Lymphangiomatosis of the ileum with perforation: A case report and review of the literature

Lymphangiomatosis is a benign proliferation of lymph vessels. Lymphatic diseases can vary from small lymphangioma to generalized lymphangiomatosis, which is a rare condition and can have several clinical manifestations. The gastrointestinal tract may be affected, but the incidence in the intestinal wall is very low. We propose in our study a case of ileal lymphangiomatosis presenting with perforation, in which the diagnosis was made after the pathological analysis of the resected intestinal tract. Although rare and not described in the literature, intestinal lymphangiomatosis could manifest itself with acute abdomen and could be a surgical urgency. This disease should be considered when intestinal perforation is observed.


Introduction
Lymphangiomatosis is a benign proliferation of lymph vessels. Lymphatic diseases can vary from small lymphangioma to generalized lymphangiomatosis, which is a rare condition and can have several clinical manifestations [1][2][3][4][5][6]. Although the underlying pathogenetic mechanism is unknown, it is generally considered as congenital malformation of the lymphatic system associated with alterations in the circulatory dynamics of the lymph [7]. It can occur anywhere in the body and also abdominal lymphangiomatosis is reported, but in many cases it involves the mesentery, omentum, mesocolon and retroperitoneum. The gastrointestinal (GI) tract may be affected, but the incidence in the intestinal wall is very low [8,9]. In the few cases described in the literature, the symptomatology was characterized mainly by abdominal pain and bleeding. Aggressive surgery should be avoided in symptomless cases, because it is now known that these lesions are benign [7].
We propose in our study a case of ileal lymphangiomatosis presenting with perforation, in which the diagnosis was made after the pathological analysis of the resected intestinal tract. In addition, the relevant medical literature on intestinal lymphangiomatosis was reviewed. This work has been reported in line with the SCARE criteria [8].

Presentation of case
A 41-year-old male presented to the Emergency Department with significant diffuse abdominal pain, nausea, vomiting and inability to pass gas or stool (constipation); the patient reported that these symptoms were present for 10 hours. He denied any significant family history of disease and he did not refer to major diseases or prior surgical interventions in his own medical history. During the physical examination, the subject was in discrete general conditions, collaborative, the sensory was intact, the decubitus indifferent, the breath eupneic and the pulse rhythmic. The vital parameters were preserved, and temperature was within normal limits. The abdominal examination revealed a flat abdomen, tender to palpation, painful to deep palpation on all quadrants, liver size appears within normal limits, Murphy's sign was negative, Blumberg's sign was positive, bowel sounds were absent. Rectal exploration indicated nothing significant. Laboratory values upon admission reported hemoglobin value of 15.5 g/dL, White Blood Cells 12.000/mmc, PCR 0.04 mg/dl. Upright abdominal films, then confirmed with computed tomography (CT) enhancement scan, revealed bowel distension and the presence of multiple gas-fluid levels. This framework suggested the presence of small bowel obstruction. As the etiology of the obstruction remained unidentified, the decision was made to perform a diagnostic laparoscopy. On entering the peritoneal cavity, the small bowel was examined: the intestinal loops were vital https://doi.org/10.1016/j.amsu.2019.03.010 Received 14 February 2019; Accepted 24 March 2019 and vascularized. At approximately 80 cm from the ileocaecal valve, a volvulus was identified, and in close proximity there was a long tubular structure, which proved to be a Meckel's diverticulum, with adhesions to parietal peritoneum. A lysis of adhesions was performed, the Meckel's diverticulum was divided at the base using a linear stapler (45 mm) and a surgical drain was placed. On the first postoperative day, the patient showed an acute abdomen: untreatable-tensely distended abdomen, painful to deep palpation on all quadrant; Murphy's sign was negative, Blumberg's sign was positive; bowel sounds were absent. Surgical drain took out enteric material and blood. The body temperature was 38°C. Laboratory values reported hemoglobin value of 12.7 g/dL, White Blood Cells 7.000/mmc, PCR 10.22 mg/dl. The patient again underwent urgent surgery. The intervention was an exploratory laparoscopy, then converted to open ileal resection for a microperforation of the bowel. The perforation site seemed to be distant above the previous diverticulum. About 20 cm of ileal resection was performed and side-to-side mechanical anastomosis was made. Two surgical drains were also placed. The postoperative course was regular, and the patient was discharged one the 10th post-operative day.
Histological examination showed stratification of fibrin and granulocytes on the serosa and presence of diffuse lymphangiomatosis (positive immunohistochemistry of D2-40 marker) involving the submucosa and, in some parts, the full-thickness muscular wall (Figs. 1 and 2).

Discussion
Lymphangiomatosis is a multisystemic disorder, characterized by congenital malformation of the lymphatic system with channels and cystic spaces of varying size. It may affect all the areas of the body; therefore, symptoms and complications are related to localization. Usually in the course of the disease patients are asymptomatic at first, but then the abnormally proliferating lymphatic channels are capable of massive expansion and infiltration into surrounding tissues. Abdominal lymphangiomatosis is quite often reported, but in many cases it arises in the mesentery, omentum, mesocolon and retroperitoneum. The GI tract may be affected, but the incidence of lymphangioma of the intestinal wall is very low, and it is even rarer in the small bowel (less than 1%) [9,10]. To the best of our knowledge, all cases reported in the literature with GI tract involvement are summarized in Table 1 [1,2,7,[10][11][12][13][14][15][16][17][18].
There is only one case report of lymphangiomatosis involving the oesophagus [18] and one case report involving fundus of the stomach [2]. Lymphangiomatosis of the colon is described in four papers [7,[13][14][15]. In these patients, the main symptoms were abdominal discomfort, bleeding and anaemia.
In the majority of patients described in the literature, diagnosis was suggested by colonoscopy and biopsy, which mainly showed protruding submucosal lesions. The diagnostic workup was sometimes integrated by contrast-enhanced CT, showing marked thickening of the walls of the bowel loops.
In five papers [10][11][12]15,16], patients were treated with surgical resection of the affected part of intestine, whereas one patient improved on conservative management and was put on low-fat and high-protein diet [1]. In all reported cases, follow-up was of short duration. In two cases patients continued to have symptoms after surgery [2] or after endoscopic mucosectomy [13].
The histological features of the lymphangiomatosis are non-specific, and the definitive diagnosis requires the demonstration of an hyperproliferation of normal lymphatic vessels with normal endothelium, predominantly in the context of submucosa, with disruption of the muscular layer and sometimes of the serosa. This condition creates a locus minoris resistentiae, and this may explain the pathogenesis of the   perforation, reported in our case. The involvement can be continuous or, more frequently, segmental. The impairment of the muscular layer and of the submucosal nerve plexus could also have contributed to the development of the intestinal obstruction, which was the symptom because our patient came to our attention. This suggests that also lymphangiomatosis should be taken into account among other rare causes of intestinal obstruction [19,20].

Conclusion
In conclusion, lymphangiomatosis of the small bowel is a rare disease that has no specific clinical features, so it is easy for a clinician to make a misdiagnosis or to miss diagnosis. In some cases, surgical resection may be required to provide definitive histological diagnosis, as occurred in our cases. We want to share our experience about this, because, although rare and not described in the literature, intestinal lymphangiomatosis could manifest itself with an acute abdomen and surgical urgency. This disease should be considered when intestinal perforation is observed. In particular, the pathologist should keep it in mind in the differential diagnosis, when he analyses a case of perforation whose cause is not very clear and specified.

Ethical approval
Ethical approval was not required.

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Author contribution Antonio Giuliani, Lucia Romano: Writing. Gino Coletti, Mohammad Walid A Fatayer, Giuseppe Calvisi: Images and contribution to the text.

Conflicts of interest
No conflict of interest.

Research registration number
None.

Consent
Written informed consent was obtained from the patient for publication of this case report and accompanying images. A copy of the written consent is available for review by the Editor-in-Chief of this journal on request.

Provenance and peer review
Not commissioned, externally peer reviewed.