Mall On 2000

Download as pdf or txt
Download as pdf or txt
You are on page 1of 5

STUDY

Circumcision and Genital Dermatoses


Eleanor Mallon, MRCP; David Hawkins, FRCP; Michael Dinneen, FRCS; Nicholas Francis, FRCPath;
Louise Fearfield, MRCP; Roger Newson, DPhil; Christopher Bunker, FRCP

Context: It is well recognized that the presence of a fore- (n = 52), lichen planus (n = 39), seborrheic dermatitis
skin predisposes to penile carcinoma and sexually trans- (n = 29), and Zoon balanitis (n = 27). Less common di-
mitted infections. We have investigated the relationship agnoses included squamous cell carcinoma (n = 4), bow-
between the presence or absence of the foreskin and pe- enoid papulosis (n = 3), and Bowen disease (n = 3). The
nile dermatoses. age-adjusted odds ratio for all penile skin diseases asso-
ciated with presence of the foreskin was 3.24 (95% con-
Objective: To determine whether there is an associa- fidence interval, 2.26-4.64). All patients with Zoon bala-
tion between circumcision and penile dermatoses. nitis, bowenoid papulosis, and nonspecific balanoposthitis
were uncircumcised. Lichen sclerosus was diagnosed in
Design: A retrospective case control study of patients only 1 circumcised patient. Most patients with psoria-
attending the department of dermatology with genital skin sis, lichen planus, and seborrheic eczema (72%, 69%, and
conditions. 72%, respectively) were uncircumcised at presentation.
The majority of men with penile infections (84%) were
Subjects: The study population consisted of 357 male uncircumcised.
patients referred for diagnosis and management of geni-
tal skin disease. The control population consisted of 305 Conclusions: Most cases of inflammatory dermatoses
male patients without genital skin disease attending the were diagnosed in uncircumcised men, suggesting that
general dermatology clinics over a 4-month period. circumcision protects against inflammatory dermato-
ses. The presence of the foreskin may promote inflam-
Main Outcome Measures: The relationship between cir- mation by a köebnerization phenomenon, or the pres-
cumcision and the presence or absence of skin disease in- ence of infectious agents, as yet unidentified, may
volving the penis was investigated. The rate of circumcision induce inflammation. The data suggest that circumcision
inthegeneral male dermatology population was determined. prevents or protects against common infective penile
dermatoses.
Results: The most common diagnoses were psoriasis
(n = 94), penile infections (n = 58), lichen sclerosus Arch Dermatol. 2000;136:350-354

I
T IS WELL RECOGNIZED that the association between circumcision and pe-
presence of a foreskin predis- nile dermatoses, we analyzed the clinical
poses to penile carcinoma1,2 and data derived from 357 patients who pre-
sexually acquired infection (in- sented with penile skin disease.
cluding genital herpes, candidia-
sis, gonorrhea, syphilis, and human pap- RESULTS
illomavirus [HPV] infection),3 but the
From the Departments of dermatology of the penis has attracted A total of 357 patients were studied.
Dermatology (Drs Mallon, scant specific attention compared with that Seven patients had more than 1 diagno-
Fearfield, and Bunker), of the vulva.4 A specific clinic was started sis: 6 had 2 diagnoses and 1 had 3 (for a
Genitourinary Medicine in our institution in 1993 for the assess- total of 365 diagnoses in the 357 men).
(Dr Hawkins), Urology
(Dr Dinneen), Histopathology
ment and research of penile dermatoses. Of 305 men without genital skin disease
(Dr Francis), and Public Health The clinic is attended by a dermatologist attending the general dermatology clin-
(Dr Newson), Imperial College (C.B.), a genitourinary physician, ie, a phy- ics, 146 (47.8%) were circumcised. The
School of Medicine, Chelsea & sician who specializes in sexually trans- mean age of the subjects was 41.9 years
Westminster Hospital, London, mitted diseases (D.H.), and a urologist (age range, 4-93 years): 46.1 years (range,
England. (M.D.). To determine whether there is an 8-97 years) for controls (Table 1), 44.0

ARCH DERMATOL / VOL 136, MAR 2000 WWW.ARCHDERMATOL.COM


350

©2000 American Medical Association. All rights reserved.


Downloaded From: http://archderm.jamanetwork.com/ by a Purdue University User on 05/24/2015
Table 1. Ten-Year Age Groups in Patients and Controls
PATIENTS AND METHODS
Age Group, y No. of Patients No. of Controls Total
0-9 1 2 3
Two hundred ninety-four patients were seen be- 10-19 5 13 18
tween 1994 and 1997 within the setting of the pe- 20-29 59 69 128
nile dermatoses clinic at Chelsea & Westminster Hos- 30-39 117 67 184
pital, London, England; 63 patients were referred from 40-49 85 32 117
2 other hospitals. A full history and complete der- 50-59 46 40 86
60-69 23 26 49
matological assessment were carried out by the same
70-79 14 31 45
clinician (C.B.). The presence or absence of the fore-
80-89 5 23 28
skin was specifically noted. 90-99 2 2 4
In cases in which diagnosis and management re- Total 357 305 662
quired histological confirmation, a 4-mm punch bi-
opsy specimen was obtained (n = 83; 23.2%). The
presence of the prepuce in the general male derma-
tology population (without genital disease) was as-
sessed in 305 men attending general dermatology clin- 2.18-4.36). Note that the odds ratio for all diseases was
ics at Chelsea & Westminster Hospital over a 4-month higher when age group was taken into account (odds
period in 1997.
Mean ages were compared between cases and
ratio, 3.24; 95% confidence interval, 2.26-4.64), so the
controls and between uncircumcised and circum- increased risk of disease in uncircumcised patients was
cised patients using unequal-variance t tests. unlikely to be attributable to confounding by age.
Uncircumcised-circumcised odds ratios were calcu- For the rarer diseases (from lichen simplex down-
lated in 2 ways. Unadjusted odds ratios (with exact ward in Table 2), the confidence intervals are very wide
confidence intervals) were calculated using a com- because the cases are very few. Therefore, although the
mercially available statistical package.5 Age-adjusted odds ratios are high for some of these rare diseases, we
odds ratios were calculated by logistic regression of cannot rule out chance as the cause of the association.
case status with respect to foreskin presence using The most common presenting conditions were pso-
another commercially available statistical package.6 riasis (n = 94); penile infections (n = 58), including HPV
Robust confidence intervals were calculated by
assigning a sampling-probability weight equal to the
(n = 38), herpes simplex virus (n = 8), mollusca (n = 9),
case-control ratio in each control’s 10-year age and candidal balanitis (n = 3); seborrheic dermatitis
group. (n = 29); lichen sclerosus (n = 52); lichen planus (n = 39);
Zoon plasma cell balanitis (n = 27); atopic eczema
(n = 21); lichen simplex (n = 6); irritant contact derma-
titis (n = 9); and vitiligo (n = 9). Less common diag-
noses included allergic contact dermatitis (n = 3), non-
years (age range, 4-93 years) for uncircumcised patients, specific balanoposthitis (n = 3), bowenoid papulosis
and 43.4 years (age range, 14-97 years) for circumcised (n = 3), Bowen disease (n = 3), and idiopathic penile
patients. The mean case-control age difference was edema (n = 5). Of 7 patients with more than 1 diagno-
−4.27 years (95% confidence interval, −7.03 to −1.52), sis, 3 had Zoon balanitis and lichen sclerosus, 2 had li-
whereas the mean uncircumcised-circumcised age dif- chen sclerosus and vitiligo, 1 had lichen sclerosus and
ference was 0.58 years (95% confidence interval, −2.33 lichen planus, and 1 had lichen sclerosus, Zoon balani-
to 3.49). On average, therefore, the patients were signifi- tis and bowenoid papulosis.
cantly younger than the controls (P = .002), whereas All patients with Zoon balanitis, nonspecific bala-
uncircumcised patients were not significantly older than noposthitis, and bowenoid papulosis were uncircum-
circumcised men (P = .70). As it was possible that age cised (odds ratio, `). Most patients with lichen sclero-
might be a confounding factor, age-adjusted odds ratios sus were uncircumcised (98%). Lichen sclerosus was
were calculated. diagnosed in only 1 circumcised patient, a 30-year-old
Unadjusted and age-adjusted odds ratios for all di- Muslim who presented with destructive balanitis
agnoses and each specific disease are presented in xerotica obliterans. It was not possible to determine
Table 2. For rare diseases, such as bowenoid papulosis from the history whether circumcision had preceded
(penile intraepithelial neoplasia), the age-adjusted odds the penile symptoms. Two other patients had persistent
ratios were based on fewer data than were the unad- shaft, glans, or periurethral lichen sclerosus, despite
justed ones, as patients were compared with controls therapeutic circumcision. One of these patients (aged
only in the same 10-year age groups. Infinite (`) or 0 49 years at presentation) had been circumcised at the
odds ratios arise when all patients are uncircumcised age of 8 years for phimosis. The other patient (aged 32
(eg, Zoon balanitis) or circumcised, respectively (eg, id- years at presentation) had progressive disease (balanitis
iopathic penile edema). Confidence intervals are given xerotica obliterans) 1 year after therapeutic circumci-
wherever applicable, but are less exact for adjusted sion. Bowen disease was present in 1 circumcised
odds ratios than for unadjusted odds ratios. The overall patient who was aged 83 years at presentation and had
unadjusted odds ratio for disease associated with pres- been circumcised at the age of 2 years. Squamous cell
ence of the foreskin was 3.08 (95% confidence interval, carcinoma was present in 1 circumcised patient who

ARCH DERMATOL / VOL 136, MAR 2000 WWW.ARCHDERMATOL.COM


351

©2000 American Medical Association. All rights reserved.


Downloaded From: http://archderm.jamanetwork.com/ by a Purdue University User on 05/24/2015
Table 2. Unadjusted and Age-Adjusted Odds Ratios (OR) and 95% Confidence Intervals (CI) for All Diagnoses*

Unadjusted for Age Adjusted for Age


Uncircumcised
Diagnosis No. Patients, No. (%) OR CI OR CI
Controls 305 159/305 (52) 1 (ref) 1 (ref)
All patients 357 275/357 (77) 3.08 2.18-4.36 3.24 2.26-4.64
Psoriasis 94 68/94 (72) 2.40 1.42-4.15 2.61 1.53-4.43
Infections† 58 49/58 (84) 5.00 2.32-11.95 5.73 2.68-12.25
Lichen sclerosus 52 51/52 (98) 46.83 7.77-1898.11 53.55 7.24-395.88
Lichen planus 39 27/39 (69) 2.07 0.97-4.64 2.11 0.99-4.47
Seborrheic dermatitis 29 21/29 (72) 2.41 0.99-6.48 2.50 1.06-5.94
Zoon balanitis 27 27/27 (100) ^ 6.25-^ ^ NA
Atopic eczema 21 10/21 (48) 0.83 0.31-2.24 0.86 0.35-2.11
Lichen simplex 6 3/6 (50) 0.92 0.12-6.97 1.11 0.21-5.86
Irritant dermatitis 9 7/9 (78) 3.21 0.60-32.09 2.83 0.56-14.40
Allergic contact 3 2/3 (67) 1.84 0.09-109.08 2.46 0.22-28.05
Vitiligo 9 6/9 (67) 1.84 0.38-11.53 2.12 0.51-8.75
Bowen disease 3 2/3 (67) 1.84 0.09-109.08 2.08 0.18-23.95
Squamous cell carcinoma 4 3/4 (75) 2.75 0.22-145.59 2.51 0.23-26.92
Bowenoid papulosis 3 3/3 (100) ^ 0.37-^ ^ NA
Balanoposthitis 3 3/3 (100) ^ 0.37-^ ^ NA
Idiopathic penile edema 5 0/5 (0) 0 0.00-1.02 0 NA

*NA indicates that the OR was too high or too low to be measured; ref, reference value.
†Human papillomavirus, herpes simplex virus, molluscum, and candidiasis.

was aged 78 years at presentation and had been circum- mosis and recurrent balanitis,10,11 but the literature is
cised at the age of 3 years. poor in defining causes for these nonspecific indica-
The majority of men with penile infections (84%) tions. In the past, both the British Medical Association12
were uncircumcised. Thirty-eight patients had HPV and the American Academy of Pediatrics13 have dis-
infection, and of these 29 (77%) were uncircumcised. couraged routine circumcision of the newborn. The
Nine patients had mollusca, and of these 8 (88%) were British General Medical Council has issued guidelines
uncircumcised. Eight patients had herpes simplex on standards of practice for physicians who are asked to
virus infection and 3 patients had candidal balanitis, perform circumcision.14
and all 8 patients with these 2 infections were uncir- We have investigated how the presence or absence
cumcised. of the foreskin relates to development of penile derma-
Most patients with psoriasis, lichen planus, and toses. The deep fold that is formed by the junction of
seborrheic eczema (72%, 69%, and 72%, respectively) the foreskin and the penis proximal to the the coronal
were uncircumcised. Atopic eczema and lichen simplex sulcus is subject to maceration from epithelial debris
were equally common in uncircumcised and circum- and glandular secretions, and is a common site of infec-
cised patients. All patients with idiopathic penile edema tion.15 Moreover, the presence of the foreskin alters the
were circumcised. appearance of dermatoses that are easily recognized at
other sites, sometimes rendering diagnosis difficult. For
COMMENT example, a plaque of psoriasis on exposed glans is easily
recognized but loses its characteristic scale when it is
Circumcision is most frequently performed for reli- covered by the prepuce.
gious or tribal reasons, and it is thought that approxi- The spectrum of penile dermatoses seen in our
mately one sixth of the world’s male population is cir- study was similar to that reported from a genitourinary
cumcised.7 There is a large reported variation between medicine clinic.16 In the majority of patients, a postive
the rate of circumcision in the United Kingdom and clinical diagnosis was obtained from formal conven-
that in the United States: in the United Kingdom, the tional dermatological assessment, and a biopsy was not
cumulative rate of circumcision for boys by the age of required. Our experience is that most dermatoses of the
15 years is reported to be almost 7%,8 while in the male genitalia are amenable to clinical diagnosis
United States the rate of circumcision among newborns obtained on the classic grounds of a complete history
is approximately 60%.9 We were surprised by the high and physical examination and that penile biopsies do
rate of circumcision in our control population, al- not need to be performed routinely.17 Many patients
though we could find no data on the prevalence of cir- with inflammatory penile dermatoses have extragenital
cumcision in the adult population of the United King- cutaneous signs, and a complete examination is essen-
dom for comparison. In the Jewish community, tial to achieve a firm clinical diagnosis. Patients with
circumcision is a religious ritual and is usually per- genital skin disease present to general practitioners or
formed on the eighth day of life. Religious circumcision to other specialists, such as those in genitourinary
is also practiced by Muslims between the ages of 4 and medicine and urology, who may have less experience in
13 years.7 Medically, circumcision is performed for phi- the diagnosis of cutaneous disease. In the genitourinary

ARCH DERMATOL / VOL 136, MAR 2000 WWW.ARCHDERMATOL.COM


352

©2000 American Medical Association. All rights reserved.


Downloaded From: http://archderm.jamanetwork.com/ by a Purdue University User on 05/24/2015
medicine clinic setting, clinical diagnosis prior to prevalent in uncircumcised individuals: it is well
biopsy has frequently been found to be inaccurate. In 1 known that sexually transmitted infectious genital dis-
study, the histological findings were consistent with the ease is more common in uncircumcised than circum-
initial clinical diagnosis in only 20 (33%) of the 60 cised patients.3
patients who underwent biopsy.16 When the clinical Some types of HPV (ie, 16, 18, 32, and 34) have
diagnosis is in doubt, a diagnostic biopsy specimen may been implicated in the pathogenesis of bowenoid papu-
be needed to achieve the diagnosis, and obtaining a losis,32 and all 3 of our cases involved uncircumcised
small (4-mm) punch biopsy specimen is a simple, mini- patients (2 were positive for human immunodeficiency
mally invasive procedure. In some clinical situations, a virus, while the third was in good health and negative
histological diagnosis may be necessary for prognostic for human immunodeficiency virus). Various HPV
purposes or to advance therapeutic decision making. types (most commonly type 16) can also be found in
Our study has shown that all patients with Zoon the lesions of penile Bowen disease (intraepithelial
plasma cell balanitis were uncircumcised at presenta- squamous cell neoplasia). 33 Of the 3 patients with
tion, a finding that is consistent with the findings of pre- Bowen disease, 2 were uncircumcised at presentation,
vious, smaller studies.18 The pathogenesis of Zoon bala- as were 3 of the 4 patients with squamous cell carci-
nitis is unclear, but it may represent a form of chronic noma. Penile squamous cell carcinoma is extraordinar-
irritant contact dermatitis.19 The relatively fragile skin of ily rare in circumcised males.34 Circumcision seems to
the glans penis is susceptible to the influence of exoge- protect against squamous cell carcinoma unless the cir-
neous agents, comparable with the vulva, where an in- cumcision was performed for penile disease.2 The rela-
creased incidence of contact dermatitis is reported.20 Cir- tive risk for development of penile cancer in uncircum-
cumcision cures Zoon balanitis.18 cised males compared with those circumcised at birth
Lichen sclerosus is thought to affect the female geni- has been shown to be 3.2; the risk decreases only to 3.0
talia more often than the male.21 It is likely that many for those circumcised after the neonatal period.2
cases in males remain undiagnosed because lichen scle-
rosus is a frequent histological finding in males who have CONCLUSIONS
been circumcised for other reasons22,23 and has been found
in 10% to 95% of boys who were circumcised for phi- Most cases of inflammatory dermatoses were diagnosed
mosis.24-26 Many circumcision specimens are routinely dis- in uncircumcised males, suggesting that absence of the
carded without submission for histological analysis. Most foreskin protects against penile inflammatory dermato-
authors consider lichen sclerosus of the penis synony- ses. Zoon balanitis occurred only in uncircumcised
mous with balanitis xerotica obliterans,27 but balanitis patients, and lichen sclerosus developed almost exclu-
xerotica obliterans may be a consequence of other fi- sively in uncircumcised patients. The presence of the
brosing dermatoses, such as lichen planus and cicatri- foreskin may promote inflammation by a Koebner phe-
cial pemphigoid. The cause of lichen sclerosus remains nomenon, or the presence of infectious agents, as yet
unknown, but infection28 or a response to injury (Koeb- unidentified, may induce inflammation. The data sug-
ner phenomenon)29 has been postulated. There is an as- gest that circumcision prevents or protects against com-
sociation with autoimmune disease, including vitiligo and mon infective penile dermatoses.
alopecia areata,30 and 2 patients in our study presented
with genital lichen sclerosus and vitiligo. Squamous cell Accepted for publication August 18, 1999.
carcinoma may be a complication of lichen sclerosus,31 Corresponding author: Christopher Bunker, FRCP,
but the risk has not been accurately quantified. Our data Department of Dermatology, Chelsea & Westminster
indicate that lichen sclerosus is very rare in circumcised Hospital, 369 Fulham Rd, London SW10 9NH, England.
individuals, although there are reports that it may fol-
low circumcision later in life than the neonatal period REFERENCES
or early childhood.22
The other inflammatory skin diseases (eg, psoria- 1. Wolbarst AL. Circumcision and penile cancer. Lancet. 1932;1:150-153.
sis, seborrheic dermatitis, lichen planus, and allergic 2. Maden C, Sherman KJ, Beckman AM, et al. History of circumcision, medical con-
and irritant contact dermatitis) were all more common ditions and sexual activity and risk of penile cancer. J Natl Cancer Inst. 1993;
in uncircumcised individuals. Psoriasis and lichen pla- 85:19-24.
3. Parker SW, Stewart AJ, Wren MN, Gollow MM, Straton JA. Circumcision and
nus classically manifest the Koebner phenomenon: the
sexually transmissible disease. Med J Aust. 1983;2:288-290.
presence of the foreskin could facilitate minor trauma. 4. Leibowitch M, Staughton R, Neill S, Barton S, Marwood R. An Atlas of Vulval
Balanitis is a common cause for presentation at geni- Disease. London, England: Martin Dunitz; 1995.
tourinary clinics.16 The term balanoposthitis refers to in- 5. Dean AG, Dean JA, Coulombier O, et al. Epi Info, Version 6: A Word-Processing,
flammation of the glans penis and mucosal surface of the Database, and Statistics Program for Public Health on IBM-Compatible Micro-
computers, 1996. Atlanta, Ga: Centers for Disease Control and Prevention; 1996.
prepuce. It is usually caused by irritation from body flu- 6. Stata [computer program]. Release 5.0. College Station, Tex: Stata Corp; 1996.
ids (eg, urine), contact with exogenous substances (eg, 7. Williams N, Kapila L. Complications of circumcision. Br J Surg. 1993;80:1231-
soaps), or infection. The low rate of diagnosis of non- 1236.
specific balanoposthitis in our study may mean that many 8. Rickwood AMK, Walker J. Is phimosis overdiagnosed in boys and are too many
such cases are amenable to more precise dermatological circumcisions performed in consequence? Ann Coll Surg Engl. 1989;71:275-277.
9. Schoen EJ. The status of circumcision of newborns. N Engl J Med. 1990;322:
diagnosis. 1308-1312.
We found that cutaneous infections (eg, Candida, 10. Robarts FH. Penis and prepuce. In: Mason Brown JJ, ed. Surgery of Childhood.
mollusca, herpes simplex virus, and HPV) were more London, England: Edward Arnold; 1962:1159-1181.

ARCH DERMATOL / VOL 136, MAR 2000 WWW.ARCHDERMATOL.COM


353

©2000 American Medical Association. All rights reserved.


Downloaded From: http://archderm.jamanetwork.com/ by a Purdue University User on 05/24/2015
11. Stenram A, Malmfors G, Okmian L. Circumcision for phimosis: a follow-up study. 24. Garat JM, Chechile G, Algaba F, Santalauria J. Balanitis xerotica obliterans in chil-
Scand J Urol Nephrol. 1986;20:84-92. dren. J Urol. 1986;136:436-437.
12. Editorial. The case against neonatal circumcision. BMJ. 1979;1:1163-1164. 25. Meuli M, Briner J, Hanimann B, Sacher P. Lichen sclerosus et atrophicus caus-
13. Thompson HC, King LR, Knox E, Korones SB. Report of the Ad Hoc Task Force ing phimosis in boys: a prospective study with 5 year followup after complete
on Circumcision. Pediatrics. 1975;56:610-611. circumcision. J Urol. 1994;152:987-989.
14. Guidance for Doctors Who Are Asked to Circumcise Male Children. London, En- 26. Rickwood AM, Hemalatha V, Batcup G, Spitz L. Phimosis in boys. Br J Urol. 1980;
gland: General Medical Council; September 1997. 52:147-150.
15. Ive FA. The male genitalia. In: Champion RH, Burton JL, Ebling FJG, eds. Text- 27. Laymon CW, Freeman C. Relationship of balanitis xerotica obliterans to lichen
book of Dermatology. Vol 4. 5th ed. Oxford, England: Blackwell Scientific Pub- sclerosus et atrophicus. Arch Dermatol Syphilol. 1944;49:57-59.
lications; 1992:2803-2824. 28. Staff WG. Urethral involvement in balanitis xerotica obliterans. Br J Urol. 1970;
16. Hillman RJ, Walker MM, Harris JRW, Taylor-Robinson D. Penile dermatoses: a 47:234-239.
clinical and histopathological study. Genitourin Med. 1993;68:166-169. 29. Potter B. Balanitis xerotica obliterans manifesting on stump of amputated penis.
17. Mallon E, Ross JS, Hawkins DA, Dinneen M, Francis N, Bunker CB. Biopsy of Arch Dermatol Syphilol. 1959;79:473-476.
male genital dermatoses. Genitourin Med. 1997;73:421. 30. Meyrick Thomas RH, Ridley CM, Black MM. The association of lichen sclerosus
18. Souteyrand P, Wong E, MacDonald DM. Zoon’s balanitis (balanitis circum- et atrophicus and autoimmune related disease in males. Br J Dermatol. 1983;
scripta plasma cellularis). Br J Dermatol. 1981;105:195-199. 109:661-664.
19. Farrell AM, Francis N, Bunker CB. Zoon’s balanitis: an immunohistochemical study 31. Dore B, Irani J, Aubert J. Carcinoma of the penis in lichen sclerosus et atrophi-
[abstract]. Br J Dermatol. 1996;135(suppl 47):57. cus. Eur J Urol. 1990;18:153-155.
20. Britz MB, Maibach HI. Human cutaneous vulvar reactivity to irritants. Contact 32. Obalek S, Jablonska S, Beaudenon S, Walczak L, Orth G. Bowenoid papulosis of
Dermatitis. 1979;5:375-377. the male and female genitalia: risk of cervical neoplasia. J Am Acad Dermatol.
21. Wallace HJ. Lichen sclerosus et atrophicus. Trans Rep St Johns Hosp Dermatol 1986;14:433-444.
Soc. 1971;57:9-30. 33. Ostrow RS, Faras AJ. The molecular biology of human papillomaviruses and the
22. Ledwig PA, Weigand DA. Late circumcision and lichen sclerosus et atrophicus pathogenesis of genital papillomas and neoplasms. Cancer Metatasis Rev. 1987;
of the penis. J Am Acad Dermatol. 1989;20:211-214. 6:383-395.
23. Schinella RA, Miranda D. Posthitis xerotica obliterans in circumcision speci- 34. Rogus BJ. Squamous cell carcinoma in a young circumcised man. J Urol. 1987;
mens. Urology. 1974;3:348-351. 138:861-862.

ARCH DERMATOL / VOL 136, MAR 2000 WWW.ARCHDERMATOL.COM


354

©2000 American Medical Association. All rights reserved.


Downloaded From: http://archderm.jamanetwork.com/ by a Purdue University User on 05/24/2015

You might also like