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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 worlds 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.
2012 Wolters Kluwer Health | Lippincott Williams & Wilkins

AIDS 2012, 26:12051213


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

Introduction
In this review, we describe the epidemiology of the
HIV/AIDS epidemic, both chronologically and by HIV
transmission route, and highlight prevention interventions and other factors potentially affecting transmission
and spread. We first discuss recognition of the epidemic,
discovery of HIV transmission routes, and initial
prevention efforts during the early to mid-1980s. We
then examine how the epidemic and prevention
approaches evolved during the pre-antiretroviral therapy
(ART) era, and conclude by describing the current
epidemic and prospects for control. In an earlier

publication, we have discussed the broader implications


of the worlds three decades of experience with HIV/
AIDS [1].

A medical mystery
What became known as AIDS was first described in a
report published on 5 June 1981. Gottlieb and colleagues
reported five young, previously healthy, homosexual men
treated for Pneumocystis carinii (now Pneumocystis jiroveci)
pneumonia (PCP) in three Los Angeles hospitals [2].
Those tested had evidence of T-lymphocyte depletion,
and two had died. Over the following months, additional
cases of PCP, other opportunistic infections, and Kaposis

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

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2012, Vol 26 No 10

sarcoma among MSM were reported from several US


cities. Although the cause of the immunodeficiency was
unknown, cases in sex partners [3] along with the results
of a national casecontrol study [4] strongly suggested a
sexually transmitted infection.
By January 1983, the major transmission routes of the still
unidentified AIDS agent had been described. Heterosexual transmission was indicated by reports of similar
immunodeficiency in female sex partners of men with
AIDS in New York [5]. Unexplained immunodeficiency
and opportunistic infections in infants born to mothers
with AIDS-related illnesses pointed to mother-to-child
transmission [6]. Several lines of evidence indicated
transmission through blood and blood products, including cases in injection drug users (IDUs) and persons with
hemophilia. Moreover, the development of the disease in
an infant in San Francisco following receipt of a platelet
transfusion from a donor with subsequent PCP was
reported [79]. Later cases in healthcare workers
(HCWs) with occupational exposure to blood were also
consistent with blood-borne transmission [10].
By February 1983, the Centers for Disease Control
(CDC) had received reports of 1000 persons with AIDS
in the United States; mortality had been 39% [11]. Almost
all were MSM, IDUs, persons with hemophilia, or,
perplexingly, recent immigrants from Haiti with undetermined risk factors. Seventy-two percent of affected
MSM were non-Hispanic whites; in contrast, about
three-quarters of affected IDUs were blacks or Hispanics.
The report of the first thousand cases concluded that
trends suggested gradual extension of an infectious agent
into new populations.
Although HIV had not yet been identified, the US Public
Health Service issued the first recommendations for
AIDS prevention in March 1983 [12]. The report noted
that having multiple sex partners increased the risk of
AIDS and recommended that members of groups at
increased risk refrain from donating plasma and/or blood.
Later that year, the causative agent was identified [13], and
in 1985, antibody testing became available [14]; this test
enabled further prevention measures such as deferral of
seropositive persons from plasma and blood donation
and heat treatment of clotting factor preparations to
inactivate the virus. Guidelines were issued for HCWs
to avoid occupational exposure to blood and for IDUs to
avoid sharing needles and other injection equipment.
Infected mothers were advised to consider delaying
pregnancy until more was known about the risk to the
infant [15].
Little was known at that time about HIV/AIDS outside of
the United States. After AIDS had been diagnosed in
Haitians recently entering the United States, cases were
described in Haiti. Although initial reports of these cases
suggested male bisexual activity and blood transfusion as

important risk factors [16], follow-up studies indicated


heterosexual transmission as the predominant mode of
spread [17]. Elsewhere, member countries of the WHO
European Region had reported 267 cases through
October 1983 [18], including cases among Africans
seeking care [19]. Initial studies in Africa revealed large
numbers of cases in heterosexual patients in central
African cities such as Kinshasa, Zaire (now the
Democratic Republic of Congo), and Kigali, Rwanda
[20,21].
Although HIV transmission routes had been established,
some feared transmission through insect bites or casual
contact with infected persons. These fears persisted until
studies from south Florida found no correlation between
HIV infection and mosquito exposure [22] and studies
from the Bronx, New York, found no casual transmission
between AIDS patients and their family members [23].

An evolving epidemic
Over the next decade, perceptions of HIV/AIDS evolved
from a medical quandary primarily affecting MSM in the
United States to a pandemic of uncertain magnitude
threatening diverse populations around the world. The
pandemic was not one phenomenon but a patchwork of
epidemics moving through different groups and countries
at different times. They were characterized by waves of
unapparent HIV infections followed by visible epidemics
of disease and death. Peak HIV prevalence was useful as an
indicator to compare the severity of epidemics between
locations and over time [24].
Molecular epidemiologic studies have provided insights
into the origin and broad geographic transmission
patterns of HIV-1 [25]. The virus is thought to have
entered human populations in the early twentieth century
through cross-species transmission of related chimpanzee
retroviruses found in western equatorial Africa [26,27].
By the early 1980s, multiple genetic subtypes of HIV-1
were present in Kinshasa, Zaire [28]. Examination of
genetic sequences of HIV-1 recovered from early Haitian
patients suggested spread of HIV-1 infection from Africa
to Haiti in the 1960s and later introduction to the United
States [29], although multiple introductions were likely.
By the mid-1990s, more than 20 million persons were
estimated to be living with HIV/AIDS, the vast majority
in sub-Saharan Africa [30]. Largely reflecting the African
epidemic, sexual transmission accounted for at least three
quarters of all new infections, most in heterosexuals.
Overall, women accounted for about 40% of infected
adults. With exceptions of sub-Saharan Africa and Haiti,
however, fears of a generalized, self-sustaining, heterosexual epidemic throughout the world did not materialize. In retrospect, lack of generalized heterosexual
spread in the large populations of Asia was one of the
most important observations for understanding global
HIV/AIDS epidemiology [31]. In the United States,

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

MSM continued to account for the majority of cases [32].


Male-to-male transmission also predominated in western
Europe, particularly in northern countries, in Australia
and New Zealand, and in parts of Latin America [30,33].
The HIV/AIDS burden in western Europe, however, was
also heavily affected by immigration from Africa, whereas
southern Europe had relatively more IDU-associated
HIV/AIDS.
Using a back-calculation method, Brookmeyer [34]
reconstructed the AIDS epidemic in the United States
and concluded that HIV incidence in MSM had peaked
in the mid-1980s and then rapidly decreased. Substantial
behavioral change among MSM contributed to early
incidence declines [35,36], but high mortality among
men most likely to transmit HIV must also have played a
role. Further, the falling incidence predated substantial
government funding for HIV prevention and likely
reflected prevention efforts within the MSM community
itself. Prevention guidelines for MSM emphasized the
need for HIV testing, informing partners of infection
status, and safe sex practices [15].
Early efforts to assess the burden of disease in Africa and
elsewhere were based on reporting of AIDS cases to
WHO using clinical case definitions [37]. Despite
incomplete diagnosis and reporting, these efforts usefully
documented the occurrence of AIDS in specific countries
and extension globally. Once serologic testing for HIV
became available, the extent of HIV spread along with its
risk factors and modes of transmission were studied
systematically. Sentinel surveillance for HIV infection was
initiated in pregnant women, who by definition were
sexually active, relatively representative of the general
population, and comparable between locations. This
approach has remained an important basis for estimating
HIV incidence and prevalence throughout the world
[38,39], although such estimates have remained controversial [4042]. But, despite providing important insights
into populations at risk and epidemic trends [43,44], the
practice of unlinked anonymous testing, especially the
inclusion of pregnant women, has been questioned [45].
Silent spread of HIV from Central Africa began in the late
1970s, and by the early-to-mid 1980s, when AIDS was
becoming apparent in Kenya, the majority of female
sex workers in Nairobi were already infected [46,47].
Although ascertainment and reporting biases may affect
our understanding, spread to countries of western Africa
occurred later in the 1980s [48,49], with extension to
southern Africa most intense from the 1990s onward.
Studies in urban centers across the continent showed
especially high rates of HIV infection in female sex
workers and other persons with high numbers of partners
[46,47,50].
In the African epidemic, genital ulcer disease, particularly
chancroid, was a strong co-factor for HIV infection

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[51,52]. Other, nonulcerative, infections such as gonorrhea also appeared to increase transmissibility by
increasing HIV shedding [53]. As chancroid became
less common in many locations, herpes simplex type 2
(HSV-2) emerged as the predominant cause of genital
ulcer disease associated with HIV [54]. Ecologic studies
also demonstrated that African countries with low
male circumcision rates (southern and, to a lesser extent,
eastern Africa) generally had high HIV infection rates and
vice versa (highly circumcised west African populations
were less heavily infected with HIV) [55]. These studies
and analytic observations [51,52] provided evidence that
lack of circumcision increased the risk for males acquiring
HIV infection and prompted later research that culminated in intervention trials and subsequent programmatic implementation.
An additional complexity in the African epidemic was a
second AIDS virus, HIV-2, first reported from west
Africa in 1986 [56]. Like HIV-1, this virus is thought to
have entered human populations through cross-species
transmission: a highly related retrovirus is present in sooty
mangabeys in this geographic area [26,27]. HIV-2 is
transmitted through sexual contact and blood, but very
rarely from mother to child [57]. Although the virus
causes AIDS, it has a slower rate of disease progression
than HIV-1 [5860] and is overall less transmissible [61].
Initial prevention efforts in sub-Saharan Africa concentrated on limiting heterosexual transmission through the
ABC strategy: abstain, be faithful, and use condoms, a
message communicated in culturally meaningful or
colorful phrases such as zero grazing and condomize
([62], this issue). The fall in HIV prevalence in childbearing
women in Uganda during the early 1990s has been
attributed to this approach, although this interpretation is
controversial [63,64]. But, as in the United States, massive
numbers of deaths of potential HIV transmitters must have
influenced epidemiology. A more clear-cut prevention
success was Thailands 100% condom campaign, which
targeted female sex workers and their clients [31,65,66].
Another early, oft-cited prevention success occurred in
Senegal, where HIV/AIDS never spread widely [65].
Senegal was exemplary in its openness and political
commitment. However, the predominance of HIV-2,
concentration of HIV-1 in high-risk groups, universal
nature of male circumcision, and traditional and religious
cultures in the country may have been more powerful
factors than specific HIV prevention campaigns.
In the late 1980s, studies in the former Zaire showed a
21% risk of HIV transmission from an infected mother to
her infant in the perinatal period [67]. Prolonged breast
feeding, the norm in sub-Saharan Africa for cultural and
socio-economic reasons, increased transmission by an
additional 14% [68], resulting in an overall transmission
risk of 3045% [69]. These breastfeeding findings caused
difficult policy choices between advocating replacement

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feeding, associated with the risk of malnutrition, diarrhea,


and respiratory disease, and continued breastfeeding,
which increased the risk of HIV infection [6971]. Not
until the advent of interventions based on antiretroviral
therapy (ART) could this conundrum begin to be
addressed [7274], ([75], this issue).
The global epidemic evolved somewhat differently in
IDUs than in MSM. Most affected were IDUs in
southern Europe, parts of south and south-east Asia, and
countries of the former Soviet Union. For example, HIV
prevalence among IDUs living in one Ukrainian city rose
from less than 2% to more than 50% in less than a year
[30]. The US Institute of Medicine concluded that
treating drug dependence, including the use of opioid
agonist medications, was the preferred risk reduction
approach for IDUs. However, the provision of clean
injecting equipment was an effective intervention when
treatment was not available or accessible [76]. Unfortunately, the use of funds from the US government, the
largest funder of HIV/AIDS programs globally, was
prohibited for needle and syringe exchange.
Whereas donor deferral and HIV screening of blood
almost eliminated transfusion-acquired HIV in industrialized countries, the risk remained in many developing
countries. Contributing factors included lack of infrastructure for blood collection, storage, and HIV testing;
use of paid or family members as donors; lack of high-risk
donor exclusion; high rates of unnecessary transfusions;
and increased transfusion needs by pregnant women and
children because of malarial anemia [77,78]. Nonetheless,
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
HIV by blood transfusion was unacceptable helped
prioritize prevention of this mode of transmission.
Additional studies in health care settings showed that the
risk of infection in HCWs exposed percutaneously to
HIV-infected blood, most often through a needle stick,
was approximately 0.3%. This risk was shown to be
reduced by about 80% with the use of zidovudine as
postexposure prophylaxis [80]. Another transmission risk
in healthcare settings was reported in a CDC investigation
of an HIV-infected dentist in Florida who transmitted the
infection to five of his patients [81]. Although the specific
route of transmission could not be determined, subsequent guidelines established procedures for restricting
the practices of infected HCWs who performed certain
invasive procedures [82]. Extensive HIV transmission
occurred in the late 1980s among abandoned Romanian
children living in chronic care hospitals and orphanages;
only 10% of mothers of infected children were themselves
HIV-infected and most children were thought to have
contracted HIV from injections with contaminated
needles and syringes or blood transfusions [83,84]. An

outbreak of nosocomial infection was also documented


in Benghazi, Libya, affecting almost 400 children [85].
Despite the occurrence of such tragic events, they were
not major contributors to pandemic spread [86].
A number of outbreaks of HIV infection have been
recognized among blood or plasma donors in whom
attention to sterility of equipment and to overall blood
safety was inadequate. The most devastating experience
was in China where up to 250 000 predominantly rural
villagers across five provinces may have been infected
with HIV through the commercial blood trade in the
early 1990s [87,88]. Commercial blood and plasma
donation was extensive in this region and hygienic
practices were inadequate, such as pooling of cell fractions
and return to donors after plasma separation. Although
these practices were corrected in the mid-1990s, high
rates of disease and death were documented a decade later
[87,88].
A defining event, 15 years after AIDS was first described,
were reports at the International Conference on AIDS in
Vancouver in 1996 of lowering of viral load and delayed
progression of HIV disease in persons taking combination
ART [87]. The advent of effective therapy for HIV
disease meant that AIDS case surveillance no longer gave
unbiased insight into earlier trends in HIV transmission
but henceforth was influenced by late diagnosis,
inadequate access to care, failure of adherence to
medications, or drug resistance. In response, CDC
shifted emphasis onto the reporting of HIV diagnoses
for surveillance purposes [88].

Now and the future


Three decades after the first description of AIDS, an
estimated 34.0 million (uncertainty range 31.6
35.2 million) people were living with HIV, 2.7 million
(uncertainty range 2.42.9 million) had become newly
infected with HIV over the previous year, including 390 000 children, and 1.8 million (uncertainty range
1.61.9 million) HIV-infected persons died [89]. More
than two-thirds of HIV infections, roughly 22.9 million
persons, were in sub-Saharan Africa, which also
accounted for close to 80% of women and 90% of
children living with HIV. South and south-east Asia were
home to some 4.0 million HIV-infected persons, and the
Americas, including the Caribbean, to about 3.0 million.
Although HIV/AIDS has caused appalling mortality in
MSM and IDUs, the experience of sub-Saharan Africa
has made HIV/AIDS the greatest challenge to global
health in modern times. Moreover, there has been a
severe secondary epidemic of HIV-associated tuberculosis, with an estimated 350 000 deaths among the
1 100 000 persons affected by both infections in 2010
[90].

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

In stark contrast to early observations from central Africa,


southern Africa is now firmly established as the global
HIV/AIDS epicenter: nine countries in southern Africa
account for less than 2% of the worlds population, but
represent about one-third of global HIV infections and
almost half of the worlds HIV-associated tuberculosis.
Lack of male circumcision and high rates of HSV-2
infection are frequently cited factors associated with high
HIV prevalence [91]. The suggested role of concurrent sex
partners [92] and putative viral subtype-specific differences
in transmissibility is controversial. Urbanization and population movement along with the sociopolitical changes that
have occurred over the past two decades have also likely
contributed to the southern African epidemic.
Globally, HIV incidence probably peaked around 1997
[89]. In many countries such as the United States,
however, incidence has remained relatively stable for over
a decade [93], and without additional prevention efforts,
the burden of HIV/AIDS continues. Determinants of
current and future HIV/AIDS epidemiology include
the natural history of regional and local epidemics
themselves, social and behavioral trends, and the effects of
public health and medical interventions. To what extent
HIV/AIDS epidemiology in Africa could have been
mitigated by early emphasis on proven public health
measures and focus on groups at highest risk, especially sex
workers and their clients, remains for discussion [94,95].
As we enter the fourth decade of the pandemic,
biomedical approaches to prevention are emerging as
more promising than current mass communication and
behavioral interventions. Randomized clinical trials have
provided strong evidence for the use of antiretroviral
drugs, both as treatment and as preexposure prophylaxis,
for preventing sexual transmission of HIV ([62,75], this
issue). In particular, the high prevention impact of
treatment among discordant couples in the HPTN 052
study [96], combined with ecologic evidence [97] and
results of mathematical modeling [98], suggest that early
and widespread initiation of ART in people with HIV
could substantially reduce sexual transmission in generalized HIVepidemics in sub-Saharan Africa, as well as the
incidence of HIV-associated tuberculosis [99]. Randomized clinical trial data from sub-Saharan Africa also
provided strong evidence that male circumcision partially
prevents female-to-male sexual transmission [100102],
and led to policy guidance [103]. Despite tremendous
progress [104] and huge prevention potential [105,106],
the extent to which these interventions can be brought
to scale remains uncertain [107], as does their current
population-level impact. For example, even in the United
States, only 28% of HIV-infected persons are estimated to
be on treatment and have suppressed viral loads [108].
Prevention of mother-to-child transmission has seen a
step-wise introduction of evidence-based interventions,
with impressive impact in industrialized countries ([62],

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this issue). In the United States, for example, nearuniversal testing of pregnant women, provision of
appropriate antiretroviral treatment or prophylaxis, and
avoidance of breastfeeding by HIV-infected mothers have
virtually eliminated new pediatric HIV infections [109].
The concern that the findings of the ACTG 076 study
[110], which showed the benefits of zidovudine
monotherapy, could not be implemented in Africa led
to the search for simpler regimens. The HIVNET 012
study [111], which used single-dose nevirapine, was
initially greeted with enthusiasm because of the simplicity,
low cost, and relatively high efficacy of the regimen
(about 50%). Unfortunately, challenges to program
adherence, transmission through breastfeeding, and
recognition that monotherapy was a risk factor for later
drug resistance all became apparent, and single-dose
nevirapine is now considered a suboptimal approach.
The most important intervention for preventing motherto-child transmission of HIV is to identify and treat
pregnant women who need ART for their own health,
currently defined as those with CD4 cell counts less than
350 cells/ml [112]. Discussion continues about
approaches that could replace WHOs complex current
recommendations for pregnant women and infants [113],
but a pragmatic approach being considered by some
countries (e.g., Malawi) would be to provide immediate
and lifelong combination ART for all HIV-infected
pregnant women irrespective of CD4 cell count.
United Nations Agencies have set a goal of reducing new
pediatric HIV infections from the 2009 baseline of
approximately 400 000 infections to less than 40 000
infections by 2015, a 90% reduction [114]. Currently,
available interventions can lower mother-to-child transmission rates in breastfeeding populations to less than 5%,
and success will require much more aggressive uptake of
HIV testing and provision of ART. Linkage of these
interventions to other efforts to improve maternal and
child health, including safe delivery in health facilities,
will be essential, especially in Africa.
Globally, about 3 million IDUs are estimated to be
infected with HIV, and drug injection accounts for almost
one-third of HIV incidence outside of sub-Saharan
Africa. The greatest number of HIV-infected IDUs
resides in eastern Europe and south-east Asia [89], where
their access to services is limited because of stigma,
discrimination, and the definition of drug dependence as
a law enforcement rather than public health issue. Along
with HIV, IDUs suffer high rates of hepatitis B and C
infections as well as tuberculosis, and can be an important
source of sexual transmission of HIV. Experience in other
parts of the world where HIV has been successfully
controlled in IDUs illustrates that currently available
interventions can be effective [115]. Ecologic evidence
also suggests that expansion of ART among HIV-infected
drug injectors has a prevention benefit [97].

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Perhaps the greatest challenge is among MSM, in whom


there is little evidence of sustained prevention success
[116]. HIV has become endemic in MSM populations in
the industrialized world; annual HIV incidence rates
around 23% are common, as are prevalence rates of
1030%. In the United States, HIV incidence in young
MSM, especially young black MSM, continues to
increase [92]. In a venue-based study in 21 American
cities, 24% of black MSM aged 2029 years were HIVpositive; most were unaware of their infection [117].

AIDS to attention, remains largely refractory to current


interventions in all countries of the world. Because
of treatment advances, HIV prevention may seem less
important to MSM in high-income settings today than in
earlier decades. In low-income and middle-income
countries, however, HIV/AIDS in MSM is just beginning to be addressed. Without changes in attitudes of
society as a whole and greater behavioral change by MSM
themselves, HIV will remain highly endemic throughout
the global community of MSM for the foreseeable future.

While largely overlooked earlier in the epidemic, recent


studies have documented populations of MSM in lowand middle-income countries, including in Africa [118].
When HIV epidemiology is studied in these groups, high
rates of infection are invariably found, typically higher
than those in the general population. Using the Incidence
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
extreme stigma, discrimination, and human rights abuses
toward people who practice same-sex behavior factors
preventing openness and active HIV prevention. Even in
more tolerant societies, however, such as in western
Europe, prevention efforts are generally failing to reduce
HIV incidence in men.

Collectively, we are at a pivotal moment in the HIV/AIDS


epidemic. We now have the tools to change the course of
the global epidemic. Whether we have the resources and
political will to use those tools remains to be determined. It
will be for future generations to judge whether we did all
that we could.

Acknowledgements
Conflicts of interest
There are no conflicts of interest.

References

Conclusions
Although heterosexual transmission remains the dominant mode of spread worldwide, we have witnessed
encouraging trends in Africas generalized epidemics
[120,121], evidence of efficacy of biomedical interventions (especially ART-based prevention and male
circumcision) [122], and successful prevention program
scale-up [104]. ART-based prevention approaches have
the potential to reduce all modes of transmission ([75],
this issue). Cautious optimism is justified when this reality
and the tools available are contrasted to the history of the
pre-ART era. However, continued funding, intensified
program implementation, massive scale-up of HIV
testing, surveillance, and appropriate intervention and
implementation science are critical to success.
Much more can be done to prevent and treat HIV
infection in IDUs and sex workers, whose needs remain
neglected and for whom targeted services can substantially reduce HIV transmission. Mother-to-child
transmission of HIV is largely preventable, trends are
encouraging, and the worlds attention is now focused on
this problem. Although continued efforts are needed
to improve blood safety [123] and reduce healthcareassociated infections, blood transfusion and medical
injections are not major modes of HIV transmission.
Strikingly, HIV among MSM, the issue that first brought

1. De Cock KM, Jaffe HW, Curran JW. Reflections on 30 years of


AIDS. Emerg Infect Dis 2011; 17:10441048.
2. Centers for Disease Control. Pneumocystis Pneumonia Los
Angeles. MMWR 1981; 30:250252.
3. Centers for Disease Control. A cluster of Kaposis sarcoma and
Pneumocystis carinii pneumonia cases among homosexual
male residents of Los Angeles and Orange Counties, California.
MMWR 1982; 31:305307.
4. Jaffe HW, Choi K, Thomas PA, Haverkos HW, Auerbach DM,
Guinan ME, et al. National casecontrol study of Kaposis
sarcoma and Pneumocystis carinii pneumonia in homosexual
men. Part 1: Epidemiologic results. Ann Intern Med 1983;
99:145151.
5. Centers for Disease Control. Immunodeficiency among female
sexual partners of males with acquired immune deficiency
syndrome (AIDS) New York. MMWR 1983; 31:697698.
6. Centers for Disease Control. Unexplained immunodeficiency
and opportunistic infections in infants New York, New
Jersey, California. MMWR 1982; 31:665667.
7. Centers for Disease Control. Update on Kaposis sarcoma
and opportunistic infections in previously healthy persons
United States. MMWR 1982; 31:294301.
8. Centers for Disease Control. Pneumocystis carinii pneumonia
among persons with hemophilia A. MMWR 1982; 31:365367.
9. Centers for Disease Control. Possible transfusion-associated
acquired immune deficiency syndrome (AIDS) California.
MMWR 1982; 31:652654.
10. Anonymous. Needlestick transmission of HTLV-III from a
patient infected in Africa. Lancet 1984; 324:13761377.
11. Jaffe HW, Bregman DJ, Selik RM. Acquired immune deficiency
syndrome in the United States: The first 1,000 cases. J Infect
Dis 1983; 148:339345.
12. Centers for Disease Control. Prevention of acquired immune
deficiency syndrome (AIDS): report of inter-agency recommendations. MMWR 1983; 32:101104.
13. Barre-Sinoussi F, Chermann JC, Rey F, Nugeyre MT, Chamaret
S, Gruest J, et al. Isolation of a T-lymphotropic retrovirus from
a patient at risk for acquired immune deficiency syndrome
(AIDS). Science 1983; 220:868871.

Copyright Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

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


14. Centers for Disease Control. Provisional Public Health Service
inter-agency recommendations for screening donated blood
and plasma for antibody to the virus causing acquired
immunodeficiency syndrome. MMWR 1985; 34:15.
15. Centers for Disease Control. Additional recommendations to
reduce sexual and drug abuse-related transmission of human
T-lymphotropic virus type III/lymphadenopathy-associated
virus. MMWR 1986; 35:152155.
16. Pape JW, Liautaud B, Thomas F, Mathurin J-R, St Amand
M-MA, Boncy M, et al. Characteristics of the acquired
immunodeficiency syndrome (AIDS) in Haiti. N Engl J Med
1983; 309:945950.
17. Pape JW, Liautaud B, Thomas F, Mathurin J-R, St Amand
M-MA, Boncy M, et al. The acquired immunodeficiency
syndrome in Haiti. Ann Intern Med 1985; 103:674678.
18. Centers for Disease Control. Acquired immunodeficiency syndrome (AIDS) Europe. MMWR 1983; 32:610611.
19. Clumeck N, Sonnet J, Taelman H, Mascart-Lemone F, De
Bruyere M, Vandeperre P, et al. Acquired immunodeficiency
syndrome in African patients. N Engl J Med 1984; 310:492
497.
20. Piot P, Taelman H, Bila Minlangu K, Mbendi N, Ndangi K,
Kalambayi K, et al. Acquired immunodeficiency syndrome in a
heterosexual population in Zaire. Lancet 1984; 324:6569.
21. Van De Perre P, Lepage P, Kestelyn P, Hekker A, Rouvroy D,
Bongaerts J, et al. Acquired immunodeficiency syndrome in
Rwanda. Lancet 1984; 324:6265.
22. Castro KG, Lieb S, Jaffe HW, Narkunas JP, Calisher CH, Bush
TJ, et al. Transmission of HIV in Belle Glade, Florida: lessons
for other communities in the United States. Science 1988;
239:193197.
23. Friedland GH, Saltzman BR, Rogers MF, Kahl PA, Lesser ML,
Mayers MM, et al. Lack of transmission of HTLV-III/LAV
infection to household contacts of patients with AIDS or
AIDS-related complex with oral candidiasis. N Engl J Med
1986; 314:344349.
24. Hargrove J. Migration, mines and mores: the HIV epidemic in
southern Africa. S Afr J Sci 2008; 104:5361.
25. Pepin J. The origins of AIDS. New York: Cambridge University
Press; 2011.
26. Sharp PM, Bailes E, Chaudhuri RH, Rodenburg CM, Santiago
MO, Hahn BH. The origin of acquired immunodeficiency
viruses: where and when? Phil Trans R Soc Lond B 2001;
356:867876.
27. Sharp PM, Hahn BH. Origin of HIV and the AIDS pandemic.
Cold Spring Harb Perspect Med 2011; 1:a006841.
28. Kalish ML, Robbins KE, Pieniazek D, Schaefer A, Nzilambi N,
Quinn TC, et al. Recombinant viruses and early global HIV-1
epidemic. Emerg Infect Dis 2004; 10:12271234.
29. Gilbert MTP, Rambaut A, Wlasiuk G, Spira TJ, Pitchenik AE,
Worobey M. The emergence of HIV/AIDS in the Americas and
beyond. Proc Natl Acad Sci U S A 2007; 104:1856618570.
30. UNAIDS. HIV/AIDS: The global epidemic. Estimates as of
December 1996. http://www.greenstone.org/greenstone3/
nzdl;jsessionid=2365BA90F2A65BDEDFD0E4BC0521582A?
a=d&d=HASH01da2574c26597a69f118659.2&c=unaids&
sib=1&dt=&ec=&et=&p.a=b&p.s=ClassifierBrowse&p.sa.
[30 Accessed January 2012]
31. United Nations. Redefining AIDS in Asia: crafting an effective
response. Report of the Commission on AIDS in Asia. New
Delhi: Oxford University Press; 2008.
32. Centers for Disease Control and Prevention. HIV/AIDS surveillance report. U.S. HIV and AIDS cases reported through
December 1995. http://www.cdc.gov/hiv/topics/surveillance/
resources/reports/pdf/hivsur72.pdf. [Accessed 30 January
2012]
33. European Centre for the Epidemiological Monitoring of
AIDS. HIV/AIDS surveillance in Europe. End year report
1999. http://ecdc.europa.eu/en/activities/surveillance/hiv/
Documents/report_eurohiv_endyear_99.pdf. [Accessed 30
January 2012]
34. Brookmeyer R. Reconstruction and future trends of the
AIDS epidemic in the United States. Science 1991; 253:37
42.
35. Wiley JA, Coates TJ, Stall R, Saika G, Morin S, Charles K, et al.
Reported changes in the sexual behavior of men at risk for
AIDS, San Francisco, 1982-84: the AIDS Behavioral Research
Project. Public Health Rep 1985; 100:622629.

1211

36. Becker MH, Joseph JG. AIDS and behavioral change to reduce
risk: a review. Am J Public Health 1988; 78:394410.
37. Colebunders R, Francis H, Izaley L, Kabasele K, Nzilambi N,
Van Der Groen G, et al. Evaluation of a clinical case-definition
of acquired immunodeficiency syndrome in Africa. Lancet
1987; 329:492494.
38. WHO, UNAIDS, CDC. Guidelines for conducting HIV
sentinel serosurveys among pregnant women and other
groups. http://www.who.int/hiv/pub/surveillance/en/ancguide
lines.pdf. [Accessed 31 January 2012]
39. Pappaioanou M, Dondero T, Petersen L, Onorato I, Sanchez C,
Curran JW. The family of HIV seroprevalence surveys: objectives, methods, and uses of sentinel surveillance for HIV in the
United States. Public Health Rep 1990; 105:113119.
40. Chin J. The AIDS pandemic. The collision of epidemiology with
political correctness. Oxon: Radcliffe Publishing; 2007.
41. UNAIDS, WHO. AIDS epidemic update, December 2007.
http://data.unaids.org/pub/EPISlides/2007/2007_epiupdate_en.
pdf. [Accessed 6 February 2012]
42. De Cock KM, DeLay P. HIV/AIDS estimates and the quest for
universal access. Lancet 2008; 371:20682070.
43. Davis SF, Byers RH Jr, Lindegren ML. Prevalence and incidence of vertically acquired HIV infection in the United
States. JAMA 1995; 274:952955.
44. Davis SF, Rosen DH, Steinberg S, Wortley PM, Karon JM,
Gwinn M. Trends in HIV prevalence among childbearing
women in the United States, 19891994. J Acquir Immune
Defic Syndr 1998; 19:158164.
45. Rennie S, Turner AN, Mupenda B, Behets F. Conducting
unlinked anonymous HIV surveillance in developing countries: Ethical, epidemiological, and public health concerns.
PLoS Med 2009; 6:3034.
46. Kreiss JK, Koech D, Plummer FA, Holmes KK, Lightfoote M,
Piot P, et al. AIDS virus infection in Nairobi prostitutes. N Engl
J Med 1986; 314:414418.
47. Piot P, Plummer FA, Rey M-A, Ngugi EN, Rouzioux C, NdinyaAchola J, et al. Retrospective seroepidemiology of AIDS virus
infection in Nairobi populations. J Infect Dis 1987; 155:1108
1112.
48. DeCock KM, Odehouri K, Moreau J, Kouadio J, Porter A,
Barrere B, et al. Rapid emergence of AIDS in Abidjan, Ivory
Coast. Lancet 1989; 334:408411.
49. De Cock KM, Barrere B, Diaby L, Lafontaine MF, Gnaore E,
Porter A, et al. AIDS: the leading cause of adult death in the
West African city of Abidjan, Cote dIvoire. Science 1990;
249:793796.
50. Mann JM, Nzilambi N, Piot P, Bosenge N, Kalala M, Francis H,
et al. HIV infection and associated risk factors in female
prostitutes in Kinshasa, Zaire. AIDS 1988; 2:249254.
51. Simonsen JN, Cameron DW, Gakinya MN, Ndinya-Achola JO,
DCosta LJ, Karasira P, et al. Human immunodeficiency virus
infection among men with sexually transmitted infections.
N Engl J Med 1988; 319:274278.
52. Cameron DW, DCosta LJ, Maitha GM, Cheang M, Piot P,
Simonsen JN, et al. Female to male transmission of human
immunodeficiency virus type 1: risk factors for seroconversion in men. Lancet 1989; 334:403407.
53. Moss GB, Overbaugh J, Welch M, Reilly M, Bwayo J, Plummer
FA. Human immunodeficiency virus DNA in urethral secretions in men: association with gonococcal urethritis and CD4
cell depletion. J Infect Dis 1995; 172:14691474.
54. Weiss HA, Buve A, Robinson NJ, Van Dyck E, Kahindo M,
Anagonou S, et al. The epidemiology of HSV-2 infection and
its association with HIV infection in four urban African
populations. AIDS 2001; 15 (Suppl 4):S97S108.
55. Bongaarts J, Reining P, Way P, Conant F. The relationship
between male circumcision and HIV infection in African
populations. AIDS 1989; 3:373377.
56. Clavel F, Guetard D, Brun-Vezinet F, Chamaret S, Rey M-A,
Santos-Ferreira MO, et al. Isolation of a new human retrovirus
from West African patients with AIDS. Science 1986; 233:
343346.
57. Adjorlolo G, De Cock KM, Ekpini E, Vetter KM, Sibailly T,
Brattegaard K, et al. Prospective comparison of mother-tochild transmission of HIV-1 and HIV-2 in Abidjan, Ivory
Coast. JAMA 1994; 272:462466.
58. Kanki PJ, De Cock KM. Epidemiology and transmission of
HIV-2. AIDS 1994; 8 (Suppl 1):S85S93.

Copyright Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

1212

AIDS

2012, Vol 26 No 10

59. Marlink R, Kanki P, Thior I, Travers K, Eisen G, Siby T, et al.


Reduced rate of disease development after HIV-2 infection as
compared to HIV-1. Science 1994; 265:15871590.
60. Jaffar S, Grant AD, Whitworth J, Smith PG, Whittle H. The
natural history of HIV-1 and HIV-2 infections in adults in Africa:
a literature review. Bull World Health Organ 2004; 82:462469.
61. DeCock KM, Adjorlolo G, Ekpini E, Sibailly T, Kouadio J,
Maran M, et al. Epidemiology and transmission of HIV-2.
Why there is no HIV-2 pandemic. JAMA 1993; 270:20832086.
62. Laga M, Piot P. Prevention of sexual transmission of HIV: real
results, science progressing, societies remaining behind. AIDS
2012; 26:12231229.
63. Collins C, Coates TJ, Curran J. Moving beyond the alphabet
soup of HIV prevention. AIDS 2008; 22 (Suppl 2):S5S8.
64. Stoneburner RL, Low-Beer D. Population-level HV declines and
behavioral risk avoidance in Uganda. Science 2004; 304:714
718.
65. UNAIDS. HIV Prevention needs and successes: a tale of three
countries. An update on HIV prevention success in Senegal,
Thailand and Uganda. 2001. http://data.unaids.org/publications/IRC-pub02/jc535-hi_en.pdf. [Accessed 6 February 2012]
66. Rojanapithayakorn W, Hanenberg R. The 100% condom
program in Thailand. AIDS 1996; 10:17.
67. Ryder RW, Nsa W, Hassig SE, Behets F, Rayfield M, Ekungola
B, et al. Perinatal transmission of the human immunodeficiency virus type 1 to infants of seropositive women in Zaire.
N Engl J Med 1989; 320:16371642.
68. Dunn DT, Newell ML, Ades AE, Peckham CS. Risk of human
immunodeficiency virus type 1 transmission through breastfeeding. Lancet 1992; 340:585588.
69. DeCock KM, Fowler MG, Mercier E, de Vincenzi I, Saba J, Hoff
E, et al. Prevention of mother-to-child HIV transmission in
resource-poor countries. Translating research into policy and
practice. JAMA 2000; 283:11751182.
70. Guay LA, Ruff AJ. HIV and infant feeding: an ongoing challenge. JAMA 2001; 286:24622464.
71. Nduati R, John G, Mbori-Ngacha D, Richardson B, Overbaugh
J, Mwatha A, et al. Effect of breastfeeding and formula feeding
on transmission of HIV-1. A randomized clinical trial. JAMA
2000; 283:11671174.
72. The Kesho Bora Study Group. Triple antiretroviral compared
with zidovudine and single-dose nevirapine prophylaxis during
pregnancy and breastfeeding for prevention of mother-to-child
transmission of HIV-1 (Kesho Bora study): a randomised controlled trial. Lancet Infect Dis 2011; 11:171180.
73. Thomas TK, Masaba R, Borkowf CB, Ndivo R, Zeh C, Misore A,
et al. Triple-antiretroviral prophylaxis to prevent mother-tochild HIV transmission through breastfeeding: the Kisumu
Breastfeeding Study, Kenya a clinical trial. PLoS Med 2011;
8:112.
74. Chasela CS, Hudgens MG, Jamieson DJ, Kayira D,
Hosseinipour MC, Kourtis AP, et al. Maternal or infant antiretroviral drugs to reduce HIV-1 transmission. N Engl J Med
2010; 362:22712281.
75. Vella S, Schwartlander B, Sow SP, Eholie SP, Murphy RL. The
history of antiretroviral therapy and of its implementation in
resource-limited areas of the world. AIDS 2012; 26:1231
1241.
76. Institute of Medicine. Preventing HIV infection among injecting
drug users in high-risk countries. An assessment of the evidence. Washington, DC: The National Academies Press; 2006.
77. Moore A, Herrera G, Nyamongo J, Lacritz E, Granade T,
Nahlen B, et al. Estimated risk of HIV transmission by blood
transfusion in Kenya. Lancet 2001; 358:657660.
78. Schutz R, Savarit D, Kadjo JC, Batter V, Kone N, Ruche LG,
et al. Exclusion of high risk donors for reducing transfusiontransmitted HIV infection in a West African city. BMJ 1993;
307:15171519.
79. Dhingra N. Making safe blood available in Africa. Committee
on International Relations. Subcommittee on Africa, Global
Human Rights and International Operations. U.S. House
of Representatives; 2006. http://www.who.int/bloodsafety/
makingsafebloodavailableinafricastatement.pdf [Accessed 1
February 2012]
80. Cardo DM, Culver DH, Ciesielski CA, Srivastava PU, Marcus
R, Abiteboul D, et al. A casecontrol study of HIV seroconversion in healthcare workers after percutaneous exposure.
N Engl J Med 1997; 337:14851490.

81. Ciesielski C, Marianos D, Ou C-Y, Dumbaugh R, Witte J,


Berkelman R, et al. Transmission of human immunodeficiency
virus in a dental practice. Ann Intern Med 1992; 116:798
805.
82. Centers for Disease Control. Recommendations for preventing
transmission of human immunodeficiency virus and hepatitis
B virus to patients during exposure-prone invasive procedures. MMWR 1991; 40 (RR-8):19.
83. Hersh BS, Popovici F, Jezek Z, Satten GA, Apetrei RC, Beldescu
N, et al. Risk factors for HIV infection among abandoned
Romanian children. AIDS 1993; 7:16171624.
84. Hersh BS, Popovici F, Zolotusca L, Beldescu N, Oxtoby MJ,
Gayle DH. The epidemiology of HIV and AIDS in Romania.
AIDS 1991; 5 (Suppl 2):S87S92.
85. Yerli S, Quadri R, Negro F, Barbe KP, Cheseaux J-J, Burgisser P,
et al. Nosocomial outbreak of multiple bloodborne viral
infections. J Infect Dis 2001; 184:369372.
86. Schmid GP, Buve A, Mugyenyi P, Garnett GP, Hayes RJ,
Williams BG, et al. Transmission of HIV-1 infection in subSaharan Africa and effect of elimination of unsafe injections.
Lancet 2004; 363:482488.
87. De Cock KM, Churchill D, Grant A, et al. Summary of
Track B: clinical science. AIDS 1996; 10 (suppl 3):S107
S113.
88. CDC. Guidelines for human immunodeficiency virus case
surveillance, including monitoring for human immunodeficiency virus infection and acquired immunodeficiency syndrome. MMWR 1999; 48 (No RR-13):127.
89. UNAIDS. World AIDS day report, 2011. How to get to zero:
faster, smarter, better. http://www.unaids.org/en/media/unaids/
contentassets/documents/unaidspublication/2011/JC2216_
WorldAIDSday_report_2011_en.pdf. [Accessed 1 February
2012]
90. World Health Organization. Global tuberculosis control
2011. http://www.who.int/tb/publications/global_report/en/.
[Accessed 15 February 2012]
91. Buve A, Carael M, Hayes RJ, Auvert B, Ferry B, Robinson NJ,
et al. The multicentre study on factors determining the differential spread of HIV in four African cities: summary and
conclusions. AIDS 2001; 15:S127S131.
92. Tanser F, Barnighausen T, Hund L, Garnett GP, McGrath N,
Newell M-L. Effect of concurrent sexual partnerships on rate
of new HIV infections in a high prevalence, rural South
African population: a cohort study. Lancet 2011; 378:247
255.
93. Prejean J, Song R, Hernandez A, Ziebell R, Green T, Walker F,
et al. Estimated HIV Incidence in the United States, 2006
2009. PLoS One 2011; 6:e17502.
94. Pepin J. The origins of AIDS. New York: Cambridge University
Press; 2011. pp. 215220.
95. De Cock KM, Mbori-Ngacha D, Marum E. Shadow on the
continent: public health and HIV/AIDS in Africa in the 21st
century. Lancet 2002; 360:6772.
96. Cohen MS, Chen YQ, McCauley M, Gamble T, Hosseinipour
MC, Kumarasamy N, et al. Prevention of HIV-1 infection
with early antiretroviral therapy. N Engl J Med 2011; 365:
493505.
97. Montaner JSG, Lima VD, Barrios R, Yip B, Wood E, Kerr T, et al.
Association of highly active antiretroviral therapy coverage,
population viral load, and yearly new HIV diagnoses in British
Columbia, Canada: a population-based study. Lancet 2010;
376:532539.
98. Granich RM, Gilks CF, Dye C, De Cock KM, Williams BG.
Universal voluntary HIV testing with immediate antiretroviral
therapy as a strategy for elimination of HIV transmission: a
mathematical model. Lancet 2009; 373:4857.
99. Williams BG, Granich R, De Cock K, Glaziou P, Sharma A,
Dye C. Antiretroviral therapy for tuberculosis control in nine
African countries. Proc Natl Acad Sci U S A 2010; 107:19485
19489.
100. Auvert B, Taljaard D, Lagarde E, Sobngwi-Tambekou J, Sitta R,
Puren A. Randomized controlled intervention trial of male
circumcision for reduction of HIV infection risk: the ANRS
1265 trial. PLoS Med 2005; 2:e298.
101. Bailey RC, Moses S, Parker CB, Agot K, Maclean I, Krieger JN,
et al. Male circumcision for HIV prevention in young men in
Kisumu, Kenya: a randomised controlled trial. Lancet 2007;
369:643656.

Copyright Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

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


102. Gray RH, Kigozi G, Serwadda D, Makumbi F, Watya S,
Nalugoda F, et al. Male circumcision for HIV prevention in
men in Rakai, Uganda: a randomised trial. Lancet 2007;
369:657666.
103. World Health Organization/Joint United Nations Programme
on HIV/AIDS. WHO/UNAIDS technical consultation on male
circumcision and HIV prevention: research implications for
policy and programming. Conclusions and recommendations.
Geneva: World Health Organization; 2007. http://data.unaids.
org/pub/Report/2007/mc_recommendations_en.pdf. [Accessed
16 February 2012]
104. WHO. Global HIV/AIDS response: epidemic update and
health sector progress towards universal access: progress
report 2011. http://whqlibdoc.who.int/publications/2011/
9789241502986_eng.pdf. [Accessed 16 February 2012]
105. Williams BG, Lloyd-Smith JO, Gouws E, Hankins C, Getz WM,
Hargrove J, et al. The potential impact of male circumcision on
HIV in sub-Saharan African populations. PLoS Med 2006;
3:10321040.
106. Cohen J. Breakthrough of the year. HIV treatment as prevention. Science 2011; 334:1628.
107. Shelton JD. ARVs as HIV prevention: a tough road to wide
impact. Science 2011; 334:16451646.
108. Centers for Disease Control and Prevention. Vital signs: HIV
prevention through care and treatment United States.
MMWR 2011; 60:16181623.
109. Centers for Disease Control and Prevention. HIV Surveillance
Report. Vol. 21; 2009. http://www.cdc.gov/hiv/surveillance/
resources/reports/2009report/#commentary. [Accessed 1
February 2012]
110. Connor EM, Sperling RS, Gelber R, Kiselev P, Scott G,
OSullivan MJ, et al. Reduction of maternal-infant transmission of human immunodeficiency virus type 1 with zidovudine treatment. N Engl J Med 1994; 331:11731180.
111. Guay LA, Musoke P, Fleming T, Bagenda D, Allen M,
Nakabiito MB, et al. Intrapartum and neonatal single-dose
nevirapine compared with zidovudine for prevention of
mother-to-child transmission of HIV-1 in Kampala,
Uganda: HIVNET 012 randomised trial. Lancet 1999; 354:
795802.
112. WHO. Antiretroviral therapy for HIV infection in adults and
adolescents. Recommendations for a public health approach:
2010 revision. http://www.who.int/hiv/pub/arv/adult2010/en/
index.html. [Accessed 1 February 2012]

1213

113. WHO. Antiretroviral drugs for treating pregnant women and


preventing HIV infection in infants. Recommendations for a
public health approach (2010 version). http://www.who.int/
hiv/pub/mtct/antiretroviral2010/en/index.html. [Accessed 1
February 2012]
114. WHO, UNICEF, UNFPA, UNAIDS. Towards the elimination of
mother-to-child transmission of HIV. Report of a WHO technical consultation; 911 November 2010; Switzerland. http://
whqlibdoc.who.int/publications/2011/9789241501910_eng.
pdf. [Accessed 2 February 2012]
115. Degenhardt L, Mathers B, Vickerman P, Rhodes T, Latkin C,
Hickman M. Prevention of HIV infection for people who
inject drugs: why individual, structural, and combination
approaches are needed. Lancet 2010; 376:285301.
116. Jaffe HW, Valdiserri RO, De Cock KM. The re-emerging HIV/
AIDS epidemic in men who have sex with men. JAMA 2007;
298:24122414.
117. Centers for Disease Control and Prevention. Prevalence and
awareness of HIV infection among men who have sex with
men 21 cities, United States, 2008. MMWR 2010; 59:1201
1207.
118. Smith AD, Tapsoba P, Peshu N, Sanders EJ, Jaffe HW. Men who
have sex with men and HIV/AIDS in sub-Saharan Africa.
Lancet 2009; 374:416422.
119. UNAIDS, World Bank. New HIV infections by mode of
transmission in West Africa: a multicountry analysis; March
2010. http://www.unaids.org/en/media/unaids/contentassets/
documents/countryreport/2010/201003_MOT_West_Africa_
en.pdf. [Accessed 2 February 2012]
120. Halperin DT, Mugurungi O, Hallett TB, Muchini B, Campbell
B, Magure T, et al. A surprising prevention success. Why did
the HIV epidemic decline in Zimbabwe? PLoS Med 2011;
8:e1000414.
121. Hargrove JW, Humphrey JH, Mahomva A, Williams BG,
Chidawanyika H, Mutasa K, et al. Declining HIV prevalence
and incidence in perinatal women in Harare, Zimbabwe.
Epidemics 2011; 3:8894.
122. Abdool Karim SSA, Abdool Karim QA. Antiretroviral prophylaxis: a defining moment in HIV control. Lancet 2011;
378:e23e25.
123. Holmberg JA, Basavaraju S, Reed C, Drammeh B, Qualls M.
Progress towards strengthening national blood transfusion
services: 14 countries, 20082010. MMWR 2011; 60:1578
1582.

Copyright Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.