Original Article
Prevention of Second Primary Tumors with Isotretinoin in Squamous-Cell Carcinoma of the Head and Neck
N Engl J Med 1990; 323:795-801September 20, 1990
- Abstract
- Abstract
Background.
Patients with head-and-neck cancers who are free of disease after local therapy remain at high risk for both recurrent and second primary tumors. Retinoids have proved efficacious in the treatment of premalignant oral lesions and are promising agents for the prevention of epithelial carcinogenesis.
Methods.
We prospectively studied 103 patients who were disease-free after primary treatment for squamous-cell cancers of the larynx, pharynx, or oral cavity. After completion of surgery or radiotherapy (or both), these patients were randomly assigned to receive either isotretinoin (13-cis-retinoic acid) (50 to 100 mg per square meter of body-surface area per day) or placebo, to be taken daily for 12 months.
Results.
There were no significant differences between the two groups in the number of local, regional, or distant recurrences of the primary cancers. However, the isotretinoin group had significantly fewer second primary tumors. After a median follow-up of 32 months, only 2 patients (4 percent) in the isotretinoin group had second primary tumors, as compared with 12 (24 percent) in the placebo group (P = 0.005). Multiple second primary tumors occurred in four patients, all of whom were in the placebo group. Of the 14 second cancers, 13 (93 percent) occurred in the head and neck, esophagus, or lung.
Conclusions.
Daily treatment with high doses of isotretinoin is effective in preventing second primary tumors in patients who have been treated for squamous-cell carcinoma of the head and neck, although it does not prevent recurrences of the original tumor. (N Engl J Med 1990; 323:795–801.)
Media in This Article
Figure 1
Kaplan–Meier Estimate of the Patients Free of a Second Primary Tumor, According to Study Group.Table 1
Characteristics of Patients Who Could Be Evaluated for Primary-Treatment Failure and Survival, According to Study Group.*Article Activity
- Article
Cancers of the lung, esophagus, and head and neck are expected to account for nearly one third of the 500,000 deaths due to cancer that have been predicted to occur in the United States in 1990. Tobacco use, which contributes to most of these cancers, continues. In the United States, 50 million people smoke and 12 million chew tobacco; worldwide, the corresponding figures are 1 billion and 600 million. Survival after treatment for these cancers has improved only marginally in 30 years.1
Surgery and radiotherapy — together, alone, or (recently) augmented by induction chemotherapy — are effective in the control of primary squamous-cell carcinoma of the head and neck.2 3 4 Yet even after successful primary therapy of early-stage or locally advanced tumors, 30 to 50 percent of patients have local or regional recurrence, 20 to 30 percent have distant metastasis, and 10 to 40 percent have a second primary tumor.5 Second primary tumors are the chief cause of treatment failure and death in patients who present with early-stage disease.6
With their classic report on oral cancer in 1953, Slaughter et al.7 opened the door for modern research into chemoprevention of head-and-neck cancer. They realized that the entire epithelial surface at risk is exposed to repeated carcinogenic insults (e.g., from tobacco use), and suggested that such exposure increases the likelihood that multiple, independent premalignant and malignant foci will develop in the exposed epithelium. This concept — field cancerization7 — postulates a basic pathogenic mechanism that links the primary epithelial carcinogenic process to the development of second primary tumors in the head and neck, esophagus, and lung.6 7 8 It suggests that these second primary tumors, unlike those of ovarian cancer and Hodgkin's disease,9 are not treatment related10 and that an agent that effectively reverses premalignant lesions may also suppress the development of multifocal primary tumors.
Accumulating data from epidemiologic investigations and studies in vitro and in animals, as well as preliminary clinical data, strongly support the role of retinoids (the natural derivatives and synthetic analogues of vitamin A) as cytostatic agents in the prevention of epithelial carcinogenesis.11 12 13 14 15 16 17 18 19 20 21 22 23 Retinoids are established modulators of epithelial-cell differentiation in vivo and in vitro. They can suppress carcinogenesis in a variety of epithelial tissues, including the skin, trachea, lungs, and oral mucosa in animals and humans.11 , 14 , 15 , 18 , 19 , 21
The precise mechanism of these anticarcinogenic effects of retinoids is not understood.11 , 12 Recent investigation suggests, however, that retinoids act primarily by regulating gene expression. Nuclear retinoic acid receptors, which belong to the family of receptors for steroid and thyroid hormones and function as ligand-activated trans-acting factors, probably mediate the effects of retinoids on gene transcription.24 It is possible that retinoids, through such a mechanism, are able to modulate the growth of premalignant cells or to suppress the progression of premalignant cells to neoplastic lesions.
Our randomized, placebo-controlled study of the synthetic retinoid isotretinoin (13-cis-retinoic acid) in the treatment of oral premalignant lesions established the effectiveness of this agent in suppressing premalignant lesions of the oral cavity.25 We now report a study of isotretinoin as adjuvant therapy in squamous-cell carcinoma of the head and neck.
Methods
Patients
The patients selected for this study were clinically free of disease after having undergone surgery or radiation therapy (or both) for histologically confirmed primary squamous-cell carcinoma of the oral cavity, oropharynx, hypopharynx, or larynx. Each primary tumor was classified as Stage I, II, III, or IV (but could not exceed N2a) in accordance with the criteria of the American Joint Committee on Cancer.26 The selection of patients began in 1983, and follow-up data on all patients entered into the study were updated in March 1990.
The evaluation of each patient before study entry included a thorough history taking and physical examination with appropriate laboratory assessments. Patients were excluded from the study if they had abnormal renal or hepatic function, had distant metastasis or a Karnofsky performance score of less than 60 percent, had previously received chemotherapy, or had received within the two years preceding the study a diagnosis of any cancer except in situ or T1 squamous-cell carcinoma of the head and neck or skin cancer other than melanoma. Women of reproductive capacity were excluded because of the teratogenicity of isotretinoin. Also excluded were patients taking large doses of vitamin A (>25,000 USP units per day).
The nature and purpose of the study were fully discussed with each patient. The trial was begun at the Boston Veterans Affairs Hospital and completed at M.D. Anderson Cancer Center. The study protocol was approved by each institution's review board for human research, and written informed consent was obtained from all patients.
Study Design
Patients were randomly assigned to receive either isotretinoin (50 to 100 mg per square meter of body-surface area per day) or placebo for 12 months. The first 44 patients received a dose of 100 mg, which was reduced to 50 mg in 13 of these patients because of toxic effects. In response to this high toxicity rate (30 percent), we amended the protocol to include a starting dose of 50 mg per square meter, which was given to the subsequent 59 patients. Patients were stratified according to their previous treatment (surgery, irradiation, or both). Randomization was performed by the pharmacy with the use of a computer-generated code, so that patients were grouped in blocks of 10 within the three previous-treatment strata. Neither the patients nor the physicians were aware of the study treatment assigned. Both the drug and the placebo (which contained butylated hydroxyanisole, edetate disodium, and hydrogenated soybean oil) were provided in identical opaque gelatin capsules (Hoffmann-LaRoche, Nutley, N.J.).
Treatment was begun no later than 10 weeks after surgery or 16 weeks after radiation therapy in patients who had received radiation alone or radiation combined with surgery as primary therapy. Patients were evaluated at monthly intervals during the treatment period and at three-month intervals during follow-up. Compliance was assessed by means of a pill count at each clinic visit and a daily calendar completed by each patient. Routine evaluations included taking a history of tobacco and alcohol use, physical examination, and laboratory studies, including measurement of fasting serum triglycerides and liver-function tests. Patients were followed up by means of chest x-ray films, obtained every six months. Other laboratory tests and radiologic examinations were performed as indicated.
The first end point of this adjuvant study was the occurrence of new disease, as tumor progression (which comprised local recurrences, regional metastases, and distant metastases) or as a second primary tumor. Biopsies were performed in all sites where failure of primary treatment was suspected. By definition, second primary tumors were not limited to the head and neck, esophagus, or lungs. A second primary tumor of the same histologic type as the first had to be separated from it by more than 2 cm of normal epithelium or had to occur at least three years after the diagnosis of the first primary tumor. Any new tumor of different histologic type qualified as a second primary tumor, without the requirement of a separation of more than 2 cm. Any new tumor of the lungs had to be solitary and histologically distinct from the first primary tumor to be considered a second, unless it occurred three or more years later. These rigorous criteria for a second primary tumor represent a modification of the definition given by Warren and Gates.27 They were applied to each new lesion by two practitioners of head-and-neck surgery working independently who were uninvolved with and blinded to the patients' therapy. A second primary tumor that developed six or more months after diagnosis of the first primary tumor was termed "metachronous"; one that developed earlier was termed "synchronous."
The second end point was survival. Both overall (absolute) survival and disease-free survival were determined, measured in each patient from the date of randomization for this study.
Statistical Analysis
The Pearson chi-square test was used for contingency-table analysis.28 Survival curves were estimated according to the method of Kaplan and Meier,29 and differences in the survival estimates between groups of patients were assessed with a log-rank test.30 , 31 All P values are two-tailed.
The effects of selected variables — age at diagnosis, site of primary disease, stage of disease, previous treatment, and current treatment (isotretinoin or placebo) — on survival and three categories of treatment-failure rates were assessed with the Cox proportional-hazards model.32 , 33 The log likelihood in a model incorporating each variable was compared with that in a model without the variable, with the use of standard chi-square tests. The effect of the categorical variables — i.e., tumor site, tumor stage, previous treatment, and current treatment — was modeled with a set of zero-or-one—valued indicators of the particular site, stage, or treatment. Age was modeled as a continuous variable.
Results
Patterns of Treatment Failure
One hundred three patients were registered in the study. Protocol violations occurred in three patients: in the placebo group, the primary diagnosis was not established histologically in one patient and lung metastases were present in another patient at the time of entry; in the isotretinoin group, lung cancer was present in one patient at entry. The characteristics of the 100 patients who could be evaluated in analyses of patterns of treatment failure and survival are shown in Table 1Table 1
Characteristics of Patients Who Could Be Evaluated for Primary-Treatment Failure and Survival, According to Study Group.*. There were no statistically significant differences between the groups, notably with regard to factors generally considered to influence treatment failure and survival: primary-tumor site, tumor stage, type of primary treatment, tumor-cell differentiation, and histories of smoking and alcohol consumption. Although not significant, there were two differences between the groups in key prognostic factors — site and stage. Patients assigned to placebo were more likely than those assigned to isotretinoin to have cancer of the oral cavity, and those assigned to isotretinoin were more likely to have pharyngeal or advanced-stage disease.Patterns of treatment failure are shown in Table 2Table 2
Incidence of Primary-Treatment Failure, According to Study Group. (median follow-up for all patients, 32 months from the date of randomization). Although the groups did not differ significantly in their percentages of patients with disease progression (whether local, regional, or distant), they did differ significantly in the number of second primary tumors (P = 0.005) (Table 2).The characteristics of the 14 patients with second primary cancer are shown in Table 3Table 3
Characteristics of Patients with Second Primary Tumors.. Both patients in the isotretinoin group had only one second primary tumor, whereas four in the placebo group had multiple second tumors. One placebo recipient (Patient 2 in Table 3) had a second primary cancer at three sites and severe dysplasia at two other sites. Thirteen of the 14 patients (93 percent) had second primary disease in the head and neck, esophagus, or lung; in 8 of the 14 (57 percent) the disease occurred at a different site or sites in the head or neck. The remaining patient (a placebo recipient, Patient 10) had acute myelogenous leukemia. The median and mean times for the development of a second primary tumor were 18 and 20 months, respectively (all 14 patients).Toxicity and Compliance
Three patients (one in the isotretinoin group and two in the placebo group) never received therapy and therefore were excluded from the analyses of toxicity. Two of the three patients with protocol violations did receive treatment and were included in these analyses. The toxic effects in the 99 patients included in the analyses were skin dryness, cheilitis, hypertriglyceridemia, and conjunctivitis; the first three of these effects were significantly more frequent in the isotretinoin group (Table 4Table 4
Incidence of Toxic Effects, According to Study Group.). The toxic effects in the isotretinoin group were predominantly mild or moderate; however, severe skin dryness, cheilitis, hypertriglyceridemia, and conjunctivitis, all of which necessitated dose reduction or temporary discontinuation of therapy, occurred in 12, 2, 6, and 8 percent, respectively, of isotretinoin recipients.Sixteen of the 49 patients in the isotretinoin group (33 percent) did not complete the 12-month course of treatment because of drug toxicity (9 patients, or 18 percent) or noncompliance (7 patients, or 14 percent). Three of the 51 patients in the placebo group (6 percent) discontinued therapy because of toxic effects.
Relative Hazards for Four End Points
The Cox proportional-hazards analysis assessed the effect of treatment on survival and three categories of treatment-failure rates: absolute survival until tumor progression, absolute survival until the development of a second primary tumor, and disease-free survival until either tumor progression or the occurrence of a second primary tumor.
The differences in survival rates between the isotretinoin and placebo groups were not significant. The median survival of the patients in the placebo group was 55 months, at which time 70 percent of the patients in the isotretinoin group were still alive. The median survival of the patients in the isotretinoin group has not yet been reached.
As compared with placebo, isotretinoin reduced treatment-failure rates in all three categories, but the effect was significant only in the category of the rate of second primary tumors (P = 0.007). Kaplan–Meier estimates of the proportions of patients free of second primary disease as a function of time are shown in Figure 1Figure 1
Kaplan–Meier Estimate of the Patients Free of a Second Primary Tumor, According to Study Group..The Cox proportional-hazards analysis also permitted determination of the relative hazard of placebo as compared with isotretinoin, or the ratio of the risks per unit of time, for each end point: 1.28 for death, 1.04 for tumor progression, 5.59 for a second primary tumor, and 1.58 for progression or a second primary tumor.
Discussion
This randomized, placebo-controlled study was designed to investigate the activity of isotretinoin administered as adjuvant therapy for squamous-cell carcinoma of the head and neck. Although we monitored both the occurrence of second primary tumors and local, regional, and distant recurrences, we had hypothesized that the retinoid would have the greatest effect on the development of second primary tumors, which proved to be the case. Whereas isotretinoin did not affect the failure rate for any of the three types of recurrence, it significantly reduced the incidence of the development of second primary tumors (P = 0.005 on direct comparison after a median follow-up period of 32 months). These data indicate that isotretinoin is highly effective in preventing second primary tumors in patients clinically free of disease after treatment of primary squamous-cell cancer of the head and neck. The rate of second primary tumors in our placebo group — 24 percent — falls within the range of rates observed in patients with head-and-neck cancer who received no adjuvant therapy — i.e., 10 to 40 percent.5 , 6 , 34 35 36
All patients in this intervention study were followed up prospectively, with close monitoring at regular intervals, thereby giving precise data on the patterns of the development of second primary tumors. In 93 percent of our patients, the second primary tumor or tumors occurred in the head and neck, esophagus, or lung. This finding corresponds with the distributions of sites of second primary tumors reported in other series of patients34 35 36 and is consistent with the concept of tobacco-related field cancerization.6 7 8
According to data collected by the Radiation Therapy Oncology Group34 and the Connecticut Tumor Registry,37 the overall annual rate of the development of second primary tumors in patients with head-and-neck cancer is constant: the risk among surviving patients does not decrease over time.6 , 34 Therefore, the cumulative incidence of treatment failure is highest among patients who present with early-stage disease, because they survive the longest after primary treatment. As diagnostic techniques, measures for supportive care, and treatment of primary lesions continue to improve, it can be expected that second primary tumors will develop in more patients with all types of head-and-neck, esophageal, and lung epithelial cancers. Current local and systemic treatments neither eliminate nor ameliorate the process by which new cancers arise.
Although smoking is indisputably a major risk factor in the development of initial primary cancers of the head and neck and the lung, it is controversial whether stopping smoking once cancer is diagnosed affects the risk of second primary tumors. Most studies38 39 40 41 42 do suggest that the risk is reduced. However, difficulties in collecting accurate data on factors related to smoking and a lack of biochemical confirmation (e.g., measurement of cotinine levels) have impeded reaching a clear quantitative conclusion. Some investigators have gone as far as questioning the association between smoking and the risk of second primary neoplasms.14 , 43 In our study, only 4 (29 percent) of the 14 patients who had a second primary tumor were currently smoking; the other 10 (71 percent) either had never smoked or had stopped. Smoking cessation may have more effect when accomplished early, before malignancy or premalignancy has been established.14 , 44 All these data on smoking underscore the need for an effective chemoprevention strategy against second primary tumors in patients with head-and-neck cancer.
We administered isotretinoin in a high dose. The toxic effects were more severe and more often intolerable in the isotretinoin group than in the placebo group. One third of the patients in the isotretinoin group did not complete the 12-month course of treatment because of toxicity or noncompliance. This comparatively high dropout rate underscores the significance of the lower rate of second primary tumors among these patients, all of whom were included in the analyses of treatment failure.
Our data on toxicity and the necessity for long-term therapy suggest a need for new chemoprevention approaches to controlling squamous-cell carcinoma of the head and neck. In the light of recent promising findings regarding the treatment of premalignancy in the oral cavity by low doses of isotretinoin,45 we are currently designing a new trial to investigate this less toxic approach to preventing second primary tumors in patients presenting with head-and-neck cancer in an early stage. Other candidate agents are vitamin A and the fairly nontoxic vitamin E and beta carotene.46 There have been encouraging results with the use of vitamin E and beta carotene against experimentally induced oral carcinoma47 , 48 and positive preliminary findings in clinical and biomarker studies of the use of vitamin A and beta carotene against oral leukoplakia.49 , 50
Through its relation with tobacco use, carcinoma of the head and neck is linked to several other epithelial cancers, including esophageal and lung carcinomas. These deadly cancers constitute a major and increasing national and world health problem, which tobacco-cessation programs have yet to control. We believe that the significant suppression of second primary tumors that we achieved with isotretinoin provides the basis for designing studies of primary and adjuvant chemoprevention with retinoids and related agents in subjects at high risk for all tobacco-related epithelial cancers.
Supported in part by grants from Hoffmann-LaRoche, and grants (CA-48303 and CA-48369) from the National Cancer Institute. Dr. Hong holds the Charles A. LeMaistre Chair in Thoracic Oncology given by W.A. "Tex" Moncrief, Jr., and Deborah Moncrief. Dr. Lippman is a recipient of the Clinical Oncology Career Development Award from the American Cancer Society.
We are indebted to Drs. Oscar Guillamondegui, Thomas Robbins, Stanley Shapshay, Charles Vaughan, Stuart Strong, and Randal Weber for their contributions; to Suzanne Simpson for editing; to Elaine White for data management; and to Pamela Walker and Cynthia Argo for assistance in the preparation of the manuscript.
Source Information
From the Departments of Medical Oncology (W.K.H., S.M.L., J.S.L., A.M.K., I.W.D.), Head and Neck Surgery (R.M.B., S.P.S., H.G.), Clinical Radiotherapy (L.J.P.), Tumor Biology (R.L.), and Biomathematics (B.W.B.), The University of Texas M.D. Anderson Cancer Center, Houston; the Department of Medical Oncology, Boston Veterans Affairs Hospital and Boston University School of Medicine, Boston (D.D.K.); and the Department of Clinical Development, Hoffmann-LaRoche, Nutley, N.J. (L.M.I.). Address reprint requests to Dr. Hong at the Department of Medical Oncology, Box 80, The University of Texas M.D. Anderson Cancer Center, 1515 Holcombe Blvd., Houston, TX 77030.
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