Neuroendocrine carcinoma of unknown primary site

INTRODUCTION  Cancer of unknown primary site (CUP) is a common clinical entity, accounting for 2 percent of all cancer diagnoses in the Surveillance, Epidemiology, and End Results (SEER) registries between 1973 and 1987 . Within this category, tumors from many primary sites with varying biologies are represented; this heterogeneity has made the design of therapeutic studies difficult.

Substantial improvements have been made in the management and treatment of some patients with CUP. The identification of specific subgroups of treatable patients has been made possible by the development of specialized immunohistologic techniques that can aid in tumor characterization, and by the recognition of several clinical syndromes that permit prediction of chemotherapy responsiveness.

The typical patient with CUP presents with symptoms referable to a metastatic site. The initial work-up, including physical examination, laboratory and radiographic study, fails to identify the primary site. Light microscopic evaluation of biopsy material places the tumor into one of five histologic categories, which then guides further evaluation:

  • Adenocarcinoma  approximately 70 percent
  • Poorly differentiated carcinoma 15 to 20 percent; an additional 10 percent represent poorly differentiated adenocarcinoma
  • Poorly differentiated neoplasm  less than 5 percent
  • Squamous cell carcinoma  5 percent
  • Neuroendocrine carcinoma  less than 5 percent.

PATHOLOGIC DIAGNOSIS  Neuroendocrine cells are distributed widely throughout the body, and neoplasms of these dispersed cells can occur at many sites. A broad spectrum of such neoplasms with differing biologic behavior is now recognized, in part because of improved pathologic methods. These tumors fall into three broad categories, each of which can present as a neoplasm of unknown primary site.

  • Most well-described adult neuroendocrine tumors have indolent biologic behavior and typical histologic features (eg, carcinoid tumors, islet cell tumors, paragangliomas, pheochromocytomas).
  • A second group of neuroendocrine tumors, typified by small cell lung cancer, has the biology and natural history of a high grade malignancy, and a typical small cell anaplastic appearance by light microscopy.
  • A third group of neuroendocrine tumors has high-grade biology and no distinctive features of neuroendocrine differentiation by light microscopy. In this group, the initial morphologic diagnosis is usually poorly differentiated carcinoma or poorly differentiated adenocarcinoma; neuroendocrine differentiation is only recognized when immunohistochemical staining or electron microscopy (EM) is performed.

Low-grade neuroendocrine carcinoma  Metastatic carcinoid or islet cell (pancreatic endocrine) tumors are occasionally found at metastatic sites without an obvious primary. In this situation, metastases almost always involve the liver, and clinical syndromes from the production of bioactive substances may be apparent. In some patients, the primary sites are subsequently found in the intestine or the pancreas.

Carcinoids or islet cell tumors of unknown primary site usually exhibit an indolent natural history, and management should follow guidelines established for metastatic tumors of these types with known primary sites.  Depending upon the clinical situation, appropriate management may include local therapy (eg, resection of isolated metastasis, hepatic artery chemoembolization), treatment of associated symptoms (eg, with the somatostatin analog octreotide), or systemic chemotherapy with 5-fluorouracil-based regimens.

Small cell carcinoma  Patients with small cell anaplastic carcinoma at a metastatic site usually have a bronchogenic primary. Computerized tomography (CT) of the chest and fiberoptic bronchoscopy should be performed and will often identify the primary site. A large number of extrapulmonary primary sites have also been described (eg, salivary gland, esophagus, bladder, prostate, ovary, cervix), and patients with localizing symptoms should have appropriate diagnostic studies performed.

Most patients in this group have tumors with a high mitotic rate and aggressive biology; the majority have widespread dissemination at the time of diagnosis. Unlike carcinoid-type neuroendocrine tumors, these tumors are chemotherapy-responsive, and all patients should be considered for systemic therapy at the time of diagnosis. Combination regimens effective in the treatment of small cell lung cancer are recommended.

Poorly differentiated neuroendocrine carcinoma  In 10 to 15 percent of poorly differentiated carcinomas that lack morphologic features of neuroendocrine differentiation, immunohistochemical staining is positive for chromogranin and/or synaptophysin, or EM identifies neurosecretory granules. Tumors with these features are referred to as poorly differentiated neuroendocrine tumors or primitive neuroectodermal .

We have reviewed our experience with 51 such patients, 29 of whom were included in the original report . Most patients had clinical evidence of a high-grade tumor, and most had metastases in multiple sites. The dominant tumor sites were:

  • Retroperitoneum 13 patients
  • Peripheral lymph nodes 7 patients
  • Mediastinum  6 patients
  • Liver 6 patients
  • Bone  5 patients
  • Other  8 patients
  • Multiple sites with none dominant  6 patients.

Thirty-three of 43 evaluable patients responded to chemotherapy with either a cisplatin-based combination or other regimen used in the treatment of small cell lung cancer, and 13 had complete responses. Eight patients remained continuously disease-free more than two years after completion of therapy. Five patients with involvement at only one site received local treatment only (surgical excision, 3; radiation therapy, 2), and four have had long-term disease-free survival.

The chemosensitivity of these neoplasms was confirmed in a prospective phase II trial of 48 patients with poorly differentiated neuroendocrine carcinoma. Treatment with paclitaxel/carboplatin/etoposide resulted in an overall response rate of 55 percent, with 13 percent complete responses

The nature of the tumor remained unclear in most of these patients throughout the course of their illness. In four, specific diagnoses were made either antemortem or at autopsy. Two patients who presented with abdominal carcinomatosis were found to have carcinoid tumors with undifferentiated growth pattern; one had small cell lung cancer, and one had an extragonadal germ cell tumor with predominant neuroendocrine differentiation. Similar patients, some with long-term survival following chemotherapy, have been classified by others as extrapulmonary small cell carcinoma of unknown primary site

The origin of these poorly differentiated neuroendocrine tumors remains unclear, but it is likely that the group is heterogeneous.

  • Some patients probably have small cell lung cancer with an occult primary site. However, many of these patients have no smoking history, and the absence of pulmonary involvement makes this diagnosis unlikely in most patients.
  • Some of these tumors probably are undifferentiated variants of well-recognized neuroendocrine tumors (eg, carcinoid tumor), albeit without a recognizable primary site. In the undifferentiated form, the clinical, as well as the pathologic, characteristics no longer resemble the characteristics of their more differentiated counterparts. (See "The carcinoid syndrome"). Metastatic anaplastic carcinoid tumors of gastrointestinal origin have also demonstrated sensitivity to cisplatin-based chemotherapy .
  • It is possible that some of these neoplasms represent a previously unrecognized type of neuroendocrine tumor.

Although the nature of these tumors remains undefined, the diagnosis of poorly differentiated neuroendocrine carcinoma identifies a potentially treatable subgroup. All of these patients should be considered for a trial of combination chemotherapy. Although the optimum regimen is undefined, a platinum/etoposide based regimen as currently used for small cell lung cancer is a reasonable choice. Some patients with a single tumor site may be curable with local treatment modalities alone; however, a course of adjuvant chemotherapy should be considered in these patients, if clinically feasible.