CRVM is a rare, gastrointestinal vascular malformation. Since CRVM was first described by Phillips 1839, more than 300 cases have been reported, and most of these have been in adults(7). Approximately 80% of CRVM lesions are located in the rectosigmoid(1, 2). The vascular malformation can present as solitary lesions, clusters of intraluminal polypoid lesions, or diffuse infiltration in the submucosa and the other layers of the intestinal wall with extension into the mesentery and adjacent organs(8). The classification and terminology of hemangioma and vascular malformation mentioned in the literature are not entirely clear, and mainly include cavernous hemangioma, angiodysplasia, arteriovenous malformation(AMV), venous malformation, and venous dilatation(9, 10). At present, CRVM is primarily reported to be a venous malformation (formerly called ‘cavernous hemangioma’), and arteriovenous malformations are rare(6, 5, 10).Previous studies have reported that CRVM affects more adult females than adult males(11), but more male children than female children(12). In our study, the results showed the morbidity of CRVM in male children was 69.6%(16/23), which is consistent with previous reports.
Chronic, recurrent, painless rectal bleeding is the most common symptom of CRVM. Occasionally, massive and life-threatening bleeding may occur(1, 6). Most patients often have a long-term and history of repeated blood transfusions throughout the course of the disease. Other reported, but rare, symptoms include abdominal discomfort, abdominal pain, diarrhea, and perianal discomfort(2, 8). CRVM may manifest as intestinal lesions in syndromic diseases, such as KTS, which is characterized by CRVM, skin capillary malformation, and asymmetric limb hypertrophy(13, 14). In this study, two children showed multiple wine-like skin spots all over the body, complicated with asymmetric hypertrophy of both lower limbs, which was considered to be KTS. Due to the rareness of CRVM and the lack of specific symptoms, a substantial number of patients have been misdiagnosed with anal fissure, hemorrhoids, rectal polyps, inflammatory bowel disease, and rectal varices. Wang et al. reported that the mean delay time between the initial symptom onset and final CRVM diagnosis was 17.63 years(2). However, the onset of CRVM in more than 50% of adults can be traced back to childhood or even infancy(1, 2). Therefore, physicians should carefully consider the possibility of CRVM in children who complain of rectal bleeding.
Due to the low incidence of CRVM and the lack of large sample data, no consensus has been formed with respect to diagnostic methods. Colonoscopy is believed to be the most useful visual examination as it depicts the luminal extension and morphology of the malformation(1, 2, 8). However, if the examiner is not experienced enough, atypical presentation by colonoscopy may lead to misdiagnosis. In the present series, 19 patients (82.6%) showed abnormal submucosal vessels with multiple focal, diffuse distributions by colonoscopy. The other four patients showed atypical mucosal or submucosal lesions, such as hyperemia, swelling, scar-like changes, and multiple thrombosis. We speculate these features seen at initial colonoscopy may have led to a diagnosis of inflammatory bowel disease.
Contrast-enhanced CT is another important examination tool to confirm a CRVM. The representative findings of CT include an irregularly enhanced and thickened rectal wall or perirectal tissue, and multiple calcified foci of pelvic phleboliths(1, 2). Some of the CT findings of CRVM are nonspecific. However, when combined with CT angiography(CTA), diagnostic efficiency can be greatly improved. CTA can clearly show even the smallest vessels of the malformation, as well as connections with other vessels of the circulatory system(15). This has important guiding significance for intraoperative bleeding control. MRI has better tissue resolution than CT, which is of great significance in evaluating the extent of intestinal wall invasion and surrounding organ involvement, and is important for guiding the choice of treatment(15). Furthermore, dynamic contrast-enhanced MR angiography(MRA) can be used to differentiate between high- and low-flow lesions(16). Typical imaging MRI findings show the rectosigmoid wall was markedly thickened with a high signal intensity on T2WI, an enhanced dynamic scan showed progressive enhancement. The addition of fat suppression on a fast spin-echo T2WI sequence is beneficial in depicting the true extent of the lesion, as it helps to differentiate the hyperintense lesion from the rectal mesentery. Digital subtraction angiography(DSA) can help to visualize the lesion and identify a vessel for embolization(4), but had a low positive rate of rectal vascular diagnosis(5/13, 38.5%) and could not show the lesion range(2). With its low sensitivity, invasiveness, and high price, DSA can be replaced by CTA and MRA. Therefore, we suggest that enhanced CT/CTA and/or MRI/MRA are recommended as first-line examination methods for children with typical CRVM clinical manifestations.
Endoscopic ultrasonography has a good application prospect in the diagnosis of CRVM, because it can accurately determine the level of intestinal wall involvement(8, 17). It can also evaluate the depth and direction of hemangiomas in the lower rectum and anal canal, especially for vascular abnormalities involving only the plasma layer, which cannot be recognized by colonoscopy. However, endoscopic ultrasonography has not been widely carried out in most children's endoscopic centers in China, and therefore, its application is limited.
CRVM treatments reported in the literature include surgical resection of the involved intestines, interventional embolization, and endoscopic treatment(1, 4, 18). Surgical resection of the diseased intestinal segment is one of the more effective methods for treating CRVM. However, there is yet to be a consensus regarding specific surgical methods. The earliest reported surgical treatment was abdominoperineal resection(APR), which involves removal of a diseased intestinal segment to effectively stop bleeding(2). Although this approach can save some patients with life-threatening severe intestinal bleeding, a permanent colostomy is undesirable, especially in young patients. Low anterior resection(LAR) can ultimately preserve sensation and defecation function of the anus(19); however, LAR cannot completely remove the diseased rectum and the probability of recurrent bleeding is very high. Therefore, this method can only be used for the treatment of vascular malformations above the sigmoid colon. In 1976, Jeffery first advocated for coloanal sleeve anastomosis for the treatment of CRVM, and this procedure has been remained popular since(20). However, this method is only able to remove the mucous layer and submucosa of the colorectum and retain a 10-cm-long rectal seromuscular layer. Therefore, vascular malformation of the seromuscular layer may invade the colon, and cause bleeding recurrence. It is also very difficult to peel off 10 cm of mucous membrane and seromuscular layer in the rectal wall with vascular malformation.
Recently, transanal total mesorectum excision(TaTME) for diffuse cavernous hemangioma of the rectum has been reported to contribute to the precise resection of the local lesion in the mid and low rectum and the anal canal with satisfactory outcomes, when applied in rectal cancer patients(1, 21). However, this operation completely removes the internal rectal sphincter and perirectal nerves, significantly influencing defecation sensation and defecation reflex functions after the operation. There is also a high risk of anastomotic leakage between a full-layer colon and low anal anastomosis.
Previous reports on surgical methods are mostly limited to adult cases. Due to the particularity of the anatomical structure of children, the adult procedure cannot be used entirely for reference. Previously, we used a modified transabdominal Soave procedure combined with Sarasola-Klose internal hemorrhoidectomy to treat CRVM, and achieved satisfactory results(6). In this procedure, the laparotomy or laparoscopy was used to explore the extent of intestinal, mesenteric, and pelvic vascular malformations. The diseased mesentery is disconnected, and the colon and rectum are completely disintegrated below the peritoneal reflection, 3–5cm proximal to the dentate line. The extent of disassociation can be determined by digital rectal examination during the operation. Turn to the perineum, a gauze roll of 1.5 cm in diameter is slowly inserted into the rectum to a depth of about 3–5 cm. The distal end of the gauze roll and the rectal mucosa proximal to the dentate line are sutured. Circumferential incisions are made on the rectal mucosa's dentate line, and the gauze coils are pulled outward at the same time. Along the submucosal plane, the dissection is continued for another 3–5cm proximal to the dentate line and enters the abdominal cavity. Then, the bowel is pulled down until normal bowel appears. After the diseased bowel is resected, the cut edges of the colon are anastomosed to the dentate line. The internal sphincter and rectum muscle sheath are preserved, and the dissection range of the rectal mucosa is shortened in this procedure. Thus, the difficulty of operation and the risk of bleeding are reduced greatly. A gauze roll is used to assist in achieving hemostasis by direct compression during dissection of the mucosa. The mucosa is fixed and retracted with tension, allowing the incision to be regular and the dissection plane to be well controlled. Due to the short distance from the peritoneal reflection to the dentate line in children, preserving a 3–5cm rectal muscle sheath can significantly reduce perirectal nerve injury and minimize the effects on defecation.
In our center, 21 CRVM patients were treated with modified Soave surgery for complete resection of the diseased intestinal segment. Only two patients presented with abnormal vascular hyperplasia near the anastomotic site and hematochezia; these were cured by endoscopic electrocautery. There was no reoperation due to the recurrence of hemangioma caused by the preservation of the muscle sheath. Therefore, even if the lesion begins from the dentate line, minor vascular malformations that might be retained in the bowel wall distal to the anastomosis after these resections can be easily managed by conservative treatment. Some children have a poor sense of defecation after operation, likely due to the removal of the sensitive area of the mucous membrane on the dentate line, which requires slow recovery. Similar to the endorectal pull-through in the procedure for Hirschsprung's disease(22), we noted an increased stool frequency in the early postoperative stage. This returned to normal by several months after the operation. Therefore, the modified transabdominal transanal Soave procedure is a good method for treatment of CRVM because it can significantly reduce operation difficulty, bleeding risk, and postoperative defecation dysfunction.
In addition, our study found that mucosal or submucosal lesions of the intestinal wall identified by colonoscopy were significantly smaller than that of serous side lesions seen during operation. Children with long-segment lesions often showed patchy or small segment lesions by colonoscopy. Therefore, transabdominal surgery to explore the extent of the lesion is of great significance to prevent the omission of the diseased intestine and to prevent postoperative rebleeding. Pelvic floor vascular malformation around the peritoneal reflection can be seen during the abdominal exploration in some children, which requires ligation around the rectum to control bleeding. In children with uterine and vaginal bleeding, the primary abnormal blood vessels around the uterus can be ligated during the operation to reduce vaginal or menstrual bleeding. Moreover, for a small number of children, abdominal lymphatic vascular malformation can be excised simultaneously with transabdominal exploration.
Nonoperative therapies to treat CRVM, such as sclerotherapy, snare polypectomy, neodymium-doped yttrium aluminum garnet (Nd:YAG) laser therapy, and argon plasma coagulation (APC), have been reported to decrease the amount and frequency of hematochezia(23-25). However, rectal bleeding eventually recurred in most patients. In our center, one patient with limited lesions was treated with sclerotherapy and had recurrent hematochezia. The scope of rectal submucosal vascular malformation was gradually increased during follow-up. Moreover, sclerosing agent injection and interventional vascular embolization increased the risk of deep venous thrombosis, intestinal necrosis, pulmonary embolism, and even death. Data from several studies suggest that medical therapies is an effective and relatively safe treatment for patients with refractory bleeding from gastrointestinal vascular malformations(11, 26). Smith et al. reported that the patient was successfully managed using a conservative approach with tranexamic acid administered as needed, avoiding the need for resection(7). However, the long-term efficacy of drugs in the treatment of CRVM remains inconclusive.