Case Report Open Access
Copyright ©The Author(s) 2024. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Clin Cases. Aug 6, 2024; 12(22): 5217-5224
Published online Aug 6, 2024. doi: 10.12998/wjcc.v12.i22.5217
Goblet cell carcinoid of the appendix: Six case reports
Toshiaki Toshima, Ryo Inada, Shinya Sakamoto, Eri Takeda, Takahiro Yoshioka, Kento Kumon, Naoki Mimura, Nobuo Takata, Motoyasu Tabuchi, Kazuyuki Oishi, Takuji Sato, Kenta Sui, Takehiro Okabayashi, Kazuhide Ozaki, Toshio Nakamura, Yuichi Shibuya, Department of Gastroenterological Surgery, Kochi Health Sciences Center, Kochi 781-8555, Japan
Manabu Matsumoto, Jun Iwata, Department of Diagnostic Pathology, Kochi Health Sciences Center, Kochi 781-8555, Japan
ORCID number: Toshiaki Toshima (0000-0003-0910-1193); Ryo Inada (0000-0002-4452-6480); Shinya Sakamoto (0000-0002-5610-6432); Eri Takeda (0000-0002-5278-7074); Takahiro Yoshioka (0000-0002-4706-5042); Kento Kumon (0000-0001-8098-8263); Naoki Mimura (0009-0003-3750-8166); Nobuo Takata (0000-0003-2115-3770); Motoyasu Tabuchi (0009-0003-4578-7396); Kazuyuki Oishi (0009-0001-9794-7537); Takuji Sato (0000-0001-8356-1062); Kenta Sui (0009-0009-5441-6005); Takehiro Okabayashi (0000-0002-4829-4306); Kazuhide Ozaki (0009-0007-3143-5073); Toshio Nakamura (0009-0002-9554-3878); Yuichi Shibuya (0000-0002-6243-8281); Manabu Matsumoto (0009-0005-9656-164X); Jun Iwata (0009-0001-7471-8336).
Author contributions: Toshima T and Inada R designed study, developed the main conceptual ideas, and wrote the manuscript; Toshima T, Sakamoto S, Takeda E, Yoshioka T, Kumon K, and Mimura N collected the data; Inada R, Oishi K, Sato T, Sui K, Okabayashi T, Ozaki K, Nakamura T, and Shibuya Y aided in interpreting the results; Takata N and Tabuchi M helped with the sentence structure; Matsumoto M and Iwata J reviewed the pathology; All authors have read and approved the final manuscript.
Informed consent statement: All study participants, or their legal guardian, provided informed written consent prior to study enrollment.
Conflict-of-interest statement: The authors declare that they have no conflict of interest to disclose.
CARE Checklist (2016) statement: The authors have read the CARE Checklist (2016), and the manuscript was prepared and revised according to the CARE Checklist (2016).
Open-Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: https://creativecommons.org/Licenses/by-nc/4.0/
Corresponding author: Ryo Inada, MD, PhD, Director, Doctor, Department of Gastrointestinal Surgery, Kochi Health Sciences Center, 2125-1 Ike, Kochi 781-8555, Japan. ryo_inada@hotmail.com
Received: April 11, 2024
Revised: May 21, 2024
Accepted: May 30, 2024
Published online: August 6, 2024
Processing time: 81 Days and 22.4 Hours

Abstract
BACKGROUND

Goblet cell carcinoid (GCC) of the appendix is a rare tumor characterized by neuroendocrine and adenocarcinoma features. Accurate preoperative diagnosis is very difficult, with most patients complaining mainly of abdominal pain. Computed tomography shows swelling of the appendix, so diagnosis is usually made incidentally after appendectomy based on a preoperative diagnosis of appendicitis. Even if a patient undergoes preoperative colonoscopy, accurate endoscopic diagnosis is very difficult because GCC shows a submucosal growth pattern with invasion of the appendiceal wall.

CASE SUMMARY

Between 2017 and 2022, 6 patients with GCC were treated in our hospital. The presenting complaint for 5 of these 6 patients was abdominal pain. All 5 patients underwent appendectomy, including 4 for a preoperative diagnosis of appendicitis and the other for diagnosis and treatment of an appendiceal tumor. The sixth patient presented with vomiting and underwent ileocecal resection for GCC diagnosed from preoperative biopsy. Although 2 patients with GCC underwent colonoscopy, no neoplastic changes were identified. Two of the six patients showed lymph node metastasis on pathological examination. As of the last follow-up (median: 15 mo), all cases remained alive without recurrence.

CONCLUSION

As preoperative diagnosis of GCC is difficult, this possibility must be considered during surgical treatments for presumptive appendicitis.

Key Words: Goblet cell carcinoid, Appendix, Preoperative diagnosis, Endoscopic diagnosis, Surgical treatment, Case report

Core Tip: Diagnosing goblet cell carcinoid (GCC) of the appendix preoperatively is very difficult, because most patients with a chief complaint of acute abdomen undergo appendectomy based on a preoperative diagnosis of appendicitis. Even if colonoscopy is performed, accurate endoscopic diagnosis is very difficult because GCCs show a submucosal growth pattern with invasion of the appendiceal wall. The possibility of GCC must always be kept in mind during surgical treatment for presumptive appendicitis. This report includes an extremely rare example of correct preoperative diagnosis of appendiceal GCC.



INTRODUCTION

Goblet cell carcinoid (GCC; recently referred to as goblet cell adenocarcinoma) is a rare tumor of the appendix that is diagnosed in less than 1% of appendectomy specimens[1]. GCC was first described by Gagné et al[2] in 1969. Histologically, GCCs show both neuroendocrine tumor (NET) and adenocarcinoma morphology. GCCs have more malignant features than NETs, and are thus classified and staged as appendiceal carcinoma[3]. GCC diagnosed histologically before surgery is extremely rare[4]. The frequency of regional nodal metastases with GCCs is about 20%[5]. Colectomy with regional lymph node dissection is therefore recommended as surgical treatment for patients with localized GCC by the American Society of Colon and Rectal Surgeons (ASCRS)[6], the North American Neuroendocrine Tumor Society (NANETS)[7], and the European Neuroendocrine Tumor Society (ENTS)[8].

This report describes 6 cases of GCC treated by ileocecal resection (ICR) in our hospital and presents a review of the literature on GCC cases.

CASE PRESENTATION
Chief complaints

Five of the six patients complained of abdominal pain and the remaining patient presented with vomiting (Table 1).

Table 1 Details of the 6 cases.
Feature
Case 1
Case 2
Case 3
Case 4
Case 5
Case 6
SexMaleFemaleFemaleMaleMaleMale
Age in year445050724769
BMI in kg/m222.83222.12527.123.2
Chief complaintVomitingAbdominal painAbdominal painAbdominal painAbdominal painAbdominal pain
Laboratory data at 1st visit
    WBC as /mm35190170608100125101948015830
    CRP in mg/dL1.010.210.0114.212.25.9
    CEA in ng/mL2.22.12.241.25.7
    CA19-9 in U/mL5.25.77.6< 0.45.63.9
Colonoscopy before operation (biopsy)Edematous mucosa of cecum (+)-----
Maximum minor diameter of appendix on CT in mm989201917
Initial diagnosisGCCAppendicitisAppendix tumorAppendicitisAppendicitisAppendicitis
1st operationICR (open)AppendectomyAppendectomyAppendectomyAppendectomyAppendectomy
Colonoscopy before 2nd operation (biopsy)-Wnl (-)-Wnl (-)Wnl (-)-
2nd operation-ICR (lap)ICR (lap)ICR (open)ICR (lap)ICR (lap)
Lymph node dissectionD3D3D3D3D3D3
T factor4a33333
N factor1b01a000
Stage by AJCCIIIBIIAIIIBIIAIIAIIA
Tumor size in mm701522501227
Adjuvant chemotherapyFOLFOX-CAPOX---
Outcomes (follow-up in mo)RFS (56)RFS (30)RFS (18)RFS (12)RFS (6)RFS (2)
History of present illness

Characteristics of the 6 patients are shown in Table 1, comprising 4 men and 2 women ranging in age from 44 years to 72 years. Diagnoses of GCC in our hospital were made pre- and postoperatively.

History of past illness

Case 3 had a history of hypertension. Case 4 had Parkinson’s disease and had undergone coronary artery bypass grafting for acute myocardial infarction 15 years earlier. This patient was receiving oral levodopa and aspirin. Case 6 had hyperthyroidism and was receiving oral thiamazole. The other 3 patients had no relevant history.

Personal and family history

All 6 patients had no notable personal or family history.

Physical examination

All patients except Case 1 displayed abdominal tenderness and rebound tenderness. Case 1 presented with abdominal distention, but no abdominal tenderness.

Laboratory examinations

With the exception of Cases 1 and 4, inflammatory markers were elevated. In Case 6, carcinoembryonic antigen (CEA) was slightly elevated.

Imaging examinations

Contrast-enhanced computed tomography: Median maximum minor diameter of the appendix was 13 mm (range, 8-20 mm) (Figure 1).

Figure 1
Figure 1 Abdominal computed tomography of the appendix in 6 patients. Arrowheads indicate the appendix for each case. A: Case 1; B: Case 2; C: Case 3; D: Case 4; E: Case 5; F: Case 6.

Colonoscopy before first and second operations: Only Case 1 underwent colonoscopy before the first operation for detailed examination of edema of an ileocecal lesion. Although no neoplastic changes were found at the cecum and appendiceal orifice, cecal and appendiceal orifice biopsies showed GCC (Figure 2A and B). Case 4 underwent colonoscopy before the second operation. Although the pathological examination of the ICR specimen as an additional excision procedure showed residual GCC around the cecum and appendiceal orifice, colonoscopy before ICR showed no neoplastic changes there (Figure 2C).

Figure 2
Figure 2 Findings on colonoscopy. A and B: In Case 1, colonoscopy shows edematous mucosa of the cecal wall (A), but no neoplastic changes are apparent at the cecum or appendiceal orifice (B); C: In Case 4, colonoscopy before additional ileocecal resection shows no neoplastic changes at the cecum or appendiceal orifice.
FINAL DIAGNOSIS
Initial diagnosis

Case 1 was diagnosed as having GCC of the appendix by biopsy of the cecal wall. Cases 2, 4, 5, and 6 were diagnosed as having acute appendicitis, and Case 3 was diagnosed as an appendiceal tumor.

Final diagnosis

All cases were diagnosed with GCC of the appendix. Pathological examination revealed a tumor cell mixed pattern composed of large goblet cells mimicking signet-ring cells, with mucus in the cytoplasm, positive on periodic acid-Schiff (PAS) staining for mucin, and immunohistostaining positive for chromogranin A (CgA), synaptophysin, CD56, cytokeratin (CK) 20, and CEA; and negative for p53 (Figure 3). The pathological examination showed primary GCC of the appendix that invaded to the cecum and the terminal ileum in Case 1, and the cecum in Case 4 (Figure 4). Cases 2, 4, 5, and 6 were diagnosed as final stage IIA (American Joint Committee on Cancer) and the others as stage IIIB.

Figure 3
Figure 3 Representative pathological examination of goblet cell carcinoid in Case 1. A: Hematoxylin and eosin (HE) staining shows a mixed pattern comprising large goblet cells mimicking signet-ring cells containing mucus; B: Periodic acid-Schiff (PAS) staining for mucin is positive; C and D: Immunohistochemical staining is positive for chromogranin A (CgA) (C) and synaptophysin (D).
Figure 4
Figure 4 Resected specimen and tumor mapping. A-C: Although no neoplastic changes are seen at the cecal surface or appendiceal orifice in Case 1 (A) or Case 4 (C), tumor cells have invaded widely into the cecum in Case 1 (B); D: Residual tumor cells are seen microscopically at the cecum around the appendiceal orifice in Case 4. Red lines show the existence of tumor cells.
TREATMENT
First operation

Case 1 underwent elective ICR with regional lymph node dissection, and the others underwent appendectomy. In Case 4, the first operation was performed for diagnosis and treatment.

Second operation

Second operations were performed for 5 cases (excluding Case 1). All but Case 1 underwent ICR with regional lymph node dissection. Four of the five cases underwent laparoscopic surgery, and the remaining one underwent open surgery. All cases received curative resection.

OUTCOME AND FOLLOW-UP

Adjuvant chemotherapy was provided for 2 cases with lymph node metastasis (Cases 1 and 3) for 6 mo. At a median follow-up of 15 mo (range: 2-56 mo), all cases were alive without recurrence after treatment.

DISCUSSION

Appendiceal GCCs have an incidence of approximately 0.01 to 0.05 per 100000 persons per year, and they are very rare tumors[9]. Appendiceal carcinomas are often found incidentally after surgery for a preoperative diagnosis of appendicitis, representing less than 1% of appendectomies[1]. Therefore, we always need to keep in mind the possibility of cancer at the time of management of appendicitis. Overall, an established preoperative histological diagnosis of a primary appendiceal tumor was reported in less than 1% of patients[4]. There are two reasons for difficulties in the preoperative diagnosis of appendiceal GCCs. The first reason is that the most frequent symptoms are acute with chronic abdominal pain and abdominal distention, and laboratory data often show elevated inflammatory markers. Computed tomography findings show swelling of the appendix, so most patients undergo emergency appendectomy with a preoperative diagnosis of appendicitis. Another reason is that accurate endoscopic diagnosis is very difficult, even if a patient coincidentally undergoes colonoscopy before surgery, because GCCs have a submucosal growth pattern with invasion of the appendiceal wall[10]. Thus, reports of the colonoscopy findings of GCCs are extremely rare. In Cases 1 and 4 of the present series, although GCCs were present in the cecum and appendiceal orifice, colonoscopy showed no neoplastic changes. In Case 1, the attending physician performed colonoscopy and biopsied the cecal wall for detailed examination of edema of the ileocecal lesion. In Case 4, biopsy was not performed. In Case 3, the first operation was performed for diagnostic treatment. Even if colonoscopy had been performed before the first operation, it might not have resulted in an accurate preoperative diagnosis.

Appendiceal cancer presents with significant histopathological variety and is further classified into adenocarcinoma, NET, mucinous cystadenocarcinoma, GCC, and signet ring cell tumor[11]. GCCs have features of both adenocarcinomas and NETs. All GCCs stain positive on PAS staining. Immunohistochemical staining reveals pronounced expression of CgA and synaptophysin, and CEA is the key marker. CK staining for CK20, CK19, and CD56 may assist the diagnosis. Ki-67 immunostaining as a marker of proliferation is widely used for NET grading and staging[12]; Ki-67 has been reported to show a positive correlation with prognosis in gastrointestinal NETs. However, GCCs comprise a heterogeneous set of tumors, which makes the Ki-67 index unreliable for GCC[13]. Therefore, Ki-67 was not investigated in the present cases.

In general, the prognosis is worse for GCCs than for NETs; therefore, GCCs are classified and staged as appendiceal carcinomas, not as NETs[3]. The optimal surgical procedure for localized GCCs is often debated. Some suggest appendectomy for localized low-grade tumors with a low proliferative index[14], whereas others suggest colectomy only if the tumor is > 2 cm in size, is poorly differentiated, involves the base of the appendix, is associated with nodal metastases, or has atypical histological features[15]. On the other hand, ASCRS, NANETS, and ENTS guidelines recommend colectomy with regional lymph node dissection for all patients with GCCs, due to the high incidence of lymph node metastasis[6,8]. In Japan, according to the Japanese Classification of Colorectal Carcinoma, ICR is recommended for appendiceal carcinoma[16]. In the present series, all cases underwent appropriate colectomy with regional lymph node dissection.

Although only a few retrospective series support a specific benefit from adjuvant chemotherapy, those studies suggest adjuvant chemotherapy in the setting of node-positive disease (Stage III), similar to recommendations for appendiceal adenocarcinomas[17,18].

A literature review of GCCs was conducted using PubMed, revealing a constant increase in the number of GCC case reports in the past decade. This is because of the establishment of a definition of GCCs and increasing the awareness of this pathology among pathologists. Therefore, the review was narrowed down to case reports including over 50 cases (Table 2)[4,15,19]. In summary, GCCs occur most frequently from the age of 50 years, and there are no sex differences. Overall, 37% (172/462) of the total patients had stage IV disease, and 5-year overall survival rates were 40%-60%. Of the above, only Tang et al[4] mentioned preoperative diagnosis of appendiceal GCC in less than 1%.

Table 2 Previously reported articles about goblet cell carcinoid.
Ref.
Cases
Median age in yr (range)
Sex as male/female
Stage I/II/III/IV by AJCC
Colectomy, %
5-yr OS, %
MST in mo
Pham et al[15]5755 (mean)21/368/20/6/23NA4547
Tang et al[4]6349 (29-80)20/432/18/3/4057 (75)5843
Olsen et al[19]8359 (31-77)56/2712/35/3/2769 (83)5883
Lamarca et al[20]7456 (26-83)34/402/29/12/2842 (57)4852
Nonaka et al[21]10554 (25-79)54/515/52/13/3545 (43)NA67
Tsang et al[22]8654 (25-91)42/4467 (I-III)/1951 (76)68NA
CONCLUSION

In summary, preoperative diagnosis of GCCs is very difficult. At the time of surgical treatment for presumptive appendicitis, the possibility of GCC must always be kept in mind.

Footnotes

Provenance and peer review: Unsolicited article; Externally peer reviewed.

Peer-review model: Single blind

Specialty type: Medicine, research and experimental

Country of origin: Japan

Peer-review report’s classification

Scientific Quality: Grade B

Novelty: Grade B

Creativity or Innovation: Grade B

Scientific Significance: Grade B

P-Reviewer: Lim SC, South Korea S-Editor: Gao CC L-Editor: Filipodia P-Editor: Xu ZH

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