Pigmented Basal Cell Carcinoma of the Eyelids

Pigmented Basal Cell Carcinoma of the Eyelids

P I G M E N T E D BASAL C E L L CARCINOMA O F T H E E Y E L I D S ALBERT HORNBLASS, M.D., A N D J O H N A. S T E F A N O , M.D. New York, New York ...

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P I G M E N T E D BASAL C E L L CARCINOMA O F T H E E Y E L I D S ALBERT HORNBLASS, M.D.,

A N D J O H N A. S T E F A N O ,

M.D.

New York, New York

In a retrospective study of 100 cases of basal cell carcinoma treated by surgical excision, we found nine pigmented lesions. The clinical diagnosis of pigmented basal cell carcinoma of the eyelid was rarely considered and the lesion was often misdiagnosed as a melanoma. The pigmented basal cell carcinoma was no different from the nonpigmented basal cell carcinoma with respect to the sex and age of the pa­ tients and the locations, durations, and recurrence rates of the lesions.

Pigmented basal cell carcinoma of the eyelids is regarded as a rare condition. 1 " 3 Several recent studies of basal cell carci­ nomas of the eyelids failed to show the pigmented basal cell carcinoma as a dis­ tinct clinical entity.4"9 We reviewed and studied 100 consecu­ tive cases of pigmented basal cell carcino­ ma treated at a major eye hospital. S U B J E C T S AND M E T H O D S

This report is based on a review of 100 consecutive cases of biopsy-proven basal cell carcinomas of the eyelids treated by surgical excision between June 1975 and June 1978. The 100 cases occurred in 96 patients, all of whom were white. Four of the patients had two lesions each (inter­ estingly, one patient had one pigmented lesion and one nonpigmented lesion). Two lesions from the same patient were counted as two different cases for statisti­ cal purposes. Probability values were cal-

culated with the Chi-square test, Stu­ dent's t-test with posted variance, or the Fisher 2 x 2 method. We divided the lesions into two groups—pigmented basal cell carcinomas (nine cases) and nonpigmented basal cell carcinomas (91 cases). We classified any case in which pigment had been men­ tioned in the clinical description as a pigmented basal cell carcinoma and any case in which pigment had not been men­ tioned in the clinical description as a nonpigmented basal cell carcinoma. The clinical data on the pigmented basal cell carcinomas are shown in Table 1. The Figure shows a representative lesion. We analyzed both groups of lesions to determine the age and sex of each patient and the durations, locations, and recur­ rence rates of the lesions. We correlated the clinicopathologic findings for the le­ sions with the clinical descriptions. RESULTS

From the Department of Oculoplastic Surgery, Manhattan Eye, Ear and Throat Hospital, New York, New York (Dr. Hornblass), the Department of Sur­ gery, Division of Ophthalmology, the State Universi­ ty of New York, Downstate Medical Center, Brook­ lyn, New York (Dr. Hornblass), and the Department of Ophthalmology, Mount Sinai Hospital, New York, New York (Dr. Stefano). Reprint requests to Albert Hornblass, M.D., 903 Lexington Ave., New York, NY 10021.

Sex and age—The male-to-female ratio was 1.1:1 for the nonpigmented basal cell carcinomas and 0.8:1.0 for the pigmented basal cell carcinomas. The men ranged in age from 33 to 93 years; their average age was 65.9 years. The women ranged in age from 29 to 88 years; their average age was 63.2 years. Both pigmented and nonpigmented

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TABLE 1 CLINICAL DATA FOR NINE PATIENTS WITH PIGMENTED BASAL CELL CARCINOMA OF THE EYELID

Case, Sex, Age (yrs)

Location of Lesion

1, F, 31

Upper eyelid

6 mos

2, F, 65 3, F, 68 4 , F , 70

Lower eyelid Upper eyelid Lower eyelid

5, F, 80 6, M, 60

Duration of Lesion

Diagnosis Before Biopsy

Clinical Description of Lesion

Unknown Unknown A few years

Pigmented basal cell carcinoma Nevus Senile keratosis Melanoma

Lower eyelid Lower eyelid

Unknown Many years

Pigmented growth Melanoma

7, M, 74

Lower eyelid

A few years

Pigmented neoplasm

8, M, 77 9, M, 82

Upper eyelid Lower eyelid

1 wk Several years

Melanoma Pigmented mass

8-mm, pigmented, ulcerated, necrotic lesion; loss of cilia Pigmented lesion Tan mass 5 X 5-mm raised pigmented lesion Small tan growth Vascularized tumor; loss of cilia and recent enlargement Pigmented lesion with raised border and recent ènlargment Melanoma-like lesion 7 x 7-mm blue-gray mass with recent enlargement

basal cell carcinomas of the eyelids occur most often in those 60 to 69 years old. There was no statistically significant dif­ ference (P>.05) between the sexes in frequency of occurrence in that age group. Patients with nonpigmented basal cell carcinomas ranged in age from 29 to 93 years and had an average age of 64.3 years, whereas those with pigmented basal cell carcinoma ranged in age from 31 to 82 years and had an average age of 67.4 years. However, of the seven cases

Figure (Hornblass and Stefano). Case 1. This 31year-old woman had had an ulcerated pigmented lesion of the left upper eyelid for one year.

of basal cell carcinoma in patients less than 40 years of age, six occurred in women. Overall statistical studies did not show any significant difference (P>.05) between the patients with pigmented and those with nonpigmented lesions with respect to age or sex. Duration—There was no significant difference between the lengths of time that the pigmented and nonpigmented basal cell carcinomas were présent before excision (P>.05). In 60 cases the lesions had been present for one year or longer. Location—In both groups, the site most commonly involved was the lower eyelid (60 cases). In the pigmented group, the second most common site was the upper eyelid (three cases); there were no cases of a pigmented basal cell carcino­ ma at the canthi. The medial canthus was the second most common site for the nonpigmented group (26 cases), followed by the upper eyelid (16 cases), and, last­ ly, the lateral canthus (12 cases). There was no statistically significant difference (P>.05) between the groups in their site predilection. Recurrence—None of the pigmented

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lesions recurred, although 18 (approxi­ mately 20%) of the nonpigmented lesions did. However, because of the small num­ ber of pigmented lesions in the study, this difference in recurrence rate was not significant (P>.05). Clinical description of the pigmented basal cell carcinoma—Aside from pig­ ment, which, of course, occurred in 100% of these lesions, the most common clini­ cal findings were a recent increase in the size of the lesion, the loss of cilia on the lesion, and the presence of a raised edge around the lesion. Accuracy of the clinical diagnosis—In only one case of pigmented basal cell carcinoma had the correct clinical diagno­ sis been made before a biopsy was per­ formed. Conversely, a correct diagnosis had been made before the biopsy was performed in 80% of the nonpigmented basal cell carcinomas. This difference was highly significant (P<.01). The most com­ mon misdiagnosis of pigmented basal cell carcinoma was melanoma. It was also confused with a nevus and senile keratosis. In three cases, a firm clinical diagno­ sis had not been made and the lesion was considered to be either a pigmented growth or pigmented neoplasm (Table 2). DISCUSSION

The pigmented basal cell carcinoma has been recognized as a clinical entity since Galloway 10 described it in 1898. In 1933, Eller and Anderson 11 published the first extensive American article on pig­ mented basal cell carcinoma. Soon after­ ward, Becker12·13 discussed a series of five cases he had observed. We found that pigmented basal cell carcinomas are more common than is generally believed. We found that 9% of the basal cell carcinomas of the eyelids in this series were clinically pigmented. This figure was similar to the 8% rate Becker12·13 found for all sites, but was higher than the 1.1% frequency Bart and

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TABLE 2 ACCURACY OF CLINICAL DIAGNOSES BEFORE BIOPSY

Clinical Diagnoses Before Biopsy Pigmented lesions Melanoma Pigmented growth Pigmented neoplasm Nevus Senile keratosis Pigmented basal cell carcinoma Total Nonpigmented lesions Basal cell carcinoma Cyst Tumor, mass, or lesion Chalazion Total*

No. of Cases 3 2 1 1 1 1 9 44 4 4 2 54

Total does not include recurrent cases or cases in which no diagnosis was made before biopsy.

Schnall 14 found in a series of lesions from all sites. Haye and Dufier, 15 reporting on eyelid lesions only, found a relative frequency of 1% in the general population of Paris; the relative frequency increased to 45% among the Mediterranean ethnic groups. Their observations confirmed previous findings for Latin-American 16 and Japa­ nese 17 individuals. Basal cell carcinomas from individuals with darker skins are more likely to be pigmented than basal cell carcinomas from lighter-skinned in­ dividuals. Interestingly, Bart and Schnall 14 found an association between the color of the iris and the relative frequency of pigmen­ tation. In our series, iris color and ethnic background were not reliably recorded. However, of the patients with pigmented lesions, one had a Hispanic and one an Italian surname. Several histologie studies18"20 have found that the pigment in basal cell carci­ nomas originates outside of the tumor cells in the surrounding normal skin tis­ sue and is picked up by the tumor. We may reasonably assume that the more

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heavily pigmented the surrounding skin tissue is, the more pigment the basal cell carcinoma picks up. Our failure to find any sex predilection for either type of basal cell carcinomas was in accord with the findings of other studies, 8,15 although Aurora and Blodi 5 found a predilection for males. They also found that females develop basal cell car­ cinoma of the eyelid at an earlier age than do males. We could not definitely confirm this observation because the average ages and the age distributions for males and females in our study were not significant­ ly different. However, most patients under the age of 40 years were females. An earlier study by Perlman and Hornblass 8 of a different set of patients from this hospital produced similar findings. We found no significant difference be­ tween the locations of pigmented and nonpigmented lesions; both types oc­ curred primarily on the lower eyelid. No pigmented lesions were found at the canthi. The second most common site of basal cell carcinomas in this study was the medial canthus (26 cases), followed by the upper eyelid (19 cases) and the lateral canthus (12 cases). This distribution pat­ tern has been noted previously. 2,57 This study showed that a clinician con­ fronted with a pigmented basal cell carci­ noma tends to be overwhelmed by the pigmentary nature of the lesion and does not note its other aspects, such as indura­ tion, hair loss, ulcération, raised edges, or umbilication, that might help him to make the correct clinical diagnosis. Haye and Dufier 15 also suggested that deter­ mining whether the pigment is mottled or intense helps to identify the lesion. A mottled appearance suggests a pigment­ ed basal cell carcinoma, whereas intense pigmentation suggests a melanoma. The difficulty of diagnosing pigmented basal cell carcinoma and, in particular, differentiating it from melanoma has been recognized for some time, 21 and also

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discussed more recently. 1,14,22 Overall, it seems that the correct clinical diagnosis is not made for two reasons: (1) the clinician who has been informed that pigmented basal cell carcinoma is a "rare" variation of the most common eyelid neoplasm is unlikely to suspect its presence; and (2) the presence of pigment in the lesion, which suggests melanoma, leads the cli­ nician to ignore other aspects of the tumor that could help him make the correct diagnosis. REFERENCES 1. Charles, N. C : Basal cell carcinoma of the eyelids. Pitfalls in diagnosis and therapy. J. Dermatol. Surg. 1:28, 1975. 2. Duke-Elder, S., and MacFaul, P. A.: The Ocu­ lar Adnexa. Diseases of the Eyelids. In Duke-Elder, S. (ed.): System of Ophthalmology, vol. 13, pt. 1. St. Louis, C. V. Mosby, 1974, pp. 420-442. 3. Reese, A. B.: Tumors of the Eye, 3rd ed. Hagerstown, Harper and Row, 1976, p. 39. 4. Aurora, A. L., and Blodi, F. C : Lesions of the eyelids. A clinico-pathological study. Surv. Ophthalmol. 15:94, 1970. 5. : Reappraisal of basal cell carcinoma of the eyelids. Am. J. Ophthalmol. 70:329, 1970. 6. Fayos, J. V., and Wildermuth, O.: Carcinoma of the skin of the eyelids. Arch. Ophthalmol. 67:298, 1962. 7. Payne, J. W., Duke, J. R., Butner, R., and Eifrig, D. E.: Basal cell carcinoma of the eyelids. A long-term follow-up study. Arch. Ophthalmol. 81:553, 1969. 8. Perlman, G. S., and Hornblass, A.: Basal cell carcinoma of the eyelids. A review of patients treated by surgical excision. Ophthalmic Surg. 7:23, 1976. 9. Petersen, R. A., Aaberg, T. M., and Smith, T. R. : Solid versus cystic basal cell epitheliomas of the eyelids. Correlation of clinical and pathological diagnoses. Arch. Ophthalmol. 79:31, 1968. 10. Galloway, cited in Cipollaro, A. C , Sachs, W., and Brodey, A. : Pigmented basal cell epithelioma. N.Y. State J. Med. 48:1931, 1948. 11. Eller, J. J., and Anderson, N. P.: Basal cell epitheliomas with excessive pigment formation. Arch. Dermatol. Syph. 27:277, 1933. 12. Becker, S. W.: Pigmented epitheliomas. Arch. Dermatol. Syph. 27:981, 1933. 13. : Melanotic neoplasms of the skin. Am. J. Cancer 22:17, 1934. 14. Bart, R. S., and Schnall, S.: Eye color in darkly pigmented basal cell carcinomas and malig­ nant melanomas. Arch. Dermatol. 107:206, 1973. 15. Haye, C , and Dufier, J. L.: Les epitheliomas pigmentes des paupières. Arch. Ophtalmol. 36:54, 1976.

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16. Smith, L., Garrett, H. D., and Hart, M. S.: Pigmented basal cell epithelioma. Arch. Dennatol. 81:133, 1960. 17. Miki, Y. : Pigmented basal cell epithelioma. I. Statistical study. Med. J. Osaka Ihiv. 14:1, 1963. 18. Bleehan, S. S.: Pigmented basal cell epithelio­ ma. Light and electron microscopic studies on tu­ mors and cell cultures. Br. J. Dermatol. 93:361, 1975. 19. Tezuka, T., Ohkuma, M., and Hirose, I.:

Fifty years ago this month in

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Melanosomes of pigmented basal cell epithelioma. Dermatologica 154:14, 1977. 20. Zelickson, A. S.: The pigmented basal cell epithelioma. Arch. Dermatol. 96:524, 1967. 21. Pardo-Castello: Pigmented epithelioma. Arch. Dermatol. Syph. 19:691, 1929. 22. Fellner, M. J., and Katz, J. M.: Pigmented basal cell cancer masquerading as superficial spread­ ing malignant melanoma. Arch. Dermatol. 113:946, 1977.

THE JOURNAL:

In 1874 Hasket Derby, of Boston, reported his observations on myopia, treated by keeping the eyes under the cycloplegic influ­ ence of atropin, which had been advocated in Europe by Profs. Junge and Schiess-Gemuseus. This plan at least fixed attention on ocular conditions and causes for myopia, and tended to dissipate the traditions and superstitions that had hung about the use of glasses, since the time of Roger Bacon's persecution for dealing in magic; because of the things he saw with the lenses he ground. In Philadelphia, Thomson, Harlan, Norris and Risley began to pre­ scribe glasses, and to observe refraction cases with the ophthalmo­ scope. Norris and Risley reported series of cases of myopia which drew attention to the congestion of the optic nerve and choroid, frequently found in the early stages of myopia. Their papers emphasized the local conditions that produce myopia, and inaugu­ rated a departure from the emphasis on hypothetical general conditions, like hereditary and congenital tendencies, that could be argued about, but did not lead to practical results. Jackson, E.: The control of myopia Am. J. Ophthalmol. 14:719, 1931