Laparoscopic resection of duodenal carcinoid: A feasible method: Single institute case series

Abstract

Background:

Duodenal carcinoids (neuroendocrine tumour) are rare tumour, but recently, increase in incidence has been noted. Various techniques for excision of tumour have been described in literature, but very few case reports and case series have mentioned about laparoscopic management of carcinoid tumour. We describe a case series of seven cases of duodenal non-periampullary carcinoids which was managed by laparoscopic method.

Aims:

The aim of the study was to check feasibility of laparoscopic management of duodenal carcinoid and technique of surgery.

Settings and Design:

This study design was a case series and prospective data were retrospectively collected.

Materials and Methods:

A total of 7 patients were operated for carcinoid tumour of duodenum mainly involving first part by laparoscopic method from February 2016 to January 2017. All patients were followed up for minimum 1-year period and various pre-operative, intra-operative findings and post-operative outcome were noted.

Results:

Out of seven patients, 6 patient were managed by laparoscopic duodenotomy and transduodenal excision whereas one patient required duodenectomy of first part. Mean operative time was 99 min, mean intraoperative blood loss was 55.7, mean hospital stay was 99.7 and no recurrence in a 1-year follow-up.

Conclusions:

Laparoscopic excision of carcinoid tumour is safe, technically reproducible and feasible method.

INTRODUCTION

Carcinoid the term came from 'karzinoide' coined by Oberndorfer in 1907.[1] They are usually slow-growing tumours arising from enterochromaffin-like cells of gastrointestinal (GI) tract. Carcinoids represent the most common neuroendocrine tumour (NET) of GI tract. GI NET has been classified by the WHO in 2000 into well-differentiated NETs, well-differentiated neuroendocrine carcinoma and poorly differentiated carcinomas based on their degree of differentiation.[2] Grading of GI tract NET has been proposed by the WHO in 2010 based on mitotic index and Ki67 proliferation index regardless of tumour size, extent or location, described in Table 1.[3] Incidence of primary carcinoid of duodenum accounts for only 2.6% of all NETs in the United States.[4] Recently, increasing in the incidence of duodenal carcinoid may be the result of generalised use of gastroduodenoscopy.[5,6] More than 90% of duodenal NETs arise from first and second part of duodenum and its incidence decreases distally in duodenum.[7,8,9,10] Mean age of presentation is the sixth decade with slightly male preponderance. We present a case series of seven cases of carcinoid tumour involving first and second part of duodenum treated by laparoscopic management in our unit. The aim of the present study was to ascertain the feasibility of laparoscopic management of duodenal carcinoid, validation of our surgical technique and elucidating their histopathological and immuno-histochemical (IHC) attributes.

Table 1.

WHO 2010 classification of neuroendocrine tumours

Grade	Mitotic count/10 HPF	Ki-67 labeling index (%)
Grade 1	<2	<3
Grade 2	2-20	3-20
Grade 3	>20	>20

HPF: High power field

MATERIALS AND METHODS

We are presenting a case series of seven patients treated in our unit; patients data collected from hospital records during the period from February 2016 to January 2017. In the present study, clinical presentation varied with non-specific symptoms such as dyspepsia, bloating and other reflux symptoms to GI haemorrhage, gastric outlet obstruction and carcinoid syndrome. Oesophagogastroduodenoscopy (OGD scopy) scopy was done in all cases which localised the lesions in duodenum and biopsy was done. OGD scopy findings include a small nodule, nodule with central depression, erosion or ulceration. Histopathological examination and immunohistochemistry (IHC) analysis with chromogranin, synaptophysin and Ki67 confirmed the diagnosis of NET. Contrast-enhanced computed tomography (CECT) abdomen was done to rule out liver metastasis and lymph nodal involvement. Serum chromogranin levels have been checked in two patients with suspicion of carcinoid syndrome.

All patients were managed by laparoscopic surgery. Intraoperatively large tumours were localised by laparoscopic palpation and small tumours were identified after duodenotomy by direct visualisation and detection of tumour corresponding to OGD scopy and CT findings. We have studied parameters such as clinical presentation, association of carcinoid syndrome, operative time, intraoperative blood loss, conversion, post-operative complications such as bleeding, resection margin and hospital stay. All patients followed up minimum for 1-year period.

Operative techniques

All patients were placed in supine position. Surgeon and first assistant showing camera stands to left of the patient and second assistant stands on the right side. Position of the monitor was above the right shoulder of the patient like in laparoscopic cholecystectomy. Ports' placement was done as shown in picture 1 [Figure 1]. One 10 mm supraumbilical port, two right hypochondrial ports – left (retraction port) and right (working hand), 12 mm epigastric port just left to midline and inferior to subcostal region. After localisation of tumour, kocherisation of the first part of duodenum was done.

Figure 1.

Ports placement

Pyloro-duodenotomy was done along the long axis of duodenum after lifting anterior duodenal wall with two stay sutures. Tumour was identified intraluminally and duodenal wall containing tumour was completely everted with the help of two mucosal stay sutures. Tumour has been resected with Laparoscopic staplers in case 1, 3, 5 and 6 and with harmonic scalpels in case 2 and 4. In case 4, a second nodule was present in second part of duodenum which was excised by submucosal dissection with harmonic scalpel. Pyloro-duodenotomy was closed vertically with V lock suture. In case 6, segmental duodenectomy was done with Laparoscopic stapler in view of small size of tumour and difficult intraoperative localisation. All specimens were retrieved through endobag.

RESULTS

In the present study, patients with duodenal carcinoid include two females and five males. The mean age of presentation was 56.1 years (range 39–67 years). Five patients presented with non-specific symptoms such as dyspepsia, bloating, regurgitation and intermittent abdominal pain. One patient (case 7) presented with fluctuation of blood pressure and high serum chromogranin level of 680. Case 3 presented with features of gastric outlet obstruction, watery diarrhoea with hypokalaemia and hyponatraemia. His serum chromogranin level is 700 and serum serotonin level was within normal limits. He developed hypocalcaemia preoperatively with a serum calcium of 6.4 mg/dl and surgery was done after 2 days after calcium correction and octreotide infusion for 24 h. Case 5 patient presented in casualty with episodes of GI bleed – haematemesis and melaena. In all patients' diagnosis confirmed by OGD scopy, biopsy and IHC except case 2, in which IHC done postoperatively [Figure 2]. Out of seven patients, three had single lesion in the anterior wall of the first part of the duodenum [Figure 3], three patients had two lesions in the first part and one patient (case 4) had one nodule each in the first and second parts of duodenum [Table 2]. Chromogranin positivity ranges from focal to diffuse in all patients. Synaptophysin was positive in all patients except in case 1 and cytokeratin was positive in all cases except in case 5. Ki 67 positivity index was <2 in five patients, <3% in case 7 and <5% in case 5 [Table 2]. CECT abdomen localised the tumour in most of the cases and none of our patient had enlarged lymph nodes or liver metastasis. Tumour size ranges from 2 mm to 3.5 cm. Mean operative time was 99 min (range 80–118 min) and mean intraoperative blood loss was 50.7 ml (range 20–90 ml) [Table 2]. There was no conversion to open procedure. Six patients had uneventful post-operative course and oral feeds started from postoperative day 3 (POD-3). One patient (case 4) had haemorrhagic aspirate of 200 ml in Ryle's tube with episodes of melena probably from stapler site oozing, in this patient Ryles tube removed on POD 4 when aspirate came down to nil and orally allowed. Mean hospital stay was 3.9 days (range 3–5 days) [Table 2].

Figure 2.

Endoscopic view of carcinoid in first part of duodenum

Figure 3.

Contrast-enhanced computed tomography abdomen s/o hyperintense nodule just distal to duodenal bulb in anterior wall of duodenum

Table 2.

Summary of various parameters observed during the study

Intraoperative findings and procedure	Opertive time (min)	Blood loss (ml)	HPE	Resection margin (cm)	Chromogranin	Synaptophysisn	Ki 67 (%)	Cytokeratin	Post -operative stay (days)
Tumour present in anterosuperior margin of duodenum and excised with Endo GIA stapler	85	20	Well-differentiated NET	1	+	-	1-2	+	3
Tumour present in anterio superior margin of duodenum and excised with Endo GIA stapler	80	30	Well-differentiated NET	0.4	+	+	2	+	3
Tumour present in anterior margin of duodenum and excised with Endo GIA stapler	104	50	Well-differentiated NET	0.5	Diffuse +	+	<2	+	5
Tumour present in anterosuperior margin of duodenum and 4 mm tumour at anterior wall. Wedge resection of wall containing large tumour and submucosal excision of small tumour with Ultrasonic shear	96	40	Well-differentiated NET	0.2	Focal +	+	<2	+	4
Tumour present in anteriosuperior margin of duodenum and excised with Endo GIA stapler	90	50	Well-differentiated NET	0.3	+	+	<5	-	4
Excised with Endo GIA stapler	118	90	Well-differentiated NET, 2 lesions 5 mm apart	0.3	+	+	2	+	5
Duodenectomy (first part) with gastrojejunostomy	120	110	Well-differentiated NET	1	+	+	<3	FAINT+	3
Mean	99	55.7							3.9

HPF: High power field, GIA: Laparoscopic stapler, NET: Neuroendocrine tumour

Histopathological analysis showed well-differentiated NET in all cases with negative margin. All patients were followed up for a minimum period of 1 year. OGD scopy done in follow-up showed no recurrence.

DISCUSSION

Duodenal carcinoid is a rare entity which constitutes 2.6% amongst all NET with slow progression and indolent course. Non-ampullary duodenal carcinoids commonly present with abdominal pain, dyspepsia, GE reflux symptoms and GI bleeding.[11,12] In the present case series, common symptoms were dyspepsia and GE reflux, one patient presented with GI bleeding and another patient presented with features of gastric outlet obstruction with carcinoid syndrome.

Surgical treatment modality proposed in literature is still controversial. The ideal treatment remains resection of tumour either by endoscopy or surgical excision.[5,7,13] Tumor <1 cm in diameter, confined to mucosa and submucosa can be treated by endoscopy because they rarely metastasise to regional lymph nodes.[14,15,16,17] Involvement of muscularis propria, size >2 cm and presence of mitotic figures are features associated with increased risk of metastasis as described by Burke et al.[18] Management of tumour of 1–2 cm is controversial. The proposed treatment for duodenal carcinoid of 1–2 cm and when tumour invasion goes beyond the submucosal layer is transduodenal full-thickness resection either by laparotomy or laparoscopy.[5,6,18,19,20]

In our series, three patients presented with <1 cm of duodenal carcinoid tumour. As depth of wall invasion was not assessed preoperatively in these cases and considering a metastatic risk of 3%–10.5%[6] in a tumour size up to 10 mm, we considered laparoscopic resection of duodenal wall containing tumour by Laparoscopic stapler in two cases [Figure 4] and segmental duodenectomy of the first part in one case [Figure 5]. In our study, three patients had tumour size of 2 cm (including two patients which had another small polyps adjacent to larger polyp) which was excised by laparoscopic resection of duodenal wall containing tumour by Laparoscopic stapler in two cases and by ultrasonic shear in one case. One patient with tumour size 3 cm × 3 cm with carcinoid syndrome [Figure 6] has been subjected to laparoscopic excision of duodenal wall containing tumour by laparoscopic stapler blue reload as there was no lymph node involvement or evidence of metastasis in pre-operative imaging.

Figure 4.

Laparoscopic resection of duodenum containing carcinoid tumor by laparoscopic stapler

Figure 5.

Laparoscopic segmental duodenectomy of first part of duodenum

Figure 6.

Discreet small blue cells in submucosa characterizing carcinoid tumor

Laparoscopic local full-thickness resection of the duodenum with or without stapler is easily reproducible and simple method.[15,21,22] In 1997, Van de Walle et al.[23] first reported laparoscopic resection of a large (5 cm diameter) duodenal tumour (they called it a benign stromal tumour). In their procedure, the tumour was dissected using an electrocautery probe; then the tumour was separated from the duodenum using a total of three endo olinear staplers. Since then, several procedures using an endo linear stapler have been reported by other investigators.[14,24,25,26,27,28] Toyonaga et al.[14] used an endo linear stapler for wedge resection of a relatively small carcinoid tumour. Inappropriate resection (i.e., resection with an inappropriate margin or unnecessary resection of the duodenal wall) is a problem when using an endo linear stapler.

Abe et al.[28] studied six patients with non-ampullary duodenal tumours including two carcinoids treated with local full-thickness resection and transduodenal excision by laparotomy for variable size of tumour from 10 to 75 mm. The operative time ranges from 81 to 230 min, with blood loss of 3 ml to 153 ml and hospital stay was minimum 7 days to a maximum of 12 days.

In the present study, all patients with variable size (2–3.5 cm) of carcinoids located mostly in the first part of duodenum have been treated laparoscopically. Mean operative time was 99 min (range 80–118 min) and mean blood loss was 50.7 ml (range 20–90 ml). Hospital stay was 3.9 days (range 3–5 days) which was less with laparoscopic treatment in comparison to local full-thickness resection by laparotomy describe by Abe et al.

CONCLUSIONS

Very few studies have been published till date except some case reports in laparoscopic management of duodenal carcinoid. This is a probably a first case series from Indian subcontinent which is describing a laparoscopic management and its feasibility for duodenal carcinoid.

Laparoscopic surgical technique used in current series by two mucosal sutures to lift complete tumour before excising it helps to get tumour-free margin. This method is easy to replicate and shows feasibility of laparoscopic complete removal of tumour along with adjacent normal mucosa.

Still more number of comparative and meta-analytic studies required in this field to understand and get best outcome.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.