 50 years
ago, but we should and could be doing better, particularly in relation to neglected tropical diseases.
Introduction
The eight Millennium Development Goals, or MDG,
enunciated by the UN are set out in Box 1. Parasitic
infections relate directly to three of these eight (namely,
numbers 4, 5 and 6) and are closely involved in two others
(namely, the important numbers 1 and 2). In making this
claim, I define parasites broadly to include both microparasites and macroparasites, in the sense defined by Anderson and May [1,2]; that is, I include viruses and bacteria
along with the protozoan, arthropod and helminth agents
of conventionally defined parasitology.
In what follows, I sketch some past and present patterns
in the interactions between humans and parasites. The
general trend here could be called ‘good news’. I then turn
to the ‘bad news’: the persisting distinction between diseases of the rich and diseases of the poor. Against this
background, I discuss possible actions to achieve a fairer
world: this discussion covers, among other things, research
priorities (basic knowledge), economic impediments to
developing medical products for diseases of the poor,
and ideas for new incentives. I conclude with some worries
about new or re-emerging infectious diseases.
Good news: the past 50 years and the present
A comparison of survivorship curves for a typical developed
country and a typical developing country 50 years ago
(Figure 1) shows that the curve for developing countries
is better, but not much better, than those inferred for our
hunter-gatherer ancestors before the dawn of agriculture
(Figure 2).
Corresponding author: May, R.M. (robert.may@zoo.ox.ac.uk).
Available online 27 September 2007.
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As a global average, life expectancy at birth 50 years ago
was 46 years, with an average difference of 26 years
between developed and developing countries. Today, as
a result of better understanding of the transmission
dynamics of infectious diseases and of methods for their
treatment and control (better hygiene, improved water
supplies, vaccination, control of vectors, simple rehydration procedures for infant diarrhoea, etc.), average life
expectancy at birth is 64 years. In India, for example,
average life expectancy in 1950 was 39.4 and 38.0 years
for males and females, respectively. The corresponding
figures in 1998 were 62.1 and 63.7. This change occurred
primarily because the average gap between developed and
developing countries has diminished to a still-distressing
12 years.
It is, however, interesting to compare Figure 1 with
Figure 3, which shows the survivorship curve in mid-19th
century Liverpool, which is fairly typical of early industrial
centres in the West. In the 19th and early 20th century
slums in Western cities, mortality rates were appalling. A
child born in Liverpool in 1860 had only a 50% chance of
living beyond five years [3]. By contrast, in 2006, !130
million children were born, and although some ten million
will not survive the first five years (for a mortality rate of
!8%), the odds are better than in the past for the developed
world.
Why are today’s developing, low-income countries much
healthier than today’s high-income countries were at comparable stages of development? Interestingly, recent studies indicate that such improvements in public health
come mainly from scientific and technological advances,
rather than simply from ‘income growth’ (as some economists have rather mystically suggested). One such study
finds that income growth explains only 10%–25% of
increasing life expectancy [4]. Another finds that a decline
in infant mortality owes 5% to income growth, as against
21% to better education (Jamieson, D.T. et al. (2001)
Commission on Macroeconomics and Health Working
Paper WG1:4, [www.cmhealth.org/docs/wgl_paper4.pdf]).
Bad news: diseases of the rich and diseases of the
poor
These encouraging trends must, however, be set against
the still-wide gap in life expectancy, and general health,
between the developed and developing worlds. A more
meaningful measure of disease burden goes beyond life
0169-5347/$ – see front matter ! 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2007.08.009
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TRENDS in Ecology and Evolution Vol.22 No.10
Box 1. UN Millennium Development Goals
These are the goals that the UN aspires to achieve as the new
millennium begins. Conspicuous by its absence is any reference to
halting population growth (although it could be seen as implicit in 3
and 7).
1. Eradicate extreme poverty and hunger.
2. Achieve universal primary education.
3. Promote gender equality and empowerment for women.
4. Reduce child mortality.
5. Improve maternal health.
6. Combat HIV/AIDS, malaria and other diseases.
7. Ensure environmental sustainability.
8. Develop a global partnership for development.
expectancy to assess Disability Adjusted Life Years
(DALY; [5]). This quantitative measure combines premature mortality with years of productive life lost owing to
morbidity or disability. One DALY equals one year of
healthy life lost.
Figures 4a and 4b contrast the causes of DALY in
high-income (developed) countries with those in lowincome (developing) countries, respectively [6]. In the rich
world, communicable infections account for only !7% of
DALY. The corresponding fraction for poor countries is an
order of magnitude higher at 57%. Table 1 reinforces the
contrast shown in Figure 4a and 4b, by giving a catalogue
of infectious diseases for which 99% of the global burden
falls on the developing world.
Some facts associated with these differences in DALY
between rich and poor countries include the following:
(i) Health care infrastructure. In Europe, there are, on
average, 3.9 physicians per 1000 people; 2.7 in the
USA, and only 0.1 in sub-Saharan Africa, where the
problem is compounded by patterns of absenteeism
(assessed at !40% in one study [6]).
(ii) Basic research on diseases of the poor. Table 2 shows
the results of a study of research papers published in
Figure 1. Typical age-specific survivorship curves for human populations in
developed (open circles) and developing (black dots) countries 50 years ago.
Modified with permission from Ref. [23].
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Figure 2. Age-specific survivorship curve for a community of pre-agricultural
people, constructed from skeletons unearthed on the Moroccan Mediterranean
coast (modified with permission from Ref. [1], from data in Ref. [22]).
four leading medical journals in 2002 and 2003 [7].
The study assessed the overall proportion of papers
relating to diseases of importance to developing
countries. Given that such papers include those on
HIV/AIDS and on tuberculosis (TB) (both of which
are also significant problems in OECD countries),
the small fraction is surprising, as well as lamentable.
(iii) Drug development. In a study by Pecoul et al. [8], of
1233 pharmaceutical drugs licensed (worldwide) in
1995–1997, only 13 (1%) were for tropical diseases.
Moreover, of these 13, five came from veterinary
Figure 3. Age-specific survivorship curves for Liverpool in 1860 (black dots) and
for England in the 1990s (dashed line) [3].
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499
Figure 4. Disease burden (in DALYs) for (a) high-income countries and (b) low-income countries [5].
research and two from modifications of existing
medicines. Another two were developed by the USA
Military, and only four were developed by
pharmaceutical companies specifically for tropical
diseases of humans.
(iv) Pharmaceutical sales. Figure 5 shows world sales
of pharmaceutical drugs, broken down by regions.
North America, Europe and Japan account for
82% of sales, wereas Africa accounts for only
1%.
(v) Disease burdens and research efforts. Table 3 shows
the global burden of disease, measured in DALY, for
several major afflictions, along with expenditure on
research and development (R&D). This R&D expenditure in relation to DALY shows great variation,
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with malaria (by this comparative measure) receiving
less than one-tenth the attention given to cardiovascular problems.
Actions for a fairer world
What is currently being done to reduce the inequities
documented above? And what more might we do?
Private benefactors
No account of actions for a fairer world can be complete
without acknowledging the example and inspiration provided by the actions of individual private benefactors, of
which those of the Rockefeller Foundation over the years,
and the Bill and Melinda Gates Foundation more recently
(selflessly enlarged very recently by a massive gift from
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TRENDS in Ecology and Evolution Vol.22 No.10
Table 1. Diseases for which at least 99% of the global burden fell
on low- and middle- income countries in 1990
Disease a
Deaths per year
Diarrhoeal diseases b
Malaria
Measles
Pertussis
Tetanus
Syphilis
Lymphatic filariasis
Anclyostomiasis and necatoriasis
(hookworm)
Leishmaniassis
Schistosomiasis
Trichoriasis
Trypanosomiasis
Trachoma
Onchoceriasis (river blindness)
Chagas disease
Dengue
Japanese encephalitis
Poliomyelitis
Leprosy
Diptheria
2 124 032
1 079 877
776 626
296 099
308 662
196 533
404
5650
DALYs
(thousands)
62 227
40 213
27 549
12 768
9766
5574
5549
1829
40 913
11 473
2 123
49 668
14
––21 299
12 037
3502
675
2268
3394
1810
1713
1640
1585
1181
951
680
433
426
184
141
114
a
Global Burden, from Ref. [19].
Diarrhoeal diseases differ from the diseases in this list because they are a variety of
diseases, caused by different pathogens.
b
the world’s second-richest person, Warren Buffet), are
particularly notable.
Public incentives for private sector drug development
One major fact that underlies many of the above-mentioned
problems is the understandable failure of free-market
Table 2. Proportion of papers published in four leading medical
journals relating to infectious diseases of developing
countriesa,b
Journal
USA: New England Journal of
Medicine
Journal of the American Medical
Association
UK: Lancet
British Medical Journal
Overall:
Proportion of articles
Jan 2002
Jan 2003
7%
(7/97)
3%
(3/118)
7%
21%
24%
(12/180)
(50/234)
(66/273)
15%
4%
(5/138)
23%
18%
(52/227)
(44/242)
12%
a
These infectious diseases are defined in accordance with the UN Global Forum on
Health Research.
b
Based on Ref. [7].
mechanisms to deliver pharmaceutical products for diseases
of the poor. Pharmaceutical companies, quite properly, have
a responsibility to deliver both useful drugs and profits to
shareholders. For many things, this works well – better than
public ‘command and control’ mechanisms. However, the
R&D that leads to safe and effective pharmaceutical drugs is
an expensive and unpredictable process. No matter now
good the intentions, it does not make sense for a wellmanaged company to make a large investment in developing
a drug whose potential beneficiaries are, in aggregate, too
poor to pay the true costs (direct and indirect) that are
involved.
One possible way out of this dilemma is for governments
or other agencies to help pay for the delivery of the drug,
once it is developed. However, the costs of producing and
delivering a drug are typically small compared with the
basic costs of research, development and clinical trials.
Figure 5. The world pharmaceutical market: sales by region in 1998. Adapted from PhRMA, Annual Survey 2000, available at http://www.phrma.org/publications/profileoo.
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Table 3. Disease burden and funding comparisona
Condition
Cardiovascular
HIV/AIDS
Malaria
TB
Diabetes
Dengue
Global Disease
Burden (million)
DALYs
148.190
84.458
46.486
34.736
16.194
0.616
RandD Funding
(US$ Millions)
RandD Funding
per DALY (US$)
9402
2049
288
378
1653
58
63.45
24.26
6.20
10.88
102.07
94.16
a
Based on Ref. [20], p. 164.
Public bodies have generally been unsympathetic to the
needs of the pharmaceutical company once the drug exists:
once their money has been spent, and an effective product
achieved, the negotiating position of the pharmaceutical
companies in respect to ex post facto subsidy for delivery
understandably tends to be weak.
An important study by Kremer and Glennerster [6]
suggests a possible way forward, of benefit to both pharmaceutical companies and the disease-afflicted poor. The
basis of the idea is that the threshold for privately financed
investment in R&D toward a new drug is higher than the
corresponding social threshold, which takes account of the
public (economic) benefit of reducing DALY. The proposal
thus is that governments, individually or collectively (e.g.
via the UN), in advance guarantee purchase of the drug at
a price that makes both producers and consumers better
off: the producers, knowing the pay-off for a successful
product in advance, can take more risks than they would
if worried about the pay-off; society benefits from a healthier population and work-force. The basic idea is not new,
but this particular application is both new and potentially
hugely important.
Opposing bureaucracy or ideology masquerading as
accountability
Figure 6 gives an impression of the mind-boggling
proliferation of different agencies and ‘stakeholders’ that
Vol.22 No.10
jostle to do good things in the developing world. The growth
of well-intentioned public private partnerships for health
adds to the complexity here [9,10]. There is arguably a need
for egos and administrative structures to be subjugated to
disciplined, coordinated and effective actions.
This need is even more important when some of the
organisations involved seek to impose inappropriate moral
values – for example, opposing condom distribution (or
even disseminating lies about their being ineffective) in
relation to HIV transmission.
Avoiding priorities set by fashion
Most current activity on ‘diseases of the poor’ focuses on the
‘Big Three’: HIV/AIDS, malaria and TB. Molyneux [11],
however, has emphasized that the burden of other, relatively neglected, tropical diseases is roughly a quarter of
the global disease burden of HIV/AIDS, a third that of TB
and half that of malaria (all as measured in DALY). More
recently, Hotez et al. [12] estimated that the aggregate
DALY tally for neglected tropical diseases is 56 million,
which exceeds the tally for both malaria (46 million) and
TB (35 million).
Table 4 sets out 13 such ‘neglected tropical diseases’
which, in total, cause roughly half a million deaths
annually.
Despite the availability of cost-effective, stable and
successful agents for the control or elimination of each of
these 13 diseases, large numbers of the world’s poor remain
afflicted or at risk from this group of parasitic infections.
Molyneux et al. [13] urge that ‘‘The low costs [for alreadyavailable integrated control of neglected tropical diseases]
represent compelling figures to advocate for a pro-poor,
proactive public health strategy of preventive chemotherapy to be delivered to all affected populations of Africa’’.
Laxminarayan et al. [14], Canning [15] and Chan [16]
further develop this message in various ways and show
that DALY, thus averted, represent very ‘good buys’ in
economic terms. Easterly [17] further urges a focus on
Figure 6. A confusing cluster of agencies aims to help Tanzania with its HIV/AIDS epidemic. Modified with permission from Ref. [20].
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Table 4. Thirteen ‘neglected tropical diseases’ and their
etiologic agentsa
Protozoan Infections
African trypanosomiasis
Kala-azar (visceral leishmaniasis)
Helminth Infections
STH Infections
Ascariasis
Trichuriasis
Hookworm infection
Schistosomiasis
Urinary schistosomiasis
Hepatobiliary schistosomiasis
Lymphatic filariasis
Onchocerciasis
Dracunculiasis
Bacterial Infections
Trachoma
Leprosy
Buruli ulcer
Agents
Trypanosoma gambiense, T.
rhodesiense
Leishmania donovani
Ascaris lumbricoides
Trichuris trichiura
Necator americanus
Schistosoma haematobium
Schistosoma mansoni
Wuchereria bancrofti
Onchocerca volvulus
Dracunculus medinenis
Chlamydia trachomitis
Mycobacterium leprae
Mycobacterium ulcerans
a
Based on Ref. [13].
Table 5. Human population density and bushmeat harvestsa
Region
Density (people/km2)
Asia
(S and SE Asia)
Africa
(Congo Basin)
South America
(Brazilian Amazon)
522
Bushmeat harvest
(tonnes per year)
Unquantified
99
1–4 million
46
!100 000
a
Based on Ref. [21].
simple things done well, rather than highly complex and
elaborately planned interventions. In brief, we need to look
at our priorities in a more objective, analytic way, free from
the understandable inertia of yesterday’s activities and
fashions.
The future
Reader, in his book Cities [18], reminds us that ’Bacterial
and viral diseases are the price humanity has paid to live in
large and densely populated cities. Virtually all the familiar
infectious diseases have evolved only since the advent of
agriculture, permanent settlement and the growth of cities.
Most were transferred to humans from animals – especially
domestic animals. Measles, for instance, is akin to rinderpest in cattle; influenza came from pigs; smallpox is related
to cowpox. Humans share 296 diseases with domestic
animals.’ And the world’s cities become more crowded every
day. Three hundred years ago they contained 10% of the
Earth’s population; a century ago, 25%; today, 50%; by 2050,
they will contain almost 70%.
The resulting high aggregations, coupled with
increasing patterns of movements of peoples, present ideal
conditions for new infectious agents to emerge, or for old
ones to re-appear. These opportunities are further enhanced
by the increasing volume (amounting almost to globalisation) of the bushmeat trade, which previously was confined
to small-scale, local operations. We would do well to remember that HIV/AIDS, in effect, came from bushmeat: HIV-1
from chimpanzees, HIV-2 from monkeys. We were luckier
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with SARS, which came from the internationalisation of the
bushmeat trade in ‘exotic animals’ (specifically civets) to
serve suburban restaurants in South East Asia. Table 5
hints at the growing volume of this trade.
Quite apart from the implications for conservation
biology, we should be worried about the probable epidemiological consequences of this rapidly growing trade.
So?
In short, the world today is a healthier place than it has
ever been, both in developed and developing countries. But
although the inequalities are less marked than they were
50 years ago and there are encouraging signs that these
problems are being addressed, work remains to be done.
We should be giving more forward-looking thought to
reducing the probability that new infectious diseases will
appear, and to being alert and prepared if they do.
Understanding both the ecology and the evolution of
infectious diseases and their hosts is central to this. In
particular, there should be more concern about the rapid
growth of the bushmeat trade [21] and its likely implications for newly emerging diseases, and there should be
more strenuous attention to planning the coordination of
international responses to such events when they occur.
More prosaically, our actions should be more objectively
proportionate to needs, and less governed by past trends or
fashions, than is currently the case.
A pessimist could argue that, above all else, we need a
better understanding of the evolution of altruistic or cooperative behaviour, which unfortunately remains the biggest unsolved problem in evolutionary biology.
References
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2 Anderson, R.M. and May, R.M. (1991) Infectious Diseases of Humans:
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3 Cairns, J. (1997) Matters of Life and Death, Princeton University Press
4 Preston, S.H. (1975) Mortality Patterns in National Populations. with
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13 Molyneux, D.H. et al. (2005) Rapid-impact interventions. How a policy
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Elsevier celebrates two anniversaries with
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In 1580, the Elzevir family began their printing and bookselling business in the Netherlands, publishing
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Myles Textbook for Midwives.
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