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Ann Thorac Surg 1995;59:78-83
© 1995 The Society of Thoracic Surgeons

Carcinoid Tumors of the Lung: Do Atypical Features Require Aggressive Management?

Charles-Henri Marty-Ané, MD, Valérie Costes, MD, Jean-Louis Pujol, MD, Michel Alauzen, MD, Pierre Baldet, MD, Henri Mary, MD

Service de Chirurgie Thoracique et Vasculaire, and Service de Pneumologie, Hôpital Arnaud de Villeneuve, and Service d'Anatomie Pathologique, Hôpital Lapeyronnie, Montpellier, France

Accepted for publication June 28, 1994.


   Abstract
Top
 Footnotes
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 References
 
Atypical carcinoids are an intermediate form of tumor between low-grade malignant typical carcinoid and high-grade malignant small cell carcinoma, which represent the two ends of the spectrum of neuroendocrine bronchopulmonary tumors. Between 1983 and 1993, 27 patients with atypical carcinoids underwent surgical treatment. The histologic diagnosis of an atypical carcinoid was established if the criteria proposed by Arrigoni and associates were fulfilled. Seven pneumonectomies, 16 lobectomies, 2 segmentectomies, and 2 wedge resections were performed. Thirteen patients (48.1%) had regional nodal metastases and 6 patients (22%) had N2 disease at the time of surgical therapy. Distant metastases developed in 5 patients (18.5%) after initial treatment. The 10-year survival in patients with an atypical carcinoid was 49%, versus the 84% 10-year survival rate observed in patients with a typical carcinoid. We conclude that the aggressive behavior of atypical carcinoids precludes the use of limited surgical resection and requires a more aggressive approach, with lobectomy and mediastinal lymph node dissection constituting a minimal procedure. The same criteria used for well-differentiated lung carcinoma should apply to this form of neuroendocrine lung tumor. Adjuvant chemotherapy is recommended for patients with stage III or distant metastases.


   Introduction
Top
 Footnotes
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 References
 
Bronchial carcinoids account for approximately 0.5% to 1% of all bronchial tumors. Initially considered a bronchial adenoma, which is a misnomer, they were distinguished from the less common cylindroid tumors by Hamperl in 1937. It is now widely held that typical carcinoids (TCs) and small cell lung carcinomas (SCLCs) represent the two ends of the spectrum of neuroendocrine bronchopulmonary tumors that arise from Kulchitsky cells. An atypical carcinoid (AC) is an intermediate form of tumor between a low-grade malignant TC (less than 5% lymph node metastasis at presentation) and a high-grade malignant SCLC. Arrigoni, Mills, and Paladugu recognized this entity and accurately described its atypical histologic characteristics. Considering the aggressive behavior of these tumors (50% lymph node metastasis at presentation), there is still much controversy with regard to the ideal forms of treatment in terms of the extent of resection and the value of systemic adjuvant therapy. We present here a retrospective review of our experience, with an emphasis on the clinicopathologic features, prognosis, and surgical management of ACs. Our data are compared with the data for bronchial carcinoids reported in the literature.


   Material and Methods
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 References
 
Between 1983 and 1993, 79 patients with bronchial carcinoids were operated on, and 27 of these had atypical carcinoids. Histologic diagnosis was established on the basis of the finding, yielded by hematoxylin-eosin-stained slides of paraffin-embedded tissue sections. Diagnosis of an AC was established according to the criteria proposed by Arrigoni and associates [1]: (1) increasing mitotic activity in presence of recognizable carcinoid pattern; (2) pleomorphism, nuclear irregularity, hyperchromatism, and abnormal nuclear-cytoplasmic ratio; (3) Hypercellularity with disorganization of the architecture; and (4) areas of tumor necrosis. Immunochemical staining with monoclonal antibodies to neuron-specific enolase, chromogranin A, and synaptophysin was performed in 49 of the 79 patients. Data on the age, sex, presenting symptoms, radiologic features, surgical procedures, and evolution of the disease in each patient were reviewed in detail. All patients were followed up, and 16 patients with ACs were followed up for more than 5 years. Definitive staging was determined according to the revised International Clinical Staging System [2]. Survival curves were calculated by the Kaplan-Meier method.


   Results
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 References
 
Atypical Carcinoids
There were 21 men and 6 women with ACs. The average age at diagnosis was 55 years (range, 26 to 75 years). No patient had an occupational history of exposure to a known carcinogen. Eight patients were smokers (four to sixty packs per year) and 1 patient was an exsmoker. The presenting symptoms were recurrent bronchopulmonary infections in 4 patients, hemoptysis in 6 patients, cough in 2 patients, and Cushing's syndrome in 2 patients (Table 1Go). Thirteen patients (48%) had no initial symptoms and the diagnosis was based on screening chest roentgenogram findings. All patients except 1 underwent fiberoptic bronchoscopy, which revealed an endobronchial lesion in 13 patients, was normal in 12 patients, and showed an extrinsic compression in 1 patient. Endoscopic biopsy was performed in 10 patients and the tissue findings permitted an accurate histologic diagnosis in 5. In these 10 patients, there were no instances of troublesome hemorrhage. In 3 patients, biopsy was not performed because of the risk of hemorrhage. Radiologic studies and computed tomographic scans showed a central mass or atelectasis in 10 patients (37%) and a small peripheral mass in 17 patients (63%). Enlarged lymph nodes were detected on the computed tomographic scans in 5 of the 6 patients with mediastinal lymph node involvement (N2 disease) identified at thoracotomy.


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  		Table 1. . Presenting Findings in Patients With Bronchial Carcinoids
 
Data on the surgical procedures are detailed in Table 2Go. In all patients, the procedure included a standard lymph node dissection. There were no operative deaths and no major postoperative complications. The definitive staging results are given in Table 3Go and findings from immunocytochemical staining of the tumor tissue are given in Table 4Go. Seven patients (26%) exhibited metastasis in the lobar or hilar lymph nodes (N1 disease) and 6 patients (22%) exhibited mediastinal lymph node metastasis (N2 disease). Five patients with N2 disease received adjuvant therapy (Table 5Go).


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  		Table 2. . Surgical Procedures
 

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  		Table 3. . Postsurgical Staging Results
 

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  		Table 4. . Results from Immunocytochemical Staininga
 

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  		Table 5. . Clinical Data in Patients With N2 Disease
 
The mean follow-up was 60 months (range, 5 to 134 months). Eighteen patients (67%) are still alive and free of disease. In the 2 patients with Cushing's syndrome, complete removal of the bronchial carcinoid led to clinical and biologic reversal of the endocrine manifestations. There were three deaths unrelated to the disease: one occurred 9 years postoperatively and was due to heart failure, one occurred 6 years postoperatively and was due to cerebral stroke, and the third patient died 4 years postoperatively of pulmonary embolus. Five patients (18.5%) suffered recurrence and 4 of them died: one at 10 months of local recurrence, one at 13 months of local recurrence and adrenal metastasis, one at 30 months of bone metastasis, and one at 84 months of liver metastasis. The 2 patients who suffered local relapse postoperatively had undergone a lobectomy. One patient is still alive 12 months postoperatively despite bone metastasis. The 2 patients (T1 N0, T2 N0) who underwent limited resections did not suffer recurrence. The follow-up findings in patients with N2 disease requiring adjuvant therapy are given in Table 4Go. One patient with an AC, initially staged as T2 N0 M0, presented with local relapse and adrenal metastasis 6 months postoperatively and died 13 months postoperatively despite radiotherapy and chemotherapy. The 10-year survival rate was 49% in our patients with AC.

Typical Carcinoids
There were 25 men and 27 women with TCs. The average age at diagnosis was 45 years (range, 14 to 75 years). The presenting symptoms are summarized in Table 1Go. Bronchoscopy revealed an endobronchial lesion in 42 patients but an accurate histologic diagnosis was possible in only 10 patients. Biopsy was not performed in 15 patients because of the risk of hemorrhage. Radiologic studies demonstrated central lesions in 34 patients and peripheral nodules in 18 patients. The surgical procedures performed and definitive staging results are given in Tables 2 and 3GoGo. Two patients presented with metastasis in the intrapulmonary nodes (N1 disease), but no patients presented with mediastinal node metastasis (N2 disease). There were no deaths related to the disease in this group of patients. The 10-year survival rate in these patients was 84%, which is significantly higher than the 49% 10-year survival rate in the 27 patients with ACs treated during the same period (Wilcoxon test, p < 0.02) (Fig 1Go).



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  		Fig 1. . Survival curves for patients with bronchial carcinoids. The 10-year survival was 49% for those with the atypical form and 84% for those with the typical form (p < 0.02).

 

   Comment
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
References
 
The three controversial aspects of ACs are the tumor nomenclature, the recommended surgical treatment, and the value of adjuvant chemotherapy. The variety of names used to refer this form of neuroendocrine lung tumor reflect the lack of understanding of the nature of ACs. The terminology proposed by Paladugu and Warren and their associates (Table 6Go) stresses the histogenetic continuum of progressively increasing malignancy starting with TC and extending to SCLC.


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  		Table 6. . Classifications of Neuroendocrine Tumors of the Lung
 
Atypical carcinoid shows no clinical specificity. About 50% of our patients had no symptoms, and diagnosis was based on the findings revealed by screening chest roentgenograms. In Mills and associates' [3] series, the tumors were detected incidentally during routine examination in 65% of the patients. Rea and colleagues [4] reported that, in their patients with bronchial carcinoids, the carcinoid syndrome was always associated with the atypical form when liver metastases had occurred. Two of our patients with carcinoid syndrome had TCs and 2 with Cushing's syndrome had ACs, with complete reversal of the symptoms after tumor removal.

Radiologic studies in our patients revealed a predominance of peripheral nodules (63%) and a central mass or atelectasis in 37% of the patients. Choplin and associates [5] noted that a round or ovoid, lobulated peripheral mass is the most common radiologic presenting feature of ACs (80%). Wilkins and co-workers [6] reported that 60% of their patients with peripheral bronchial carcinoids had ACs. Forster and colleagues [7] suggested that tumor size may be a prognostic factor in the differentiation of neuroendocrine lung tumors. They concluded that any tumor measuring more than 2.5 cm on a computed tomographic scan is more likely to be an AC than a TC. On contrast-enhanced computed tomographic scans, bronchial carcinoids enhance uniformly, and this can be differentiated from the lesser enhancement typical of bronchial carcinomas [8]. The positive yield for bronchoscopy was low in patients with ACs, in that tumors were revealed in 50% of our patients and the histologic diagnosis was accurate in 20%. Endoscopy revealed an endobronchial tumor in 81% of the patients with TCs, but biopsies were not performed in 15 of 52 patients (29%) because of the risk of hemorrhage. Attempts at partial or complete endoscopic removal of the tumor can precipitate serious hemorrhage, and this must be avoided. Todd and associates [9] noted that 26% of the biopsies performed in their patients were associated with considerable hemorrhage, but no patients went on to require blood transfusions or thoracotomy.

Atypical carcinoids have no specific identifying gross characteristics except massive necrosis. There have been difficulties in distinguishing between an AC and SCLC in microscopic studies of tissue obtained by bronchoscopic biopsy because of the limited amount of tissue available. Cytologic studies of bronchial brushing specimens and percutaneous transthoracic needle biopsy specimens obtained under computed tomographic control are not useful for establishing diagnosis. However, accurate diagnosis can be achieved through careful examination of the entire tumor by an experienced pathologist because an AC and SCLC can be easily distinguished on large sections. Pathologic confirmation of typical or atypical carcinoid is usually based on the appearance of routine light microscopic sections prepared with standard stains (Figs 2, 3GoGo). Arrigoni [1] and Paladugu [10] and their colleagues have described the histologic features that are currently recommended in the diagnosis of ACs. Any of these pathologic findings are considered sufficient to identify a carcinoid as histologically atypical. The most common features of an AC that differentiate it from a TC are necrosis and increased mitotic activity [10]. Argyrophilic staining techniques and the use of electron microscopy to demonstrate neurosecretory granules are useful for confirming the neuroendocrine nature of tumors, and thus excluding other pulmonary tumors such as non-SCLCs and lymphomas. Studies of immunocytochemical staining have shown that chromogranin and neuron-specific enolase are good markers for tumors with neuroendocrine features, but are not useful for accurately identifying the neuroendocrine tumor subtypes. Ultrastructural studies performed with electron microscopy have shown that neurosecretory granules tend to become smaller and less numerous along the spectrum from TC to SCLC. Image analysis of the nuclear DNA content has revealed a significantly progressive increase in the DNA content from TC to SCLC, suggesting a correlation between the increased DNA content and tumor aggressiveness [10, 11]. Warren and co-workers [12] noted that preoperative serum neuron-specific enolase levels may be useful in distinguishing bronchial carcinoids (TCs) or well-differentiated neuroendocrine carcinomas (ACs), which have normal or slightly elevated neuron-specific enolase levels, from intermediate-sized cell neuroendocrine carcinomas (large cell undifferentiated carcinoma) and SCLC, which show significantly elevated levels of neuron-specific enolase.



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  		Fig 2. . Typical bronchial carcinoid tumor composed of small uniform cells arranged in cords and nests with an acinar pattern. (Hematoxylin and eosin; x250 before 54% reduction.)

 


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  		Fig 3. . Atypical carcinoid tumor. High-power view showing small spindle cells with irregular nuclear features, hyperchromatism, mitosis, and disordered architecture. (Hematoxylin and eosin; x250 before 54% reduction.)

 
There are currently many controversies concerning the ideal forms of treatment and the extent of resection required to accomplish local control of ACs. In our series, 48% of the patients presented with lymph node metastasis and 22% with mediastinal lymph node metastasis (N2 disease). Distant metastasis was detected during follow-up in 18.5% of the patients. In other series, lymphatic involvement was found in 30% to 66% of the patients and distant metastasis in 9% to 19.5% (Table 7Go). De Caro and co-workers [13] noted that half of their patients with ACs were in stage III at the time of diagnosis.


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  		Table 7. . Metastatic Extension of Bronchial Carcinoidsa
 
Because of its metastatic potential, an AC behaves like an authentic malignant tumor, with a postoperative survival rate of 50% to 64% (Table 8Go). In contrast, TCs are characterized by slow growth, a low incidence of lymph node metastasis, very uncommon distant metastasis, and very high survival rates (see Tables 7, 8GoGo). In our series of patients with TCs, major resections were performed in patients with central lesions (in or near a segmental bronchus), in those with obstructing tumors with distal suppuration, and in the event of an incorrect preoperative diagnosis of bronchial carcinoma. We consider that the aggressive behavior of ACs calls for a large resection, and this led us to perform major procedures (lobectomy or pneumonectomy) in 85% of our patients and lesser procedures (segmentectomy or wedge resection) in 15%. Conservative surgical procedures (bronchoplastic procedures, segmentectomy, or wedge resection) are justified in patients with TCs without lymph node metastasis and distal pulmonary suppuration. In those with ACs, we recommend lung-sparing procedures if the preoperative pulmonary assessment indicates that conventional resections are not possible. Okike and associates [14] reported 18 successful bronchoplastic procedures, but all their patients had small peripheral TCs without lymph node metastasis (N0) or distal suppuration. When endoscopic resection (laser) was performed, diagnosis, staging, and excision proved to be incomplete, and this method should therefore be reserved for patients with centrally localized tumors whose respiratory state rules out performance of a thoracotomy [15].


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  		Table 8. . Postoperative Survival Rates in Patients With Bronchial Carcinoidsa
 
Some authors [1, 9, 10, 12, 16] advocate a more conservative approach, as recurrence in patients with ACs more commonly involves distant metastasis than local redux. Paladugu and co-workers [10] recommend a conservative approach consisting of minimal pulmonary resection that includes the entire tumor with free section margins. However, these authors reported performing large resections in 85% of their patients and lesser procedures in 15%, thus probably explaining the low incidence of local recurrence in their series. The malignant behavior of ACs requires an aggressive approach to surgical treatment, with lobectomy and lymph node dissection the minimal procedure [4, 6, 1517–19]. Regardless of the extent of resection, systematic mediastinal lymph node dissection must be routinely performed to ensure accurate staging and adequate tumor management. In 40% of the patients, peroperative decision-making is sometimes thwarted by the inability of pathologists to determine an accurate histologic diagnosis based on the frozen section findings [15]. In such situations, conventional pulmonary resection is required, as is the case for primary lung cancer [4, 15]. It is widely held that it is very difficult to distinguish between an AC and SCLC when the biopsy specimens are small. The good results reported for the surgical treatment of SCLC should be evaluated with regard to the common confusion between AC and SCLC in microscopic examinations [20].

The role of adjuvant chemotherapy is not clear and only limited data are available on its effects on ACs. The long-term survival potential, even in patients with distant metastasis, emphasizes the slow growth of this type of tumor. Systemic treatment is recommended for the management of metastatic disease at the time of presentation or at the time of systemic recurrence. Because of the life-threatening side effects and unproven benefits with regard to prolonged survival, the use of chemotherapy as an adjuvant treatment for an apparently controlled stage I or II AC is still controversial. However, chemotherapy for the control of a stage III AC seems justified. Paladugu and associates [10] reported that their 7 patients with grade II Kulchitsky's cell carcinoma (AC) and distant metastasis, treated with surgical removal and adjuvant chemotherapy, were still alive from 23 to 127 months postoperatively. Grote and co-workers [21] noted a 40% response rate in a series of 8 patients with metastatic disease treated with chemotherapy. The chemotherapy regimen they used was similar to that used in the treatment of small cell carcinoma, but the response rate was not as high as that seen for small cell carcinoma. The use of systemic adjuvant therapy in patients with ACs is still controversial, and should be the subject of cooperative clinical trials.

Atypical carcinoid is a distinct clinicopathologic entity, with surgical resection the only curative therapy. Because of the aggressive behavior and high rate of lymphatic spread typical of this tumor, the same treatment criteria that apply to lung cancer should be applied to this neuroendocrine tumor subtype, which is comparable to well-differentiated carcinoma of the lung.


   Footnotes
Top
 Footnotes
Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 
Address reprint requests to Dr Marty-Ané, Service de Chirurgie Thoracique et Vasculaire, Hôpital Arnaud de Villeneuve, Centre Hospitalier Universitaire, 34295, Montpellier Cedex 5, France.


   References
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 

  1. Arrigoni MG, Woolner LB, Bernatz PE. Atypical carcinoid tumors of the lung. J Thorac Cardiovasc Surg 1972;64:413–21.[Medline]
  2. Mountain CF. A new international system for lung cancer. Chest 1986;89(Suppl):225S-33S.[Free Full Text]
  3. Mills SE, Walker AN, Cooper PH, Kron IL. Atypical carcinoid tumors of the lung. Am J Surg Pathol 1982;6:643–54.[Medline]
  4. Rea F, Binda R, Spreafico G, et al. Bronchial carcinoids: review of 60 patients. Ann Thorac Surg 1989;47:412–4.[Abstract]
  5. Choplin RH, Kawamoto EH, Dyer RB, Geisinger KR, Mills SE, Pope TL. Atypical carcinoid of the lung: radiologic features. AJR 1986;146:665–8.[Abstract/Free Full Text]
  6. Wilkins EW Jr, Grillo HC, Moncure AC, Scannell JG. Changing times in surgical management of bronchopulmonary carcinoid tumor. Ann Thorac Surg 1984;38:339–44.[Abstract]
  7. Forster BB, Muller NL, Miller RR, Nelems B, Evans KG. Neuroendocrine carcinomas of the lung: clinical, radiologic, and pathologic correlation. Radiology 1989;170:441–5.[Abstract/Free Full Text]
  8. Aronchick JM, Wexler JA, Christen B, Miller W, Epstein D, Gefter WB. Computed tomography of bronchial carcinoids. J Comput Assist Tomogr 1986;10:71–4.[Medline]
  9. Todd TR, Cooper JD, Weissberg D, Delarue NC, Pearson FG. Bronchial carcinoid tumors. J Thorac Cardiovasc Surg 1980;79:532–6.[Abstract]
  10. Paladugu RR, Benfield JR, Pak HY, Ross RK, Teplitz RL. Bronchopulmonary Kulchitsky cell carcinomas. Cancer 1985;55:1303–11.[Medline]
  11. Wain JC, Pak SH, Benfield JR. Immunohistochemistry and new trends in the diagnosis of carcinoids. In: Martini N, Vogt-Moykopf I, eds. International trends in general thoracic surgery, vol 5. St. Louis: Mosby, 1989:249-57.
  12. Warren WH, Faber LP, Gould VE. Neuroendocrine neoplasms of the lung. J Thorac Cardiovasc Surg 1989;98:321–32.[Abstract]
  13. De Caro LF, Paladugu RR, Benfield JR, Lovisati L, Pak H, Teplitz RL. Typical and atypical carcinoids within the pulmonary APUD spectrum. J Thorac Cardiovasc Surg 1983;86:528–36.[Abstract]
  14. Okike N, Bernatz PE, Payne SW, Woolner LB, Leonard PF. Bronchoplastic procedures in the treatment of carcinoid tumors of the tracheobronchial tree. J Thorac Cardiovasc Surg 1978;76:281–91.[Abstract]
  15. McCaughan BC, Martini N, Bains MS. Bronchial carcinoids. J Thorac Cardiovasc Surg 1985;89:8–17.[Abstract]
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  17. Attar S, Miller JE, Hankins J, et al. Bronchial adenomas: a review of 51 patients. Ann Thorac Surg 1985;40:126–32.[Abstract]
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M. Garcia-Yuste, J. M. Matilla, T. Alvarez-Gago, J. L. Duque, F. Heras, L. J. Cerezal, and G. Ramos
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M. H. Kulke and R. J. Mayer
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