Can Routine Neonatal Circumcision Help Prevent Human Immunodeficiency Virus Transmission in the United States?

Abstract

Primary prevention of human immunodeficiency virus (HIV) continues to pose an important challenge in the United States. Recent clinical trials conducted in Kenya, South Africa, and Uganda have demonstrated considerable benefit of male circumcision in reducing HIV seroincidence in males. These results have ignited debate over the appropriateness of implementing routine provision of neonatal circumcision in the United States for HIV prevention. This article discusses major contextual differences between the United States and the three African countries where the clinical trials were conducted, and cautions that the applicability of the scientific data from Africa to this country must be carefully considered before rational policy recommendations regarding routine neonatal circumcision can be made as a strategy to prevent the spread of HIV in the United States.

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American Journal of Men's Health
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The online version of this article can be found at:
DOI: 10.1177/1557988308323616
2009 3: 79 originally published online 23 September 2008Am J Mens Health
Xiao Xu, Divya A. Patel, Vanessa K. Dalton, Mark D. Pearlman and Timothy R. B. Johnson
the United States?
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79
routine provision of neonatal circumcision in the
United States for HIV prevention (McNeil, 2007).
Evidence on Male Circumcision as a
Preventive Strategy and Implications for
the United States
Until these recent clinical trials, there have been no
randomized studies assessing male circumcision as a
preventive strategy for heterosexual acquisition of
HIV in men (Siegfried et al., 2003). A systematic
review assessing the role of male circumcision in pre-
venting heterosexual acquisition of HIV in men using
evidence from 37 observational studies published in
or before 2004 reported that many studies failed to
control for confounding factors, such as genital ulcer
disease, co-occurring sexually transmitted infections
(STIs), unsafe medical practices, viral load, religion,
culture, socioeconomic status, condom use, migra-
tion status, age, and study location (Siegfried et al.,
2005). Because the vast majority of these 37 studies
were conducted in Africa and Asia, we have a limited
understanding of the effects of male circumcision on
HIV prevention in the United States.
P
rimary prevention of human immunodefi-
ciency virus (HIV) continues to pose an
important challenge in the United States. An
estimated 1.0 to 1.2 million Americans are living
with HIV (Glynn & Rhodes, 2005) and 40,000 new
infections occur each year (Centers for Disease
Control and Prevention, 2006a). Despite recent
advances in HIV/AIDS treatment, including highly
active antiretroviral therapy (HAART), HIV remains
an incurable condition (Hamers & Downs, 2004). In
2006, 14,627 Americans died of AIDS (Centers for
Disease Control and Prevention, 2008).
Recent clinical trials conducted in Kenya, South
Africa, and Uganda have demonstrated considerable
benefit of male circumcision in reducing HIV
seroincidence in males (51% to 60% reduction in
the relative risk; Auvert et al., 2005; Bailey et al.,
2007; Gray et al., 2007). These results have ignited
debate over the appropriateness of implementing
Can Routine Neonatal Circumcision
Help Prevent Human Immunodeficiency
Virus Transmission in the United States?
Xiao Xu, PhD, Divya A. Patel, PhD, MPH, Vanessa K. Dalton, MD, MPH,
Mark D. Pearlman, MD, and Timothy R. B. Johnson, MD
Primary prevention of human immunodeficiency virus
(HIV) continues to pose an important challenge in the
United States. Recent clinical trials conducted in
Kenya, South Africa, and Uganda have demonstrated
considerable benefit of male circumcision in reducing
HIV seroincidence in males. These results have ignited
debate over the appropriateness of implementing rou-
tine provision of neonatal circumcision in the United
States for HIV prevention. This article discusses major
contextual differences between the United States and
the three African countries where the clinical trials
were conducted, and cautions that the applicability of
the scientific data from Africa to this country must be
carefully considered before rational policy recommen-
dations regarding routine neonatal circumcision can
be made as a strategy to prevent the spread of HIV in
the United States.
Keywords: human immunodeficiency virus; neonatal
circumcision; prevention
From the Department of Obstetrics and Gynecology, University
of Michigan, Ann Arbor, Michigan.
Address correspondence to Xiao Xu, PhD, Department of
Obstetrics and Gynecology, University of Michigan, L4000
Women’s Hospital, 1500 East Medical Center Drive, Ann Arbor,
MI 48109; e-mail: xiaox@med.umich.edu.
American Journal of
Men’s Health
Volume 3 Number 1
March 2009 79-84
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Furthermore, though several studies have been
conducted, the cost-effectiveness of routine neona-
tal circumcision has not yet been established for the
U.S. setting. Research by Lawler, Bisonni, and
Holtgrave (1991) and Ganiats, Humphrey, Taras, and
Kaplan (1991) in the early 1990s found minimal dif-
ferences in lifetime cost and utility between circum-
cised and uncircumcised newborns (without
considering the spread of STI). By incorporating
data on additional medical sequelae, as they became
available, particularly the transmission of HIV and
STI, Van Howe (2004) conducted the most recent
cost-effectiveness analysis in the U.S. setting. The
study demonstrated that over the lifetime, neonatal
circumcision is associated with $828 incremental
costs and a 0.0153 reduction in quality adjusted life
years (QALYs) for each neonate. Poor quality data
were identified as the “greatest handicap in the
development” of these cost-effectiveness analyses
(Van Howe, 2004). Notably, this analysis preceded
the recent clinical trials conducted in Kenya, South
Africa, and Uganda.
These clinical trials have methodological advan-
tages over most previous studies, and hence provide
better quality data. Beyond using the randomized
controlled study design, the clinical trial in Kenya
adjusted for baseline variables that were slightly
imbalanced between the two study groups (despite
randomization; Bailey et al., 2007) and the Ugandan
trial adjusted for postulated potential confounders
identified in previous studies, including baseline age,
marital status, and sexual risk behaviors (Gray et al.,
2007). Still, caution should be taken in adopting
these data in any rigorous evaluations of a policy for
routine provision of neonatal circumcision to prevent
HIV in the United States because of major contextual
differences between the United States and Africa.
Major Contextual Differences Between
the United States and Africa
Several factors differ between these two distinct
regions, such as age at circumcision, dominant mode
of HIV transmission, biological factors, HIV trans-
mission dynamics, and health care system factors.
Adult Versus Neonatal Circumcision
In the United States, the majority of adult men are
already circumcised (Xu, Markowitz, Sternberg, & Aral,
2007); male circumcision is generally practiced at
birth. National Hospital Discharge Survey data indi-
cate that the overall rate of neonatal circumcision
has remained near 65% since data collection began
in 1979, and that 56% newborn males born in U.S.
hospitals were circumcised in 2003 (Child Trends
DataBank, 2004). In contrast, the minimum age of
enrollees in the recent clinical trials in Kenya, South
Africa, and Uganda was 15 years. This major differ-
ence in age at circumcision precludes direct com-
parison of the effectiveness of circumcision between
the two geographic regions. Assessment of the effec-
tiveness of a prevention intervention initiated at
birth entails parameters beyond age at circumcision.
In particular, 39.3% of ninth grade male students in
the U.S. have had sexual intercourse and 8.8% of
male students have their first sexual intercourse
before age 13 (Centers for Disease Control and
Prevention, 2006b). Because in the United States
circumcision is generally performed at birth, sexual
exposures during young adolescent age must be con-
sidered when evaluating the effects of circumcision
on HIV prevention in the United States.
Dominant Modes of HIV Transmission
In the United States, the most common mode of
transmission for HIV infection was penile-anal sex-
ual contact, accounting for about 49% of all
reported HIV or AIDS cases diagnosed in 2006
(Centers for Disease Control and Prevention, 2008).
This is followed by high-risk heterosexual contact
and use of nonsterile drug injecting equipment,
accounting for 33% and 13% of the reported
HIV/AIDS cases diagnosed in 2006, respectively
(Centers for Disease Control and Prevention, 2008).
These patterns differ from the population in which
the three randomized trials in Kenya, South Africa,
and Uganda were conducted where heterosexual
transmission of the HIV was the predominant mode
(Chen et al., 2007; Kahn, Marseille, & Auvert,
2006). Because the African clinical trials focused on
the risk of heterosexual HIV transmission from
females to males, the potential impact of male cir-
cumcision on reducing HIV infection associated
with other modes of transmission, such as male-
to-male and injection drug use transmission, remains
largely unknown (National Institute of Allergy and
Infectious Diseases, 2006). A recent systematic
review identified only two studies of male circumci-
sion in relation to the risk of male-to-male HIV
80 American Journal of Men’s Health / Vol. 3, No. 1, March 2009
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transmission (Fankem, Wiysonge, & Hankins, 2007).
The authors of the review cautioned against any
conclusions regarding the biological effect of male
circumcision on HIV transmission in the male-to-
male population because of the potential for unmea-
sured confounding factors in these two observational
studies.
In addition, 27% of American adults and adoles-
cents living with HIV/AIDS in 2006 were women
(Centers for Disease Control and Prevention, 2008).
Of them, 73% were infected during high-risk het-
erosexual contact (Centers for Disease Control and
Prevention, 2008). Moreover, 92% of HIV/AIDS
cases in children (<13 years) were attributable to
vertical transmission from mother (Centers for Disease
Control and Prevention, 2008). The Kenyan, South
African, and Ugandan trials primarily examined HIV
acquisition among circumcised versus noncircum-
cised males; hence the impact of circumcision on
reduction in male-to-female transmission is unknown
to date (Auvert et al., 2005; National Institute of
Allergy and Infectious Diseases, 2006). To fully
assess the benefit of any HIV prevention strategy, it
is essential to consider the effect among both men
and women.
Biological Factors
and Transmission Dynamics
HIV acquisition and transmission are associated
with several biologic factors including seropreva-
lence, viral load, co-occurring STI, stage of disease,
duration of infectiousness, genetic haplotype, viral
subtype, and levels of mucosal immune response
(Aral & Holmes, 1999; Quinn, 2006), several of
which differ significantly between the United States
and Africa. For instance, the prevalence of HIV
infection among adults and adolescents in the
United States was estimated at 0.14% at the end of
2005 in the 37 areas with confidential name-based
HIV infection reporting (Centers for Disease
Control and Prevention, 2006a). In contrast, HIV
prevalence in the countries in which the circumci-
sion trials were conducted range from an estimated
6.2% to 7% in Uganda and Kenya to nearly 25% in
South Africa (Joint United Nations Programme on
HIV/AIDS [UNAIDS], 2006). Applying the number
needed to treat concept (Laupacis et al., 1988), the
markedly different prevalence of HIV infection in
the United States raises considerable questions about
the number of procedures necessary to prevent a
single case of HIV transmission compared with
Africa. The number of males needed to be circum-
cised to prevent one new HIV infection could be
substantial in the United States. This raises the
potentially controversial issue of recommending
widespread prevention, when only a small targeted
group might benefit. Moreover, this makes the cost-
effectiveness of male circumcision less promising in
the United States than in African countries.
The transmission dynamics of HIV are also
influenced by the phase of the epidemic, population
prevalence, transmission probability, and specific
characteristics of transmission networks (e.g., sexual
mixing, partner concurrency). The presence of co-
occurring STIs, such as gonorrhea, chlamydia, her-
pes simplex virus, or syphilis, also increases the risk
of HIV transmission during unprotected sexual con-
tact between an infected and uninfected partner
(Cameron et al., 1989). Between- and within-
country differences in patterns of sexual behavior,
including age at sexual initiation, current and life-
time number of sex partners, frequency and consis-
tency of sexual activity, mode of recruitment of sex
partners, and duration of sexual partnerships (Aral
& Holmes, 1999) have important implications for
HIV prevention strategies. For example, studies
show that the higher likelihood of having more than
one long-term sexual partner at a time among
Ugandan men than men in Thailand and the United
States has contributed to the more generalized spread
of HIV in Uganda (Morris, 2002). Five percent of
the study participants in the Kenyan circumcision
trial had Chlamydia trachomatis (Bailey et al., 2007),
whereas in the United States the rate of chlamydial
infection was 348 per 100,000 population in 2006
(Centers for Diseases Control and Prevention,
2007). Moreover, 34% of the participants in the
Ugandan trial had two or more sexual partners in the
past 12 months (Gray et al., 2007) and 42% of
the participants in the Kenyan circumcision trial
had at least two partners in the previous 6 months
(Bailey et al., 2007). This compares with 19.5% of
American males aged 15 to 44 years who had two
or more sexual partner in the past 12 months (U.S.
Census Bureau, 2008). Regional differences in
these factors must be considered.
Health Care System
Fundamental differences between health care sys-
tems in the United States and Africa could influence
Neonatal Circumcision and HIV Prevention / Xu et al. 81
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the rates of HIV transmission, as well as the cost-
effectiveness of HIV prevention interventions. There
is better public health infrastructure and access to
clinical, laboratory, and pharmacy in the United
States, which could lead to early detection and treat-
ment of HIV-infected patients and patients with
other STIs. Moreover, utilization rates of advanced
medical technologies are higher among patients in
the United States, particularly with regard to
HAART therapy. Seventy percent of HIV-infected
Americans receive antiretroviral therapy (UNAIDS,
2007), while in sub-Saharan Africa, it is estimated
that less than one quarter (23%) of those in need of
antiretroviral treatment are receiving it (UNAIDS,
2006). Use of HAART could substantially lower
viral load and shorten the level and duration of
infectiousness.
In addition, infection control in the health care
setting varies across countries. The transmission
probabilities for contaminated medical injections and
contaminated blood products have been estimated at
0.45% and 92.5%, respectively (Baggaley, Boily,
White, & Alary, 2006). Thus, differences between
countries in the exposure to blood-borne pathogens in
the health care setting also affect the probability of
infection among susceptible individuals (Hu, Kane, &
Heymann, 1991). It was estimated that 6% of HIV
infections in Africa was due to blood transfusions and
1.6% was due to contaminated medical injections and
other health care procedures (Chin, Sato, & Mann,
1990; Gisselquist, Potterat, Brody, & Vachon, 2003).
More recent data suggest that unsafe health care
exposures in sub-Saharan Africa might have played an
even larger role in the spread of HIV (Deuchert &
Brody, 2006; Gisselquist et al., 2003). In contrast, the
risk of transfusion-transmitted HIV infection is
extremely low in the United States (1 in 677,000
units; Glynn et al., 2000; Kleinman, Busch, Korelitz,
& Schreiber, 1997).
Finally, as an incurable condition, HIV/AIDS
requires costly lifelong treatment (Hamers & Downs,
2004). Differences in the cost of medical care between
countries could significantly influence the cost-
effectiveness of an HIV prevention intervention. The
per capita health expenditure in the United States
was $6,096 in 2004 compared with $748, $135, and
$86 in South Africa, Uganda, and Kenya, respec-
tively (United Nations Development Programme,
2007). An intervention found to be cost-effective in
one country may not prove to be cost-effective in
another because of such wide differences in cost of
care. Caution needs to be taken when translating
HIV-prevention strategies across countries.
Future Directions and
Emphasis for Research
Encouraging data from the recent clinical trials in
Kenya, South Africa, and Uganda have raised the
question regarding the implications for HIV preven-
tion in the United States. However, acceptability of
routine neonatal circumcision in the United States
is an issue at the intersection of medicine, public
health, religion, culture, ethics, law, and human
rights. Before neonatal circumcision can be recom-
mended as a strategy to prevent the spread of HIV in
the United States, the applicability of the clinical
trial data from Kenya, South Africa, and Uganda to
this country must be carefully considered.
Assessment of the impact of male circumcision
in the United States must consider exposures occur-
ring during adolescence (because in the United
States, circumcision is generally performed at birth),
differences in factors influencing HIV transmission
dynamics, including the heterogeneity in HIV preva-
lence, as well as differences in other biological and
behavioral factors that affect transmission. In addition,
despite the widely recognized burden of HIV-/AIDS-
related diseases, resources available to combat the
epidemic are limited (Marseille et al., 2002).
Comprehensive cost-effectiveness analysis consider-
ing the various elements of HIV transmission in the
context of the United States will be instrumental in
elucidating the potential cost, benefit, and risks of
HIV-prevention strategies.
Clearly, more research addressing the following
questions would greatly inform the discussion
regarding the utility of routine neonatal circumci-
sion in HIV prevention in the United States: What
is the effect on HIV transmission when circumcision
is performed at birth? What is the effect on HIV pre-
vention specifically in the context of the U.S. epi-
demic (particularly seroprevalence and predominant
mode of transmission)? What is the magnitude of
the impact of circumcision on reduction in male-
to-female transmission? Whether it is cost-effective
to perform routine neonatal circumcision in pre-
venting HIV transmission in the U.S. setting? These
important questions must be answered before
rational policy recommendations regarding neonatal
circumcision can be made.
82 American Journal of Men’s Health / Vol. 3, No. 1, March 2009
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Acknowledgments
DAP is supported by a grant from the National
Cancer Institute/National Institutes of Health (1 K07
CA120040-01). VKD’s effort on this project was in
part supported by grant number 1 K08 HS015491
from the Agency for Healthcare Research and Quality.
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