Superficial x-ray in the treatment of basal and squamous cell carcinomas: A viable option in select patients

ORIGINAL ARTICLE

Superﬁcial x-ray in the treatment of basal and

squamous cell carcinomas: A viable option in

select patients

Armand B. Cognetta, MD,

Brett M. Howard, BA,

Henry P. Heaton, BA,

Earl R. Stoddard, MD,

Hyokyoung Grace Hong, PhD,

and W. Harris Green, MD

Tallahassee, Florida; Brooklyn and New York, New York; and Pocatello, Idah o

Background: Effective nonsurgical modalities are limited in the treatment of basal cell carcinoma (BCC)

and squamous cell carcinoma (SCC).

Objective: We sought to evaluate the efﬁcacy and viability of superﬁcial x-ray therapy in the treatment of

BCC and SCC in an outpatient setting.

Methods: A retrospective analysis was performed on 1715 histologically conﬁrmed primary cutaneous

BCC and SCC treated with superﬁcial x-ray therapy at Dermatology Associates of Tallahassee in Florida

between 2000 and 2010.

Results: Of the 1715 tumors reviewed during this period, 712 were histologically proven BCC (631 nodular

and 81 superﬁcial), 994 were SCC (861 SCC in situ and 133 invasive SCC), and 9 displayed distinct features

of both BCC and SCC in the same biopsy specimen. Kaplan-Meier estimates (with 95% conﬁdence intervals)

of cumulative recurrence rates of all tumors at 2 and 5 years were 1.9% (1%-2.7%) and 5.0% (3.2%-6.7%),

respectively; of BCC at 2 and 5 years were 2% (0.8%-3.3%) and 4.2% (1.9%-6.4%), respectively; and of all

SCC at 2 and 5 years were 1.8% (0.8%-2.8%) and 5.8% (2.9%-8.7%), respectively. Tumors on male patients

and those with a diameter greater than 2 cm were associated with a statistically signiﬁcant increase in

recurrence likelihood.

Limitations: This study represents only patients treated in 1 dermatology ofﬁce in North Florida and may

not be representative of the general patient population.

Conclusions: Superﬁcial x-ray therapy remains a viable nonsurgical option for the treatment of primary

BCC and SCC in patients where surgical intervention is declined, unadvisable, or potentially associated with

signiﬁcant cosmetic or functional limitations. ( J Am Acad Dermatol 10.1016/j.jaad.2012.06.001.)

Key words: basal cell carcinoma; photon therapy; radiation; radiation therapy; skin cancer; squamous cell

carcinoma; superﬁcial radiation therapy; superﬁcial x-ray therapy; x-ray; x-ray therapy.

uperﬁcial x-ray therapy (SXRT) has been used

by dermatologists for over a century for skin

cancers. It differs from modern electron beam

radiotherapy (EBRT) in that light is the energy source

rather than a charged particle, the machines are

smaller and less expensive as a linear accelerator is

From Dermatology Associates of Tallahassee

; Florida State Uni-

versity College of Medicine

; State University of New York

Downstate Medical Center, Brooklyn

; Idaho Skin Institute

; and

Department of Statistics and Computer Information Systems,

Baruch College, City University of New York.

Funding sources: None.

Disclosure: Dr Cognetta has served as a medical advisor for Topex

(Now Sensus Healthcare), has served as an advisor for Sensus

Health Care, was given a stock option by Sensus Healthcare for

his advisory role during the company’s early stages, and was an

initial investor in the company. Mr Howard, Mr Heaton, and Drs

Stoddard, Hong, and Green have no conflicts of interest to

declare.

Accepted for publication June 5, 2012.

Reprint requests: W. Harris Green, MD, Dermatology Associates of

Tallahassee, 1707 Riggins Rd, Tallahassee, FL 32308. E-mail:

[email protected].

Published online July 18, 2012.

0190-9622/$36.00

Ó 2012 by the American Academy of Dermatology, Inc.

http://dx.doi.org/10.1016/j.jaad.2012.06.001

not required, and the applied physics and dosimetry

are inherently simpler. With SXRT, a bolus is not

needed to deliver 100% of the dose to the skin surface

as is required with EBRT. In addition, the beam and

delivered dose with SXR T are more tightly cuffed

with less lateral edge beam drop-off in the umbra of

the treatment site.

1,2

Although SXRT is more cost-

effective in terms of equip-

ment and patient costs, EBRT

can be used to treat broader

areas of the skin than can

typically be used with SXRT

and has an established role in

adjunctive therapy in tumors

with perineural invasion and

in the treatment of cutaneous

T-cell lymphoma.

3-5

Despite the low recur-

rence rates, favorable cosme-

sis, ease of use, lack of

patient discomfort, and rela-

tively low costs of outpatient

SXRT, the percentage of

dermatology clinics in the

United States administering

SXRT has decreased signiﬁ-

cantly over the years for a

variety of reasons, including

the development and avail ability of Mohs micro-

graphic surgery (MMS).

6,7

Amidst a relative paucity

of large-scale studies on the subject in the literature,

the aim of this study is to evaluate the efficacy and

viability of SXRT in the treatment of basal cell

carcinoma (BCC) and squamous cell carcinoma

(SCC) in an outpatie nt setting.

METHODS

Using records obtained from Dermatology

Associates of Tallahassee in Florida, a retrospective

analysis was performed on 1715 histologically con-

ﬁrmed primary, nonaggressive cutaneous BCC and

SCC treated with SXRT between 2000 and 2010 in this

practice. Pertinent clinical information regarding the

tumor characteristics was recorded including ana-

tomic location, lesion diameter, histologic morphol-

ogy, and evidence of recurrence at follow-up. Initial

and recurrent carcinomas were staged according to

the American Joint Committee on Cancer staging

system for nonmelanoma skin cancer.

Patients

The patients in the study were patients referred to

our practice for MMS. All tumors treated were

reviewed histologically by one of us (A. B. C.) to

address whether the tumor was aggressive or

nonaggressive and to ascertain the tumor depth.

During informed consent process, if appropriate,

patients older than 65 years with nonaggressive

nonmelanoma skin cancers of the face or scalp

were given various treatment options including

radiation therapy. If the tumors were aggressive

and the patient opted for radiation therapy, they

were referred to a local radi-

ation oncologist or to a

nearby teaching hospital

where EBRT was typically

used. The tumors in this

study include only the ones

treated at our practice.

Equipment

Between 2000 and

September 2008, a Universal

T reatmaster Superﬁcial X-Ray

Unit (Universal X-Ray

Products Inc) was used,

which was backed up by a

Picker Superﬁcial X-Ray Unit

(Picker X-Ray Corporation)

The Universal unit was pre-

dominantly used at 80 kV, 5

mA, with a time dose factor

(TSD) of 12.5 cm, half value depth (D1/2) of 6.7 mm

with a 3-cm cone and 6.4 mm with a 5-cm cone. From

2008 until the present, the majority of lesions were

treated with the TOPEX SRT-100 (TOPEX, Inc) (now

Sensus SRT-100 [Sensus Healthcare]) machine while

the Universal machine was kept as a backup. TSD, kV,

milliamperes, cone size, and D ½ values varied with

the newer machines yet the overall dosages, fraction-

ation scheme, and time dose factors were unchanged.

Treatment

The patients’ lesions were treated with 5 sessions

(fractions) of 700 cGy for a total of 3500 cGy.

Occasionally, 7 sessions of 500 cGy were used

when we were treating areas such as the lip, as

mucositis was a concern. Lead eye shielding and

thyroid shielding were regularly performed while

lead intranasal, buccal, and eye shields were used

when appropriate. The radiation ﬁeld of every tumor

was determined by delineation of the clinical border

of the tumor by careful examination. A radiation ﬁeld

was then drawn out 5 to 10 mm (the umbra) beyond

the tumor into clinically uninvolved skin and a lead

shield was custom made to treat both the tumor and

the umbra. All patients were treated with various size

cones, which overlapped the lead cutout shields.

Treatments were performed 3 times a week for a total

of 5 to 7 treatments. The exposure and fractionation

CAPSULE SUMMARY

Superficial x-ray therapy has been

successfully used by dermatologists for

the treatment of skin cancers for almost

a century.

Our 10-year experience and reported

data suggest that superficial x-ray

therapy yields reasonable 2- and 5-year

clearance rates for primary

nonaggressive basal and squamous cell

carcinoma.

Superficial x-ray therapy remains a viable

treatment option for select tumors in

some patients who are poor surgical

candidates or who decline surgery.

JAM ACAD DERMATOL

2 Cognetta et al

schemes were set up in such a manner to maintain a

time dose factor within the optimal range between 90

and 110.

Statistical methods

Because length of follow-up varied, recurrence

rates were calculated using Kaplan-Meier method,

and the statistical differences were assessed using the

log rank test. The x

test was used to determine

possible significant differences between variables.

The Cox proportional hazards model was used for

multivariate analysis. In our data set, 1715 tumors

were discovered in 1149 patients, indicating that

approximately one third of patients had 2 or more

tumors treated with SXRT. Therefore, to account for

possible within-subject correlations, the frailty

model was used. P values less than .05 were consid-

ered statistically significant. Because of the small

number of patients, ‘‘combined’’ type was not in-

cluded in the statistical analyses. Statistical analyses

were performed using an R software package (R

Development Core Team, Vienna, Austria).

Recurrence determination

Any tumor that arose in or contiguous to a

radiation treatment ﬁeld (which extended 5-10 mm

beyond the clinical tumor) was counted as a recur-

rence unless it was a different tumor histologically

(eg, a superﬁcial BCC arising in or contiguous to a

previous SCC in situ treatment site). If there was any

doubt whether the lesion was contiguous or outside

the radiation treatment ﬁeld, it was counted as a

recurrence.

RESULTS

A total of 1715 tumors in 1149 patients were

treated with SXRT from 2000 and 2010 at our prac-

tice. Of the 1715 tumors reviewed during this period,

712 were histologically proven BCC (631 nodular

and 81 superﬁcial), 994 were SCC (861 SCC in situ

and 133 invasive SCC), and 9 displayed distinct

features of both BCC and SCC in same biopsy

specimen. The locations of the tumors are listed in

Table I and the tumor types and recurrences are

listed in Table II. The male-to-female ratio was 2:1.

The mean age at the time of diagnosis was 79 years.

The length of follow-up was calculated from the date

that the radiation therapy was initiated and the

average duration of follow-up was 31.5 months

ranging from 1 to 120 months.

The raw recurrence rate of all tum ors treated was

2.6%. Because of the variation in follow-up lengths

among patients, Kaplan-Meier estimates were used

to estimate the control rates. Kaplan-Meier estimates

(with 95% conﬁdence intervals) of cumulative recur-

rence rates of all tumors at 2 and 5 years were 1.9%

(1%-2.7%) and 5.0% (3.2%-6.7%), respectively; of

BCC at 2 and 5 years were 2% (0.8%-3.3%) and 4.2%

(1.9%-6.4%), respectively; of all SCC (including SCC

in situ) at 2 and 5 years were 1.8% (0.8%-2.8%) and

5.8% (2.9%-8.7%), respectively; of invasive SCC at 2

and 5 years were 1.2% (0%-3.7%) and 6.7% (0%-

14.5%), respectively; and of SCC in situ were 1.9%

(0.7%-3.0%) and 5.5% (2.5%-8.3%) (Fig 1). The

recurrence-free rate of tumors 2 cm or smaller was

significantly lower than tumors larger than 2 cm

(P\.001). Male patients received significantly worse

prognosis than female patients (P = .02). There was

no difference in recurrence-free rate among patients

with different age, tumor types, sites, and T stage.

The clinicopathological variables tested in the uni-

variate analysis are shown in Table III. In multivariate

analyses, male compared with female sex and tumor

size greater than 2 cm compared with less than or

equal to 2 cm were associated with higher recurrence

(likelihood ratio P = .06; Wald P = .02; score (log

rank) P = .02; Cox proportional hazards model)

(Table III). The frailty model gave similar results with

the multivariate survival analysis using the Cox

proportional hazard model. The adjustment on the

within-subject correlation might not be significant

because of the high censoring rates in this data set.

Male compared with female sex and tumor size

greater than 2 cm compared with less than or equal

to 2 cm were associated with higher recurrence

(likelihood ratio P = .06; Wald P = .03; score (log

rank) P = .02; frailty model).

DISCUSSION

Of the 1715 primary lesions treated with SXRT in

our study, 45 were cons idered to be recurrent at

follow-up. The raw recurrence rate for all tumors

treated was 2.6%. Because of the variation in follow-

up lengths among patients, Kaplan-Meier est imates

were used to estimate the control rates for all tumors

at 2- and 5-year intervals and were found to be 98.1%

and 95.0%, respectively. These numbers are conser-

vative for a number of reasons. Any tumor in the

study that arose within or contiguous to the treat-

ment site was counted as a recurrence. The treatment

sites included both the carefully delineated clinical

lesion and an additional 5- to 10-mm umbra or rim of

Abbreviations used:

BCC: basal cell carcinoma

EBRT: electron beam radiotherapy

MMS: Mohs micrographic surgery

SCC: squamous cell carcinoma

SXRT: superﬁcial x-ray therapy

JAM ACAD DERMATOL

Cognetta et al 3

clinically uninvolved skin. Many of these patients

had extreme sun damage and, at baseline, were

exhibiting multiple skin cancers arising synchro-

nously or metasynchron ously in individual areas of

the head and neck. This display of multiple discon-

tiguous tumor growths in such patients has often

been attributed to the ﬁeld effect ﬁrst described by

Slaughter et al

and is often encountered with

superficial, multicentric BCC and SCC in situ tumors

in heavily sun-damaged areas of the skin. In o ur

study, any occurrence in or contiguous to the radi-

ation treatment field could represent a de novo

cancer but was always counted as a recurrence. In

cases where it was not possible to adequately judge

from the clinical presentation and the medical doc-

umentation photographs whether a new cancer was

outside, contiguous to, or within the previous treat-

ment site, it was counted as a recurrence.

Furthermore, the Kaplan-Meier estimates tend to

overestimate recurrence rates in the context of high

follow-up dropout by patients who continued sub-

sequent care under their referring physician, who

experienced no reportable problems with the treat-

ment site, or who died from other health problems in

their advanced age. It is common for patients and the

referring physicians to report back in follow-up

when there is problem within the treatment site

and, in this way, the proportion of patients in follow-

up at 5 years without recurrences to those who have

a suspected recurrence is very low often creating an

overestimation of the proportion of patients with

recurrence in the Kaplan-Meier estimations.

Nevertheless, the success rates in this study remain

favorable and are comparable with the success rates

of SXRT reported in previous smaller studies in the

last few decades.

4,10-19

In 1992, Silverman et al

reported 5-year recur-

rence rates of 862 primary BCC at 7.4%. Similarly, in

1992, according to Goldschmidt et al,

Pannizon

reported estimated recurrence rates of 5.1% in 297

nonsclerosing BCC and 22% in 36 BCC with a

sclerosing component during a follow-up of 7.9

years. In 2003, Zagrodnik et al

reported 5-year

Kaplan-Meier recurrenc e rates of 8.2% for 103

nodular BCC, 26.1% for 25 superficial BCC, and

27.7% for 47 sclerosing BCC treated with SXRT in

154 patients.

In our study, there was no signiﬁcant correlation

between age of the patient, tumor type, or anatomic

location and control rates. Tumors of male patients,

and those of a stage of T2 (having a diameter [2 cm)

were more likely to have a recurrence than tumors on

female patients and those of smaller diameters. It is

unclear as to why male patients had a signiﬁcantly

higher likelihood of recurrence when the treatment

regimens were identical. All of the recurrences had a

stage of T1 or less, had an average recurrent size of

0.89 cm, and were amenable to surgical salvage. The

average time interval until recurrence was 34.7

months. There was no evidence of metastasis in any

of the patients and no tumor-related deaths occurred.

Although cosmesis was not included as a quanti-

ﬁable variable in this study, it is the opinion of the

authors that cosmesis was good to very good in all of

the patients. None of the results were considered

poor. Fig 2 shows an example of a typical result after

radiotherapy. The most common cosmetically unfa-

vorable side effects experienced were hypopigmen-

tation and a relative increase in telangiectasias within

long-standing treatment areas. Cosmesis could have

been improved by using a higher fractionation pro-

tocol. A large majority of tumors were on the alar rim,

where, in the authors’ opinion, the cosmetic result

with superficial radiation in this sebaceous area

surpasses the cosmetic result of MMS with closure

by plastic surgery while offering comparable cure

rates. Another adv antage of radiation therapy is that,

in certain cases, it may produce better functional and

cosmetic results than surgical excision for carcino-

mas that are larger than 1 cm and involve the eyelids;

tip or other areas of the nose; or skin of the upper

lip.

2,11,22,23

A practical limitation of this study is that it does

not provide information regarding the treatment of

Table I. Number of patients in categories by site,

and final diagnosis

Site

Nodular

BCC

Superficial

BCC

Invasive

SCC

SCC in

situ Combined

Cheek 48 13 40 259 1

Nose 522 51 32 210 6

Forehead 30 9 18 135 1

Lips 6 2 3 5 0

Neck 2 0 0 2 0

Chin 10 0 0 0 0

Mastoid 0 0 0 1 0

Scalp 13 6 40 249 1

All sites 631 81 133 861 9

BCC, Basal cell carcinoma; SCC, squamous cell carcinoma.

Table II. Type-specific recurrences after therapy

Type No. of tumors No. of recurrences

Nodular BCC 631 20

Superficial BCC 81 2

Invasive SCC 133 4

SCC in situ 861 19

Combined 9 0

Total 1715 45

BCC, Basal cell carcinoma; SCC, squamous cell carcinoma.

JAM ACAD DERMATOL

4 Cognetta et al

aggressive BCC and SCC with SXRT. There are

several reports in the literature regarding the suc-

cessful treatment of aggressive BCC with SXRT albeit

with signiﬁcantly lower cure rates than those re-

ported with the treatment of nona ggressive

BCC.

13,21,24

All of the tumors treated in this study

were reviewed histologically by the lead author

before treatment selection and determined to be

nonaggressive and amenable to SXRT. Tumors

regarded as aggressive were either treated with

MMS or a referral was made to a nearby teaching

hospital if the patient declined surgery and opted for

radiation therapy. At the outside facilities, EBRT was

typically used by a radiation oncologist.

Although the estimated 5-year recurrence rates of

primary BCC and SCC treated with SXRT in our study

are excellent among nonsurgical treatment modali-

ties, they are not superior to reported recurrence

rates where MMS is used. In a review of over 3

decades of studies, Rowe et al

reported 5-year

recurrence rates of primary BCC treated with MMS to

be 1.0%. In a large 10-year study in Australia,

Leibovitch et al

26,27

reported 5-year recurrence rates

of primary SCC and primary SCC in situ treated with

MMS to be 2.6% and 2.5%, respectively. In terms of

tumor clearance rates, M MS remains superior and a

first line of treatment.

In conclusion, our study and reported experience

suggest that SXRT continues to serve as a reasonable

nonsurgical opt ion for the treatment of primary,

nonaggressive BCC and SCC in patients where sur-

gical intervention is declined, una dvisable because

Fig 1. Kaplan-Meier estimates (with 95% conﬁdence intervals) of basal cell carcinoma (BCC )at

2 and 5 years were 2% (0.8%-3.3%) and 4.2% (1.9%-6.4%), respectively; of all squamous cell

carcinoma (SCC ) (including SCC in situ) at 2 and 5 years were 1.8% (0.8%-2.8%) and 5.8%

(2.9%-8.7%), respectively; of invasive SCC at 2 and 5 years were 1.2% (0%-3.7%) and 6.7% (0%-

14.5%), respectively; and of SCC in situ were 1.9% (0.7%-3.0%) and 5.5% (2.5%-8.3%).

JAM ACAD DERMATOL

Cognetta et al 5

of comorbidities, or potentially associated with sig-

niﬁcant cosmetic or functional limitations. Although

not superior to MMS in terms of tumor recurrence

rates, superﬁcial radiation therapy, when used

properly and responsibly, continues to serve as an

important tool in the dermatologic armamentarium

for the management of skin cancer amidst an in-

creasing elderly and frail patient population.

Table III. Results of univariate and multivariate analysis for recurrence, according to patient and tumor

characteristics

Characteristic

Univariate Multivariate

HR 95% CI P value HR 95% CI P value

Age, y 0.98 0.94-1.01 .32 0.99 0.95-1.02 .43

Sex

Male*

Female 0.41 0.19-0.89 .02* 0.42 0.19-0.92 .03*

Type

BCC*

SCC 1.14 0.62-2.06 .67 1.06 0.33-3.39 .93

Stage

S0 (Tis)*

S1(T1 or T2)

0.90 0.49-1.66 .74 0.90 0.30-2.72 .86

Site

Cheek*

Nose 0.98 0.42-2.29 .98 1.19 0.43-3.25 .74

Forehead, lips, neck, chin, mastoid 0.97 0.28-3.33 .97 0.93 0.27-3.20 .90

Scalp 1.40 0.51-3.88 .51 0.87 0.30-2.49 .79

Size, cm

# 2*

[2 3.94 1.74-8.89 \.001* 4.18 1.66-10.53 .002*

BCC, Basal cell carcinoma; CI, confidence interval; HR, hazard ratio; SCC, squamous cell carcinoma.

*Base groups in Cox analysis are: Male, BCC, S0(Tis), Cheek, Size # 2 cm.

Because of small number of patients, ‘‘combined’’ type was not included in statistical analyses.

Fig 2. Patient with nodular basal cell carcinoma of right ala before (A), 3 years after (B), and 6

years after (C) superficial radiation therapy.

JAM ACAD DERMATOL

6 Cognetta et al

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