SPECIAL REVIEW

The evolving epidemiology of HIV/AIDS

Kevin M. De Cocka, Harold W. Jaffea and James W. Curranb

Following its recognition in 1981, the HIV/AIDS epidemic has evolved to become the
greatest challenge in global health, with some 34 million persons living with HIV
worldwide. Early epidemiologic studies identified the major transmission routes of the
virus before it was discovered, and enabled the implementation of prevention strategies.
Although the first identified cases were in MSM in the United States and western Europe,
the greatest impact of the epidemic has been in sub-Saharan Africa, where most of the
transmission occurs between heterosexuals. Nine countries in southern Africa account
for less than 2% of the world’s population but now they represent about one third of
global HIV infections. Where broadly implemented, HIV screening of donated blood
and antiretroviral treatment (ART) of pregnant women have been highly effective in
preventing transfusion-associated and perinatally acquired HIV, respectively. Access to
sterile equipment has also been a successful intervention for injection drug users.
Prevention of sexual transmission has been more difficult. Perhaps the greatest
challenge in terms of prevention has been in the global community of MSM in which
HIV remains endemic at high prevalence. The most promising interventions are male
circumcision for prevention of female-to-male transmission and use of ART to reduce
infectiousness, but the extent to which these interventions can be brought to scale will
determine their population-level impact.
ß 2012 Wolters Kluwer Health | Lippincott Williams & Wilkins

AIDS 2012, 26:1205–1213

Keywords: antiretroviral therapy, epidemiology, history, HIV/AIDS, prevention

Introduction publication, we have discussed the broader implications

of the world’s three decades of experience with HIV/
In this review, we describe the epidemiology of the AIDS [1].
HIV/AIDS epidemic, both chronologically and by HIV
transmission route, and highlight prevention interven- A medical mystery
tions and other factors potentially affecting transmission What became known as AIDS was first described in a
and spread. We first discuss recognition of the epidemic, report published on 5 June 1981. Gottlieb and colleagues
discovery of HIV transmission routes, and initial reported five young, previously healthy, homosexual men
prevention efforts during the early to mid-1980s. We treated for Pneumocystis carinii (now Pneumocystis jiroveci)
then examine how the epidemic and prevention pneumonia (PCP) in three Los Angeles hospitals [2].
approaches evolved during the pre-antiretroviral therapy Those tested had evidence of T-lymphocyte depletion,
(ART) era, and conclude by describing the current and two had died. Over the following months, additional
epidemic and prospects for control. In an earlier cases of PCP, other opportunistic infections, and Kaposi’s

a
Centers for Disease Control and Prevention, and bRollins School of Public Health, Emory University, Atlanta, Georgia, USA.
Correspondence to Kevin M. De Cock, MD, Centers for Disease Control and Prevention (MS D-69), 1600 Clifton Road, Atlanta,
GA 30333, USA.
Tel: +1 404 639 7420; e-mail: kmd2@cdc.gov
Received: 3 April 2012; accepted: 3 April 2012.

DOI:10.1097/QAD.0b013e328354622a

ISSN 0269-9370 Q 2012 Wolters Kluwer Health | Lippincott Williams & Wilkins 1205
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
1206 AIDS 2012, Vol 26 No 10

sarcoma among MSM were reported from several US important risk factors [16], follow-up studies indicated
cities. Although the cause of the immunodeficiency was heterosexual transmission as the predominant mode of
unknown, cases in sex partners [3] along with the results spread [17]. Elsewhere, member countries of the WHO
of a national case–control study [4] strongly suggested a European Region had reported 267 cases through
sexually transmitted infection. October 1983 [18], including cases among Africans
seeking care [19]. Initial studies in Africa revealed large
By January 1983, the major transmission routes of the still numbers of cases in heterosexual patients in central
unidentified ‘AIDS agent’ had been described. Hetero- African cities such as Kinshasa, Zaire (now the
sexual transmission was indicated by reports of similar Democratic Republic of Congo), and Kigali, Rwanda
immunodeficiency in female sex partners of men with [20,21].
AIDS in New York [5]. Unexplained immunodeficiency
and opportunistic infections in infants born to mothers Although HIV transmission routes had been established,
with AIDS-related illnesses pointed to mother-to-child some feared transmission through insect bites or ‘casual’
transmission [6]. Several lines of evidence indicated contact with infected persons. These fears persisted until
transmission through blood and blood products, includ- studies from south Florida found no correlation between
ing cases in injection drug users (IDUs) and persons with HIV infection and mosquito exposure [22] and studies
hemophilia. Moreover, the development of the disease in from the Bronx, New York, found no casual transmission
an infant in San Francisco following receipt of a platelet between AIDS patients and their family members [23].
transfusion from a donor with subsequent PCP was
reported [7–9]. Later cases in healthcare workers An evolving epidemic
(HCWs) with occupational exposure to blood were also Over the next decade, perceptions of HIV/AIDS evolved
consistent with blood-borne transmission [10]. from a medical quandary primarily affecting MSM in the
United States to a pandemic of uncertain magnitude
By February 1983, the Centers for Disease Control threatening diverse populations around the world. The
(CDC) had received reports of 1000 persons with AIDS pandemic was not one phenomenon but a patchwork of
in the United States; mortality had been 39% [11]. Almost epidemics moving through different groups and countries
all were MSM, IDUs, persons with hemophilia, or, at different times. They were characterized by waves of
perplexingly, recent immigrants from Haiti with unde- unapparent HIV infections followed by visible epidemics
termined risk factors. Seventy-two percent of affected of disease and death. Peak HIV prevalence was useful as an
MSM were non-Hispanic whites; in contrast, about indicator to compare the severity of epidemics between
three-quarters of affected IDUs were blacks or Hispanics. locations and over time [24].
The report of the first thousand cases concluded that
trends suggested ‘gradual extension of an infectious agent Molecular epidemiologic studies have provided insights
into new populations’. into the origin and broad geographic transmission
patterns of HIV-1 [25]. The virus is thought to have
Although HIV had not yet been identified, the US Public entered human populations in the early twentieth century
Health Service issued the first recommendations for through cross-species transmission of related chimpanzee
AIDS prevention in March 1983 [12]. The report noted retroviruses found in western equatorial Africa [26,27].
that having multiple sex partners increased the risk of By the early 1980s, multiple genetic subtypes of HIV-1
AIDS and recommended that members of groups at were present in Kinshasa, Zaire [28]. Examination of
increased risk refrain from donating plasma and/or blood. genetic sequences of HIV-1 recovered from early Haitian
Later that year, the causative agent was identified [13], and patients suggested spread of HIV-1 infection from Africa
in 1985, antibody testing became available [14]; this test to Haiti in the 1960s and later introduction to the United
enabled further prevention measures such as deferral of States [29], although multiple introductions were likely.
seropositive persons from plasma and blood donation
and heat treatment of clotting factor preparations to By the mid-1990s, more than 20 million persons were
inactivate the virus. Guidelines were issued for HCWs estimated to be living with HIV/AIDS, the vast majority
to avoid occupational exposure to blood and for IDUs to in sub-Saharan Africa [30]. Largely reflecting the African
avoid sharing needles and other injection equipment. epidemic, sexual transmission accounted for at least three
Infected mothers were advised to consider delaying quarters of all new infections, most in heterosexuals.
pregnancy until more was known about the risk to the Overall, women accounted for about 40% of infected
infant [15]. adults. With exceptions of sub-Saharan Africa and Haiti,
however, fears of a ‘generalized,’ self-sustaining, hetero-
Little was known at that time about HIV/AIDS outside of sexual epidemic throughout the world did not materi-
the United States. After AIDS had been diagnosed in alize. In retrospect, lack of generalized heterosexual
Haitians recently entering the United States, cases were spread in the large populations of Asia was one of the
described in Haiti. Although initial reports of these cases most important observations for understanding global
suggested male bisexual activity and blood transfusion as HIV/AIDS epidemiology [31]. In the United States,

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 The evolving epidemiology of HIV/AIDS De Cock et al. 1207

MSM continued to account for the majority of cases [32]. [51,52]. Other, nonulcerative, infections such as gonor-
Male-to-male transmission also predominated in western rhea also appeared to increase transmissibility by
Europe, particularly in northern countries, in Australia increasing HIV shedding [53]. As chancroid became
and New Zealand, and in parts of Latin America [30,33]. less common in many locations, herpes simplex type 2
The HIV/AIDS burden in western Europe, however, was (HSV-2) emerged as the predominant cause of genital
also heavily affected by immigration from Africa, whereas ulcer disease associated with HIV [54]. Ecologic studies
southern Europe had relatively more IDU-associated also demonstrated that African countries with low
HIV/AIDS. male circumcision rates (southern and, to a lesser extent,
eastern Africa) generally had high HIV infection rates and
Using a back-calculation method, Brookmeyer [34] vice versa (highly circumcised west African populations
reconstructed the AIDS epidemic in the United States were less heavily infected with HIV) [55]. These studies
and concluded that HIV incidence in MSM had peaked and analytic observations [51,52] provided evidence that
in the mid-1980s and then rapidly decreased. Substantial lack of circumcision increased the risk for males acquiring
behavioral change among MSM contributed to early HIV infection and prompted later research that cul-
incidence declines [35,36], but high mortality among minated in intervention trials and subsequent program-
men most likely to transmit HIV must also have played a matic implementation.
role. Further, the falling incidence predated substantial
government funding for HIV prevention and likely An additional complexity in the African epidemic was a
reflected prevention efforts within the MSM community second AIDS virus, HIV-2, first reported from west
itself. Prevention guidelines for MSM emphasized the Africa in 1986 [56]. Like HIV-1, this virus is thought to
need for HIV testing, informing partners of infection have entered human populations through cross-species
status, and safe sex practices [15]. transmission: a highly related retrovirus is present in sooty
mangabeys in this geographic area [26,27]. HIV-2 is
Early efforts to assess the burden of disease in Africa and transmitted through sexual contact and blood, but very
elsewhere were based on reporting of AIDS cases to rarely from mother to child [57]. Although the virus
WHO using clinical case definitions [37]. Despite causes AIDS, it has a slower rate of disease progression
incomplete diagnosis and reporting, these efforts usefully than HIV-1 [58–60] and is overall less transmissible [61].
documented the occurrence of AIDS in specific countries
and extension globally. Once serologic testing for HIV Initial prevention efforts in sub-Saharan Africa concen-
became available, the extent of HIV spread along with its trated on limiting heterosexual transmission through the
risk factors and modes of transmission were studied ‘ABC’ strategy: abstain, be faithful, and use condoms, a
systematically. Sentinel surveillance for HIV infection was message communicated in culturally meaningful or
initiated in pregnant women, who by definition were colorful phrases such as ‘zero grazing’ and ‘condomize’
sexually active, relatively representative of the general ([62], this issue). The fall in HIV prevalence in childbearing
population, and comparable between locations. This women in Uganda during the early 1990s has been
approach has remained an important basis for estimating attributed to this approach, although this interpretation is
HIV incidence and prevalence throughout the world controversial [63,64]. But, as in the United States, massive
[38,39], although such estimates have remained contro- numbers of deaths of potential HIV transmitters must have
versial [40–42]. But, despite providing important insights influenced epidemiology. A more clear-cut prevention
into populations at risk and epidemic trends [43,44], the success was Thailand’s ‘100% condom campaign’, which
practice of unlinked anonymous testing, especially the targeted female sex workers and their clients [31,65,66].
inclusion of pregnant women, has been questioned [45]. Another early, oft-cited ‘prevention success’ occurred in
Senegal, where HIV/AIDS never spread widely [65].
Silent spread of HIV from Central Africa began in the late Senegal was exemplary in its openness and political
1970s, and by the early-to-mid 1980s, when AIDS was commitment. However, the predominance of HIV-2,
becoming apparent in Kenya, the majority of female concentration of HIV-1 in high-risk groups, universal
sex workers in Nairobi were already infected [46,47]. nature of male circumcision, and traditional and religious
Although ascertainment and reporting biases may affect cultures in the country may have been more powerful
our understanding, spread to countries of western Africa factors than specific HIV prevention campaigns.
occurred later in the 1980s [48,49], with extension to
southern Africa most intense from the 1990s onward. In the late 1980s, studies in the former Zaire showed a
Studies in urban centers across the continent showed 21% risk of HIV transmission from an infected mother to
especially high rates of HIV infection in female sex her infant in the perinatal period [67]. Prolonged breast
workers and other persons with high numbers of partners feeding, the norm in sub-Saharan Africa for cultural and
[46,47,50]. socio-economic reasons, increased transmission by an
additional 14% [68], resulting in an overall transmission
In the African epidemic, genital ulcer disease, particularly risk of 30–45% [69]. These breastfeeding findings caused
chancroid, was a strong co-factor for HIV infection difficult policy choices between advocating replacement

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1208 AIDS 2012, Vol 26 No 10

feeding, associated with the risk of malnutrition, diarrhea, outbreak of nosocomial infection was also documented
and respiratory disease, and continued breastfeeding, in Benghazi, Libya, affecting almost 400 children [85].
which increased the risk of HIV infection [69–71]. Not Despite the occurrence of such tragic events, they were
until the advent of interventions based on antiretroviral not major contributors to pandemic spread [86].
therapy (ART) could this conundrum begin to be
addressed [72–74], ([75], this issue). A number of outbreaks of HIV infection have been
recognized among blood or plasma donors in whom
The global epidemic evolved somewhat differently in attention to sterility of equipment and to overall blood
IDUs than in MSM. Most affected were IDUs in safety was inadequate. The most devastating experience
southern Europe, parts of south and south-east Asia, and was in China where up to 250 000 predominantly rural
countries of the former Soviet Union. For example, HIV villagers across five provinces may have been infected
prevalence among IDUs living in one Ukrainian city rose with HIV through the commercial blood trade in the
from less than 2% to more than 50% in less than a year early 1990s [87,88]. Commercial blood and plasma
[30]. The US Institute of Medicine concluded that donation was extensive in this region and hygienic
treating drug dependence, including the use of opioid practices were inadequate, such as pooling of cell fractions
agonist medications, was the preferred risk reduction and return to donors after plasma separation. Although
approach for IDUs. However, the provision of clean these practices were corrected in the mid-1990s, high
injecting equipment was an effective intervention when rates of disease and death were documented a decade later
treatment was not available or accessible [76]. Unfortu- [87,88].
nately, the use of funds from the US government, the
largest funder of HIV/AIDS programs globally, was A defining event, 15 years after AIDS was first described,
prohibited for needle and syringe exchange. were reports at the International Conference on AIDS in
Vancouver in 1996 of lowering of viral load and delayed
Whereas donor deferral and HIV screening of blood progression of HIV disease in persons taking combination
almost eliminated transfusion-acquired HIV in industri- ART [87]. The advent of effective therapy for HIV
alized countries, the risk remained in many developing disease meant that AIDS case surveillance no longer gave
countries. Contributing factors included lack of infra- unbiased insight into earlier trends in HIV transmission
structure for blood collection, storage, and HIV testing; but henceforth was influenced by late diagnosis,
use of paid or family members as donors; lack of high-risk inadequate access to care, failure of adherence to
donor exclusion; high rates of unnecessary transfusions; medications, or drug resistance. In response, CDC
and increased transfusion needs by pregnant women and shifted emphasis onto the reporting of HIV diagnoses
children because of malarial anemia [77,78]. Nonetheless, for surveillance purposes [88].
through WHO and donor leadership in prioritizing
national blood transfusion services, numerous HIV
infections were averted each year in sub-Saharan Africa
[79]. Further, the consensus belief that any transmission of Now and the future
HIV by blood transfusion was unacceptable helped
prioritize prevention of this mode of transmission. Three decades after the first description of AIDS, an
estimated 34.0 million (uncertainty range 31.6–
Additional studies in health care settings showed that the 35.2 million) people were living with HIV, 2.7 million
risk of infection in HCWs exposed percutaneously to (uncertainty range 2.4–2.9 million) had become newly
HIV-infected blood, most often through a needle stick, infected with HIV over the previous year, includ-
was approximately 0.3%. This risk was shown to be ing 390 000 children, and 1.8 million (uncertainty range
reduced by about 80% with the use of zidovudine as 1.6–1.9 million) HIV-infected persons died [89]. More
postexposure prophylaxis [80]. Another transmission risk than two-thirds of HIV infections, roughly 22.9 million
in healthcare settings was reported in a CDC investigation persons, were in sub-Saharan Africa, which also
of an HIV-infected dentist in Florida who transmitted the accounted for close to 80% of women and 90% of
infection to five of his patients [81]. Although the specific children living with HIV. South and south-east Asia were
route of transmission could not be determined, sub- home to some 4.0 million HIV-infected persons, and the
sequent guidelines established procedures for restricting Americas, including the Caribbean, to about 3.0 million.
the practices of infected HCWs who performed certain Although HIV/AIDS has caused appalling mortality in
invasive procedures [82]. Extensive HIV transmission MSM and IDUs, the experience of sub-Saharan Africa
occurred in the late 1980s among abandoned Romanian has made HIV/AIDS the greatest challenge to global
children living in chronic care hospitals and orphanages; health in modern times. Moreover, there has been a
only 10% of mothers of infected children were themselves severe secondary epidemic of HIV-associated tuber-
HIV-infected and most children were thought to have culosis, with an estimated 350 000 deaths among the
contracted HIV from injections with contaminated 1 100 000 persons affected by both infections in 2010
needles and syringes or blood transfusions [83,84]. An [90].

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 The evolving epidemiology of HIV/AIDS De Cock et al. 1209

In stark contrast to early observations from central Africa, this issue). In the United States, for example, near-
southern Africa is now firmly established as the global universal testing of pregnant women, provision of
HIV/AIDS epicenter: nine countries in southern Africa appropriate antiretroviral treatment or prophylaxis, and
account for less than 2% of the world’s population, but avoidance of breastfeeding by HIV-infected mothers have
represent about one-third of global HIV infections and virtually eliminated new pediatric HIV infections [109].
almost half of the world’s HIV-associated tuberculosis. The concern that the findings of the ACTG 076 study
Lack of male circumcision and high rates of HSV-2 [110], which showed the benefits of zidovudine
infection are frequently cited factors associated with high monotherapy, could not be implemented in Africa led
HIV prevalence [91]. The suggested role of concurrent sex to the search for simpler regimens. The HIVNET 012
partners [92] and putative viral subtype-specific differences study [111], which used single-dose nevirapine, was
in transmissibility is controversial. Urbanization and popu- initially greeted with enthusiasm because of the simplicity,
lation movement along with the sociopolitical changes that low cost, and relatively high efficacy of the regimen
have occurred over the past two decades have also likely (about 50%). Unfortunately, challenges to program
contributed to the southern African epidemic. adherence, transmission through breastfeeding, and
recognition that monotherapy was a risk factor for later
Globally, HIV incidence probably peaked around 1997 drug resistance all became apparent, and single-dose
[89]. In many countries such as the United States, nevirapine is now considered a suboptimal approach.
however, incidence has remained relatively stable for over
a decade [93], and without additional prevention efforts, The most important intervention for preventing mother-
the burden of HIV/AIDS continues. Determinants of to-child transmission of HIV is to identify and treat
current and future HIV/AIDS epidemiology include pregnant women who need ART for their own health,
the natural history of regional and local epidemics currently defined as those with CD4þ cell counts less than
themselves, social and behavioral trends, and the effects of 350 cells/ml [112]. Discussion continues about
public health and medical interventions. To what extent approaches that could replace WHO’s complex current
HIV/AIDS epidemiology in Africa could have been recommendations for pregnant women and infants [113],
mitigated by early emphasis on proven public health but a pragmatic approach being considered by some
measures and focus on groups at highest risk, especially sex countries (e.g., Malawi) would be to provide immediate
workers and their clients, remains for discussion [94,95]. and lifelong combination ART for all HIV-infected
pregnant women irrespective of CD4þ cell count.
As we enter the fourth decade of the pandemic,
biomedical approaches to prevention are emerging as United Nations Agencies have set a goal of reducing new
more promising than current mass communication and pediatric HIV infections from the 2009 baseline of
behavioral interventions. Randomized clinical trials have approximately 400 000 infections to less than 40 000
provided strong evidence for the use of antiretroviral infections by 2015, a 90% reduction [114]. Currently,
drugs, both as treatment and as preexposure prophylaxis, available interventions can lower mother-to-child trans-
for preventing sexual transmission of HIV ([62,75], this mission rates in breastfeeding populations to less than 5%,
issue). In particular, the high prevention impact of and success will require much more aggressive uptake of
treatment among discordant couples in the HPTN 052 HIV testing and provision of ART. Linkage of these
study [96], combined with ecologic evidence [97] and interventions to other efforts to improve maternal and
results of mathematical modeling [98], suggest that early child health, including safe delivery in health facilities,
and widespread initiation of ART in people with HIV will be essential, especially in Africa.
could substantially reduce sexual transmission in gener-
alized HIVepidemics in sub-Saharan Africa, as well as the Globally, about 3 million IDUs are estimated to be
incidence of HIV-associated tuberculosis [99]. Random- infected with HIV, and drug injection accounts for almost
ized clinical trial data from sub-Saharan Africa also one-third of HIV incidence outside of sub-Saharan
provided strong evidence that male circumcision partially Africa. The greatest number of HIV-infected IDUs
prevents female-to-male sexual transmission [100–102], resides in eastern Europe and south-east Asia [89], where
and led to policy guidance [103]. Despite tremendous their access to services is limited because of stigma,
progress [104] and huge prevention potential [105,106], discrimination, and the definition of drug dependence as
the extent to which these interventions can be brought a law enforcement rather than public health issue. Along
to scale remains uncertain [107], as does their current with HIV, IDUs suffer high rates of hepatitis B and C
population-level impact. For example, even in the United infections as well as tuberculosis, and can be an important
States, only 28% of HIV-infected persons are estimated to source of sexual transmission of HIV. Experience in other
be on treatment and have suppressed viral loads [108]. parts of the world where HIV has been successfully
controlled in IDUs illustrates that currently available
Prevention of mother-to-child transmission has seen a interventions can be effective [115]. Ecologic evidence
step-wise introduction of evidence-based interventions, also suggests that expansion of ART among HIV-infected
with impressive impact in industrialized countries ([62], drug injectors has a prevention benefit [97].

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1210 AIDS 2012, Vol 26 No 10

Perhaps the greatest challenge is among MSM, in whom AIDS to attention, remains largely refractory to current
there is little evidence of sustained prevention success interventions in all countries of the world. Because
[116]. HIV has become endemic in MSM populations in of treatment advances, HIV prevention may seem less
the industrialized world; annual HIV incidence rates important to MSM in high-income settings today than in
around 2–3% are common, as are prevalence rates of earlier decades. In low-income and middle-income
10–30%. In the United States, HIV incidence in young countries, however, HIV/AIDS in MSM is just begin-
MSM, especially young black MSM, continues to ning to be addressed. Without changes in attitudes of
increase [92]. In a venue-based study in 21 American society as a whole and greater behavioral change by MSM
cities, 24% of black MSM aged 20–29 years were HIV- themselves, HIV will remain highly endemic throughout
positive; most were unaware of their infection [117]. the global community of MSM for the foreseeable future.

While largely overlooked earlier in the epidemic, recent Collectively, we are at a pivotal moment in the HIV/AIDS
studies have documented populations of MSM in low- epidemic. We now have the tools to change the course of
and middle-income countries, including in Africa [118]. the global epidemic. Whether we have the resources and
When HIV epidemiology is studied in these groups, high political will to use those tools remains to be determined. It
rates of infection are invariably found, typically higher will be for future generations to judge whether we did all
than those in the general population. Using the Incidence that we could.
by Mode of Transmission Model, UNAIDS and The
World Bank have estimated that MSM may account for
7.5%–14% of all new HIV infections in Nigeria, for
example [119]. Studies in these countries often document Acknowledgements
extreme stigma, discrimination, and human rights abuses
toward people who practice same-sex behavior – factors Conflicts of interest
preventing openness and active HIV prevention. Even in There are no conflicts of interest.
more tolerant societies, however, such as in western
Europe, prevention efforts are generally failing to reduce
HIV incidence in men.
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