How does male circumcision protect against HIV infection?
BMJ 2000; 320 doi: https://doi.org/10.1136/bmj.320.7249.1592 (Published 10 June 2000) Cite this as: BMJ 2000;320:1592
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Th e-letter from Judith E Brown serves as a reminder of the cross-cultural
problems associated with research of the kind presented by Short and Szabo.
Western researchers have a clear idea of what they understand by "circumcision",
but do not appreciate that "circumcision" in other parts of the
world may refer to many differing procedures with differing characteristics
and effects. The effects of one practice may not, indeed probably do not,
read across to the others.
While some of those looking at the effects of circumcision on HIV in
Africa are no doubt innocents drawn unwittingly into the fray, many "researchers"
are seeking to use African data of spurious relevance to proselytise for
their own form of "circumcision" in their own culture.
The recent Los
Angeles Times article Spreading Islam With His Scalpel (Monday, May
21, 2001) shows that circumcisers consider they have a role in expanding
the political and economic influence of their countries. Medical research
should not be subverted by those with similar ambitions.
Competing interests: No competing interests
EDITOR - We are currently investigating male circumcision in central
Kenya, so we found helpful Szabo and Short's discussion of the mechanisms
that may link an intact foreskin with heightened risk of HIV infection.
They offer two possibilities: (a) Langerhans' cells with HIV receptors on
the inner surface of the foreskin, and (b) a vascularised frenulum
susceptible to trauma during intercourse.1
We must not assume, however, that we all know what "circumcision" is.
When Tanzanian researchers compared men's self reports of their
circumcision status with clinical observations, agreement was only 81%.
When they asked the same men on two different occasions whether they were
circumcised; agreement between the men's own first and second reports was
77-90%.2 Several African investigators, in performing genital
examinations, have added to the categories "circumcised" and
"uncircumcised" a third category, such as "partially circumcised" or
"functionally uncircumcised".3
In our area, on the eastern slopes of Mt. Kenya, men uniformly report that
they were circumcised during adolescence. Three very different procedures
are practiced, though, varying by ethnic sub-group and by the person doing
the circumcision. Two of the procedures (one performed by hospital nurses
and the other by traditional circumcisers) produce identical results after
healing, but they employ quite different surgical techniques and remove
different parts of the foreskin. The third procedure, also a traditional
technique, removes the tip of the foreskin and leaves the rest as an
appendage on the ventral side of the penile shaft. Besides questions and
clinical exams, detailed knowledge of local languages and customs is
essential to determine exactly what parts of the foreskin were removed and
which are left attached.
These different circumcision procedures raise new questions about risks of
infection. Does a partial foreskin put the man as much at risk as a
complete foreskin? When part of the foreskin remains, are Langerhans
cells still present? Is the frenulum still susceptible to trauma? What
if the inner surface of the prepuce is scraped, while the outer surface is
left intact? Is it possible that certain styles of circumcision, rather
than offering some protection, actually constitute an added risk of
infection? More answers are needed before we can recommend male
circumcision as a risk-reducing intervention.
Judith E Brown
medical anthropologist
Chogoria Hospital, PO Box 35, Chogoria, Kenya
Kenneth D Micheni
nursing finalist
Elizabeth MJ Grant
consultant in community health
James M Mwenda
nursing tutor
Francis M Muthiri
nursing tutor
Angus R Grant
general practitioner
1. Szabo R, Short RV. How does male circumcision protect against HIV
infection? Brit Med J 2000;320:1592-4.
2. Urassa M, Todd J, Boerma JT, Hayes R, Isingo R. Male circumcision
and susceptibility to HIV infection among men in Tanzania. AIDS
1997;11:73-80.
3. Moses S, Bailey RC, Ronald AR. Male circumcision : assessment of
health benefits and risks. Sex Trans Inf 1998;74:368-73.
Competing interests: No competing interests
Dear Sir
Re Male circumcision and protection against HIV infection
Recently Szabo and Short in an educational article (BMJ 2000;320:592-
94) have suggested that the increased number of Langerhans' cell on the
surface of the foreskin explains why circumcised men are less likely to
become HIV infected. The authors failure to mention an issue that has
long dogged debate on the protective effect of circumcision on incidence
of cervix cancer and now increasingly prostate cancer 1,2, i.e. how much
are improved hygiene and affluence are confounding variables to the
benefits of circumcision. This is exemplified by the lower incidence of
cervix cancer in educated high caste women in India whose husbands were
not circumcised than in the less educated Muslim women with circumcised
husbands 3. Undoubtedly the increased numbers of Langerhans' cells with
HIV receptors in the foreskin may well contribute to an increased
susceptibility to HIV.
Evidence that nutritional status and other STDs
also plays a role in acquisition of HIV Infection prompted us to examine
the role of the foreskin in the occurrence of HIV infection in a series of
new patients 83 (40 of whom i.e. 48% HIV positive) attending a Urethritis
clinic at East and West Drakefontein Gold Mines Carltonville, Gauteng
South Africa as part of a study of the impact of HIV/STD on serum PSA 2 .
The miners, after signing informed consent, received a questionnaire and
were examined in relationship to ascertaining circumcision status
including whether the glans penis was visible and retractability of
foreskin. In addition a limited history of sexual activity was recorded.
As expected the frequency of HIV was significantly lower in those who were
circumcised (Table). Possibly more interesting was that the small
subgroup circumcised after puberty seemed to have some benefit in reducing
the incidence of HIV. Even more interesting in light of Szabo &
Short's hypothesis about the increased numbers of Langerhan's in the
foreskin, was the observation that contrary to what might be expected if
their hypothesis was correct, the HIV frequency was less in men with long
foreskins that were difficult to retract than in those with short easily
retractable short foreskins.
Clearly this observation is based on too small a sample size to be
totally confident in the results. However these observations added to
those on the role of hygiene versus circumcision in reducing cervix cancer
3 from India do suggest that further studies in this issue could well help
to clarify Szabo and Short's hypothesis and need to be done before
implementation of widespread use of circumcision in an attempt to reduce
spread of HIV infection. Furthermore work needs to be done on the
influence of circumcision after puberty as performing such a procedure
after the first STD infection could be a more effective approach than
total population based circumcision.
Yours sincerely
RTD Oliver, JC Oliver, R Ballard.
Table
______________________________________________________
No. of cases HIV sero positive
______________________________________________________
Circumcised:
All 20 29%a
pre puberty 9 22%
post puberty 12 33%
Non-circumcised:
All 62 55%b
Exposed glans/ 31 61%c
easy retraction
Long foreskin/ 31 48%d
difficult retraction
______________________________________________________
a v b chi2 = 4.33 p=.037, c v d chi2 =1.04 p=0.308
References:
1. Ross R, Shimizi H, Paganini-Hill A, Honda G, Henderson B. Case-
control studies of prostate cancer in blacks and whites in southern
California. J Natl Cancer Inst 1987;78(5):869-74.
2. Oliver J, Oliver R, Ballard R. Influence of circumcision and sexual
behaviour on PSA levels in patients attending a sexually transmitted
disease (STD) clinic. Prostate Cancer and Prostate Diseases 2000;In press.
3. Gajalakshmi C, Shanta V. Association between cervical and penile
cancers in Madras, India. Acta Oncologica 1993;32(6):617-620.
Competing interests: Table ______________________________________________________ No. of cases HIV sero positive ______________________________________________________ Circumcised:All 20 29%apre puberty 9 22%post puberty 12 33%Non-circumcised: All 62 55%bExposed glans/ 31 61%ceasy retractionLong foreskin/ 31 48%ddifficult retraction______________________________________________________ a v b chi2 = 4.33 p=.037, c v d chi2 =1.04 p=0.308
Dear Sirs,
I am appalled at the advocating of Male Genital Mutilation
(circumcision) to reduce the risk of contracting HIV or Aids. It is
totally irresponsible to even suggest such a thing.
This suggestion of gaining protection by cutting off a pefectly
healthy and useful pleasure sensor like the foreskin has grave negative
effects.
When this skin is removed it reduces sensitivity by at least 50%, the
glans dry out and through abrasion on clothing will keratenize loosing
even more sensitivity. The older you get the worse the effects. This
makes sex more aggressive and prolonged to the point where the woman will
often become 'dry', the vagina will sustain abrasion and often become
sore. My wife suffered many bouts of 'Thrush' a fungal infection over the
many years of
marriage. When I spent years of stretching what skin was left to the
point of having enough coverage to protect and moisten the glans both
myself and my wife noticed a marked difference to the functionality and
gentle pleasure the foreskin can provide. As a result she has not
suffered with this type of infection in the last five years. What effect
could the aggressive and prolonged sex act of the circumcised man have
when HIV is concerned?
Australian research has shown that condoms are more likely to split
when a circumcised male is involved than an intact male. The circumcised
male will be so de-sensitised that he will be reluctant to use a condom if
it was at all avoidable. The only safe way to prevent HIV is an
impermeable barrier such as a condom and it is irresponsible to say
anything to discourage their
use.
What about the insanitary conditions that this form of mutilation may
be carried out? There are deaths in the developed rich country's of the
world through circumcisions, we know that there are many deaths in Africa
due to this practice.
I fail to understand the obsession that some people have to cut off
sexual bits from defenceless children that cannot chose.
Yours disgusted,
Kevin Elks.
Competing interests: No competing interests
To the Editor - We read with interest the opinion piece by Szabo and
Short.[1]
While a number of studies suggest an association between the foreskin and
HIV infection, a simple tallying of studies is both unscientific and
misleading.[2,3] Systematic review using meta-analysis has demonstrated a
significant degree of between-study heterogeneity, which calls into
question the validity of the summary results. Analysis suggests that men
who engage in high-risk behaviors may be placed at further risk by having
a foreskin, but in the general population circumcision status is not a
significant risk factor.[4,5] Based on the number of factors that
influence sexual behavior and the susceptibility to HIV, it is
irresponsible to focus blame on normal anatomy.
The authors report finding Langerhans cells in the preputial mucosa. This
is nothing new: all mucosal tissues have Langerhans cells. The authors
failed to report the concentration of these cells in comparison to other
mucosal tissues, their concentration in the glans, the foreskin
remnant and circumcision scar in circumcised men, the presence of
associated T-cell infiltration, and how their findings in elderly cadavers
correlate to sexually active 20- to 30-year-old men in Africa. The authors
presumptively state "the inner surface of the foreskin ... and the
frenulum ... must be regarded as the most probable sites for viral entry
of primary HIV infections in men;" however, without quantitative
comparative data their statements are
pure speculation.
To date, the only reports of preputial Langerhans cells have been in
specimens from neonates[6,7] and elderly cadavers. If normal genital
mucosa is at risk, the concentration of
Langerhans cells in these tissues is essential information in determining
which normal genital tissue needs to be removed. We need to know the
concentration in healthy men, men with multiple sexual partners, men with
genital infections, men with HIV, and men of differing races and ages
before any recommendations can be made. Because the infectivity of
Langerhans cells may be linked to inflammatory T-cells,[8] their presence
also needs to be documented.
Finally, citing a pro-circumcision tract, the authors dismiss the
complications of circumcision as having a "low incidence." In contrast,
the rate of immediate complications in the United States is between
3.1%[9] and 9%,[10] and another 5% can later expect to develop meatal
stenosis,[11] a common cause of obstructive renal failure.[12] Although it
has never been directly measured, a higher rate of complications is
believed to follow circumcisions performed
in the developing world, where circumcision has been linked to
tuberculosis,[13] tetanus,[14] penile amputation,[15] and death.[16]
HIV transmission is heavily dependent on certain sexual behaviors, not
anatomy. The authors have not provided any new information to alter this
fact, but have taken the discussion off on a needless tangent. Although
medicalized ritualistic circumcision appears to be an easy answer,
as popularized by some Western researchers, this surgery is unproven and
does not address the core behavioral issues that have fueled this
pandemic. As a result, it will not alter the course of AIDS in Africa.
Robert S. Van Howe, MD
Minocqua, Wisconsin USA
Christopher J. Cold, MD
Marshfield, Wisconsin USA
Michelle R. Storms, MD
Hazelhurst, Wisconsin USA
1. Szabo R, Short RV. How does male circumcision protect against HIV
infection? BMJ 2000; 320:
1592-4.
2. Greenland S. Quantitative methods in the review of epidemiological
literature. Epidemiol Rev 1987; 9: 1-30.
3. Hedge LV, Olkin I. Vote-counting methods in research synthesis.
Psychol Bull 1980; 88: 359-69.
4. Van Howe RS. Circumcision and HIV infection: review of the
literature and meta-analysis. Int J STD AIDS 1999; 10: 8-16.
5. O'Farrell N, Egger M. Circumcision in men and the prevention of
HIV infection: a "meta-analysis" revisited. Int J STD AIDS 2000; 11: 137-
42.
6. Hussain LA, Lehner T. Comparative investigation of Langerhans'
cells and potential receptors for HIV in oral, genitourinary and rectal
epithelia. Immunol 1995; 85: 475-84.
7. Weiss GN, Sanders M, Westbrook KC. The distribution and density of
Langerhans cells in the human prepuce: site of a diminished immune
response? Isr J Med Sci 1993; 29: 42-3.
8. Pope M, Frankel SS, Mascola JR, Trkola A, Isdell F, Birx DL, Burke
DS, Ho DD, Moore JP. Human immunodeficiency virus type 1 strains of
subtypes B and E replicate in cutaneous
dendritic cell-T-cell mixtures without displaying subtype-specific
tropism. J Virol 1997; 71: 8001-7.
9. O'Brien TR, Calle EE, Poole WK. Incidence of neonatal circumcision
in Atlanta, 1985-1986. South Med J 1995; 88: 411-5.
10. Sutherland JM, Glueck HI, Gleser G. Hemorrhagic disease of the
newborn: breast feeding as a necessary factor in the pathogenesis. Am J
Dis Child 1967; 113: 524-33.
11. Van Howe RS. Variability in penile appearance and penile
findings: a prospective study. Br J Urol 1997; 80: 776-82.
12. Eke FU, Eke NN. Renal disorders in children: a Nigerian study.
Pediatr Nephrol 1994; 8: 383-6.
13. Annobil SH, Al-Hilfi A, Kazi T. Primary tuberculosis of the penis
in an infant. Tubercle 1990; 71: 229-30.
14. Bennett J, Schooley M, Traverso H, Agha SB, Boring J. Bundling, a
newly identified risk factor for neonatal tetanus: implications for global
control. Int J Epidemiol 1996; 25: 879-84.
15. Özdemir E. Significantly increased complication risks with mass
circumcisions. Br J Urol 1997; 80: 136-9.
16. Phillips K, Ruttman T, Viljoen J. Flying doctors, saving costs. S
Afr Med J 1996; 86: 1557-8.
Competing interests: No competing interests
I was greatly perplexed by Adrian Viens’ dithering suggestion that
perhaps, in the case of developing countries, circumcision may be a
medically and ethically viable option in helping to reduce HIV
transmission eventho the forced amputation of the male and female prepuce
is seen as unnecessary and unethical in developed countries.
What we know about the hypothetical relationship between HIV
transmission and circumcision status is tenuous and contradictory at best
and the data suspect at worst. Under such circumstances, how could
applying mass, forced, sexually diminishing amputations on only the male
population of a given country possibly be, under any concept of ethics or
sexism accepted by rational people, an ethical and non-sexist
consideration? The logical slight of mind, let alone the moral gymnastics
required of such a suggestion, fit well into the medical/ethical
nightmares witnessed in our recent history. We have only to look at the
Tuskegee experiments and the festivities of the Third Reich for
instruction.
All serious AIDS researchers and indeed, the thrust of the recent
conference in Durban, agree that education is the key to solving the AIDS
pandemic, not universal, involuntary amputations. HIV acquisition is the
result of unsafe sexual behaviour. If Mr. Viens or anyone else ever
develops a surgical technique that will amputate poor behaviour choices
from willing volunteers, he may have something of interest.
Sadira Bolt, MD, MPH
Competing interests: No competing interests
Editor - Szabo and Short (1) in their recent article on the role of
male circumcision on HIV transmission raises important substantive
questions with respect to developing nations. Although in developed
nations (such as the
United States and Canada) the incidence of male circumcision as a routine
intervention has recently decreased for various medical and ethical
reasons, its possible use in developing nations to combat HIV transmission
is uncertain.
Current antiviral drugs such as reverse transcriptase inhibitors and
protease inhibitors, along with proposed AIDS vaccines are too expensive
for many developing nations with a high prevalence of HIV infection. In
developing nations where debt repayment or militarization often greatly
exceeds health expenditures, it is tremendously unrealistic to expect that
a cure or treatment for HIV will be successful in these countries. A good
example is the prevalence of tuberculosis in developing nations. Although
a treatment for tuberculosis has been around for approximately 40 years
and its administration is relatively cheap, we continue to see the
increased prevalence of tuberculosis infection around the world. We need
to examine
other alternative modalities of treatment, such as male circumcision, to
reduce HIV transmission in developing nations.
However, is it morally justifiable to have two standards with regard to
the acceptance of male circumcision in developing versus developed
nations? If we think that there are sufficient medical and ethical
reasons to limit the
routine use of circumcision, should not the same standards be held in
developing nations? Pragmatically, I do not know if this is so clear.
In developed nations, we see routine male circumcision as unnecessary
because a slight increased risk of urinary tract infection and penile
cancer does not justify removing the foreskin. However, in developing
nations where prevention strategies such as education and condoms are not
widely used (2), the existence of epidemiological evidence that shows a
lower incidence of HIV infection in circumcised men (3), and minimal
governmental expenditures on health care, male circumcision may be a
medically and ethically viable
option in helping to reduce HIV transmission in these nations.
References:
1. Szabo R, Short RV. How does male circumcision protect against HIV
infection? BMJ 2000;320:1592-4.
2. Quinn TC, Wawer MJ, Sewankambo N, Serwadda D, Li C, Wabwire-Mangen
F, et al. Viral load and heterosexual transmission of human
immunodeficiency virus type 1. N Engl J Med 2000;342:921-9.
3. Halperin DT, Bailey RC. Male circumcision and HIV infection: 10
years and counting. Lancet 1999;354:1813-5.
Adrian Viens
35 Ormskirk Avenue, Suite 514,
Toronto, Ontario, Canada M6S 1A8
Competing interests: No competing interests
Circumcisers: Penis Parasites
Circumcision: Sexual Act of Surgical Sadism
The AIDS & Circumcision Connection
Thousands of circumcised men are dying of AIDS. Perpetrating circumcision
as a preventive for AIDS is a willful act of misrepresentation. It is a
disgrace and discredit to the medical profession.
Cut Before the Victim is of Age to Refuse
Sexual surgery on non-consenting, tethered, protesting infants, under the
leal age of informed consent or refusal is a violation of the patient’s
legal rights. Amputating healthy erogenous sexual tissue is genital
surgical abuse.
Cut Before the Victim Knows the Lubricating, Gliding, and Erogenous
Sexual Benefits
Inform the public about the immunologic, lubricating, gliding, and
erogenous sexual benefits of the foreskin. Once a man and his mate
experience the erogenous pleasure of his God-given foreskin, they will
never consent to a mortal circumciser cutting it off.
http://www.InformedConsent.com/Circumcision.html
Circumcision: A Sexual Act of Surgical Sadism
The most treacherous and pervasive penis parasite is the circumciser. The
circumciser gives pain and takes pleasure. The British Journal of
Psychiatry and Bizarre Behavior can have a field day with the perversion
that is circumcision. History will look with contempt upon the
circumciser. They bring shame upon their children and their children’s
children. Stop the surgical sexual violence of our newborns. Take the
circumcisers hands off.
Eileen Marie Wayne, M.D.
Founder,
InformedConsent.com Foundation, Inc.
http://www.InformedConsent.com"
EileenWayneMD@InformedConsent.com
Competing interests: No competing interests
I received the following missive, anonymously, from someone with a
rather different view of the brouhaha over the recent recommendations made
by Szabo and Short regarding circumcision. Being unsure of whether or not
it was meant as satire, and since I've a haunting feeling its sentiments
may be widely shared among those who circumcise, I thought I'd bring it to
the attention of readers.
(It certainly does seem to suggest that Circumcision is not without
merit as a subject of psycho-sexual study - and that perhaps this aspect
of it ought to be more widely investigated and discussed.)
A Modest Proposal To Szabo and Short
Gentlemen:
Bravo! Bravo! Wonderful! It was with the most fascinated interest
that I read your splendid recommendation that circumcision be initiated,
world-wide, as a prophylactic to the acquisition of AIDS. Indeed, chill-
laden quivers of delight caressed my spine for long minutes after my first
reading!
However, if I may be so bold, may I modestly suggest what I believe
to be a long overdue revision to the tremblingly delightful procedure of
circumcision itself? To wit:
In all cases, instead of limiting removal of tissue to mere excising
of the foreskin, shift the site of ablation to the juncture of the groin
and penis - and sever, with clean, surgical finality, this desease-
seeking, lust laden, terrible wand of iniquity.
I'm sure you'll agree standardization on this slight but eminently
feasible modification will result not only in a fabulous decrease in AIDS,
but also harbors the awesome potential for wiping out almost all STDs
contracted by males across our globe - as well as truly
going that rare extra mile in ameliorating the current catastrophic but
still increasing population crisis.
If you concur, may I further suggest that this newly revised
procedure be applied first to those pioneers who would implement it?
Indeed, what finer example could be set by these future, far-sighted
geniuses (who, like you, will have so unselfishly put the betterment of
mankind before any trivial, personal consideration) than to be its
progenitors, destined for immortality in the annals, not only of our own
civilization, but those of other, supplanting species to come?
Yours in Swiftian admiration,
A True Believer
Competing interests: No competing interests
Safe Circumcisions in Africa ? When ?
From a UN Title : The circumcision surgery has serious risks if
performed in unhygienic settings by poorly trained providers or with
inadequate instruments, as often happens in Africa.
According to ONUSIDA and to WHO "The risks involved in male
circumcision are generally low" (with no reference to corresponding
research reports) while admitting that “Information on traditional
practices is required” and recognizing that "high complication levels have
been observed when the circumcision is undertaken in unhygienic settings
by poorly trained providers or with inadequate instruments".
WHO recognizes that "Health services in many developing countries are
weak and (that) there is a shortage of skilled health professionals".
It recognizes that “the safety of male circumcision depends on the
setting, equipment and expertise of the provider”.
It therefore recommends that “Supervision systems for quality
assurance should be established along with referral systems for the
management of adverse events and complications” and "that the training (in
standardized procedures) and certification” of providers should be
rapidly implemented” in the public and private sectors.
Any observer of the African scene knows that the expression “rapidly”
is only an example of the xylographic headquarters’ style and is of no
practical consequence in the field.
"quotes" :from WHO/UNAIDS News Release/10, of March 28, 2007, and
from Conclusions and Recommendations, WHO/UNAIDS Technical Consultation,
Montreux, 6-8 March 2007 (embargoed: 28 march 2007)
JJ.Guilbert, M.D., Ph.D.(educ), D.Hc. 30 April 2007
Competing interests:
None declared
Competing interests: No competing interests