circumcision influence sexually transmitted diseases?
A literature review
Medical College of Wisconsin, Department of Pediatrics, Marshfield
Clinic, Lakeland Center, Minocqua, Wisconsin, USA
Despite the wide availability of condoms and the fear of HIV infection,
sexually transmitted diseases (STDs) continue to be a serious public
health concern. In the medical literature about preventive measures,
circumcision is rarely if ever mentioned as an effective preventive
measure: however, articles promoting the routine practice of
circumcision invariably mention the surgery's benefit of reducing STDs.
One author refers to over 100 medical articles supporting this thesis
. In the present review, the medical literature is examined to
determine what influence, if any, circumcision has on STDs.
Medline search was conducted using the keyword 'circumcision' and titles
located were examined to determine if they applied to the topic. Other
articles were identified through cited studies. Studies with
identifiable control groups were included for analysis. Only 31 studies
met this criterion [2-32]. Where data were available, odds ratios (ORs)
and 95% CI were calculated; an OR of > 1.0 denotes a positive
correlation with the presence of a foreskin.
reliability of the control group is a problematic issue. For example,
several studies used men with no STD as controls, without controlling
for the number of sexual partners. It is likely that men in the control
group had fewer partners and thus less exposure risk, making them
inappropriate controls. In Hand's 1949 study , Jews made up 17% of
the entire study population, but only 2.2% of the general publication
. Blacks in Hand's control group were more likely to be circumcised
than control white Gentiles (OR 1.41, 95% CI 0.87-2.27), which conflicts
with reliable published data . Some studies combined men with no
particular STD to form control groups. Some studies considered only men
with a different STD as the control group. Where the data were
available, results are reported in this review using a control group of
men with a STD other than the one in question, in an attempt to control
for exposure risk.
of the studies before 1994 made no attempt to control for known
confounding factors such as race, age, socio-economic status, level of
education, number of lifetime sexual partners, frequency of sexual
contact, or previous STD. The importance of these factors cannot be
understated. For example, Laumann et al.  found that as a man
increases the number of sexual partners, the risk of contracting STD
does not increase linearly, but nearly exponentially. Without
controlling for these factors, the results of these studies are of
limited value and make it impossible to determine whether circumcision
status is a marker for a significant risk factor or whether circumcision
status is the risk factor.
all of the studies published to date used information collected at STD
clinics. While an STD clinic will concentrate clinical material at one
location, study populations and controls derived from the clientele of
STD clinics may not reflect the population as a whole, and may introduce
a population bias that could unduly influence the results generated
. For example, Wilson compared seasoned soldiers who had STDs with
new recruits . To generalize the results of studies conducted in STD
clinics, it must be assumed that circumcised men use these health
facilities in the same manner. However, this is not the case, as
socio-economic and cultural factors often differ between these groups.
In the USA, men of higher socio-economic status are more likely to be
circumcised and more likely to have an STD treated by a physician in
private practice rather than at an STD clinic. Circumcised men may
exhibit different health-seeking behaviour than uncircumcised men, being
more likely to seek care for minor abrasions, thus being placed in the
control group more often than their uncircumcised cohorts . This
would cause the association between the foreskin and various STDs,
including HIV infection to be overestimated, if not spuriously generated
. In one African study, circumcised men had more lifetime partners,
were more likely to smoke, drink alcohol, or have contact with
prostitutes. They were less likely to be married ; none of these
factors were controlled for in that study.
most reliable type of study is a random population survey; to date only
a couple have been published [28,31,32]. The drawbacks of these studies
is that more subjects are needed to make a significant difference and
circumcision status is determined by history, but the lack of population
bias may compensate for these shortcomings.
et al. , in their retrospective chart review, found that
circumcision status was documented in 86% of clinic notes. Taylor and
Rodin recorded circumcision status in 89% of their charts ; these
percentages are strikingly high. The Mayo clinic could not identify
circumcision status in 16% of their cases of penile cancer .
et al.  found a high correlation between history and physical
examination, with a sensitivity (Sen) of 98%, specificity (Sp) of 99%, a
positive predictive value (PPV) of 99%, and a negative predictive value
(NPV) of 98%, while other studies have found no correlation. In a study
in 1960 of men in New York and Los Angeles, only half of circumcised men
correctly identified themselves as circumcised (Sen 51%, Sp 96%, PPV
93%, NPV 35% , men in Latin America (Sen 89%, Sp 84%, PPV 41%, NPV
98%) , and men in Africa (Sen 94%, Sp 72%, PPV 69%, NPV 95%) 
yielded similar results.
The history of the role of circumcision in STDs
the development of the germ theory of disease and modern epidemiology,
it was noted that Jews had a lower incidence of syphilis , but a
higher incidence of gonorrhoea, than Gentiles . One rationale that
developed to explain this finding was that Jews were protected from
syphilis by circumcision. The influence of religion on sexual practices
and the ban on Christian prostitutes consorting with Jews  were not
considered in deriving this theory. Since then, the theory has been
perpetuated and embellished.
studies cited as supporting a role of circumcision in the prevention of
STDs are not case-controlled. Several studies make unsubstantiated
estimates of male circumcision rates in the general population to use
for comparative purposes. Other studies use ethnicity and tribal
affiliation as an indicator of circumcision status. While these measures
are crude and unscientific, the available data have been used to assess
risk and statistical significance. The characteristics of the studies
using identifiable control groups are listed in Table 1. Most studies
that were not random population surveys were conducted at STD clinics.
Normal microbial flora
studies are summarized in (Table 2). Urethral smears of healthy
uncircumcised males are less likely to have Gram-positive organisms (OR
0.40, 95% CI 0.18-0.91) , while Staphylococcus aureus is
cultured significantly more often from periurethral swabs of circumcised
boys 12 months and younger . Not surprisingly, pyoderma is more
common after circumcision in male infants than do those not circumcised
[45,46]. Facultative Gram-negative rods and Escherichia coli are
commonly found in the periurethral flora of uncircumcised males (OR
3.72, 95% CI 0.84-16.54 ; E. coli OR 5.52, 95% CI 2.95-10.33
). What impact this has on the susceptibility to illness has yet to
conjectured that Mycobacterium smegmaticus could be a cause of
urethritis. A study looking for acid-fast bacilli in urethral smears of
men with urethritis failed to detect circumcision status as a
significant factor (OR 1.38, 95% CI 0.15-2.23) .
Controversy exists over whether Ureaplasma urealyticum and
Mycoplasma hominis are normal flora or STDs. While some studies have
found these organisms more commonly in men with urethritis, others have
found their prevalence to be nearly identical in men with urethritis and
asymptomatic controls [8,11]. A few studies have investigated
circumcisions impact on the prevalence of mycoplasmas. One of the
significant variables is the location of the organisms. Both U.
urealyticum and M. Hominis were more likely to be obtained
from the coronal sulcus in men with foreskins. When only urethral swabs
are considered, U. urealyticum is more common in circumcised men
A change in sub-preputial flora takes place with the onset of sexual
activity, making this flora more like that of the adult female vagina.
It has not been shown whether organisms cultured from the coronal sulcus
affect urethral flora or disease.
Krieger et al.  found that uncircumcised men were more likely to
have Trichomonas vaginalis detected on a urethral swab or
first-void urine cultures (OR 1.95, 95% CI 1.03-3.67). However, when
logistic regression is applied (controlling for age, race, age at sexual
debut, exposure to T. vaginalis, number of sexual partners, and
previous treatment for T. vaginalis, gonorrhoea, or non-specific
urethritis), circumcision status was not a significant factor. (OR 1.1,
95% CI 05--2.3).
studies looking for the presence of yeast, Rodin and Kolator  and
Davidson  detected no difference in carriage of yeast between those
with and without a foreskin. However, circumcised carriers were more
likely to be asymptomatic, making these men a more serious vector for
the spread of yeast infections to women. . It is likely that Parker
et al. only cultured swabs from symptomatic men for yeast .
This lack of random sampling may explain their findings.
Genital ulcer disease vs. urethritis
Instead of comparing individual disease entities, several studies have
compared genital ulcer disease (GUD), which includes syphilis, chancroid,
herpes simplex, etc., to urethritis, which includes gonorrhoea,
chlamydia, and urethritis (Table 3). Instead of using a control group,
these studies included those with either GUD or urethritis and compared
the two entities. Similarly, the earliest study suggesting a protective
role for circumcision found that Jews in London were more likely to get
gonorrhoea and Gentiles were more likely to get syphilis (OR 6.59, 95%
CI 3.27-13.27) . Wolbarst likewise found that circumcised men were
more likely to present with gonorrhoea than with syphilis [3-5]. It can
be gathered from these studies that circumcised men presenting with an
STD are more likely to have urethritis, while uncircumcised men are more
likely to present with GUD. Because there is no true control group, no
inference regarding disease prevention can be drawn from this
random population survey addressing urethritis, uncircumcised men were
less likely to have it (OR 0.61, 95% CI 0.43-0.87; Table 3). The authors
noted that most cases of urethritis is that region were from gonorrhoea
. Two STD clinic studies from Africa failed to document a difference
of the data for the incidence of gonorrhoea have come from STD clinic
studies (Table 3); the results have been inconsistent. When appropriate
control groups are applied to the studies from the 1940s [6,7],
circumcised white men are at higher risk for gonorrhoea. When the data
from Smith et al. were categorized by race, no difference in
gonorrhoea rates could be detected between those men with and without a
foreskin . In a study of 537 sailors examined for gonorrhoea before
and after sexual exposure during shore leave in the Far East,
circumcision status did not affect susceptibility in blacks, and
although uncircumcised whites had higher rates of gonorrhoea than
circumcised whites, the difference was not statistically significant
(P>0.10) . In a random population survey, Laumann et al. 
discovered that the number of lifetime partners dramatically affected
the impact of circumcision on gonorrhoea. While circumcised men with
5-20 lifetime partners were at lower risk for gonorrhoea, circumcised
men with <20 lifetime partners were at significantly higher risk of
gonorrhoea than uncircumcised men with a similar number of lifetime
partners. It may be that more partners increases the diversity of the
subpreputial flora, thus offering some protection to the uncircumcised
urethritis (NGU) is not prevented by circumcision and may be more common
in circumcised men (Table 3). Some of the studies distinguished between
chlamydia and NGU [15,26,31]. A significant correlation between the
foreskin and NGU has yet to be detected and a negative correlation
appears likely. Chlamydia is most commonly the cause of NGU: the data
suggest that circumcised men are at greater risk of chlamydial
Genital ulcer disease
Several of the HIV studies examining the role of circumcision have also
provided data on its role in the incidence of GUD (Table 4). The
findings have been inconsistent but suggest that uncircumcised men may
be at greater risk for GUD.
the difficulties in studying syphilis is its low prevalence. Most of the
recent studies have been unable to detect a statistically significant
difference because there are too few cases. Even the large population
survey by Laumann et al. could not detect a difference . The
results by Kreiss and Hopkins  cannot be generalized to the
population at large because both circumcision and syphilis status were
obtained by history from a study population that only included men
engaging in homosexual activity. When the African data reported in a
study by Urassa et al.  are controlled for background
characteristics, including HIV status, no difference is detectable (OR
1.05, 95% CI 0.97-1.27).
Circumcision was once proposed as a treatment for chancroid [48,49]
until antibiotics were shown to be effective . Although it is
generally reported that chancroid is more common in uncircumcised males
[51-55], a review of the medical literature found no case-controlled
study to support this assertion, other than the study by Hand .
When the proper control group is applied to Hand's data, an interesting
finding emerges. Chancroid is significantly more common in uncircumcised
white males, but significantly more common in circumcised black males.
In two studies from Singapore STD clinics, Malays, who are predominantly
Islamic, were less likely to have chanchroid, but in neither study was
the finding statistically significant., as there were too few Malays
[56,57]. In one of the studies, Indians were more likely to develop
chancroid than Chinese (OR 20.77, 95% CI 8.11-53.17). When Malays were
compared with Chinese, Malays had a higher incidence of chancroid (OR
3.12, 95% CI 0.81-12.08) . In both studies, calculations were based
on assumptions of ethnic prevalence in the population and ethnic
associations with circumcision status. If chancroid is related to
circumcision status, Malays, who routinely circumcise, would be expected
to have a lower incidence of chancroid than the Chinese who do not.
outbreak of chancroid in Winnipeg, Manitoba, Canada, the community of
Native Indians and Métis (mixed Indian and Caucasian) were the focus of
the outbreak, rather than Caucasians . The published evidence
suggests that race and ethnicity are more likely to be a factor in
chancroid infection than circumcision status. This finding is consistent
with the recognized tendency of highly contagious STDs to concentrate in
'core' populations 
results for genital herpes have been inconsistent. Hand, without
providing data, reported that circumcision had no impact on the
incidence of genital herpes . When Taylor and Rodin's data are
analysed by race, the significance of the foreskin for those originally
from the UK disappears .
Human papillomavirus and genital warts
attention has been paid to human papillomavirus (HPV) since it was
linked with cervical and penile cancers [37,58] (Table 5). The
epidemiology of these cancers mimics that of STDs. Genital warts have
consistently been a significant risk factor for penile cancer [59,60].
The role of circumcision in the prevention of penile cancer is
controversia, especially in light of a recent report from Seattle in
which 42% of men with penile cancer were circumcised . In recent
studies, HPV-associated lesions are either equally common [15,23,27] or
more common in circumcised men. A larger cohort of circumcised men in
the USA is reaching the age at which penile cancer occurs. This has
resulted in more circumcised men with penile cancers than seen
previously [61,62]. How the higher risk of genital warts in circumcised
men will affect penile cancer has yet to be determined. The use of
condoms and screening men at risk for HPV infection using acetic acid
and colposcopy may be the best use of resources for preventing penile
and cervical cancers. [63,64].
Israeli study of the prevalence of hepatitis B surface antigen in 9182
school children, the investigators speculated as to whether male
circumcision could be an important mode of infection, explaining both
the male predominance and the striking seasonal trend among boys that
their study revealed . An Ethiopian study suggested that
circumcision may play a role in HBV transmission , but a Gambian
study failed to find an association . Likewise, Donovan et al. 
and Laumann et al. found no difference in hepatitis between men
with and without a foreskin.
recently, no studies have examined the impact of circumcision on overall
STD incidence. The data indicate that circumcised men may be a higher
risk for an STD (Table 5). This is consistent with trends seen in the
USA. As routine neonatal circumcision has been implemented, the rate of
STDs has increased rather fallen. Among first-world nations, the USA has
one of the highest rates of STDs. HIV infection and male circumcision.
In the report by Cook et al.  the average uncircumcised man
had 2.16 STDs diagnosed, while in the average circumcised man it was
2.32; in an Australian study, there was no difference (1.48 vs 1.44 STDs
diagnosed per patient) .
have been 36 case-controlled studies published in peer-reviewed journals
addressing the relationship between the foreskin and HIV infection; the
results have been inconsistent. Several studies performed in STD clinics
have found the foreskin to be a risk factor [17,18,21,25,29,30,68-72],
while several random population surveys, which do not have the
population bias of an STD clinic study, have found circumcised men to be
at higher risk [32,73-75]. Several studies have failed to detect a
statistically significant difference between men with and without a
foreskin [31,76-87]. In several studies, when the populations are
controlled for GUD, number of sexual partners and other factors, the
results differ significantly from the raw data. The USA has the highest
incidence of HIV infection, as well as the highest incidence of male
circumcision amongst developed nations. This speaks against the
protective effect of circumcision . The inconsistency of the results
and the number of confounding factors make it impossible to link the
foreskin to HIV infection [36,90].
impossible to assert a causal relationship based on retrospective data.
Hill developed criteria for assessing whether a strong case can be made
for causality based on retrospective data .
If an association has a high OR, it weighs in favour of a causal
relationship. Few of the associations have had an OR of > 2.0. Moreover,
the studies that randomly accessed portions of the population outside of
STD clinics have found circumcised men to be at higher risk for an STD
Consistency: Results among studies have been very inconsistent:
this speaks against causality.
Specificity: There are several confounding factors: circumcision
is not chose randomly . Significant factors such as race,
socio-economic status, education level and number of partners are often
not controlled for in the published studies. In most studies where these
factors have been controlled for, the foreskin is not a significant
factor. For example, a US Army study of soldiers in Japan reported that
uncircumcised men were more likely to have a penile lesion than were
random controls (OR 22.78, 95% CI 6.00-86.29), but men with penile
lesions were more likely to be black (OR 15.00, 95% CI 3.12-72-07) or to
have had a previous STD (OR 4.41, 1.71-11.34) . No attempt was made
to control for these significant factors.
Temporality: Most males are circumcised before beginning sexual
activity. While some effort has been made to promote circumcision as an
HIV preventive in Africa , no studies of the effects of later
circumcision on disease prevention have been published.
Biological gradient: One study of HIV found that circumcised men
with more residual foreskin were at higher risk of HIV-2 infection .
It is difficult to make any conclusion from this one study.
Biological plausibility: Moses et al.  suggested: (a)
that minor inflammatory conditions can occur underneath the foreskin,
resulting in mucosal discontinuity that may provide a portal of entry
for viruses and bacteria: (b) that the foreskin may be more susceptible
to minor trauma during intercourse: (c) that the warm, moist environment
under the foreskin may provides an environment conducive to prolonged
survival of pathogens; and (d) in the case of HIV, that Langerhans
cells, plentiful in the foreskin of male macaque monkeys, are highly
susceptible to simian immunodeficiency virus (SIV) .
While the warm moist environment under the prepuce allows for the
growth of all bacteria, including pathogens, the immunological
protection provided the subpreputial flora , secretory
immunoglobulins, and lytic secretions from the prostate, urethra, and
seminal vesicles  have not been adequately investigated. Undisturbed
preputial flora and mucosal immunological defences may protect the
uncircumcised male for infection .
The role of Langerhans cell in the transmission of HIV is unclear.
While they are present in the mucosal prepuce of monkeys  and adult
males , Weiss et al. were not able to detect their presence
on the inner surface of prepuces taken from newborns . These cells
initiate the immune response to infectious agents. In the primate study
referred to by Moses et al.  it was Langerhans-like cells in the
lamina propria, and not in the epithelium, that appeared to be infected
with SIV . It is unclear whether this observation can be
extrapolated to the Langerhans cells in the epithelium of the prepuce in
Beaugé suggests that the loss of penile skin from circumcision
frequently results in tightened skin over the erect penis. This
increases friction during intercourse and increases the likelihood of
abrasions through which a pathogen can be introduced systemically,
making the circumcised penis more likely to contract an STD . The
increased likelihood of circumcised men engaging in active anal sex 
may also increase a circumcised man's susceptibility to STDs.
Coherence: Circumcision as a preventive measure for STDs needs to
fit into a coherent explanation that takes other know risk factors into
account. To date, the only theory proposed is the 'subpreputial space as
a cesspool' explanation provided by Weiss . If the 'cesspool"
theory is extended to women, then one would expect that women, who have
significantly more genital mucosa, would have markedly more STD's than
men, whether circumcised or not; this is not the case . Nearly all
of the associations between STDs and the foreskin can be explained on
the basis of racial, socio-economic, cultural, ethnic, and
healthcare-seeking behavioural differences. Studies controlling for
these factors have failed to confirm the efficacy of circumcision in
Experimental evidence: There is none.
Analogy: Is there another illness to which the foreskin makes a
man more susceptible? Can it be equated with the acquisition and
transmission of STDs? Lower urinary tract infections in infancy may be
associated with the foreskin, but showing analogy to STDs would be a
formidable task. Upper urinary tract infections in males are most often
related to anatomical anomalies in the male rather than the foreskin
, and unrelated to behaviour patterns. The aetiologies of these
maladies are so disparate that forming an analogy is impossible. Based
on the above criteria, a causal relationship between the foreskin and
STDs cannot be inferred.
began as speculation has resulted a century later in 60-75% of American
boys being circumcised with no clearly confirmed medical benefit. In the
interim, no solid epidemiological evidence has been found to support the
theory that circumcision prevents STDs or to justify a policy of
involuntary mass circumcision as a public health measure. While the
number of confounding factors and the inability to perform a random,
double-blind, propective trial make assessing the role of circumcision
in STD acquisition difficult, there is no clear evidence that
circumcision prevents STDs. The only consistent trend is that
uncircumcised males may be more susceptible to GUD, while circumcised
men are more prone to urethritis. Currently, in developed nations,
urethritis is more common than GUD . In summary, the medical
literature does not support the theory that circumcision prevents STDs.
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R. S. Van Howe, MD, FAAP, Clinical Instructor.
Medical College of Wisconsin, Department of Pediatrics,
Marshfield Clinic, Lakeland Center, 9601 Townline Road,
PO Box 430, Minocqua, Wisconsin 54548-1390, USA