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World J Gastroenterol. Jan 14, 2015; 21(2): 432-438
Published online Jan 14, 2015. doi: 10.3748/wjg.v21.i2.432
Gastric foregut cystic developmental malformation: Case series and literature review
Yan-Hua Geng, Chang-Xing Wang, Jiang-Tao Li, Qing-Yu Chen, Xiu-Zhen Li, Hao Pan
Yan-Hua Geng, Xiu-Zhen Li, Hao Pan, Department of Pathology, Second Affiliated Hospital of Zhejiang University College of Medicine, Hangzhou 310009, Zhejiang Province, China
Chang-Xing Wang, Department of Osteology, Second Affiliated Hospital of Zhejiang University of Traditional Chinese Medicine, Hangzhou 310005, Zhejiang Province, China
Jiang-Tao Li, Department of Surgery, Second Affiliated Hospital of Zhejiang University College of Medicine, Hangzhou 310009, Zhejiang Province, China
Qing-Yu Chen, Department of Gastroenterology, Second Affiliated Hospital of Zhejiang University College of Medicine, Hangzhou 310009, Zhejiang Province, China
Author contributions: Geng YH and Wang CX designed the research and wrote the paper; Li JT, Chen QY, Li XZ and Pan H collected and analyzed the data.
Supported by The Science and Technology Project of Zhejiang Province, China, No. N20120675.
Open-Access: This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (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: http://creativecommons.org/licenses/by-nc/4.0/
Correspondence to: Geng Yan-Hua, Associate Chief Physician, Master of Medicine, Department of Pathology, Second Affiliated Hospital of Zhejiang University College of Medicine, Building 9, No. 88 Jie-Fang Road, Hangzhou 310009, Zhejiang Province, China. yhgeng@sina.cn
Telephone: +86-571-87767185 Fax: +86-571-87767185
Received: July 26, 2014
Peer-review started: July 27, 2014
First decision: August 15, 2014
Revised: September 4, 2014
Accepted: October 21, 2014
Article in press: October 21, 2014
Published online: January 14, 2015

Abstract

Foregut cystic developmental malformation (FCDM) is a very rare lesion of the alimentary tract, especially in the stomach. We discuss the concepts of gastric duplication cyst, bronchogenic cysts, and FCDM. Nomenclature has been inconsistent and confusing, but, by some definitions, gastric duplication cysts involve gastric mucosa and submucosal glands, bronchogenic cysts involve respiratory mucosa with underlying cartilage and glands, and FCDM lacks gastric mucosa or underlying glands or cartilage but has pseudostratified ciliated columnar epithelium (PCCE). We searched our departmental case files from the past 15 years and identified 12 cases of FCDM in the alimentary tract. We summarize the features of these 12 cases including a report in detail on a 52-year-old man with a submucosal cyst lined with simple PCCE and irregular and stratified circular muscle layers that merged with gastric smooth muscle bundles near the lesser curvature of the gastric cardia. A literature review of cases with this histology yielded 25 cases. We propose the term gastric-FCDM for such cases. Our own series of 12 cases confirms that preoperative recognition of the entity is infrequent and problematic. The rarity of this developmental disorder, as well as a lack of understanding of its embryologic origins, may contribute to missing the diagnosis. Not appreciating the diagnosis preoperatively can lead to an inappropriate surgical approach. In contrast, presurgical recognition of the entity will contribute to a good outcome and reduced risk of complications.

Key Words: Endoscopic ultrasound-guided fine-needle aspiration, Foregut duplication cyst, Gastric duplication cyst, Laparoscopic surgery, Pseudostratified columnar ciliated epithelium

Core tip: Gastric foregut cystic developmental malformation is a rare lesion that has been reported intermittently in recent decades. Its classification was inconsistent. It has often been misdiagnosed preoperatively. By missing the nature of the diagnosis, the surgical management was quite different. Through a review of the case series and literature concerning their clinical and radiologic features, and recognition of its embryologic and histological origin, we found that it is not an irregular disease and is an easily missed diagnosis. It can be cured by rational surgery, contributing to a good outcome and reduced risk of complications.



INTRODUCTION

Gastric foregut cystic developmental malformation (G-FCDM) is a rare lesion and is composed of an intramural cyst in the stomach with a lining of pseudostratified ciliated columnar epithelium (PCCE). Cysts of this nature have been reported for several decades and were given various names including duplication cyst of the stomach with ciliated lining[1-4], bronchogenic cyst of the stomach[5-12], and foregut duplication cyst of the stomach[13-21]. Preoperatively, a misdiagnosis as gastrointestinal stromal tumor (GIST) and leiomyoma was not unusual[2,8,9,11,12,15]. With the aforementioned shared histopathologic characteristics and clinicoradiologic features that mimic GIST, are cysts with PCCE truly a form of gastric duplication cyst[4]? Recent reanalysis has led to the conclusion that a cystic developmental malformation of the primitive foregut vestiges may be a reasonable embryologic explanation for the entity[14,22,23]. In this paper, we review the features of the aforementioned gastric cysts and review those that only have PCCE, along with a series of secondary changes arising in the developmental process of the cyst, which could help with choosing the appropriate surgical procedure[24].

CLINICAL SUMMARY

One month prior to admission, a 52-year-old man had epigastric discomfort and noted a mass. As he did not have chills, fever, nausea, vomiting, or diarrhea, he did not attach importance to it initially. However, his symptoms persisted, prompting him to seek medical attention. Endoscopy of the upper gastrointestinal tract revealed a gastric submucosal eminence at the subphrenic gastroesophageal junction. Pathologic diagnosis was chronic nonatrophic gastritis. Abdominal frontal and transversal computed tomography (CT) showed a well-circumscribed, homogeneous, non-enhancing, low-density, submucosal cystic mass measuring 3.0 cm × 4.2 cm on the lesser curvature of the stomach near the cardia, with a CT number of 17 Hu (Figure 1). Preliminary suspicion was of a GIST with cystic change. On physical examination, he was in good condition and laboratory studies were within the normal range. He had an exploratory laparotomy under general anesthesia. Intraoperatively, the liver, peritoneum, and pelvis were free of metastatic disease, and no ascites was detected. A soft 4.0 cm × 3.0 cm mass was noted at the lesser curvature, near the cardia. He underwent proximal gastrectomy with lymph node dissection. The postoperative course was uneventful and there was no recurrence after 5 mo.

Figure 1
Figure 1 Computed tomography. A: Frontal abdominal contrast-enhanced computed tomography (CT); B: Transversal abdominal CT demonstrating a homogeneous, low-density and well-circumscribed, subserosal cystic mass on the lesser curvature of the gastric cardia.
PATHOLOGIC FINDINGS

Gross examination of the proximal stomach showed that the cystic lesion was embedded in the gastric muscular layer and intimately associated with the submucosal lesser curvature near the cardia. It was located towards the esophageal margin of the proximal gastrectomy specimen (Figure 2). Thick, pale-yellow liquid was present within the cyst. The cyst did not communicate with the gastric lumen and measured 6.5 cm × 5 cm × 5 cm with a wall thickness that ranged from 0.1 to 0.3 cm.

Figure 2
Figure 2 Gross appearance of the resected specimen of proximal gastrectomy. A cyst measured 6.5 cm × 5 cm was embedded in the gastric muscular layer, and did not communicate with the gastric lumen.

The cyst wall was lined by a simple columnar epithelium and had a criss-crossing and stratified circular muscle layer (Figure 3A), and part of the cystic wall was lined with irregular longitudinal muscle bundles (Figure 3B). This circular muscle was stratified and merged with the muscular wall of the stomach at the attachment site, and the myenteric plexus was seen (Figure 4). Cartilaginous tissue, seromucinous glands, gastric epithelium and submucosal glands were not identified. Squamous metaplasia of the PCCE was detected (Figure 5). Cholesterol crystals and a histocytic response were present. All the dissected systematic lymph nodes were negative.

Figure 3
Figure 3 Submucosal cystic lesion. Hematoxylin and eosin staining showing the cyst wall lined by pseudostratified ciliated columnar epithelium (A) and submucosal cystic wall with irregular longitudinal muscle bundles (B), magnification × 200.
Figure 4
Figure 4 Regular, double-stratified, circular and longitudinal smooth muscles of the cyst and well-developed muscle layers continuous with gastric smooth muscle bundles, cartilaginous tissue, seromucous gland, or gastric epithelium were not identified. Hematoxylin and eosin staining (magnification × 200).
Figure 5
Figure 5 Squamous metaplasia tendency of the pseudostratified ciliated columnar epithelium. Hematoxylin and eosin staining (magnification × 200).
EMBRYOLOGY AND HISTOLOGY

G-FCDM may represent a congenital anomaly with late differentiation rather than imperfect involution of embryonic vestiges, but the undifferentiated foregut vestiges undergo transition and differentiate during the embryonic period[20]. One model postulates that the primitive lung bud derives from the respiratory laryngotracheal tube of the ventral foregut but is incompletely separated from the dorsal foregut in week seven of fetal development[24]. Several hypotheses to explain the dissociated foregut malformations suggest that they probably arise from pinching off and form the budding remnants[25], migration of the aberrant rest, supernumerary lung buds, and incomplete involution of the connecting stalk or fistula that connects with the digestive or respiratory tract[26-28].

Some authors would classify our described case as gastric bronchogenic cyst. Bronchogenic cysts are thought to be in the spectrum of foregut cystic malformations. Traditional embryology theory postulates that the basic difference between the two entities is the timing of budding. Foregut cysts are derived from pinching off at the time of bronchiolar differentiation, which is later than that of bronchogenic cysts; hence, the presence of cartilage and glandular tissue in the wall of the bronchogenic cyst[29]. Histologically, the foregut cysts are lined with PCCE, subepithelial connective tissue followed by a smooth muscle layer and an outer fibrous layer[29,30], but bronchogenic cysts additionally contain cartilage and glandular tissues in the cyst wall[16,23].

Gastrointestinal duplication cysts are rare congenital malformations that may occur anywhere from the mouth to the anus[31-33]. Cunningham et al[19] have suggested that the term gastric duplication implies the presence of gastric epithelium. Ladd and Grossa[34], later supported by Parker et al[35], have proposed more detailed criteria: close proximity to the gastrointestinal tract; a lining that resembles some part of the gastrointestinal tract; and a smooth muscle layer that shares the muscle wall with the gut, or is intermingled with the muscular layer of the bowel. Abiding by these criteria, cysts lined with PCCE do not qualify as gastrointestinal duplication cysts, including our 12 cases, because they lack archenteric epithelium. Similarly, in our cases, neither cartilaginous tissue nor seromucinous glands were present, so they do not qualify as bronchogenic cysts. In the literature, most reported cysts lined with PCCE are often described as foregut duplication cysts of the stomach[19].

CLINICAL FEATURES

Our literature search gathered 24 reports including 25 cases listed in Table 1[1-22,36]. From the literature review, gastric foregut cyst lined simply by PCCE is a delayed-onset disease (14 women and 11 men from 25 to 76 years-old). Our own series of patients in Table 2 also consisted of adults (age: 32-83 years) and had an equal sex distribution (6 women and 6 men). Most of the previously reported lesions involved the lesser curvature of the stomach and were near the gastroesophageal junction or cardia (12/24; 50%). Our series had a slight predominance of esophageal lesions (5/12; 42%), which was consistent with the literature reports of lesions above the diaphragm involving the esophagus[2,16]. Whether the predilection site of esophagus is related with the closest adjacency between the ventral embryo vestiges and dorsal tubes remains unknown. It is usually asymptomatic and occasionally found as a gastric wall mass on physical examination. Some patients present with epigastric pain. Patients with an older age or with a longer clinical history of symptoms tend to present with a larger mass and are more likely to have epigastric discomfort, gastric ulcer, gastroesophageal reflux, or occasionally canceration[37,38]. Some of these signs and symptoms are presumably related to the effect of the mass on adjacent structures[20]. Morphologically, the lined epithelium with focal squamous metaplasia were also sporadically reported[4,22]. As a result of the cyst location within the gastric muscular layer and a lack of communication with the gastric lumen, many such lesions are preoperatively misdiagnosed as intramural GIST and leiomyoma, which present with different imaging findings, although they probably share similar clinical representation. It has been proposed that all foregut developmental anomalies, including gastric duplication cyst with PCCE lining and bronchogenic cyst without cartilage and glandular tissue, should be grouped under the heading of foregut cystic malformations because they all share a common origin from the foregut and differ from each other in migration, location, and degree of differentiation[23,27,28,39]. Gastric cysts with PCCE are not true duplication cysts of the foregut, but the cystic development of foregut embryologic vestiges. Therefore, we suggest designating this as G-FCDM. With regard to the predominant location of G-FCDM at the lesser curvature of the stomach, it remains to be established whether this is due to migration of the embryo vestiges or some other reason.

Table 1 Summary of gastric foregut cystic developmental malformation.
No.SexAge (yr)ComplaintsLocationSize (cm)Ref.
1M56NoNGEJ, AW5 × 3 × 3Napolitano et al[13], 2013
2F34EP, GRNGEJ, GC4.5 × 3.2 Montemurro et al[1], 2011
3M29APFundus GC8.5 × 5.5 × 4.8Khoury et al[14], 2011
F26EPMiddle body LC5 × 2.2 × 2
4M76NoNGEJ, LC4 × 4Jiang et al[2], 2011
5M42Left lumbar painAGIJ, LC4.5 × 5.2Mardi et al[15], 2010
6F25EPGastric fundus3 × 2.5 × 2Jiang et al[5], 2010
7F60NoCardia, LC3Sato et al[6], 2008
8F72NoMiddle body, LC2 × 1.5Murakami et al[16], 2008
9M37EPNGEJ, LC4 × 4Wakabayashi et al[7], 2007
10M40EDNGEJ, LC6 × 5Hall et al[17], 2007
11F46VomitingPW of fundus;8 × 5.5Theodosopoulos et al[18], 2007
Gastrosplenic ligament3 × 3
12F38NoCardia, LC7 × 5Lee et al[8], 2006
13F63Fever, APPW of fundus10 × 7.6Cunningham et al[19], 2006
14F39NoFundus4 × 2.5 × 1Melo et al[9], 2005
15M26EPNANARubio et al[10], 2005
16F62NoNGEJ, LC3.5 × 2.5 × 1.5Song et al[11], 2005
17F59NoPW of stomach, LC7 × 5Hedayati et al[12], 2003
18M35EPNGEJ, LC7 × 6 × 5Kim et al[20], 2000
19M34NoGClargeIkehata et al[3], 2000
20M25NoPW of fundus6.5 × 5 × 5Takahara et al[4], 1996
21F35EP, nauseaPW5.5 × 2.5 × 2Laraja et al[21], 1995
22F61Heart failureCardia, intramural2 × 1.5Shireman[36], 1987
23F46NoNGEJ, GC6 × 8Gensler et al[22], 1966
24M52EDLC, NGEJ6.5 × 5Present case
Table 2 Foregut cystic developmental malformation of alimentary tract in our recent 15 years.
No.SexAge (yr)ComplaintsLocationSize (cm)Surgical option
1F35CTEsophagus2.5 × 1.5 × 1CE
2M51EDLower esophagus3 × 2CE
3F44NoPT, lesser omental sac8 × 3 × 2CE
4M76NoNGEJ, LC4 × 4Total gastrectomy with SLND
5F54EDLower esophagus4 × 2.5 × 2CE
6M40NABiliary tract3 × 2.5CE
7F42CTEsophagus4 × 2.5 × 1CE
8F32NoPT, gastrosplenic ligament5 × 4 × 3CE
9M41NoPW, LC3.5 × 2.5 × 0.8CE
10F42NAEsophagus2.5 × 1.8CE
11M83NADistal ileum6.7 × 5 × 4.1CE
PresentM52EDLC, NGEJ6.5 × 5Proximal partial gastrectomy with SLND
IMAGING FEATURES AND DIAGNOSIS

In symptomatic and occasionally discovered G-FCDM, CT can detect the presence of the abdominal mass, but it frequently fails to recognize its cystic nature due to the thick cyst wall[8]. Despite the fact that GIST is clinically more common than G-FCDM, it does not often show necrosis and cystic change. In the imaging study, cystic changes in GIST tend to be focal with irregular internal surfaces rather than smooth as in congenital cysts, and usually do not involve the whole tumor. Moreover, the proteinaceous cyst fluid[16,40] of G-FCDM is very helpful in identifying the necrosis of GIST. G-FCDM, but not GIST, can alter their shape with changing posture when they are large enough and with low tension. Leiomyoma is similar. Endoscopic ultrasound (EUS) is helpful in identifying the intramural or extramural relation of the gastrointestinal tract[41-45]. CT[46,47], magnetic resonance imaging or ultrasonography could indicates the presence of an abdominal cystic lesion or mass incidentally, but it cannot identify the nature of the lesion[2,21,40,48,49]. EUS-guided fine-needle aspiration (EUS-FNA)[50], CT-guided needle biopsy and intraoperative frozen section diagnosis can provide histologic diagnosis of G-FCDM and guide operative plans. The presence of PCCE and absence of neoplastic cells confirm the nature of the cyst[43], but considering the complications, some people do not advise performing a biopsy to confirm the diagnosis of resectable GIST because it can lead to tumor dissemination or hemorrhage[51,52].

THERAPIES

The management of asymptomatic cases remains controversial[41]. Watchful waiting is suggested after confirming the benign nature of these cysts by EUS-FNA, and Ponder and Collins[19] concluded that surgery is not necessary if the respiratory-type epithelial cells are diagnosed on EUS-FNA. For single symptomatic cases, the recommended management is complete cyst excision without violation of the gastric lumen[53]. Segmental or total gastrectomy is only a secondary alternative in the case of an indefinite diagnosis before operations[54]. However, if the cyst communicates with the gastric lumen that can easily induce infection, or with other serious gastric mucosal complications, such as ulceration, perforation, bleeding[55], fistula formation[38], obstruction and even malignant change, although rare, partial gastrectomy may be required[2,5,16]. From Table 2, we can see surgical treatment typically involved excision of the lesion without injury to attached organs, except the stomach. Of our three cases of G-FCDM, only one was correctly identified preoperatively and the cyst was successfully removed laparoscopically. The other two cases were incorrectly treated as GISTs, which are more common than congenital cysts, and led to unnecessary segmental gastrectomy and systematic lymph node dissection. With advances in medical technology and further understanding of G-FCDM, the advisable laparoscopic surgery for cyst removal has become more common in recent studies[16,24].

CONCLUSION

In summary, G-FCDM lined by PCCE is a rare lesion derived from foregut developmental malformation. The clinical manifestation is usually nonspecific, and it is easily misdiagnosed radiologically and clinically as a GIST or leiomyoma. EUS-FNA/CT-guided needle biopsy and frozen section diagnosis could be helpful in identifying the nature of the cyst and guide the surgical options. Although rare, better understanding of the origins of G-FCDM lined by PCCE and taking precise auxiliary examinations could help differential diagnosis from gastric wall masses, and surgically cure them without overtreatment.

Footnotes

P- Reviewer: Narattaphol C, Takayuki M, Uwe K S- Editor: Yu J L- Editor: AmEditor E- Editor: Ma S

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