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Arquivos de Gastroenterologia

Print version ISSN 0004-2803On-line version ISSN 1678-4219

Arq. Gastroenterol. vol.54 no.1 São Paulo Jan./Mar. 2017 


Primary neuroendocrine neoplasm of the esophagus – Report of 14 cases from a single institute and review of the literature

Neoplasia neuroendócrina primária de esôfago - Relato de 14 casos e revisão de literatura

Francisco TUSTUMI1 

Flavio Roberto TAKEDA2 

Rodrigo Hideki UEMA3 

Guilherme Luiz Stelko PEREIRA2 

Rubens Antonio Aissar SALLUM1 


1Cirurgia do Aparelho Digestivo, Faculdade de Medicina, Hospital das Clínicas, Universidade de São Paulo, Sao Paulo, Brazil

2 Instituto do Câncer, Faculdade de Medicina, Hospital das Clínicas, Universidade de São Paulo, Sao Paulo, Brazil

3 Faculdade de Medicina, Hospital das Clínicas, Universidade de São Paulo, Sao Paulo, Brazil



Most prevalent esophageal neoplasm is squamous cell carcinoma and adenocarcinoma. Other tumors are uncommon and poorly studied. Primary neuroendocrine esophageal neoplasm is a rare carcinoma and most of its therapy management is based on lung neuroendocrine studies. Neuroendocrine tumors can be clustered in the following subtypes: high grade (small cell carcinoma or large cell carcinoma) and low grade (carcinoids).


The present study aims to assess clinical and pathological neuroendocrine esophageal tumors in a single oncologic center.


A retrospective analysis of patients and review of the literatures was performed.


Fourteen patients were identified as neuroendocrine tumors, 11 male and 3 female patients. Mean age was 67.3 years old. Ten patients were classified as small cell, 3 as large cell and 1 as carcinoid. Four patients presented squamous cell carcinoma simultaneously and 1 also presented adenocarcinoma. Main sites of metastasis were liver, peritoneum, lung and bones. Most patients died before 2 years of follow-up. Patient with longer survival died at 35 months after diagnosis.


Neuroendocrine esophageal tumors are rare; affect mainly men in their sixties or seventies. High grade tumors can be mixed to other subtypes neoplasms, such as adenocarcinoma and squamous cell carcinoma. Most of these patients have poor overall survival rates.

Headings: Esophageal neoplasms; Carcinoid tumor; Neuroendocrine carcinoma



As neoplasias esofágicas mais prevalentes são o adenocarcinoma e o carcinoma espinocelular. Outros subtipos histológicos são incomuns e pouco estudados. Neoplasia neuroendócrina esofágica é uma patologia rara e seu manejo atualmente se baseia nos conhecimentos prévios de tumores neuroendócrinos de pulmão. Tumores neuroendócrinos podem ser divididos nas seguintes formas: alto grau (pequenas células ou grandes célula) e baixo grau (carcinoides).


Avaliar clínica e patologicamente os tumores de esôfago em um centro oncológico referenciado.


Foi realizada análise retrospectiva e revisão da literatura de neoplasias neuroendócrinas de esôfago.


Foram identificados 14 pacientes com tumores neuroendócrino, sendo 11 homens, 3 mulheres. Idade média foi de 67,3 anos de idade. Desses pacientes, 10 foram classificados como pequenas células, 3 como grandes células e 1 como carcinoide. Foram encontrados quatro casos de tumor misto neuroendócrino e carcinoma espinocelular, e um caso de tumor misto adenoneuroendócrino. Principal sítio de metástases foi fígado, peritônio, pulmão e ossos. A maioria dos pacientes foi a óbito em até 2 anos de seguimento. Paciente com sobrevida mais longa foi a óbito após 35 meses do diagnóstico.


Neoplasias neuroendócrinas de esôfago são raras, afetam principalmente o sexo masculino na 7ª ou 8ª década de vida. A maioria dos pacientes com tumores de alto grau tem sobrevida curta.

Descritores: Neoplasias esofágicas; Tumor carcinoide; Carcinoma neuroendócrino


Esophageal cancer is a rapidly progressive disease with poor survival rates. Most of these tumors are either adenocarcinoma or squamous cell carcinoma histologic types. Less frequent cancer subtypes, such as melanoma, lymphomas or neuroendocrine tumors are uncommon and poorly explored34.

Neuroendocrine esophageal neoplasms are rare and most of studies are case reports. The classification and nomenclature are not well established and knowledge acquired in neuroendocrine neoplasms of lungs and certain gastrointestinal sites, such as pancreas, usually guide esophageal neuroendocrine management.

Neuroendocrine neoplasm subtypes are grouped based upon shared neuroendocrine features. The subtypes comprise small cell carcinoma, large cell neuroendocrine carcinoma, typical carcinoid, and atypical carcinoid140.

This article is a descriptive report of clinical and pathological features of cases of neuroendocrine esophageal tumors in our institute, along 8 years of experience, and a review of the literature.


All esophageal cancer patients' charts of our institution were reviewed, between 2008 and 2016. Cases of neuroendocrine neoplasm were identified and clinical and pathological features of these patients were assessed.

For review of the literature, database search was performed in MEDLINE, with search algorithm: ("neuroendocrine" [All Fields] OR "carcinoid tumor" [MeSH Terms] OR "carcinoid" [All Fields] OR "small cell carcinoma" [MeSH Terms] OR "large cell carcinoma") AND ("oesophagus" [All Fields] OR "esophagus" [All Fields] OR esophageal [All Fields]). Period searched up to 2016, with no idiom restriction. Review studies and no full-text studies were excluded. When more than one publication of a single trial existed, only the publication with the most complete data was included.


A total of 1,574 of esophageal cancers were reviewed. Fourteen (0.89%) cases of neuroendocrine neoplasm were selected, 3 female and 11 male patients (Table 1). Mean age was 67.3 (range 47 to 80) years old. Table 2 shows immunohistochemical panel of neuroendocrine neoplasm.

TABLE 1 Main characteristics of the 14 patients diagnosed with neuroendocrine tumor 

Patient Age Sex KPS ECOG Stage Histologic subtype Associated neoplasm Site Survival (months) Esophagectomy Chemotherapy Radiotheraphy
1 79 M 50 4 Unstaged SCCE No Lower 2 No No No
2 65 M 90 1 IIIA SCCE No Middle Alive at 26 months Yes No No
3 60 M 80 1 IIIB LCCE No Middle and lower 13 No IP 30 cGy
4 65 M 30 4 IA Carcinoid No Lower 7 No No No
5 75 F 90 1 IIA LCCE No Lower 13 Yes IP, PC 45 cGy
6 51 M 100 0 IIIC SCCE No Upper and middle Lost to follow-up at 4 months No EP No
7 58 M 80 2 IV SCCE SCC Middle 2 No No No
8 64 M 100 0 IIIA SCCE SCC Middle and lower 35 Yes IP, PT 45 cGy
9 47 M 100 0 IV SCCE No Lower 10 No IP, PT 50.4 cGy
10 78 F 70 1 IV SCCE SCC Lower 13 No IP, PT 45 cGy
11 75 M 80 1 IIIC SCCE No Upper and middle 12 No IP 45 cGy
12 80 F 50 3 IV SCCE SCC Middle 6 No No No
13 76 M 60 3 IV SCCE No Middle 5 No IP No
14 69 M 90 1 IIIB LCCE EA Lower 18 Yes XP (neoadjuvant), IP No

SCEC: small cell esophageal cancer; LCEC: large cell esophageal cancer; KPS: Karnofsky Performance Status; ECOG: Eastern Coorporative Oncology Group; SCC: squamous cell carcinoma; EA: esophageal adenocarcinoma; PC: Paclitaxel and Carboplatin; PT: Cisplatin and Paclitaxel; IP: Irinotecan and Cisplatin; EP: Etoposide and Cisplatin; XP: Capecitabine and Cisplatin.

TABLE 2 Immunohistochemical panel of patients with esophageal neuroendocrine neoplasm 

Patient Grade of cellular differentiation Syp CgA Ki-67(%) Ber-EP4 Ck7 AE-1/AE-3 35BH11 P63 CD 56 TTF-1 Vimentin
1 Poorly + NP >90 NP NP NP NP NP + NP NP
2 Poorly NP - 80-90 NP NP NP + - + + NP
3 Poorly NP + 90 + NP - NP - NP NP NP
4 Well + + <1 NP NP NP NP NP NP NP NP
5 Poorly + + >90 NP + NP NP - NP NP NP
6 Poorly + + 90 NP NP NP NP NP NP + NP
7 Poorly + + NP + NP NP NP + NP NP NP
8 Poorly - + 50 NP + + NP + + + +
9 Poorly + + 80-90 NP NP NP + - +e NP NP
10 Poorly + + NP NP - + + - + + NP
11 Poorly NP - NP - NP + + - + NP NP
12 Poorly + + 90 NP NP + NP + + NP NP
13 Poorly NP NP NP NP NP + + + + + +
14 Poorly + + 70 - + NP NP - NP NP NP

(+): positive; (-): negative; Syp: Synaptophysin; CgA: Chromogranine A; Ck: Cytokeratin; NP: not performed.

Three were classified as large cell esophageal carcinoma (LCEC), 10 as small cell carcinoma (SCEC), and 1 as carcinoid. Distal and middle esophagus were more often affected.

Endoscopic appearance was usually a vegetating and infiltrative tumor, except carcinoid subtype. (Figure 1).

FIGURE 1 Endoscopic view of a high grade neuroendocrine neoplasm. It shows a circumferential infiltrative and ulcerating tumor. 

Main symptoms were dysphagia (14∕14) and weight loss (mean 11.7 ± Std Dev 6.3 kg). Duration of symptoms prior to diagnosis was 6.2 ± Std Dev 3.3 months.

Associated squamous cell carcinoma could be seen in 4∕14 cases and associated adenocarcinoma (adenoneuroendocrine) in 1∕14. Immunohistochemical panel can be seen in Table 2.

Of these patients, 10∕14 had previous history of high amount of alcohol intake and 12∕14 were tobacco smokers.

Most cases were diagnosed at late stages (III and IV), accordingly AJCC 7th Edition122. Metastasis sites were lungs, liver, adrenal, peritoneal and bones.

Cause of death was pneumonia in five cases, urinary tract infection in one case, and sepsis of unknown origin in one case. The five remaining patients, cause of death was not clearly established.

Curative intent surgery was performed in 4∕14 patients, of which one is still alive at 26 months of follow-up.

Most cases had low survival rates (see Figure 2). Patient who lived longer died at 35 months of pneumonia. Patient "2" is still alive without disease up to this paper publication. Patients "6" lost to follow-up, with disease. The remaining patients died with disease.

FIGURE 2 Kaplan-Meir curve for survival of patients with esophageal neuroendocrine neoplasm 

Patient diagnosed with carcinoid tumor presented myelofibrosis during follow-up, leading to pancytopenia and early death.

Review of the literature

For review of the literature, a total number of articles by database search were 1007. After excluding duplicates and screening by title and abstract, 154 articles remained1-33,35-79,81-115,117-119,121,123-139,141-162.

A cumulative sample size of 2,957 patients was evaluated, in 20 different countries. Of this patients, 2,899 were SCEC (77% in East countries; 23% in West countries); 35 were LCEC (6% in East countries; 94% in West countries); and 23 were carcinoid (54% in East countries; 43% in West countries).

Among all esophageal malignances, prevalence of SCEC was 1.05% in East countries and 0.72% in West countries. There are few studies data concerning carcinoid tumors and LCEC prevalence. Most of the studies approaching LCEC were performed in West countries.

Neoplasms were staged as limited disease (LD) or extend disease (ED). LD is defined as disease confined to the esophagus and adjacent organs with or without regional lymph node involvement while ED is defined for neoplasm with distant spread59. Main features and differences concerning neuroendocrine subtypes are presented in Table 3.

TABLE 3 Main features and differences concerning neuroendocrine subtypes 

SCEC % LCEC % Carcinoid %
Prevalence East countries 1,527 (145,717) 1.048 Unknown - Unknown -
West countries 533 (73,290) 0.727 5 (1,105) 0.452 Unknown -
Age Mean 63.8 - 62.1 - 58.3 -
< 60 yr 542 48.26 0 0 12 57.1
≥ 60 yr 581 51.74 4 100 9 42.9
Sex M 1,517 69.5 32 88.9 14 70
F 666 30.5 4 11.1 6 30
Mixed SCC 82 (786) 10.4 2 (36) 5.6 0 (13) 0
Adenocarcinoma 31 (786) 4 14 (36) 38.9 0 (13) 0
Tumor site Upper 202 12.4 1 10 1 7.7
Middle 904 55.5 5 50 2 15,4
Lower/GEJ 523 32.1 4 40 10 76.9
Stage LD 1,519 70.2 16 55.2 13 100
ED 645 29.8 13 44.8 0 0
Tumor size < 5 cm 423 42.2 2 66 9 64.3
≥ 5 cm 580 578 1 33 5 35.7
OS 1 yr 803 (1,744) 46 1 (2) 50 9 (10) 90
2 yr 275 (1,250) 22 0 (1) 0 6 (7) 86
3 yr 234 (1,693) 13.8 0 (1) 0 6 (7) 86
5 yr 144 (1,853) 7.7 0 (1) 0 6 (7) 86

OS: overall survival; GEJ: gastroesophageal junction; SCEC: small cell esophageal cancer; LCEC: large cell esophageal cancer.


Neuroendocrine esophageal neoplasms are exceedingly rare, and hence there are few large sample clinical studies approaching this issue. Consequently, most of the knowledge is based on neuroendocrine lung neoplasms.

Neuroendocrine lung tumors are classified as low grade (carcinoids) or as high grade (SCEC and LCEC)120.

SCEC have nuclear appearance, with finely granular chromatin; lack of predominant nucleoli; nuclear fragility; fusiform cells; scant cytoplasm and indistinct cells borders; high mitotic rate; and large area of necrosis120. (Figure 3).

FIGURE 3 Small cell esophageal carcinoma (SCEC). High power view of infiltrative proliferation of round small cells with scanty cytoplasm and dark nuclei with intense crush artifacts lined by ulcerative epithelium (a) (HE, 200x). CD56 positive (b) (400x). 

LCEC presents non-small cell nuclear features (vesicular clumpy chromatin, predominant nucleoli), abundant cytoplasm, and large cell size120. (Figure 4).

FIGURE 4 Large cell esophageal carcinoma (LCEC). Solid nests of large and intermediate cells, with eosinophilic cytoplasm, vesicular nuclei and prominent nucleoli, focal necrosis and high mitotic rate (a) (HE, 200x). Chromogranin positive (400x) (b). 

Carcinoids typical morphology includes coarsely granular "salt and pepper" chromatin, overall uniformity, prominent vascularity, lack of prominent nucleoli, low mitosis rate. Usually no necrosis is seen120.

Esophageal high grade tumors tend to be aggressive. Usually, patients are diagnosed lately, with widespread disease, and with poor prognosis. Currently, clinical treatment strategies of high grade cancers neuroendocrine neoplasms are very limited and full of contradiction. High grade neoplasms are often regarded as a systemic disease and, just like in lung cancer, chemotherapy is the mainstay of therapy17. Additional therapy (surgery or radiotherapy) should be considered, but randomized controlled trials still unavailable80,116.

Our data suggests a much good prognosis for low grade neuroendocrine tumors, with high overall survival rate. For limited disease (LD) carcinoid, surgical intervention is the treatment of choice18.

Although low incidence of esophageal neuroendocrine tumors, our results give a better picture of the behavior of this rare condition. The present study shows this disease affects mainly men in sixties or seventies. Middle and lower esophageal thirds are most frequently affected. Nevertheless, future multicenter efforts are needed for randomized clinical trials evaluating therapeutic guidelines.

Authors' contributions

Tustumi F: study elaboration and data collect. Takeda FR: study elaboration. Uema RH: data collect. Pereira GLS: oncologic review. Sallum RAA: orientation of the study. Cecconello I: orientation of the study.


We would like to state our acknowledgment for Rafaela Brito Bezerra Pinheiro efforts on pathology analysis and microscopy pictures.


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Disclosure of funding: no funding received

Received: July 09, 2016; Accepted: August 22, 2016

Correspondence: Francisco Tustumi. Faculdade de Medicina, do Hospital das Clínicas, da Universidade de São Paulo. Rua Teodoro Sampaio, 632, ap. 71 - CEP: 05406-000 - São Paulo, SP, Brasil. E-mail:

Declared conflict of interest of all authors: none

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