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Ann Thorac Surg 1995;60:1783-1789
© 1995 The Society of Thoracic Surgeons

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Original Articles: Cardiovascular

De Novo Solid Malignancies After Cardiac Transplantation

Division of Cardiothoracic Surgery, Department of Surgery, Columbia University College of Physicians & Surgeons, New York, New York

Accepted for publication August 11, 1995.

	Abstract

Top Footnotes Abstract Introduction Patients and Methods Results Comment References

 
Background. As long-term survival after cardiac transplantation improves, neoplastic complications are increasingly being discovered. Although lymphoproliferative disorders predominate, the incidence and clinical spectrum of solid tumors in a uniform population of heart transplant recipients remains uncertain.

Methods. We reviewed our experience with 712 patients who underwent cardiac transplantation. Clinical charts were reviewed and telephone interviews were conducted, when possible.

Results. De novo solid malignancies were identified in 3.3% of patients at risk (21 of 633 patients). Twenty patients were male; mean age was 51.5 ± 8.6 years. Most patients reported a significant smoking history. Pulmonary, urologic, and Kaposi's sarcoma were the most common malignancies identified. Mean interval from transplantation to diagnosis was 35 months. Six patients were diagnosed within 6 months of transplantation. One-year and 5-year survival after transplantation were 90% and 49%, respectively. One-year and 3-year survival after cancer diagnosis were 60% and 52%, respectively.

Conclusions. De novo solid malignancy after transplantation occurred with about half the frequency of lymphoproliferative disorders. A striking male predominance was noted. The interval from transplantation to the appearance of cancer is variable, and no clustering was identified. A significant smoking history warrants aggressive search for occult malignancy during pretransplantation evaluation of potential heart recipients.

	Introduction

Top Footnotes Abstract Introduction Patients and Methods Results Comment References

 
Malignancies have long been recognized as a complication of immunosuppressive therapy after solid-organ transplantation [1]. Lymphoproliferative disorders, carcinomas of the skin and lips, and cervical carcinoma comprise the large majority of these tumors [2, 3]. Solid tumors are relatively uncommon but no less responsible for complications and death. We reviewed our 17-year cardiac transplantation experience at Columbia-Presbyterian Medical Center (CPMC) to investigate the incidence and spectrum of noncutaneous solid tumors.

	Patients and Methods

Top Footnotes Abstract Introduction Patients and Methods Results Comment References

 
Between February 1977 and November 1994, 712 patients underwent 730 orthotopic cardiac transplant procedures at CPMC. The population at risk was considered to comprise all patients surviving more than 1 month after transplantation, leading to a total of 633 patients.For editorial comment, see page 1559.

Three major immunosuppressive protocols evolved over the 17-year experience at CPMC. From 1977 to early 1983, double-therapy immunosuppression was employed using steroids and azathioprine. Between 1983 and 1985, the protocol was modified to include cyclosporin A instead of azathioprine in the double-therapy regimen. Since April 1985, triple therapy has been instituted with cyclosporin A, azathioprine, and steroids.

Cyclosporine therapy was adjusted during the first 3 months to a target serum level between 200 and 300 ng/mL (radioimmunoassay), 100 to 200 ng/mL between months 4 and 8, and 100 to 150 ng/mL thereafter. Steroids were initially administered intravenously, then given orally, and ultimately tapered so that all patients received 10 mg daily at 6 months and are off, or on minimal steroid therapy, 1 year after transplantation. Azathioprine was initially administered at 4 mg/kg and then at 2 mg/kg. The dose was adjusted downward if leukopenia, thrombocytopenia, or hepatic dysfunction developed. After discharge from the hospital, patients were routinely followed up in transplant clinic and underwent echocardiography, endomyocardial biopsy, and blood work according to institutional criteria [4].

The incidence and spectrum of posttransplantation lymphoproliferative disorders (PTLDs) at CPMC have been previously described by us [5]. Cutaneous malignancies (squamous cell, basal cell, and melanoma) were not included in this analysis. Noncutaneous solid tumors developed in 21 of the 633 patients at risk; their clinical charts were retrospectively reviewed and served as the basis of this study. When possible, data were gathered by telephone interview. Eighteen of the 21 patients in whom solid tumors developed received standard triple-drug immunosuppression. Of the remaining 3 patients, one underwent retransplantation for accelerated graft atherosclerosis 13 months before the diagnosis of a solid tumor. The immunosuppressive protocol after the first transplantation consisted of perioperative rabbit antithymocyte globulin and double therapy (azathioprine and steroids). After retransplantation, immunosuppression consisted of standard triple-drug therapy. The other 2 patients received double therapy with cyclosporin A and steroids.

	Results

Top Footnotes Abstract Introduction Patients and Methods Results Comment References

 
Patient Characteristics
Twenty-two cardiac transplant procedures were performed in 21 patients in whom nonskin solid tumors later developed (Table 1). Twenty patients were male. This sex discrepancy is significantly greater than that of the population at risk. Mean age at the time of transplantation was 51.5 ± 8.6 years, with a range of 28 to 67 years. The study population was significantly older than the transplant population at large. The cause of end-stage cardiomyopathy was ischemic in 10 patients, idiopathic in 10 patients, and valvular in 1 patient. A comparison with the transplant population at large is depicted in Table 2. Most patients in the series reported a moderate to heavy smoking history before transplantation. Type A and O blood were the most commonly seen blood types, paralleling the blood type distribution of our transplant population at large.

View larger version (32K): [in this window] [in a new window]   Fig 1. . Distribution and frequency of de novo solid malignancies developing in 21 heart transplant recipients.

Eleven patients were diagnosed with malignancies at an early stage, whereas the remaining 10 patients presented with advanced or metastatic disease. With regard to treatment, 17 of the patients received either operation, chemotherapy, or radiation as sole treatment, whereas 4 patients received combination therapy.

Specific Malignancies
LUNG NEOPLASMS.
Lung neoplasms were the most common tumors encountered, with an incidence of 1.1% (7 of 633 patients). Among the 7 patients, 3 were diagnosed to have non-small cell tumors, 2 patients to have small cell tumors, 1 to have a pleural malignancy (mesothelioma), and one to have a carcinoid. The mean age of these patients at the time of diagnosis was 51 years, with a range of 43 to 59 years.

The mean interval from transplantation to diagnosis of a lung malignancy was 35.7 months, with a range of 3 to 130 months. In 3 patients, the tumor was diagnosed within 6 months of transplantation. Six of the 7 patients in whom lung cancer developed had a significant smoking history, averaging 41 pack-years (range, 10 to 75 pack-years). In the seventh patient, who denied prior smoking, a carcinoid tumor developed that has not been etiologically associated with cigarette smoking. A malignant mesothelioma developed in 1 patient with prior exposure to asbestos; none of the remaining patients reported occupational exposures to other known carcinogens.

Either because of underlying histology or extent of disease at the time of diagnosis, only the patient with carcinoid was amenable to curative resection. The remaining 6 patients underwent palliative chemotherapy, radiation, or both (see Table 2). Survival of the 6 patients in whom lung carcinoma (excluding carcinoid) developed was dismal, with 5 patients dying within 1 year of diagnosis. The sixth patient remains alive 14 months after diagnosis of a disseminated small cell carcinoma. Survival after diagnosis ranged from 0.8 to 84.6 months. Mean survival after diagnosis was 16.6 months, but if the patient with the carcinoid tumor is excluded, mean survival falls to 5.3 months. Only the patient with carcinoid has lived for more than 1 year, and all deaths were due to metastatic disease. These figures compare unfavorably with the experience of Mountain [7], who reported a 1-year survival for patients with advanced lung cancers (stages IIIA-IV) ranging from 18% to 52%.

UROLOGIC MALIGNANCIES.
Taken together, urologic malignancies appeared with an incidence of 0.79% in the heart transplant population at risk. Prostate adenocarcinoma was the most common tumor (n = 3), followed by papillary bladder cancer (n = 2). Mean age at the time of transplantation in this group of patients was 53.4 years and ranged from 47 to 62 years.

Tumors were diagnosed as early as 2 weeks and as late as 97 months after transplantation, with a mean interval of 36.5 months. Risk factor analysis revealed that both patients in whom bladder cancers developed reported a moderate to heavy smoking history; exposure to aryl amines was not elicited from either patient. High circulating testosterone levels and high degree of sexual activity have been advanced as possible etiologic factors for prostatic carcinoma [8]; such information was not available from the 3 patients in whom prostate carcinoma developed. Radiation therapy was employed for the 2 patients with localized prostate adenocarcinoma, whereas surgical decompression and radiotherapy were necessary to palliate the patient with advanced disease. Both patients with bladder tumors presented with disease localized to the bladder. One patient underwent resection and intravesicular chemotherapy, and the second patient was treated with intravesicular chemotherapy only. Survival after diagnosis and treatment for these patients averaged 27 months and ranged from 9.8 to 40 months. The only death in this group was due to metastatic disease.

KAPOSI'S SARCOMA.
Kaposi's sarcoma was diagnosed in 4 patients, comprising 0.63% of the transplant population at risk. Mean age of the patients at the time of transplantation was 47 years and ranged from 28 to 58 years. The mean interval from transplantation to diagnosis was 14.3 months with a range of 3 to 20 months. All 4 patients were human immunodeficiency virus (HIV) negative at the time of transplantation.

The association between KS and acquired immunosuppressed states is well established. Three of 4 patients in whom KS developed either became HIV positive or possessed significant risk factors for HIV disease in spite of negative screening tests. One patient HIV converted after receiving a unit of contaminated blood during transplantation before the commercial test for the HIV antibody became widely available. Two years later, KS developed in him. A second patient described a history of multiple anonymous homosexual contacts although he had remained monogamous for the 5 years before transplant evaluation. He tested negative for HIV and was diagnosed with KS 14 months after transplantation. The third patient was a Haitian man who also tested negative for the HIV antibody before transplantation. Visceral KS was diagnosed 3 months after transplantation. In the fourth patient, KS developed despite negative HIV status. None of the patients reported intravenous drug abuse or other risk factors for acquired immunodeficiency syndrome.

In 3 patients, KS first manifested with skin involvement, whereas in the fourth the disease was widespread at presentation. The former 3 patients received chemotherapy. The fourth patient, who presented with disseminated (liver, stomach, hard palate, and skin) disease, received radiotherapy to the liver as palliative therapy for his pain; hepatic involvement contraindicated the use of the standard hepatotoxic chemotherapy.

Survival after diagnosis averaged 23.6 months and ranged from 2 to 42 months. Two of the deaths were thought to be related directly to KS, whereas the third patient died of acute rejection in the setting of disseminated KS.

HEAD AND NECK MALIGNANCIES.
Head and neck tumors (thyroid, salivary gland, tongue) developed in 3 patients (0.47% incidence) at 6, 26, and 58 months after transplantation. Mean age at transplantation was 58.6 years. The 2 patients in whom squamous cell carcinomas developed reported previous heavy alcohol consumption and cigarette use. Two of the 3 presented with localized disease and were successfully treated with local therapy. The third patient (salivary gland tumor) presented with locoregional disease and underwent resection and adjuvant chemotherapy. Mean survival after diagnosis for these patients was 16.4 months, with a range of 12 to 23 months. The 2 patients with localized disease remain alive; the third patient had recurrent disease requiring further surgical resection. Despite this, metastases developed and he succumbed to his disease 23 months after diagnosis.

A fibrohystiosarcoma and an ovarian tumor were diagnosed in advanced stages in 2 patients. Both patients underwent systemic chemotherapy and both died shortly after diagnosis.

Overall Survival
Mean survival after a diagnosis of noncutaneous solid tumor was 19.4 months, with a range of 0.8 to 84.6 months. Survival after transplantation averaged 54 ± 7 months (± standard error of the mean) and ranged from 4.8 to 130.8 months. Figure 2 depicts a comparison of survival after transplantation between the study group and the transplant population at large (includes all transplant recipients living at least 1 month). The 1-year and 5-year actuarial survivals after transplantation for the study group were 90% and 58%, respectively, compared with 84% and 68% for the transplant population at large (p = 0.12). Survival after diagnosis of a solid malignancy is depicted in Figure 3. One-year and 5-year survivals are 62% and 23%, respectively.

View larger version (22K): [in this window] [in a new window]   Fig 2. . Kaplan-Meier estimate for survival after transplantation (all cause mortality) for the study population (squares) and the institutional transplant population (triangles). The dotted line illustrates that the estimate is taken for the duration of follow-up.

View larger version (17K): [in this window] [in a new window]   Fig 3. . Kaplan-Meier estimate for survival after diagnosis of malignancy among 21 heart transplant recipients. The squares represent individual cancer-related deaths, positioned along the horizontal axis at the time of death and actuarially along the vertical axis. The dotted line illustrates that the estimate is taken for the duration of follow up.

	Comment

Top Footnotes Abstract Introduction Patients and Methods Results Comment References

The bulk of the literature on malignancies after organ transplantation is derived from the Cincinnati Transplant Tumor Registry, a worldwide tumor database [1]. Due to the large clinical experience needed, data describing the incidence and clinical spectrum of solid malignancies arising in heart transplant recipients with uniform guidelines for evaluation, immunosuppression, and follow-up are scarce. The information that is available regarding tumors after cardiac transplantation mostly comprises case reports predominantly reporting de novo PTLDs [9–12]. Scattered reports such as those from Couetil and associates [13], Krikorian and colleagues [14], and Lanza and associates [15] document a small number of solid tumors after cardiac transplantation. In view of this limited literature, we have reviewed the experience of one institution to determine the risk, histology, site, and clinical course of solid malignant tumors developing in cardiac allograft recipients.

The incidence of de novo nonskin solid malignancies was 3.3%, about half of that for PTLDs in the same population. The spectrum of malignancies found was broad and includes soft tissue, urologic, pulmonary, gynecologic, and head and neck tumors of diverse histologies. The average length of time from transplantation to the diagnosis of cancer was 35.1 months; if tumors diagnosed shortly after transplantation (within 6 months) are excluded, this figure increases to 47.1 months. This interval is shorter than the 61 months described by Penn [1] for the worldwide tumor database. However, the latter includes all tumors (PTLDs and solid cancers) for recipients of all organs; a breakdown for cardiac recipients is not provided.

Intriguingly, more than 95% of the malignancies occurred in male patients; in fact, if ovarian tumors are excluded, all malignancies were seen in male patients. This striking prevalence is not readily explained. Most patients in whom de novo malignancies developed were blood type A or O; however, this we believe is a reflection of the frequency of these blood types in the transplant population [11, 14] rather than a perceived risk. On the other hand, although the smoking history of all cardiac recipients was not available, an alarming proportion of patients in whom malignancies developed had a moderate to heavy smoking history. One may speculate on the potentiation of the carcinogenic effects of cigarette smoking by immunosuppressive therapy.

In our small series, tumors of the lung were particularly common, accounting for 33% of the solid malignancies. Furthermore, 2 additional patients have been recently diagnosed with lung tumors. One patient is currently refusing further work-up and a second patient is undergoing metastatic evaluation. Both were excluded from the present study. The occurrence of lung cancer after cardiac transplantation has been occasionally reported [16, 17]. In our series, the affected patients appear to share age distribution and risk factors with nontransplant lung cancer cohorts [18]. The clinical course of these patients was one of accelerated and inevitable death. The fact that clinical disease developed in 3 patients within 6 months of transplantation is disquieting. Taken together, these findings suggest a need to consider a more thorough and aggressive search for occult malignancy during transplant evaluation of potential candidates with a smoking history.

The link between immunosuppression and KS has been strengthened by the epidemic frequency of KS in patients with acquired immunodeficiency syndrome and by the reports of Penn [6] and Lanza and associates [15] describing a strikingly increased incidence of this neoplasm among allograft recipients. The incidence of KS among 967 heart transplant recipients from the European Registry [19] was 0.41%, similar to that found in our study. In our series, KS was diagnosed in 4 of 645 cardiac allograft recipients at risk (0.62%), an incidence approximately 80 times higher than that seen in the general population in the pre-acquired immunodeficiency syndrome era [20]. Our findings with regard to KS support previous reports with respect to its high incidence, cutaneous and gastrointestinal preferential distribution, and varied disease progression [2, 21].

Penn [6] introduced the concept of endocrine-related tumors on review of cancers appearing after cyclosporine therapy [6]. His definition encompassed tumors that (1) occur in endocrine organs (ovary, thyroid), (2) develop in organs whose function is hormonally mediated (prostate), or (3) are characterized by the presence of neuroendocrine features (small cell lung tumors). In our small series, 8 of 21 tumors (38%) were endocrine-related. Investigators have described the effects of cyclosporine on the hypothalamic pituitary axis hormones including adrenocorticotropic hormone [22], thyroid-stimulating hormone, and prolactin [23]. Although the high incidence observed (1.24%) may represent a fortuitous finding, it has been speculated that such cyclosporine-induced hormonal changes may be causally related to the induction of neoplasia [6].

The approach to treatment of solid malignancies in this group of patients followed the conventional management of tumors in nonimmunosuppressed patients. Early-stage tumors were treated with surgical excision or radiation, whereas disseminated disease was managed with chemotherapy. Unlike in patients with PTLD, the treatment of the tumors was not accompanied by modification in the immunosuppressive therapy. Some evidence suggests that Kaposi's lesions may regress with a reduction in immunosuppression [2]. Whether patients with other solid malignancies would benefit from a reduction in immunosuppressive therapy, to our knowledge, has not been investigated. Although the use of cytotoxic agents has been described in a small number of solid-organ recipients with tumors [24–26], the theoretical risk of direct cytotoxicity and allograft loss must be considered.

Parallel to the experience with cancer in nontransplant patients, survival after diagnosis was largely dependent on extent of disease at presentation. Of the 11 patients who presented with local disease, 8 (73%) remain alive. Only 1 of the deaths was due to recurrent disease. In contrast, 9 of the 10 patients (90%) with advanced disease at the time of diagnosis died. The tenth patient remains alive 14 months after diagnosis of disseminated small cell lung cancer. Eight of these 9 (89%) died of disseminated disease at a mean interval of 10 months after diagnosis.

In spite of the paucity of literature on the subject and the small series here examined, certain points seem worthy of mention. First, the risk for development of solid noncutaneous tumors in cardiac recipients is appreciable but does not reach the risk of de novo PTLD (6.2% in our experience). The reasons for the striking male predominance and the high incidence of lung neoplasms in our series remain unexplained at this time.

Second, the interval from transplantation to appearance of cancer is variable, and although KS seemed to occur earlier than other tumors, no clustering could be identified. The high incidence of sarcomas (KS and fibrohystiosarcoma) reported elsewhere is substantiated in this study.

Third, early (1-year) survival after transplantation parallels that seen in the transplant population at large. The long-term survival, however, declines as a result of the development of noncutaneous solid malignancies at an average of 35 months after transplantation.

Finally, our data suggest that in the process of pretransplantation evaluation, patients with a history of moderate to heavy cigarette use should undergo a more aggressive search for occult malignancies. Continued clinical experience will provide further understanding of the effects of immunosuppression on the development of neoplasia in the heart transplant recipient.

	Footnotes

Top Footnotes Abstract Introduction Patients and Methods Results Comment References

 
Address reprint requests to Dr Michler, Milstein Hospital, 7th Fl, 177 Ft Washington Ave, New York, NY 10032.

	References

Top Footnotes Abstract Introduction Patients and Methods Results Comment References

 

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This Article Abstract Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Daniel J. Goldstein Mehmet C. Oz Eric A. Rose Robert E. Michler Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Goldstein, D. J. Articles by Michler, R. E. Search for Related Content PubMed PubMed Citation Articles by Goldstein, D. J. Articles by Michler, R. E.