Literature survey on epidemiology and pathology of gangliocytic paraganglioma
© Okubo et al; licensee BioMed Central Ltd. 2011
Received: 24 September 2010
Accepted: 20 May 2011
Published: 20 May 2011
Although gangliocytic paraganglioma (GP) has generally been regarded as a neuroendocrine tumor, its origin remains unclear. We therefore aimed to investigate the details of this disease by carefully analyzing and extracting common features of the disease as presented in selected publications.
We searched for English and Japanese cases of GP using the PubMed and IgakuChuoZasshi databases on August 2010. We then extracted and sampled raw data from the selected publications and performed appropriate statistical analyses. Additionally, we evaluated the expression of hormone receptors based on our previously reported case.
192 patients with GP were retrieved from the databases. Patient ages ranged from 15 y to 84 y (mean: 52.3 y). The gender ratio was 114:76 (male to female, 2 not reported). Maximum diameter of the tumors ranged from 5.5 mm to 100 mm (mean: 25.0 mm). The duodenum (90.1%, 173/192) was found to be the most common site of the disease. In 173 patients with duodenal GP, gastrointestinal bleeding (45.1%, 78/173) was found to be the most common symptom of the disease, followed by abdominal pain (42.8%, 74/173), and anemia (14.5%, 25/173). Rate of lymph node metastasis was 6.9% (12/173). Our statistical analysis indicated that significant differences were found for gender between GP within the submucosal layer and exceeding the submucosal layer. Furthermore, our immunohistochemical evaluation showed that both epithelioid and pancreatic islet cells showed positive reactivity for progesterone receptors.
Our literature survey revealed that there were many more cases of GP exceeding the submucosal layer than were expected. Meanwhile, our statistical analyses and immunohistochemical evaluation supported the following two hypotheses. First, vertical growth of GP might be affected by progesterone exposure. Second, the origin of GP might be pancreatic islet cells. However, it is strongly suspected that our data have been affected by publication bias and to confirm these hypotheses, further investigation is required.
Duodenal gangliocytic paraganglioma with lymph node metastasis
Chief Clinical presentation
Follow up (months)
Buchler et al. .
Inai et al. .
Hashimoto et al. .
Takabayashi et al. .
Dookhan et al. .
Additional surgical intervention
Recurrence 11 years after first surgical intervention
Sundararajan et al. .
Bucher et al. .
Anemia, subclinical jaundice
Wong et al. .
Witkiewicz et al. .
Mann et al. .
Abdominal pain, vomiting, weight loss
Okubo et al. 
Epigastralgia, tarry stool
Saito et al. .
Gastrointestinal bleeding, anemia
Few studies reported the epidemiology, pathology, and clinical characteristics of the disease. We then evaluated the details of the disease by carefully analyzing and extracting common features of the disease as presented in these selected publications.
We searched English and Japanese cases of GP published from 1957 to the early trimester of 2010 using the PubMed http://www.ncbi.nlm.nih.gov/pubmed/ and IgakuChuoZasshi http://www.jamas.or.jp/ databases on August 2010 by conducting a search of "gangliocytic paraganglioma" with case report options as an additional tool. As a result, 4574 English and 27 Japanese publications were retrieved.
We checked the abstracts and 73 English and 24 Japanese (total 97) publications were regarded as cases of GP and 4504 publications were excluded.
Since this disease entity has been reported under other names, prior to Kepes et al. naming it as a GP , such as "ganglioneuroma", "non-chromaffin paraganglioma", and "paraganglioneuroma", we checked the references of 97 selected publications.
The characteristic three components could be confirmed in the manuscript or a figure.
The paper was cited in other publications as a GP report.
These 105 publications contained reports on 192 patients with GP. In the present study, we conducted a non-systematic literature review using 173 patients with duodenal GP.
We extracted and sampled raw data from the selected publications, such as clinical findings (age, sex, clinical symptoms, operation method, and outcome), histopathological findings (site, maximum diameter of the tumor, diagnostic rate from biopsy before operation, the depth of the tumor invasion, and with or without lymph node metastasis), and immunohistochemical findings.
In addition, we performed appropriate statistical analyses using the extracted data. Statistical analyses were performed using the non-parametric Mann-Whitney U test or Chi-square test.
Differences were considered significant at P < 0.05.
Additionally, we evaluated gender differences based on the results of our statistical analyses. Moreover, we evaluated the expression of hormone receptors in relation to estrogen and progesterone based on our previously reported case .
Finally, we declare that our study may be affected by publication bias because it comprises a cumulating case series.
192 patients with GP were retrieved from the PubMed and IgakuChuoZasshi databases. Patient ages ranged from 15 y to 84 y (mean: 52.3 y). The gender ratio was 114:76 (male to female, 2 not reported). Maximum diameter of the tumors ranged from 5.5 mm to 100 mm (mean: 25.0 mm). The duodenum (90.1%, 173/192) was found to be the most common site of the disease, followed by the low-level spinal cord (2.1%, 4/192) [7–10], respiratory system (2.1%, 4/192) [11–14], jejunum (1.6%, 3/192) [5, 15, 16], and esophagus (1.0%, 2/192) [17, 18]. There were individual cases involving the stomach , appendix , retromediastinum , pancreas , and mature teratoma  (constituent of the lesion), as well as a case of double focus in the duodenum and pancreas  (0.5%, 1/192, respectively). In accordance with these findings, the present study focuses on the duodenal lesion, which represents the site for the overwhelming majority of cases of the disease.
173 patients with duodenal GP were retrieved from the PubMed and IgakuChuoZasshi databases. Patient ages ranged from 15 y to 84 y (mean: 52.6 y). The gender ratio was 102:69 (2 not reported).
Gastrointestinal bleeding (45.1%, 78/173) was found to be the most common symptom of the disease among the symptoms reported in the papers, followed by abdominal pain (42.8%, 74/173), and anemia (14.5%, 25/173). In contrast, biliary obstruction was extremely rare (4.6%, 8/173). The follow-up period ranged from 12 months to 96 months, and no death from GP was reported. With the exception of a patient that had part of a previous tumor at the initial operation , no recurrence has been reported. There is only one report of a patient who underwent radiotherapy after surgical intervention . 15 patients underwent an endoscopic procedure for removal [26–40], and one patient required additional surgical intervention due to the presence of a tumor residue following her first endoscopic intervention .
Histopathological findings from forceps biopsies performed prior to surgical intervention were described in 35 patients. Among these cases, 4 patients were correctly diagnosed as GP, 24 patients did not show evidence of tumor cells (specimens did not contain tumor cells), and 7 patients were diagnosed or suspected of having a different neuroendocrine tumor (3 carcinoid tumors, 2 paragangliomas, 1 ganglioneuroma, and 1 case involving atypical cells).
The maximum diameter of the tumors ranged from 5.5 mm to 100 mm (mean: 24.2 mm). The depth of the tumor invasion was described in 108 patients, comprising 42 patients with submucosal invasion, 62 with muscularis propria invasion, and 4 with connective tissue beneath the muscularis propria. In summary, 42 patients had GP within the submucosal layer and 66 patients had GP exceeding the submucosal layer. Moreover, 12 of these patients showed lymph node metastasis that involved one submucosal lesion [Table 1].
Representative findings for each of the three characteristic components of tumor cells are as follows. In epithelioid cells, neuron specific enolase (NSE) showed the highest positive rate (93.9%, 77/82), followed by synaptophysin (90.0%, 36/40), pancreatic polypeptide (PP; 89.7%, 70/78), somatostatin (81.8%, 63/77), chromogranin-A (67.4%, 60/89), cytokeratins (48.3%, 28/58), and serotonin (22.0%, 13/59).
In spindle-shaped cells, S-100 protein showed the highest positive rate (94.2%, 98/104), followed by NSE (84.0%, 63/75), and synaptophysin (64.7%, 22/34).
Immunohistochemical findings for each of the three characteristic components of the tumor.
Neuron specific enolase
Vasoactive intestinal polypeptide
Comparative analysis of clinicopathological findings
To determine significant factors associated with the progression of the tumor, the following comparative analyses were carried out.
When we employed evidence of metastasis as an indicator of progression, a significant difference was found only for the ages of patients among the clinicopathological findings concerning those with and without lymph node metastasis (Mann-Whitney U test: p = 0.01), and patients with metastasis were significantly younger than those without metastasis. In contrast, no significant differences were found in the maximum diameter of the tumors or gender when comparing patients with and without lymph node metastasis (Mann-Whitney U test: p = 0.10 or Chi-square test: p = 0.55, respectively).
Comparison of clinicopathological findings between patients with and without lymph node metastasis.
Patients with lymph node metastasis
Patients without lymph node metastasis
Number of patients
17 to 67 (mean: 43.5)
15 to 84 (mean: 53.4)
Significant difference was found
(Mann-Whitney U test: p = 0.01)
Maximum diameter of the tumor (mm)
5.5 to 65 (mean: 29.8)
10 to 100 (mean: 23.5)
No significant difference was found
(Mann-Whitney U test: p = 0.10)
Gender (male to female)
96:63 (2 not reported)
No significant difference was found
(Chi-square test: p = 0.55)
Comparison of clinicopathological findings between GP within and exceeding the submucosal layer.
Gangliocytic paraganglioma within the submucosal layer
Gangliocytic paraganglioma exceeding the submucosal layer
Number of patients
28 to 84 (mean: 54.1)
15 to 73 (mean: 50.0)
No significant difference was found (Mann-Whitney U test: p = 0.23)
Maximum diameter of the tumor (mm)
5.5 to 65 (mean: 21.7)
10 to 100 (mean: 26.8)
No significant difference was found (Mann-Whitney U test: p = 0.18)
Gender (male to female)
Significant difference was found
(Chi-square test: p = 0.02)
Rate of lymph node metastasis
Significant difference was found
(Chi-square test: p = 0.03)
However, no significant differences were found for the maximum diameter of the tumor or the age of a patient between males and females. In addition, Spearman's rank correlation coefficient was calculated to assess any potential relationship between the maximum diameter of the tumors and ages of patients, but no significant relationships were found.
Immunohistochemical evaluation of female sex hormone receptors
We collected as many publications written in English or Japanese involving GP and examined them to extract characteristic features of the tumor as presented in clinical and histopathological findings.
We focused on determining the significant factors associated with the progression of the tumor. Here we discuss the clinical, histopathological, and immunohistochemical findings in reference to matters that emerged from our research.
In the present study, we found gastrointestinal bleeding as the most common symptom, followed by abdominal pain. This fact has been previously accepted and our data confirm it. All patients without autopsies and having clinically incidental focus had surgical interventions, including 15 patients with endoscopic intervention. Indeed, one patient required additional surgical intervention due to a residue of the tumor at her first endoscopic procedure , while other patients showed a good outcome without recurrence or metastasis. Furthermore, there was no record of a patient dying from GP, and patients with this tumor, therefore, have an extremely good prognosis. However, one patient has been reported as showing a recurrence due to a residue of a previous tumor at his initial surgical intervention . Accordingly, we emphasize the importance of both a histopathological assessment of extensive tumor components at the surgical margin and imaging examinations to monitor for recurrence or metastasis after the operation.
Although one patient received irradiation after surgical intervention , we maintain that patients without residual tumor require no adjuvant therapy because no recurrence or metastasis has been reported in such patients. By contrast, it is still unclear whether a residual tumor can be controlled by irradiation or chemotherapy alone without surgical intervention.
The immunohistochemical findings on the tumors need consideration since the identification of three cellular components are essential for diagnosis. Epithelioid and ganglion-like cells showed a high positive rate for several kinds of immunohistochemical neuroendocrine markers, such as synaptophysin, chromogranin A, and NSE. In addition, epithelioid cells showed a high positive rate for PP. In contrast, spindle-shaped cells had the highest positive rate for S-100. These results are consistent with other previous publications. Furthermore, positive rates for each hormone, such as somatostatin, serotonin, gastrin, glucagon, and insulin in epithelioid cells, were significantly different and the meaning of this finding is worth investigating. However, these extracted immunohistochemical findings should be regarded as hints or suggestions because it is thought that results involving negative data have not been described in previous publications. In fact, our previous case report did not describe the immunohistochemical evaluation of each hormone according to negative reactivity.
Incidentally, we previously tried to establish the immunohistochemical prognostic indicators of GP using bcl-2, p53, and Ki-67, which are acceptable prognostic indicators in several kinds of neuroendocrine tumors [41–44]. However, all of these indicators showed a negative reactivity.
Unfortunately, there were no other cases of GP that included an immunohistochemical evaluation using bcl-2 and p53, and the value of these factors as prognostic indicators of GP remains unclear.
In contrast, two cases without lymph node metastasis were described with the Ki-67 labeling index in GP [45, 46]. However, both showed extremely low Ki-67 labeling index values. Therefore, we suggest that immunohistochemical evaluation using Ki-67 may have a limited prognostic value in GP.
Finally, we gained insight into the progression of GP tumors and related factors. It has been accepted that GP usually arises from the submucosal or muscular layer, which may make the diagnosis difficult using a forceps biopsy prior to surgical intervention. In fact, we revealed that the diagnostic rate by biopsy before surgical intervention was only 11.4% (4/35). In addition, we showed that many more cases of GP exceeding the submucosal layer were reported (61.1%, 66/108) than expected, and GP exceeding the submucosal layer is a risk factor for lymph node metastasis. These facts emphasize the importance of imaging examinations prior to surgical interventions.
It is interesting to note that significant differences were found for gender between GP within the submucosal layer and exceeding the submucosal layer. On the basis of our investigation, a hypothesis emerged that asserted no significant relationship for gender and that female gender induces vertical growth of the tumor. To confirm part of our hypothesis, we focused on female-specific factors and initially evaluated tumor cells immunohistochemically using anti-estrogen and progesterone receptor antibodies. As a result, our immunohistochemical evaluation revealed that epithelioid cells showed positive reactivity for the progesterone receptor. Furthermore, some investigators reported that progesterone regulates neural differentiation [47, 48]. These facts suggest that the vertical growth of GP might be affected by progesterone exposure.
Additionally, it is interesting to note that normal pancreatic islet cells also showed positive reactivity for the progesterone receptor. It has been reported that normal pancreatic islet cells and pancreatic neuroendocrine tumors showed positive reactivity for the progesterone receptor , and our literature survey demonstrated that epithelioid cells showed a high positive rate for PP (89.7%, 70/78) immunohistochemically. These facts indicate the relationship between GP and pancreatic islet cells. However, immunohistochemical evaluation for estrogen receptors differs between epithelioid cells and normal pancreatic islet cells, and our immunohistochemical evaluation was based on only one patient. Furthermore, it is strongly suspected that our data have been affected by publication bias.
To confirm these hypotheses, further investigation is required (e.g. compare the positivity between the metastatic cases [6, 24, 25, 36, 46, 50–56] and non-metastatic cases for the immunohistochemical antigen expression).
Our literature survey revealed that there were many more cases of GP exceeding the submucosal layer than were expected, and significant differences were found in gender between GP within the submucosal layer and exceeding the submucosal layer. Furthermore, our immunohistochemical evaluation showed that both epithelioid cells and normal pancreatic islet cells showed strongly positive reactivity for progesterone receptors. These immunohistochemical results support the following two hypotheses. First, vertical growth of GP might be affected by progesterone exposure. Second, the origin of GP might be the pancreatic islet cells. However, further investigation is required to confirm these hypotheses.
Since the data of this study were extracted and sampled from previous publications, written informed consent for publication from patients does not exist with the exception of our previous publication. As for our previously reported cases, written informed consent was obtained from the patients for publication of this study as well as any accompanying images. A copy of the written consent is available for review by the Editor-in-Chief of this journal. Furthermore, the anonymity of all patients was strictly protected.
neuron specific enolase
This work was supported by the Health Science Research Grants for Research on Emerging and Re-emerging Infectious Diseases (H16-Shinko-6 and H19-Shinko-8), Measures for Intractable Diseases (H20 nannchi ippann 35) from the Ministry of Health, Labor and Welfare of Japan, by a Grant of the Strategic Basis on Research Grounds for Non-governmental Schools at Heisei 20th from the Ministry of Education, Culture, Sports, Science and Technology Japan to K. S, and Toho University project grant to Y. O.
The authors thank Minoru Shinozaki for his excellent technical support and Tsutomu Hatori, Aki Mitsuda, Chikako Hasegawa and Takayuki Hirano for their histopathological advice.
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