Jejunoileal Neuroendocrine Tumors Complicated by Intestinal Ischemic Necrosis Are Associated With Worse Overall Survival.
Rarely, JINETs come to clinical attention because of tumor-induced intestinal ischemia, and the resected surgical specimen shows intestinal ischemic necrosis (IIN) in the nonneoplastic small intestine. The largest series of JINETs with IIN was published in 1970 and included 10 cases, all of which were discovered at autopsy. (12) Since then, several case reports and small series of JINETs with IIN in surgical resections have been described, (13-22) but the prognostic significance of IIN has not, to our knowledge, been assessed after controlling for other clinicopathologic features. The present study aims to determine whether and to what extent JINET-induced IIN is associated with overall survival.
MATERIALS AND METHODS
With institutional review board approval, we searched the pathology database at University of Pittsburgh Medical Center (Pittsburgh, Pennsylvania) for surgical resections of JINETs with IIN between January 1, 2001, and June 30, 2014. This search included resections that were done at either our main academic hospital (Presbyterian University Hospital) or our affiliated community hospitals. For a control group, we searched the pathology database for JINETs without IIN that were resected at Presbyterian University Hospital between January 1, 2001, and December 31, 2010, that had hematoxylin-eosin slides available. Poorly differentiated neuroendocrine carcinomas and recurrent neuroendocrine tumors were not included in the study.
Hematoxylin-eosin slides and gross descriptions were reviewed, and pathologic features were assessed, including American Joint Committee on Cancer stage, (23) WHO grade, (24) tumor size, perineural invasion, vascular invasion, tumor multifocality, mesenteric tumor deposits, and synchronous carcinoma.
Tumors were graded based on the Ki-67 and mitotic indices, following the WHO guidelines. (24) If the Ki-67 grade and the mitotic index yielded discrepant grades, the higher grade was assigned to the tumor.
Mesenteric tumor deposits were defined as discrete mesenteric tumor nodules 1 mm or larger with irregular growth profiles that clearly did not result from extranodal extension or direct contiguous spread by the primary lesion. (11)
Features used to support IIN included mucosal necrosis, withered crypts, hyalinization and/or hemorrhage of the lamina propria, ulceration, regenerative epithelial changes, and attenuated or necrotic muscularis propria.
An immunohistochemical panel of serotonin, gastrin, somatostatin, insulin, and glucagon was performed on whole sections for all cases with IIN for which tumor blocks were available and for a matching number of the most recent cases without IIN.
For cases with IIN by pathologic examination, intraoperative reports were examined to determine whether IIN was apparent before the pathologic assessment.
Patients' electronic medical records were reviewed to determine the presence of risk factors for atherosclerosis, including hypertension, dyslipidemia, diabetes, and tobacco use.
Clinical laboratory testing was reviewed for results of serum serotonin, gastrin, insulin, glucagon, vasoactive intestinal peptide, and urine 5-hydroxyindoleacetic acid (5-HIAA).
Overall Survival Information
Overall survival was determined from the date of surgery. Dates of death were obtained from the Social Security Death Index and electronic medical records with vital status determined as of August 1, 2014. For patients without a documented date of death in the Social Security Death Index or electronic medical records, the duration of survival was censored at the date of their last clinical encounter.
Data are presented as counts and percentages or medians and interquartile ranges (IQRs). Differences in categorical variables between those with and those without IIN were analyzed by the Fischer exact test. Differences in continuous variables were evaluated by the Mann-Whitney U test. Survival information was analyzed by the Kaplan-Meier method. A Cox proportional hazards model was used to estimate the effect of IIN on mortality unadjusted and controlling for age, advanced stage (stage III or IV), tumor grade, and synchronous carcinoma. Statistical analyses were performed using SPSS software (version 22, IBM, Armonk, New York). A P value of less than .05 was considered significant.
We identified 10 consecutive cases of JINETs with IIN resected between January 1, 2001, and June 30, 2014, at Presbyterian University Hospital and affiliated community hospitals. For the control group, we identified 52 consecutive cases of JINETs without IIN resected between January 1, 2001, and December 31, 2010, at Presbyterian University Hospital that had hematoxylin-eosin slides available.
Overall Clinicopathologic Features
Clinicopathologic features are summarized in the Table for the overall cohort and stratified by IIN.
The median age of the patients was 66.8 years (IQR, 55.073.2). Of the 62 patients in the study, 33 (53%) were male. Forty patients (65%) had hypertension, 24 (39%) had dyslipidemia, 9 (15%) had type 2 diabetes mellitus, and 35 (57%) had a history of tobacco use.
Tumors from 55 patients (89%) were WHO grade 1, and 7 (11%) were WHO grade 2. Tumors from 51 patients (82%) were stage III or greater, and 18 (29%) were stage IV. Tumors from 53 patients (86%) had vascular invasion, and 31 (50%) had perineural invasion. Tumors from 25 patients (40%) were multifocal. Tumors from 40 patients (65%) had mesenteric tumor deposits.
Four patients (6%) had synchronous carcinoma of another organ, which was resected during the same procedure. One patient underwent a distal esophagectomy for esophageal adenocarcinoma. Another underwent a distal pancreatectomy for pancreatic ductal adenocarcinoma. The third patient underwent a hysterectomy for complex atypical hyperplasia and, upon resection, was also found to have a microscopic focus of endometrioid adenocarcinoma. The fourth patient underwent a right hemicolectomy for colonic adenocarcinoma; the neuroendocrine tumor was in the jejunum and was resected separately.
For 6 patients (10%), a neuroendocrine tumor was identified within the small bowel mesentery, but overlying tumor was not identified in the small bowel. These are represented in the Table as indeterminate for primary location. Importantly, none of these 6 patients had a documented primary neuroendocrine tumor of another organ in the electronic medical record or pathology database either before or after their surgery.
For 11 patients (18%), no lymph nodes were identified grossly or microscopically.
Clinicopathologic Features of Neuroendocrine Tumors With and Without IIN
Intraoperative notes were available for 8 of the 10 patients with IIN, and 6 of those notes described grossly apparent ischemic changes of the small intestine. A seventh patient with IIN, for whom an operative note was not available, had a preoperative computed tomography scan which showed bowel wall pneumatosis and portal venous gas, features that were interpreted by the radiologist as being consistent with ischemic bowel.
In all cases with IIN, the tumor was in the immediate vicinity of the ischemic portion of bowel. Furthermore, all cases with IIN had either mesenteric or lymph node involvement by tumor or extensive adhesions, such that the tumor was considered to have caused the IIN, as opposed to representing an unrelated finding. No vascular thrombosis was identified in any case with IIN.
Two cases with IIN showed entanglement of the mesenteric vascular structures by gross examination. One of those 2 cases also had associated mesenteric calcification and ossification and is illustrated in Figure 1, A through C. A second representative case with IIN is illustrated in Figure 1, D through F.
Patients with IIN were significantly older than those without IIN (median age, 83 years versus 65.5 years; P = .001). Patients with IIN were more likely to have mesenteric tumor without a primary tumor identified, with 40% (4 of 10) of the patients with IIN showing mesenteric tumor without a primary tumor identified, compared with 4% (2 of 52) of the patients without IIN (P = .005). No significant differences between the 2 groups were found for the remaining clinical or pathologic features.
Forty-two (68%) of the 62 patients had available test results for serum serotonin and/or urine 5-HIAA. Thirty of the 42 tested patients (71%) had elevated serum serotonin (median, 615.5 ng/mL IQR, 415.3-851.3 ng/mL; reference range, 101-283 ng/mL) and/or 24 hour urine 5-HIAA (median, 23.5 mg/24 h; IQR, 8.4-44.5 mg/24 h; reference range, 0.1-6.0 mg/24 h).
Nine of 62 patients (15%) had serum testing for gastrin, insulin, glucagon, and/or vasoactive intestinal peptide, and in no cases were these abnormally elevated.
Two of the 10 cases with IIN (20%) had available test results for serum serotonin and/or urine 5-HIAA, and both cases showed abnormal elevations. For one case, serum serotonin was elevated at 1220 ng/mL (reference range, 101-283 ng/ mL), and for the other case, urine 5-HIAA was elevated at 30.4 mg (reference range, 0.1-6.0 mg/24 h). Thirty-eight of 52 cases without IIN (73%) had available test results for serum serotonin and/or urine 5-HIAA. Twenty-six of those 38 patients (68%) had abnormally elevated serum serotonin (median, 615.5 ng/mL; IQR, 455.3-790.5 ng/mL; reference range, 101-283 ng/mL) and/or 5-HIAA (median 13.8 ng/mL; IQR 8.1-28.8 ng/mL; reference range, 0.1-6.0 mg/24 h).
Nine of the 10 cases with IIN had tumor blocks available for immunohistochemical staining. All 9 cases (100%) with IIN and all 9 tested cases (100%) without IIN were diffusely positive for serotonin. Two cases, both without IIN, showed positivity for gastrin (one patchy and one focal). The case with patchy gastrin positivity had a serum gastrin level within reference range, whereas the case with focal gastrin positivity had no serum gastrin testing available. Two cases, one with IIN and one without IIN, showed focal positivity for somatostatin. None showed positivity for insulin or glucagon.
Association Between IIN and Overall Patient Survival
Twenty-six of the 62 patients (42%) in the study died during the follow-up period. The median length of follow up for patients who did not die during that period was 5.2 years (IQR, 4.0-7.4 years).
The 1-year survival rate was 40% (4 of 10) for patients with IIN and 94% (49 of 52) for patients without IIN (P < .001). Seven (70%) of the patients with IIN died during the follow-up period, and all those deaths occurred within the first 2 years after resection, including 3 deaths within the first week: 1 on postoperative day 1, 1 on postoperative day 2, and 1 on postoperative day 7. Of note, all 3 patients who died within the first week had intraoperative notes describing bowel ischemia, which was apparent upon laparotomy, indicating that the ischemia preceded the surgery and was not a procedural complication.
Having IIN was associated with a 4.3-fold increased risk of death (95% confidence interval, 1.75-10.56; P = .001; Figure 2). After controlling for age, advanced stage (stage III or IV), tumor grade, and synchronous carcinoma, IIN showed a trend toward significance with a 2.31-fold increased risk of death (95% confidence interval, 0.856.27; P = .10).
The principal finding of our study is that JINET-induced IIN was associated with early mortality and showed a trend toward a significant association with mortality after controlling for age and other important pathologic factors.
Our study has 2 main strengths. One is the relatively large number of JINET resections with IIN. Another is the comprehensive pathologic assessment of the JINETs with and without IIN, which allowed us to assess the independent contribution of IIN to patient mortality.
Three patients with IIN died during the first postoperative week. Often, oncologic studies with survival data exclude deaths occurring within a short time (eg, 1 month) following surgery because the deaths are attributed to complications of surgery, rather than to the true biologic aggressiveness of the tumor. However, we chose to include them in the survival analysis because, for all 3 patients, the intra-operative notes described ischemic bowel, which was immediately apparent upon laparotomy, indicating that intestinal ischemia was not a complication of surgery. Therefore, we considered it more likely that these patients died as a result of tumor-induced IIN and not as a result of surgery, and for this reason we included them in the survival analysis.
One potential weakness of the study is that, for several cases, including 4 of the cases with IIN, tumor was identified within the small bowel mesentery but not in the overlying small bowel. All of these tumors could still be assigned an American Joint Committee on Cancer stage because they showed lymph node and/or distant metastases. As mentioned in the "Results," none of those 4 patients had a documented primary neuroendocrine tumor of another organ in the electronic medical record or pathology database either before or after their surgery. Considering that even JINETs smaller than 1 cm can metastasize, (25) it is possible that the primary tumors were missed intraoperatively by the surgeon. We considered these tumors to most likely represent mesenteric involvement by a primary JINET, but technically the origin was indeterminate because the primary tumor was not identified.
All JINETs have unique features that may contribute to IIN. They often spread to the mesentery and form bulky masses; thus, their growth is often close to the mesenteric vasculature. In addition, they elicit abundant stromal fibrosis by secretion of growth factors, (26) which can cause distortion of the mesentery and kinking of the blood vessels. The JINETs also produce serotonin, which is known to have a role in platelet aggregation and vasoconstriction, (27) among other roles. Therefore, the effects of JINET-derived serotonin and growth factors could have a role in the development of IIN.
Considering the frequent production of serotonin by JINETs, we attempted to compare serotonin expression and levels of serum serotonin and urine 5-HIAA between cases with and without IIN. We did not detect differences in serotonin expression between cases with and without IIN because all tested tumors were diffusely positive for serotonin. We could not reliably compare the levels of serum serotonin or 5-HIAA between the 2 groups because only 2 of the 10 cases with IIN (20%) had serum serotonin and/or urine 5-HIAA testing available. Thus, we were unable to definitively implicate serotonin in the pathogenesis of IIN but postulate that it may have a role, particularly in older patients with preexisting vascular disease.
Another mechanism by which JINETs may induce IIN is mesenteric vascular elastosis, which is frequently seen in association with JINETs and which was apparent to some degree in most of our cases with or without IIN. Mesenteric vascular elastosis is characterized by thick deposition of elastic tissue in the adventitia of mesenteric arteries and veins. (28) Some authors have suggested that mesenteric vascular elastosis associated with JINETs can cause IIN. (12, 13, 17, 28)
Finally, it is conceivable that decreased blood flow from preexisting cardiovascular disease, such as mesenteric arterial atherosclerosis, and decreased cardiac function could predispose to JINET-induced IIN. Although no significant differences in hypertension, dyslipidemia, diabetes, and smoking status were found between patients with and without IIN, age itself is a risk factor for atherosclerosis. The older average age of the patients with IIN suggests that these patients may have had a higher burden of atherosclerotic disease.
Regarding the overall frequency of JINETs presenting with IIN, the 10 cases with IIN in our study were identified by searching our entire pathology database, which included our main academic hospital (Presbyterian University Hospital) and affiliated community hospitals, for a 13.5-year period. In contrast, the control group of 52 cases without IIN was identified from our main academic hospital alone during a 10-year period. Furthermore, a number of cases without IIN that were in our pathology database were excluded because slides were not available. By factoring in these considerations, the overall frequency at which initial resections of JINETs show IIN is approximately 5% at our institution. A search of our pathology database showed that 3645 small-intestinal resections showed ischemic changes from January 1, 2001, to June 30, 2014. Thus, initial resections of JINETs with IIN represent approximately 0.3% of the total number of small-intestinal resections with ischemic changes at our institution.
In summary, our study highlights a pathologic feature associated with JINETs, which, when present, portends a significantly worse overall survival.
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Michael Landau, MD; Stephen Wisniewski, PhD; Jon Davison, MD
Accepted for publication August 10, 2015.
From the Department of Pathology, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania (Drs Landau and Davison); and the Department of Epidemiology, University of Pittsburgh, Graduate School of Public Health, Pittsburgh (Dr Wisniewski).
The authors have no relevant financial interest in the products or companies described in this article.
Reprints: Michael Landau, MD, Department of Pathology, University of Pittsburgh Medical Center, Presbyterian Hospital, A616, 200 Lothrop St, Pittsburgh, PA 15217 (email: email@example.com).
Caption: Figure 1. Two cases of jejunoileal neuroendocrine tumor (A-C and D-F) with mesenteric involvement and intestinal ischemic necrosis. A, Mesenteric involvement by neuroendocrine tumor with entrapment of mesenteric blood vessels (see inset) and small intestinal mucosal necrosis (right). B, Ischemic small intestine with ulceration, mucosal necrosis, and hemorrhage. C, Mesenteric neuroendocrine tumor with calcification and ossification. D, Mesenteric involvement by neuroendocrine tumor and small intestine with dusky and edematous appearance. E, Small-intestinal mucosa with attenuated ("withered") epithelium (right) adjacent to mucosal necrosis (left). F, Neuroendocrine tumor with anastomosing nests of monotonous cells, stromal fibrosis, and perineural invasion (hematoxylin-eosin, original magnifications X20 [B] and X100 [C, E, and F]).
Caption: Figure 2. Kaplan-Meier curves showing overall survival of patients with jejunoileal neuroendocrine tumors with and without intestinal ischemic necrosis (IIN) (P =.002, log rank). The dashed line represents cases with IIN, and the solid line represents cases without IIN.
Please Note: Illustration(s) are not available due to copyright restrictions.
Clinicopathologic Features of 62 Patients With Jejunoileal Neuroendocrine Tumor Stratified by Intestinal Ischemic Necrosis (IIN) All Cases, n = 62 Age, y (IQR) 66.8 (55.0-73.2) Sex, M, No. (%) 33 (53.2) Hypertension, No. (%) 40 (64.5) Dyslipidemia, No. (%) 24 (38.7) Diabetes, No. (%) 9 (14.5) Tobacco use, No. (%) 35 (56.5) Tumor size, cm (range) 1.7 (1.0-2.4) Grade, No. (%) 1 55 (88.7) 2 7 (11.3) Vascular invasion, No. (%) 53 (85.5) Perineural invasion, No. (%) 31 (50.0) Multifocal tumors, No. (%) 25 (40.3) Mesenteric tumor deposits, 40 (64.5) No. (%) Synchronous carcinoma, 4 (6.5) No. (%) Stage, No. (%) I 2 (3.2) IIA 3 (4.8) IIB 6 (9.7) IIIA 2 (3.2) IIIB 31 (50.0) IV 18 (29.0) Stage group, No. (%) I or II 11 (17.7) III or IV 51 (82.3) Primary location, No. (%) Jejunoileal 56 (90.3) Indeterminate 6 (9.7) Cases With IIN, n = 10 Age, y (IQR) 83.0 (68.9-89.3) Sex, M, No. (%) 6 (60.0) Hypertension, No. (%) 7 (70.0) Dyslipidemia, No. (%) 3 (30.0) Diabetes, No. (%) 3 (30.0) Tobacco use, No. (%) 7 (70.0) Tumor size, cm (range) 1.4 (1.0-2.3) Grade, No. (%) 1 8 (80.0) 2 2 (20.0) Vascular invasion, No. (%) 8 (80.0) Perineural invasion, No. (%) 3 (30.0) Multifocal tumors, No. (%) 2 (20.0) Mesenteric tumor deposits, 8 (80.0) No. (%) Synchronous carcinoma, 1 (10.0) No. (%) Stage, No. (%) I 0 (0) IIA 1 (10.0) IIB 1 (10.0) IIIA 0 (0) IIIB 6 (60.0) IV 2 (20.0) Stage group, No. (%) I or II 2 (20.0) III or IV 8 (80.0) Primary location, No. (%) Jejunoileal 6 (60.0) Indeterminate 4 (40.0) Cases Without P Value IIN, n = 52 Age, y (IQR) 65.5 (53.2-71.1) .001 Sex, M, No. (%) 27 (51.9) .74 Hypertension, No. (%) 33 (63.5) >.99 Dyslipidemia, No. (%) 21 (40.4) .73 Diabetes, No. (%) 6 (11.5) .15 Tobacco use, No. (%) 28 (53.8) .49 Tumor size, cm (range) 1.9 (1.0-1.9) .72 Grade, No. (%) .31 1 47 (90.4) 2 5 (9.6) Vascular invasion, No. (%) 45 (86.5) .63 Perineural invasion, No. (%) 28 (53.8) .30 Multifocal tumors, No. (%) 23 (44.2) .18 Mesenteric tumor deposits, 32 (61.5) .47 No. (%) Synchronous carcinoma, 3 (5.8) No. (%) Stage, No. (%) .83 I 2 (3.8) IIA 2 (3.8) IIB 5 (9.6) IIIA 2 (3.8) IIIB 25 (48.1) IV 16 (30.8) Stage group, No. (%) >.99 I or II 9 (17.3) III or IV 43 (82.7) Primary location, No. (%) .005 Jejunoileal 50 (96.2) Indeterminate 2 (3.8) Abbreviation: IQR, interquartile range.
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|Title Annotation:||Original Articles|
|Author:||Landau, Michael; Wisniewski, Stephen; Davison, Jon|
|Publication:||Archives of Pathology & Laboratory Medicine|
|Date:||May 1, 2016|
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