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Carcinoids and high-grade neuroendocrine carcinomas of the ampulla of Vater: a comparative analysis of 139 cases from the surveillance, epidemiology, and end results program--a population based study.

Neuroendocrine tumors of the ampulla of Vater are uncommon and constitute a heterogeneous group of neoplasms both clinically and morphologically. (1) Histologically, they resemble those that arise in the rest of the tubular gastrointestinal tract, (2) the uterus, (3) and the lung. (4) During the last 20 years, the occurrence of 2 morphologic variants of neuroendocrine neoplasms in the ampulla has been recognized: carcinoid tumors, first recognized in 1939, (5) and high-grade neuroendocrine carcinomas, characterized more recently as small cell carcinomas and large cell neuroendocrine carcinomas. (6-13) However, most publications on neuroendocrine tumors of the ampulla are based on case reports or small series14-25 and, therefore, little is known about their demographics and clinical course.

In the current study, we analyzed the demographics and the 5- and 10-year relative survival rates of 139 patients with neuroendocrine tumors of the ampulla, including 82 carcinoids; 15 high-grade neuroendocrine carcinomas; and 42 neuroendocrine carcinomas, not otherwise specified (NOS) collected by the Surveillance, Epidemiology, and End Results (SEER) Program of the National Cancer Institute during a 34-year period (1973-2006).

MATERIALS AND METHODS

Data Source

The SEER Program has collected demographic, morphologic, and extent of disease characteristics for cancer patients since 1973. Patients are followed for life to determine survival and mortality status. For this study, we used SEER registry 17, the largest of the SEER registries, to obtain case listings and 5- and 10-year survival rates for patients with carcinoids and high-grade neuroendocrine carcinomas of the ampulla of Vater. Registry 17, which began in 2000, includes registries 9 and 13 and covers 26% of the US population. Registry 9 was started in 1973 and expanded to registry 13 in 1992.

Tumor size, lymph node status, and number of positive nodes were recorded in SEER from 1988-2006. However, the 3rd edition of the American Joint Committee on Cancer (AJCC) staging system was first incorporated into the SEER Program in 1988; therefore, not all cases retrieved from registry 17 had associated tumor sizes and nodal status reported.

Histopathologic and Site Codes

All cases of neuroendocrine tumors of the ampulla were identified in the SEER Program with the International Classification of Diseases for Oncology, 3rd edition, published by the World Health Organization. We used the site-specific code "241" to identify neoplasms of the ampulla of Vater. We selected carcinoid tumors by specifying carcinoid NOS (8240), somato statinoma (8156), enterochromaffin cell (8241), goblet cell (8243), and composite (8244)-type carcinoids. We selected neuroendocrine carcinomas by specifying neuroendocrine NOS (8246), small cell neuroendocrine carcinoma (8041), and large cell neuroendocrine carcinoma (8013) types.

RESULTS

Frequency and Demographic Distribution

From 1973-2006, a total of 6081 malignant neoplasms of the ampulla of Vater were recorded in SEER. Of these malignant neoplasms, 139 were carcinoids and neuroendocrine carcinomas of the ampulla: 82 carcinoids (1.3%) and 57 high-grade neuroendocrine carcinomas (0.94%). Seventy-six patients were men and 63 women. Of the patients with carcinoid tumors, 42 were men and 40 were women. Of the patients with high-grade neuroendocrine carcinomas, 34 were men and 23 were women. The mean age at diagnosis was 61.6 years for ampullary carcinoid tumors and 67.5 years for high-grade neuroendocrine carcinomas. Demographic breakdown by race showed most ampullary carcinoid tumors were found in whites (80%), while persons of African American and Asian/ Pacific Islander descent, combined, contributed to the other 20% of carcinoid cases. Of the 82 carcinoids, 74 carcinoids NOS, 5 goblet cell types, 2 somatostatinomas, and 1 composite/mixed cell type were recorded. Of the 57 high-grade neuroendocrine carcinomas, 42 neuroendocrine carcinomas NOS, 9 small cell carcinomas, and 6 large cell neuroendocrine carcinomas were recorded. Because the demographics and the 5- and 10-year relative survival rates of patients with small cell carcinomas, large cell neuroendocrine carcinomas, and neuroendocrine carcinomas NOS were essentially the same, we will refer to this group of neoplasms as high-grade neuroendocrine carcinomas throughout the article.

Tumor Size

Because the 3rd edition of the AJCC staging system was not incorporated into the SEER Program until 1988, many of the tumors listed in SEER did not have recorded tumor sizes. Twenty-three of 82 ampullary carcinoid cases had recorded tumors sizes, and 16 of 57 high-grade neuroendocrine carcinomas had recorded tumor sizes. Ampullary carcinoid tumors ranged from 0.2 to 4.0 cm, with a mean size of 1.76 cm.

High-grade neuroendocrine carcinomas ranged from 1.4 to 6 cm, with a mean size of 3.05 cm.

Nodal Status

Of the 82 carcinoid cases, 28 had recorded lymph node status, 8 (28.5%) of which had lymph node metastasis. Of the 57 high-grade neuroendocrine carcinomas, 21 had recorded lymph node status, 13 (62%) of which had lymph node metastasis.

Second Primary Tumors

Twenty-three of 97 cases (24%) of ampullary carcinoid and small and large cell carcinomas were associated with additional primary malignant tumors. Of the 23 cases, the carcinoid or neuroendocrine carcinoma was the primary tumor in 4 cases, and in 17, the carcinoid or neuroendocrine carcinoma was the second or third primary tumor. The additional malignant neoplasms were primarily adenocarcinomas of the colon, stomach, prostate, and breast.

Survival

Survival was higher among patients with carcinoid tumors of the ampulla of Vater than patients with highgrade neuroendocrine carcinomas. Survival rates for patients with carcinoid tumors were 82.2% and 70.9% at 60 and 120 months, respectively. Survival rates associated with high-grade neuroendocrine carcinomas were 15.7% at both 60 and 120 months. Figure 1 displays these data. Furthermore, men have slightly better survival rates than women. Figure 2 displays comparative survival rates by sex for ampullary carcinoids.

COMMENT

The SEER database provides perhaps the largest number of neuroendocrine neoplasms of the ampulla of Vater ever registered. The analysis of the case material relied on the histologic nomenclature integral to the SEER program. A pathologic review of the neuroendocrine tumors reported to SEER would be ideal. Review, however, would be difficult or impossible because access to the SEER case material is restricted because of confidentiality and geographic dispersal. With this limitation in mind, we proceeded to analyze the registered material and review the literature on the subject.

Carcinoids and high-grade neuroendocrine carcinomas of the ampulla are exceedingly rare neoplasms. Among 6081 malignant neoplasms of the ampulla of Vater, collected by SEER during a 34-year period (1973-2006), were 139 neuroendocrine neoplasms (2%), including 82 carcinoids and 57 high-grade neuroendocrine carcinomas. Among the latter, 42 neuroendocrine carcinomas NOS, 9 small cell carcinomas, and 6 large cell neuroendocrine carcinomas were registered. Both carcinoids and high-grade neuroendocrine carcinomas were more common in men than in women. This is in contrast to carcinoid tumors and small cell carcinomas of the gallbladder and extrahepatic bile ducts, which are more common in women. (26) Patients with carcinoid tumors of the ampulla were younger (mean age, 61.6 years) than those with ampullary high-grade neuroendocrine carcinomas (mean age, 67.5 years). This age difference is similar to that reported for carcinoid tumors and small cell carcinomas of the gallbladder and extrahepatic bile ducts. (26) Carcinoid tumors of the ampulla were smaller than ampullary small cell carcinomas and large cell neuroendocrine carcinomas. The mean size for 23 carcinoids from the SEER program was 1.76 cm, while the mean size for high-grade neuroendocrine carcinomas was 3.05 cm. The mean tumor size of 14 high-grade neuroendocrine carcinomas reported by Nassar et al (13) was 2.5 cm.

[FIGURE 1 OMITTED]

[FIGURE 2 OMITTED]

Although carcinoid tumors, small cell carcinomas, and large cell neuroendocrine carcinomas belong to the family of neuroendocrine neoplasms of the ampulla, they differ in clinical manifestations, histologic and immunohistochemical features, and biologic behavior. Since 1970, ampullary carcinoid tumors had been described in association with type 1 neurofibromatosis. (16-19,24,27,28) Later, a variety of endocrine syndromes including the Zollinger-Ellison syndrome, carcinoid syndrome, multiple endocrine neoplasia type 1 syndrome, and Cushing syndrome were reported in association with ampullary carcinoids. (20,29) None of these syndromes have been reported in patients with high-grade neuroendocrine carcinomas. (13) Unfortunately, the SEER Program does not provide information about the association of endocrine syndromes with carcinoid tumors or high-grade neuroendocrine carcinomas of the ampulla. More recently, an association between ampullary carcinoids and gastrointestinal stromal tumors has been established. (30-35)

Approximately half of high-grade neuroendocrine carcinomas of the ampulla arise from intestinal-type adenomas and some coexist with ampullary adenocarcinomas or squamous cell carcinomas. (13) In contrast, the association of carcinoids with adenomas has not been documented in the ampulla, whereas carcinoid tumors of the colon can arise in adenomas. (36-38) However, a single example of composite carcinoid adenocarcinoma (39) was found in the SEER cases. Some13 have suggested that the association of high-grade neuroendocrine carcinomas with adenomas and conventional adenocarcinomas of the ampulla of Vater reflects a common pathway in the carcinogenesis of these tumors.

Among the unusual variants of carcinoid tumors reported to SEER, 5 were goblet cell carcinoids, which are more common in the appendix, (40) and 2 were somatostatin-producing carcinoids, which usually show a glandular pattern. (21) There were no cases of clear cell carcinoids associated with the von Hippel-Lindau syndrome, as described in the gallbladder (41) and extrahepatic bile ducts. (42) Likewise, no gastrin-producing or corticotropin-producing carcinoid tumors were reported to SEER.

In 1983, somatostatin was detected in ampullary carcinoids associated with neurofibromatosis predominantly in black patients. (43,44) These glandular carcinoids often contain psammoma bodies but do not produce the somatostatinoma syndrome as reported in patents with pancreatic endocrine D cell tumors. (45) Somatostatin-producing carcinoid tumors of the ampulla were later described in patients without neurofibromatosis. (46-48) Subsequently, a variety of peptide hormones were shown by immunohistochemistry in ampullary carcinoids, including gastrin (associated with Zollinger-Ellison syndrome or multiple endocrine neoplasia type 1 syndrome), vasoactive intestinal peptide, pancreatic polypeptide, corticotropin (associated with Cushing syndrome), insulin, cholecystokinin, and calcitonin. (20,22,23,49) In 1 study, (49) about 39% of ampullary carcinoids also labeled with serotonin. When liver metastasis occurs in these serotonin-producing neoplasms, the carcinoid syndrome may develop. (20) None of these hormones/amines have been demonstrated in high-grade neuroendocrine carcinomas of the ampulla, which, on the other hand, often show loss of retinoblastoma protein expression. (13) Of interest is the demonstration of calcitonin and the occasional presence of stromal amyloid in ampullary carcinoids, reminiscent of medullary thyroid carcinoma. (50,51) Non-syndromic gastrin-producing carcinoid tumors associated with Helicobacter pylori gastritis and long-term use of proton pump inhibitors have been reported in the duodenum but not in the ampulla. (52)

Small cell carcinomas often show a component of large cell neuroendocrine carcinoma in the ampulla and in many other sites, which suggests a close relationship between these 2 neoplasms. In fact, we, as well as others, believe that these tumors represent different morphologic expressions of the same tumor. (53) Carcinoid tumors, on the other hand, do not coexist with high-grade neuroendocrine carcinomas in the ampulla as well as in many other anatomic sites, including the lung, the uterus, and the tubular gastrointestinal tract, which suggests that these 2 types of neuroendocrine neoplasms are not closely related.

Lymph node status was reported in 28 of 82 resected ampullary carcinoids and 8 (28.5%) had metastatic deposits. Of these 8 carcinoid tumors, 5 measured between 0.2 and 1.0 cm, and 1 tumor measuring 0.8 cm metastasized to lymph nodes. Small metastasizing carcinoids measuring 0.7 to 0.8 cm with low proliferative activity have been previously reported, (54-56) providing support to the idea that all carcinoid tumors are malignant and should not be designated neuroendocrine tumors, an ambiguous term that does not specify their malignant potential. Likewise, we believe that the term neuroendocrine carcinoma, not otherwise specified is unacceptable because it is a generic term that includes 4 different types of neuroendocrine neoplasms. Because of the presence of lymph node metastasis in carcinoid tumors measuring 0.7 to 0.8 cm, radical surgery has been recommended for all well-differentiated carcinoid tumors of the ampulla. (57-59) The incidence of lymph node metastasis in high-grade neuroendocrine carcinomas from the SEER Program was 62%. Most authors agree that radical surgery is fully justified in this group of neuroendocrine tumors. (13)

As expected, striking differences in the biologic behavior of carcinoid tumors and high-grade neuroendocrine carcinomas of the ampulla were found in SEER. The 5- and 10-year relative survival rates for patients with carcinoid tumors were 82% and 71%, respectively. This 5-year survival rate contrasts with the 5-year survival rate of 60% for patients with carcinoid tumors of the small intestine, the 62% survival rate for patients with colonic carcinoids, (60) and the 96% survival rate for patients with carcinoids of the duodenum. (61) The 5- and 10-year relative survival rates associated with high-grade neuroendocrine carcinomas were 15.7%. A similar clinical course was found in carcinoids and high-grade neuroendocrine carcinomas of the extrahepatic bile ducts. (26) Among 14 patients with highgrade neuroendocrine carcinomas of the ampulla, as reported by Nassar et al, (13) 64% died of disease, but the mean size of their tumors was 2.5 cm and follow-up of the patients was shorter, which may explain the better survival rate than that seen in the SEER cases.

In conclusion, neuroendocrine neoplasms of the ampulla of Vater constitute a heterogeneous group of neoplasms that can be classified as carcinoid, the most common type, and high-grade neuroendocrine carcinoma, including small cell carcinomas and large cell neuroendocrine carcinomas. Several histologic variants of carcinoid tumors are recognized including the classic type with trabecular, nesting, or insular patterns and unusual variants including the glandular, goblet cell, and the mixed or composite carcinoid-adenocarcinoma type. In addition, somatostatin-producing, gastrin-producing, and corticotropin-producing carcinoid tumors have been identified and may give rise to endocrine manifestations or be associated with neurofibromatosis or gastrointestinal stromal tumors, especially the somatostatin-producing carcinoid tumor. Both carcinoid tumors and high-grade neuroendocrine carcinomas are more common in men than in women. Carcinoid tumors are smaller than high-grade neuroendocrine carcinomas. The mean age of patients with carcinoid tumors was 61 years, and it was 67.5 years for patients with high-grade neuroendocrine carcinomas. Carcinoids are relatively low-grade malignant tumors with 5- and 10-year relative survival rates of 82% and 71%, respectively. By contrast, the 5- and 10-year relative survival rates of high-grade neuroendocrine carcinomas were both 15.7%.

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Jorge Albores-Saavedra, MD; Alexandra Hart, BS; Fredy Chable-Montero, MD; Donald E. Henson, MD

Accepted for publication February 4, 2010.

From the Department of Pathology, Instituto Nacional de Ciencias Medicas y Nutricion "Salvador Zubiran" and Hospital Medica Sur, Mexico City, Mexico (Drs Albores-Saavedra and Chable-Montero); and George Washington University Cancer Institute, Office of Cancer Prevention and Control, Washington, District of Columbia (Ms Hart and Dr Henson).

The authors have no relevant financial interest in the products or companies described in this article.

Reprints: Jorge Albores-Saavedra, MD, Department of Pathology, Instituto Nacional de Ciencias Medicas y Nutricion Salvador Zubiran, Vasco de Quiroga No.15, Tlalpan, Mexico D.F. C.P. 14000 (e-mail: alboresjorge@yahoo.com).
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Author:Albores-Saavedra, Jorge; Hart, Alexandra; Chable-Montero, Fredy; Henson, Donald E.
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Date:Nov 1, 2010
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