Mounting anomalies in the
epidemiology of HIV
in Africa: cry the beloved paradigm
Devon D Brewer
PhD1,
Stuart Brody
PhD2,
Ernest Drucker
PhD3,
David Gisselquist
PhD4,
Stephen F Minkin
BA6,
John J Potterat
BA5,
Richard B Rothenberg
MD MPH7
and François Vachon
MD8
(Authors are
listed alphabetically)
1University
of Washington, Seattle, Washington, USA,
2Institute
of Medical Psychology and Behavioral Neurobiology, University of
Tübingen, Germany,
3Department
of Epidemiology and Social Medicine, Montefiore Medical
Center/Albert Einstein College of Medicine, New York City, USA,
4Hershey,
PA, USA,
5Colorado
Springs, Colorado, USA,
6Network
for Infection Prevention, Brattleboro, Vermont 05302, USA,
7
Department of Family and Preventive Medicine, Emory
University School of Medicine, Atlanta, GA, USA,
8University
of Paris 7, France
Keywords: HIV,
Africa, risk factors, epidemiology, heterosexual transmission,
medical transmission
Introduction
There is substantial
dissonance between much of the epidemiologic evidence and the
current orthodoxy that nearly all of the HIV burden in
sub-Saharan Africa can be accounted for by heterosexual
transmission and the sexual behaviour of Africans. The mounting
toll of HIV infection in Africa is paralleled by a mounting
number of anomalies in the many studies seeking to account for
it. We Propose that existing data can no longer be reconciled
with the exceptional role of sex in the African AIDS epidemic.
Anomalies in sub-Saharan Africa
Discontinuity
between HIV and STIs During the 1990s HIV propagated rapidly in
Zimbabwe, increasing at an estimated rate of 12% annually. At
the same time, the overall sexually transmitted infections (STI)
burden declined an estimated 25% and while there was a parallel
increase in reported condom use by high-risk persons
(prostitutes, lorry drivers, miners, and young people)1.
This example frames the problem: why would a relatively low
efficiency sexually transmitted virus like HIV outrun more
efficiently transmitted STI2?
In the notable four-cities study3,
many common sexual risk factors linked to HIV transmission (eg,
high rate of partner change, sex with prostitutes, and low
condom use) were not correlated with HIV prevalence-although
some risk markers (young age at first coitus or marriage, large
age difference between partners) and presumed facilitating
factors (lack of circumcision, genital herpes, and
trichomoniasis, but not bacterial STI) were. In addition,
concurrency of sexual partnerships was not correlated with HIV
prevalence, yet was associated with bacterial STI4.It
is of concern that many key sexual transmission variables are
not associated with a large HIV epidemic in Africa, yet do
correlate, as expected, with other STIs.
Transmission efficiency
A study of HIV
transmission efficiency in Africa, using data from
serodiscordant couples5,
produced estimates remarkably similar to those reported for
couples in the developed world6.
Observed probabilities presumably reflect some of the influence
of facilitating factors (eg, unorthodox sexual practices,
circumcision status, STI exposure, etc) recruited to explain the
'turbo effect'7
noted in Africa's epidemiologic context. Recent empiric research
casts doubt that such co-factors can sufficiently amplify the
force of infectivity to account for observed trends in the
sexual transmission of HIV in Africa8.
The anomalies regarding transmission efficiency are well
illustrated by a recent study in South Africa9.
The authors recognized that, to explain HIV acquisition by 16-18
year old women in their study, they needed to postulate a per
partnership transmission probability of 0.92 (0.49, assuming
double the number of reported partnerships per woman). By
extension, the per-contact probability of transmission would be
0.34, making heterosexual sex in this context second only to
transfusion in HIV transmission efficiency. Similarly, a model
developed to assess the impact of STI on transmission of HIV
posited an extraordinary 33-fold increase in transmission
efficiency of the latter in the presence of the former10.
Reported sexual activity
Levels of sexual
activity reported in a dozen general population surveys in
Africa11
are comparable to those reported elsewhere, especially in North
America and Europe. Perhaps more importantly, there appears to
be little correlation with the level of risky sexual behaviour
shown in these surveys and the epidemic trajectories observed in
these countries. (Comparison with country-specific data reported
by UNAIDS 2000; data not shown.) The four-city study provides
similar discordance12.
For example, Yaounde (in Cameroon, a nation with low and stable
prevalence) had the highest level of risky behavioural markers.
Ndola (in Zambia, a nation that has experienced a rapid rise in
HIV) had the smallest proportion of both men and women who
reported a non-spousal sex partner in the previous 12 months.
Ndola's other markers were similar to those in Dakar, Senegal
and Cotonou, Benin, other areas with low, stable prevalence.
Transmission dynamics
Rapid propagation
(of at least bacterial STI) has been associated with core groups13,
which make up a small proportion of the susceptible population
and are proposed to be responsible for most community
transmission. Such groups appear to be associated with differing
forms of sexual net-work 'geometry'. This geometry demonstrably
differs with transmission intensity14-16.
Evidence suggests that endemic and declining HIV/STI burdens are
associated with dendritic (many open-ended termini) patterns of
sexual partner connections, while epidemicity is associated with
cyclic (closed loops, reflecting cohesiveness and density)
patterns. There are few data on the architecture of sociosexual
networks in Africa, but the available information suggests
predominantly dendritic patterns (eg, contact with prostitutes
and then contact with stable and usually monogamous consorts who
are network termini). We are aware of no study from sub-Saharan
Africa suggesting cyclic sexual network architecture. Without
evidence of appropriate network configurations on a scale
considerably larger than that observed in developed countries,
rapid propagation of HIV in Africa would be difficult to
sustain.
Studies have
associated putative sexual core groups with HIV transmission in
Africa. For example, women who work as prostitutes and their
partners have frequently been observed to have high HIV
prevalence. Confusion may arise, however, over conflating the
terms 'high risk person' and 'core group'. The former have been
labelled in some way, but are not necessarily part of an
interconnected group of individuals through whom infection
percolates (ie, core group). As noted, such persons would have
to be part of an interactive, cyclic group, rather than nodes
along a dendritic chain.
Other anomalous findings
A higher HIV
prevalence has been observed in women seen in prenatal,
postpartum, and induced abortion settings than in their
community counter-parts17.
In a number of studies, there appears to be a discrepancy
between the observed prevalence in women undergoing reproductive
medical care, and the prevalence that would be observed in such
a group from heterosexual transmission alone. Though few in
number, there continue to be reports of HIV seropositivity in
persons denying coital exposure and in persons claiming a sole
lifetime sexual partner who is reportedly HIV negative17.
Similarly, there are persistent reports of HIV in infants with
seronegative mothers17.
A recent large survey from South Africa measured an HIV
prevalence of 5.6% in children 2-14 years of age 18. Given
mortality from HIV among children who acquire it in Africa,
there would appear to be a substantial proportion of such a
disease burden that is unexplained by maternal and sexual
transmission.
Alternatives
A number of these
observations raise the question of an alternative route of
transmission, for which medical care and the use of injections
are prime candidates17,19-22.
Prostitutes, for example, are often recruited for studies from
STI clinics, where treatment is frequently given by injection,
where non-sterile equipment is used with high frequency, and
wherein the underlying prevalence of HIV is high7.
Many studies that have assessed the impact of sexual activity on
HIV transmission -notably those in Mwanza and Rakai, whose
discordant results are still a subject of debate23-failed
to consider the potential confounding effects of medical care in
the propagation of HIV24.
Rapid HIV
transmission in Africa has often occurred in countries with good
access to medical care, like Botswana, Zimbabwe, and South
Africa. For example, high rates in rural South Africa have
paralleled aggressive efforts to deliver health care to rural
populations. It is difficult to understand how improved access
to health care, with its offers of public health messages, free
condoms, and preventive services, would be associated with
increased HIV transmission. Similarly, HIV prevalence is often
higher in cities and among persons of high socioeconomic
attainment than in rural areas or among less fortunate persons.
Favourable access to health care is one of the differences that
distinguishes between these groups.
Reactions to the anomalies and alternatives
Since early in the
African epidemic, when AIDS was demographically associated with
sexually active populations25,
studies of HIV transmission in Africa have generally failed to
control for possible parenteral confounding26.
The importance of this route of infection was well known in the
West and in Asia but quickly dismissed in Africa27.
The risk of parenteral transmission of HIV is based on good
estimates of transmission efficiency, which varies depending on
type of injection and circumstances that produce reuse of
contaminated equipment. For example, needle stick exposure (HIV
transmission probability: about one in 30028,
medical injection (recently estimated at approximately one in 3020),
or illicit-drug injection (about one in 10029),
is much more efficient than penile-vaginal exposure (about one
in 100030).
There is the
expectation that, were iatrogenic transmission of HIV common,
one would notice substantial HIV prevalence in populations of
(non-sexually experienced) children. Regrettably, although a
large proportion of Africa's population falls in that category,
few serosurveys conducted in Africa have included large enough
samples from, say, children aged five through 12 to confidently
dismiss this possibility. As more information accumulates that
addresses this issue, a clearer perspective on the magnitude of
non-sexual, non-maternal transmission in children will emerge.
The risk of exposure
to HIV via medical injections is likely to vary with background
prevalence and with the specific medical practices in different
settings. The demand for consistency and coherence that we have
placed on the heterosexual hypothesis should be applied to
estimating the role of medical transmission. Its role should
vary with background (initial) prevalence, and should be related
to the degree of medical hygiene exercised. The same biological
basis that exists for heterosexual transmission should be
established for medical transmission. (As an aside, such a
demonstration poses substantial ethical problems. No
investigator should knowingly observe the use of a needle that
has a high probability of being contaminated with HIV, but at a
minimum, the demonstration of HIV RNA in needles that were to
have been used on patients would be an important element in
establishing a biological base.) The transmission of blood-borne
pathogens with differing biological characteristics, notably
hepatitis B and C31,
should be consistent with parenteral transmission of HIV.
Finally, the social epidemiology of HIV (male to female ratios,
for example) should be consistent with observations about
non-sexual exposure.
Conclusion
In North America,
Europe, and many parts of Asia, the ignition of regional
epidemics and rapid HIV transmission has been associated
principally with the sharing of contaminated injecting equipment
and with anal intercourse. Though heterosexual intercourse has
been virtually the sole explanation offered for the AIDS
epidemic in sub-Saharan Africa, to our knowledge in no other
part of the world has penile-vaginal exposure (as opposed to
'heterosexual sex') been demonstrated to initiate or sustain
rapid HIV propagation.
HIV is not
transmitted by 'sex', but only by specific risky practices. It
is not transmitted by 'injections', but only by contaminated
implements, which need to be clearly differentiated as to type
and frequency of injection and by the conditions of the exposure
setting. In virtually all societies affected by HIV to date,
both routes seem to play important roles. If we are to
understand and intervene in each of these epidemics,
well-designed studies at both the population and individual
levels are urgently needed. It is vital that these be properly
controlled for parenteral exposure, specific sexual practices,
and other co-factors2,17,24,32
and the complex and specific social patterns and networks that
accompany them33.
Dispassionate
assessment of our conclusions admittedly depends on a willing
suspension of disbelief, since the current paradigm is deeply
embedded. Counter arguments can (and will) be levelled at each
of the anomalies noted, but the depth and breadth of concerns
deserve fair scrutiny.
At issue in a
re-evaluation of the heterosexual hypothesis are the profound
implications for our interventive approach, and for the kinds of
social and financial commitments that must be made. Finally,
Africans deserve scientifically sound information on the
epidemiologic determinants of their calamitous AIDS epidemic.
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Correspondence to: Mr J J Potterat,
301 South Union Blvd,
Colorado Springs, Colorado USA 80910
E-mail:
jjpotterat@earthlink.net
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