Gastrointestinal stromal tumours (GIST) are the most common type of mesenchymal tumours found in the gastrointestinal tract (1). For years, GISTs have been defined as smooth gastrointestinal muscle tumors and have been called under various names and often misdiagnosed as leiomyomas, schwannomas and sarcomas (2). Currently, the distinctive feature of GIST is the mutation in the c-kit protooncogene leading to gain-of-function and subsequent cell proliferation (3-5). GISTs are rare, with relative annual incidence of 14.5 per million and prevalence of 129 per million (6). GIST may occur anywhere in the digestive tract, but are more frequently located in the stomach (60–70%) and midgut (25%) and less often in colon and rectum (5–10%) (7). Extravisceral GIST occurs in less than 10% of patients, most frequently in mesentery, intrabdominal, pelvis and retroperitoneal space (7). Duodenal GISTs (dGIST) represent only 4–5% of all GISTs, but accounted for 6–21% of surgical resected ones (8-10). The complex anatomy of the duodeno-pancreatic region can make their diagnosis and treatment extremely challenging. Anatomical closeness to noble structures (i.e., to the head of the pancreas, kidney and biliary structures) can lead to misdiagnosis and inappropriate management (11). Additionally, several factors complicate the management of dGISTs such as the relative lack of experience, the ambiguous clinical manifestations that often mimic a wide range of clinical conditions, the anatomical complexity and the lack of consensus on treatment.
The publication of solid research findings (3,12) that characterize the pathogenesis and histology of GIST have created a discontinuity in the terminology used to describe this entity. Due to the unclear terminology of scientific literature published before 2000, it is very difficult to analyse and interpret the previous reports, but the researches published since then has significantly increased (4).
Herein, we aimed to perform a state-of-the-art review of available English literature to improve the understanding of dGIST and to outline the best options for surgical treatment.
Comprehensive research has been conducted to identify all clinical studies that report the occurrence of dGIST. The search was carried out on the electronic databases MEDLINE, Scopus, EMBASE and Cochrane Libraries. The research strategy included all studies published after 2000 and focused on relevant articles using the following keywords: “gist”, “duodenal”, “stromal gastrointestinal cancer”, “surgery” and associated free terms. No language restrictions have been imposed to limit results.
Studies were selected for consideration in this analysis provided they reported cases with dGIST. In order to select only those studies that certainly dealt with dGIST, only those studies in which the immunohistochemical analysis of the cKIT was reported and were positive were included.
The inclusion criteria were used to examine the title, abstracts and full texts of the studies obtained from the research results. Two reviewers independently examined all citations on titles and abstracts produced by the search strategy and retrieved all potentially relevant reports. Two other independent readers then screened the full text of the studies to identify the entries that met the inclusion criteria. Any disagreements have been resolved by consensus. Differences in data extraction have been resolved by consensus, with references to the original article.
The initial search produced 185 potentially relevant articles (Figure 1) (Tables 1,2,3,4,5) that were suitable for subsequent screening. The titles and abstracts of these articles were screened to determine the relevance and eligibility for inclusion—53 papers were excluded for different reasons: non-duodenal GISTs, no surgery type reported, and no patient data reported leaving 132 studies for inclusion in the present review. Of them, 46 studies did not report the data about cKIT and were excluded thus leaving 86 studies included in the analysis. The patients excluded for non-duodenal GIST were 7,142, those excluded for no surgery type reported were 1,039 and 1,002 patients were excluded because of no cKIT reported. The characteristics of the included studies have been summarized in Tables 1,2,3,4,5. All studies were published between 2001 and 2017. Eighty-two papers with 539 cases reported data on the signs and symptoms at the time of hospital admission, whereas in four studies there were no data. Upon admission, the most common symptoms were GI bleeding and melena, followed by abdominal pain and discomfort. Symptoms of fatigue, fainting, vomiting, and ankle edema were also reported but occurred far less frequently. In the majority of cases dGISTs were located in the second portion of the duodenum. Several cases reported dGIST localization in both the second and third portions of the duodenum.
The included studies summoned a total of 549 patients with dGIST—27 patients treated with pancreatoduodenectomy (PD) (Table 1), 96 patients treated with local resection (Table 2), and 426 patients treated with either PD or segmental/wedge resections (Tables 3,4,5).
Among patients treated with PD (Tables 1,6), the majority were females (n=14, 52%; males: n=11, 41%; not reported: n=2, 7%), with a median age of 50 years (Table 1). Most patients presented with symptoms of anemia (n=11, 40%), melena (n=8, 27%), fatigue (n=4, 15%), and weight loss (n=4, 15%). However, in 3 patients the information was not reported. For most patients, the dGIST were located in the second portion of the duodenum (first: n=1, 4%; second: n=19, 70%; third: n=1, 4%; not reported: n=5, 18%) (Table 1). Four studies (13,19,21,25) reported dGIST tumors that extended beyond the duodenum. All PDs were performed by open procedure. While some patients received imatinib as a neoadjuvant treatment (n=7, 26%), a greater proportion received the treatment post-operatively (n=9, 33%) (Table 6). For most patients, no long term survival data were reported (n=21, 75%). Notably, the PD studies reported histological information on KIT, DOG1, or CD34.
Among patients treated with local resection (Tables 2,7) there was a slight preponderance of males (n=51, 53%; females: n=45, 47%) with a median age of 57.3 years (Table 2). Upon admission, patients most commonly presented with nausea (n=1, 1%), abdominal pain (n=8, 8%), undetermined pain (n=18, 19%), melena (n=20, 21%), dizziness (n=3, 3%), and/or GI bleeding (n=14, 16%). No data on presenting signs and symptoms was available for 7 patients (Table 2).
Within this group, most dGIST were located in the second and third portions of the duodenum (first: n=16, 17%; second: n=29, 30%, third: n=32, 33%; fourth: n=12, 12%; not reported: n=7, 7%), with tumors extending beyond the duodenum in four cases. For all local resections reported, surgical access was predominantly achieved by either open (n=89, 92%) or laparoscopic procedure (n=5, 5%). Patients treated with a local resection received less neoadjuvant (n=13, 13%) and post-operative (n=22, 23%) treatment with imatinib (Table 8), as compared to patients treated with a pancreaticoduodenectomy (Table 6), and four patients underwent multiple visceral resections.
Of the patients whose histological or molecular data were provided (Table 7), most tested positive for cKIT (n=85, 46%), CD34 (n=48, 26%) and DOG1 (n=20, 11%). A minority of patients tested positive for either smooth muscle actin (n=5, 3%), S100 (n=7, 4%) or desmin (n=1, 1%).
Four hundred twenty-six patients were treated with either PD or segmental/wedge resections. Within this group, there was preponderance of males (n=218, 51%) vs. females (n=183, 43%), not reported (n=25, 6%). At the time of admission, patients frequently presented with symptoms of bleeding (n=137, 32%), abdominal pain or discomfort (n=258, 60%) and melena (n=235, 55%). Five patients were asymptomatic (Tables 3,4,5). dGISTs were predominantly located in the second and third portions of the duodenum in this group (first: n=47, 11%; second: n=164, 38%; third: n=83, 19%; fourth: n=41, 9%). In many cases the tumors extended into multiple portions of the duodenum simultaneously. All of these studies reported data on cKIT and several studies reported data on CD34 and DOG1.
Within this cohort the most common type of surgical treatment was local resection (n=151, 35%), followed by PD (n=92, 21%) and segmental (n=97, 15%) or wedge resections (n=32, 7%). No data on the type of surgical treatment were available for 51 patients. Within this group of patients, both neoadjuvant and post-operative treatment with imatinib were rarely applied (neoadjuvant treatment: n=23, 5%; adjuvant treatment: n=30, 7%). Most patients received no imatinib treatment prior to surgery (n=160, 38%) or post-operatively (n=149, 35%).
There are three main surgical options: pancreatoduodenectomy (PD) (10,24), wedge resection (40,60,63,97) and segmental resection. PD is indicated in the cases with involvement of major duodenal papilla, pancreas or pancreatic duodenal wall and is required in 20–40%. Based on the literature, the following options for surgical reconstruction according to the localization and extent of duodenal resection are available:
First and second duodenal portions:
- wedge resection with primary transverse closure of duodenum (39) or retrocolic Roux-en-Y loop to cover a large defect (97);
- segmental resection, closure of distal stump and duodenojejunostomy by retrocolic Roux-en-Y loop (99);
- segmental resection with antrectomy with side-to-side posterior or Roux-en-Y gastrojejunostomy (55,59);
- subtotal resection with side-to-side duodenojejunostomy (100);
- sleeve resection with gastroduodenostomy (the case with situs inversus totalis) (82);
- ampullectomy with sphincteroplasty (55).
Third and fourth duodenal portions:
- segmental resection with closure of distal stump and side-to-side (93) or end-to-side/end-to-end duodenojejunostomy (62,92);
- segmental resection, end-to-end anastomosis, pylorus closure and gastroenterostomy with/without feeding jejunostomy (77);
- segmental resection, closure of distal stump near leg. Treitz and end-to-side duodenojejunostomy with first jejunal loop (99);
- segmental resection with end-to-side or end-to-end duodenojejunostomy to the left of the superior mesenteric vessels (66,72,75) segmental resection, closure of distal stump on the right of superior mesenteric vessels, papilloplasty, end-to-side duodenojejunostomy, transcystic tube and transjejunal tubes draining the main pancreatic duct and decompressing duodenum (38);
- segmental resection of third and fourth part of duodenum, closure of second portion stump and side-to-end duodenojejunostomy (49);
Duodenal GIST is typically seen in individuals between the ages of 60–70 years old. There were few papers reporting an occurrence of dGIST in children and teenagers, all of which manifested with severe bleeding (80,97,101). The median age of the patients with dGIST is 56 years with a slight preponderance of males (54% vs. 46%) (1,5).
Most cases are sporadic, whereas familial clustering is reported in only 1.5–4% of the cases (69,102). Familial GIST is an autosomal dominant condition caused by germline mutations of cKIT or PDGFRA and manifests at earlier age. GIST may be part of Carney’s triad (gastric GIST, paraganglioma, and pulmonary chondroma) or Carney-Stathakis syndrome, which are caused by germline mutations in SDH (89). It is a well-known fact that von Recklinghausen neurofibromatosis type 1 (NF 1) is associated with an increased risk for GIST. GISTs in NF 1 occur in 6–7%, affect duodenum in 22–31%, and tend to be smaller, multiple and with lower mitotic count and occur at younger age (89,103,104). Hakozaki et al. described a case of dGIST and rectal cancer in a patient with NF 1 (87). Malignant carcinoid of ampulla Vateri and bilateral feochromocitoma have been also described with low responses to imatinib (105). Few papers reported extremely rare combination with pancreatic neuroendocrine neoplasia (64) and somatostatinoma in NF 1 (35) and Brunner’s gland cysts (78).
Most dGISTs develop in the second (59–63%) and third portion (22%) of duodenum (55,106), whereas the first and forth are less frequently affected. GIST of ampulla Vateri is extremely rare and according to the review of Kobayashi et al. only 12 cases have been described till 2014 (30). In all cases pain, jaundice and melena were the most frequent symptoms. Despite its rarity, this localization requires meticulous differential diagnosis (neuroendocrine tumors, carcinoma, paraganglioma) because usually the radical treatment requires PD (107).
Histopathology and molecular characteristics
Histologically, dGISTs do not differ from other GIST localizations. The most frequently reported pattern was spindle cell (67%), but epithelioid (11%), pleomorphic, mixed (22%), hemangioma-like or hemangiopericytoma-like patterns can also be seen (9,13,55,93,99,101,108-114). Immunohistochemistry staining of the specimens revealed the following distribution of the markers: CD117 (c-kit) (92–100%), and less frequently CD34 (54–70%), smooth muscle actin (20–30%), S-100 protein (10–20%), and neurofilament 68 (14%), DOG1 protein (6%) (9,12,65,94,115). Lack of DOG-1 expression was associated with poor prognosis in a recent study with 332 patients (93). The differential diagnosis includes fibromatosis (110), schwannomas, leiomyomas, inflammatory fibroid tumors, solitary fibrous tumor, mesenteric sclerosing fibrotic lesions, sarcomas, metastasis from malignant melanoma, glomus tumors, paragangliomas, ectopic pancreas (65,92,98).
At the molecular level, approximately 96% of GISTs have cKIT (CD117) mutation, typically in exon 11, but mutations in exons 9, 13, and 17 may also occur (101). Exon 11 mutations carry a better prognosis and respond well to standard dose (400 mg/dayly) of imatinib (116). Some authors reported worse outcomes in exon 9 mutation (102). Approximately 8% of the cases have PDGRFA mutation, which is mutually exclusive with cKIT but is associated with longer relapse-free interval (43,59,116). Some PDGFRA are resistant to imatinib (65). The so-called wild type is observed in 10–15% of the cases and in 90% of children. It is caused by germline mutations in BRAF V600E, RAS family or succinate dehydrogenase subunits (SDH A-D). GISTs in NF1 are usually wild type with possible implication of RAS-MAPK pathway (104,117-119). This subset of GISTs is relatively resistant to the treatment with imatinib. Further large studies are needed to elucidate the individual prognosis according to the mutational status.
Approximately 70% of the cases manifest with symptoms, while 21% are found incidentally and 10% on autopsy (120). Our analysis revealed that in contrast to the other localizations the most frequent manifestation of dGIST is the upper gastrointestinal bleeding, which is in accordance with the literature (21,74,121). Constant/intermittent dull pain/discomfort or abdominal palpable mass are less frequent initial symptoms (10,32,71). Rarely, however, dGISTs may have various initial presentations leading to misdiagnosis. Millonig et al. reported extrahepatic cholestasis and Takotsudo cardiomyopathy in a patient with undiagnosed NF1 (122). The extremely rare dGIST of ampulla Vateri can also manifest with jaundice (30). In certain cases, extramural growth may mimic pancreatic head tumor (26,44,84,97), large duodenal cyst (61), bleeding or uncomplicated duodenal diverticula (33, 46). Wall et al. reported a rare case with duodenal-jejunal intussusception (23). Lin et al. described two cases with bleeding small dGISTs (<2 cm) initially misdiagnosed as hemobilia (123). A case mimicking refractory peptic ulcer treated for 8 years was also described (76), even hypercalcemia due to elevated serum calcitriol in metastatic disease as well (124).
The recurrence risk and survival outcomes for dGIST are difficult to be determined based solely on the histopathological characteristics. Multiple factors have been proposed as predictive of survival outcomes, including tumor location and size, mitotic rate, kinase mutational status, and incidence of tumor rupture. However, tumor size and mitotic rate are the two most widely accepted risk indicators (125,126).
The Fletcher’s and subsequently the modified National Institute of Health classification are the most popular risk classifications (95). Miettinen et al., based on the follow-up of 140 cases with dGIST, proposed a distinct risk stratification of dGIST in which group 1 (<2 cm and <5 mitoses) is considered benign, whereas group 6 (>5 cm and >5 mitoses) carries an extremely poor prognosis with 86% mortality (18/21) within 21 months (9). The overall mortality in their series was 34%. This classification was externally validated by the French Sarcoma group in a series with 114 patients (119). The overall doubling time for dGIST is 17 months in comparison to leiomyoma (231 months). According to the risk group the doubling time is 24, 17 and 4 months in low, intermediate and high risk dGISTs (115).
Generally, there are contradictory results in the literature regarding the prognosis of dGIST in comparison to the other localizations. Certain authors reported worse outcome in comparison to small bowel and gastric GISTs (43), whereas others reported similar prognosis with small bowel localization. The more recent, population-based study of Guller et al. reported similar survival in gastric, duodenal and small bowel GISTs in contrast to colonic and extravisceral localizations (127). This finding was corroborated after subgroup analysis of two periods (1998–2004 vs. 2005–2011) thus eliminating a possible cofounding factor associated with the implementation of imatinib therapy.
Although it may be straightforward in most cases, certain considerations should be kept in mind due to their occasionally misleading manifestation (128). Differential diagnosis includes adenocarcinoma, endocrine tumors, benign tumors and rare entities such as intrabdominal fibromatosis (110), ectopic pancreas (129), and Brunner’s gland cysts (78).
Because most of dGISTs present with acute bleeding or chronic anemia endoscopic evaluation of upper gastrointestinal tract should be the first step (101). It allows for biopsy and can be also therapeutic. In case of failure, transarterial embolization is a method of choice, either as definitive hemostasis or as a bridging procedure before surgical intervention (39). Occasionally, endoscopy may be misleading, especially in small intramural lesions without mucosal involvement (ulceration or central depression) or located near the papilla Vateri. In such cases of diagnostic uncertainty, endoscopic ultrasound (EUS) is an invaluable modality. Usually dGISTs appears as hypoechoic and well-vascularized lesion. Two small series reported a significant correlation between the presence of intratumoral vessels on contrast-enhanced or color Doppler EUS and the malignant potential of dGISTs (130,131). EUS provides a precise evaluation of the size, border, layer of origin, echogenicity and heterogeneity of the lesions thus facilitating the differential diagnosis (lipomas, hemangiomas, ectopic pancreas, and cysts) and decision-making process (112). Additionally, EUS allows also fine needle or trucut biopsy with 100% specificity and 84% sensitivity (92,112,131,132). Percutaneous biopsy should be avoided when possible because of the risk for tumor spillage and dissemination.
Abdominal US is useful screening tool in the cases with dull pain in upper abdomen, but computed tomography (CT) and magnetic resonance imaging (MRI) are mandatory to make an exact staging and preoperative planning of surgery (107,113). On CT dGISTs appear as well-defined, heterogeneously enhanced, hypervascular mass with prominent feeding arteries and intra- or extramural growth (107,114). In contrast, the ectopic pancreas has intraluminal growth and ill-defined border with enhancement of the overlying mucosa (129). The periampullary pancreatic cancer is usually hypodense on arterial phase with concomitant pancreatic duct dilatation, periampullary neuroendocrine tumors reveal hypervascular enhancement, calcifications, lack of ductal obstruction, central necrosis and cystic degeneration, whereas solid periampullary tumors demonstrate heterogeneous hypoenhancement in both phases (114). Fluorodeoxyglucose positron emission tomography (FDG-PET) is not routine tool but can be useful to monitor the effect from imatinib treatment and follow-up (133,134).
The ESMO guideline suggests that tumors under 2 cm has low aggressive behaviour and therefore could be followed annually by endoscopic ultrasound, “although an evidence-based optimal surveillance policy is lacking” (109). In contrast to the other localizations, in dGIST there is no uniformly adopted surgical strategy because of the low incidence, lack of enough experience, and the complex anatomy of the duodenum. Therefore, individually tailored surgical approach is recommended. In fact, there are three main surgical options: pancreatoduodenectomy (PD), wedge resection and segmental resection.
PD is indicated in the cases with involvement of major duodenal papilla, pancreas or pancreatic duodenal wall and is required in 20–40% (101,135). In some cases, it can be performed successfully in emergency setting due to life-threatening bleeding (10,24,111) even with second-stage pancreatojejunostomy (17). Tien et al. found that size >5 cm and preoperative diagnosis of dGIST were more frequently treated by PD (89). In another series, the patients with PD had larger tumor size and higher mitotic count (118). A recent meta-analysis of seven comparative studies confirmed categorically the above-mentioned findings (89).
Imatinib mesylate have played a key role as a neoadjuvant therapy in the management of GISTs (21,122). In locally advanced disease neoadjuvant imatinib may downstage the tumor to allow R0 resection or even an organ preserving intervention (11,122,136-138) despite the risk of bleeding (111). Ludvigsen et al. reported a successful PD en-block with right kidney and suprarenal gland (19). Fukuyama et al. reported even avoidance of PD after downstaging neoadjuvant therapy with imatinib (67). Recently, successful organ-preserving duodenectomies after neoadjuvant therapy in 9 of 10 cases was reported (92) similarly to other authors (82).
PD is, however, burdened by significant morbidity and longer hospital stay in comparison to local resection, probably due to the “soft” pancreas and small caliber of pancreatic duct (116,118,119). Moreover, several studies reported no significant difference in recurrence rate and disease specific survival between limited resection and pancreatoduodenectomy (55,97,101,104), which is categorically supported from the meta-analysis of Chok et al. (122) and the experience of the French Sarcoma Group (119).
R0 resection with 1–2 cm clear margin is sufficient treatment and lymph node dissection is not recommended due to the low incidence of lymphatic metastases (102). There are several options for local resection and surgical reconstruction according to the localization of the tumour. The rupture of GIST during the surgery should be avoided because is associated with nearly 100% risk for recurrence (125). Therefore, the good knowledge of anatomy, gentle handling of the tissues, and careful dissection of duodenal wall from the inferior border of pancreas, meticulous hemostasis and knowing of the possible options for duodenal reconstruction are mandatory for successful outcomes.
Laparoscopic resection is feasible and safe with reported subtotal resection with side-to-side duodenojejunostomy (100) and wedge resection (85,139). Tanaka et al. reported eighth cases successful segmental resections of duodenojejunal junction with side-to-side anastomosis comparable with 11 open procedures (140). Some authors reported laparoscopically assisted endoscopic submucosal resection of 20 mm GIST located in the third portion (57).
Although in most cases wedge and segmental resections could be relatively straightforward, severe complications may occur such as acute pancreatitis, pancreatic fistula, significant blood loss and anastomotic stenosis (117,118). Delayed gastric emptying treating with gastrojejunostomy and the fearsome anastomotic failure necessitated secondary PD (101) and injury of the mesenteric root managed by total enterectomy have been described in the literature (132). The pitfalls in segmental resections are associated with the superior mesenteric vessels lying on the third portion, adjacent pancreas and the common blood supply, necessity to preserve ampulla Vateri (107,117).
dGIST is a very rare entity. It may be asymptomatic or may involve symptoms of upper GI bleeding and abdominal pain at presentation. Because of the misleading clinical presentation the differential diagnosis may be difficult. Gastrointestinal endoscopy is the most common initial diagnostic procedure while abdominal and thoracic CT scan are mandatory for accurate oncologic staging and surgical planning.
Tumours smaller than 2 cm have a low biological aggressiveness and can be followed annually by endoscopic ultrasound; the biggest tumors should undergo radical surgery (R0) (144). In contrast to the other localizations, dGIST have no uniformly adopted surgical strategy because of the low incidence, lack of experience, and complex anatomy of the duodeno-pancreatic region. Therefore, individually tailored surgical approach is recommended. R0 resection with 1–2 cm clear margin is sufficient treatment and lymph node dissection is not recommended due to the low incidence of lymphatic metastases. Tumor rupture should be avoided.
Conflicts of Interest: The authors have no conflicts of interest to declare.
Ethical Statement: The review of literature does not need evaluation by Ethical committee and by Institutional/Regional/National Ethics committees/boards.
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Cite this article as: Popivanov G, Tabakov M, Mantese G, Cirocchi R, Piccinini I, D’Andrea V, Covarelli P, Boselli C, Barberini F, Tabola R, Pietro U, Cavaliere D. Surgical treatment of gastrointestinal stromal tumors of the duodenum: a literature review. Transl Gastroenterol Hepatol 2018;3:71.