Multiple hemangiomas of the gastrointestinal tract in children

Multiple Hemangiomas of the Gastrointestinal Tract in Children R. W. PAUL

Hemangiomas of the gastrointestinal tract are uncommon [I]. Wood [2] lists hemangiomatosis of the bowel as 2 to 12 per cent of all bowel hemangiomas. Hemangiomatosis of the intestinal tract is thus rare, but probably not as rare as the paucity of reports in the surgica1 literature would suggest. Individual clinicians are likely to see only a single case, and this may account for a reluctance to report them. Hansen [3], in 1948 in his sixty-six collected cases, classified eight as angiomatosis localized to the intestinal tract, but only four of these patients had multiple hemangiomas. Gentry, Dockerty, and Claggett [4], in their excellent and ‘exhaustive review in 1949, classified the lesions in 16 of their 283 cases as multiple diffuse cavernous angiomas of the intestinal tract. Excision of one or a few hemangiomas of the bowel presents no surgical problem [5,6 J, but when these lesions number several hundred, the task may be life-threatening. This report concerns the surgical management of two children who have each had several hundred hemangiomas throughout the length of the bowel. In each child progressive hemorrhage from the gastrointestinal tract was the indication for operative intervention. Case Reports CASE I. A black female child (CH), born on October 3, 1956, came to the Children’s Hospital of Philadelphia in December 1958 with a history of severe anemia. She had had a hospital admission at the age of one year for four procedures to remove a hemangioma from the left foot. At that time she was found to have a sickle cell trait and significant anemia, requiring several blood transfusions. She was hospitalized again at twenty-three months of age with a hemoglobin of 2 gm per cent and a hematocrit of 9 per cent. Investigations included multiple stool examinations which were negative for blood by benzidine and guaiac tests. The presence of the sickle cell trait was confirmed. Radiologic examination included an upper gastrointestinal series, small bowel series, and barium enema, all of which were within normal limits. Sigmoidoscopy showed nothing abnormal. Platelet count From the Division of Pediatric Surgery, University of Vermont, Burlington, Vermont 05401. This study was supported in part by USPHS Grant RR109, General Clinical Research Centers Branch, and by a grant from the John A. Hartford Foundation, Inc. Presented at the Fifty-First Annual Meeting of the New England Surgical Society, West Harwich. Massachusetts, October 1-3, 1970. 412

MELLISH,

MD,

Burlington,

Vermont

was reported as 118,000 per mm3. The anemia was corrected by transfusion, but recurred in a few weeks. Upon her transfer to the Children’s Hospital, the hemoglobin was reported as 5.9 gm per cent, her red cells 2.78 million, and platelets 268,000 per mm3. Shortly after admission gross melena developed. The diagnosis of possible hemangiomas of the gastrointestinal tract was made despite the previous negative x-ray studies. Because of the severity of the bleeding, we explored the abdomen after correction of the blood loss (operation 1). Multiple hemangiomas were found extending throughout the small bowel and colon. These varied in size from a few millimeters to 2 cm. The small bowel lumen contained obvious blood. Approximately fifty lesions, extending from the ligament of Treitz to the rectum, were either excised, clamped and ligated, or ligated. In February 1959 extensive gastrointestinal bleeding recurred, demanding re-exploration (operation 2). Again, approximately fifty hemangiomas were excised or transfixed and ligated. In August 1959 she was readmitted with recurrent massive gastrointestinal bleeding. An upper gastrointestinal series revealed a 2 cm filling defect in the duodenum. She was re-explored (operation 3) with excision of the duodenal lesion and multiple other hemangiomas. After this operation she required tracheostomy for airway difficulty. TABLE

List of Operations

I

Number -

Date

in Case I (CH)

Procedure

Four operations to excise hemangioma of the left foot December 1958 Abdominal exploration, appendectomy; approximately 50 hemangiomas excised or ligated February 1959 Exploration: approximately 50 hemangiomas of the bowel excised or clamped and ligated Abdominal exploration; multiple exciAugust 1959 sion and ligation of hemangiomas of gastrointestinal tract including excision of a 2.0 cm hemangioma from the duodenum Exploration; excision and ligation of July 1960 approximately 36 hemangiomas Exploration: 57 hemangiomas treated May 1965 by ligation excision: three small pedunculated hemangiomas excised from the perineal region Exploration for intestinal obstruction May 1965 with lysis of adhesions 1957

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Figure 1. Case II. The patient at 2 days of age showing the cavernous hemangioma of the back and some of the small surface lesions.

II

Composite Chart of Operations, Each Year (Case I)

of Gastrointestinal

Figure 2. Case II. The cavernous has been excised.

hemangioma

Tract

of the back

body surface. The infant showed a low platelet count (60,000 per mm3) with a normal bone marrow. Because of the unsightly lesion and the risk of platelet trapping with the thrombopenia, a decision was made to excise the hemangioma. Chest radiographs demonstrated no evidence of intrathoracic extension of the lesion. On the fifth day of life the hemangioma was excised. (Figure 2.) Pathologic examination showed a large cavernous hemangioma with flattened endothelial lining and smooth muscle in the wall. Over the next months the infant developed well, but the hemangioma of the back largely recurred. A decision was made to re-excise the mass. The platelet count was 264;OO0 per mm3. Bleeding and clotting times were normal. A radiopaque dye was injected directly into the hemangioma to exclude large communicating channels into the thoracic cavity. None was found. At operation the hemangioma showed poorly defined borders, and the deep surface extended beyond the eroded ribs. Hemostasis was difficult. Postoperatively, there was oozing from the wound which required several transfusions. Pathologic examination showed no cellular or nuclear atypia and no disorganization, but the whole lesion was pushing between muscle bundles. During the next thirty months, the child developed intermittent mild problems with various surface hemangiomss. Several of these bled and had to be excised. The majority of the three hundred odd surface hemangiomas were treated by electrocoagulation. In August 1968 a blood stool was noted by the mother. In April 1969 the mother reported gross melena. The child’s hemoglobin fell to 4.8 gm per cent and she required three transfusions during the month. She also noted occasional attacks of cramping abdominal

From the end of 1959 until July 1960 she was maintained by blood transfusions. In July 1960 increasing blood loss prompted re-exploration (operation 4) and thirty-six hemangiomas were removed. From then until 1964 she was supported by multiple blood transfusions. In 1964 an isotope study was carried out using chromiumsl-labeled red cells. This demonstrated a shortened red blood cell life span, no increased activity of the spleen, and an average blood loss of 50 ml per day from the gastrointestinal tract. In July 1965 after careful review of the problem, we reopened the abdomen (operation 5) because of hemorrhage. Once again, numerous hemangiomas were identified throughout the gastrointestinal tract including some in the stomach. Fifty-seven of these were excised or suture-ligated. Ten days postoperatively acute intestinal obstruction developed which necessitated lysis of the adhesions (operation 6). She also required tracheostomy at that time. The abdominal explorations are listed in Table I. Since that time, she has required no further abdominal surgery, and the last blood transfusion was given about one year ago. The blood transfusions are listed in Table II. She is a well developed, intelligent, fourteen year old girl who weighs 119 pounds. The patient stated recently that she holds no grudge against the medical profession and feels quite kindly toward them. CASE II. A white female child (KG) was born on October 29, 1964 at the DeGoesbriand Unit of the Medical Center Hospital of Vermont. The most striking finding was the presence of a very large cavernous hemangioma on the left side of the back. (Figure 1.) She had hundreds of tiny hemangiomas all over the TABLE

Hemangiomas

Volume of Blood Transfused,

and Number

of Episodes Requiring

Transfusion

Year Data Age Episodes requiring blood transfusion Total volume Operation

Volume

121, ADril 1971

1963

1964

1965

1966

1967

1968

1969

6

7

8

9

10

11

12

13

0 0

2 1,950

24 9,195

20 9,105 5 6

9 3,600

15 5,980

9 5,300

9 3,500

1961

1962

4

5

3

0 0

1958

1959

1960

2

3

5 1,200 1

4 1,935 23

3,625 4

-.~

413

blood cell loss in the stool averaged 80 ml per day. Because of the persistent low serum fibrinogen, a plan was made to obtain biologically active Ilsl-labeled fibrinogen to try to localize any active sites of entrapment of fibrinogen. If entrapment could be demonstrated, treatment could be directed to these areas prior to surgical exploration of the intestine. Some delay ensued in obtaining the Pl-labeled fibrinogen from Europe. During this time, the child required a number of transfusions. She had attacks of abdominal pain which suggested mild intussusception. A barium enema in October 1969 showed multiple hemangiomas of the colon. Because of reports of success with steroid therapy [7’,8], a course of dexamethazone was given for thirtyfour days. At the end of this course a second chromium51 study was carried out to estimate the blood loss. Measured loss into the bowel averaged 160 ml per day, and transfusion was becoming more frequent. Because of the extensive blood loss, a trial with heparin was not considered justified. In December 1969 the Dal-labeled fibrinogen was given and a total body scan was carried out to determine any evidence of sequestration. Using the gamma scanning camera, no evidence of any sequestration was found except the evident loss into the gastrointestinal tract. Fibrin-split products were measured on two occasions and there was no evidence of excessive split products in the serum

[9JOl.

Figure 3. Case II. Hemangiomas multiple fi//ing defects.

of stomach

showing

as

pain. An upper gastrointestinal series at this time showed numerous lesions throughout the upper gastrointestinal tract. (Figure 3.) In an attempt to localize the bleeding lesions a selective celiac and superior mesenteric arteriogram was taken. This demonstrated an accumulation of contrast material on several tortuous irregular vessels in the region of the terminal ileum. The child developed considerable oozing from the arteriotomy site on the right femoral artery after this procedure. Although the platelet count remained at fairly normal levels, a significant finding was a persistent low level of serum fibrinogen at this time. Levels ranged from 5 to 43 mg per cent. The mother reported that the child had episodes of swelling of deep hemangiomas on the extremities and the chest wall which were apparently unrelated to trauma. She also thought that melena became evident after these episodes. It was postulated that she might have selective depletion of fibrinogen with sequestration at the sites of swelling. Surgical exploration was delayed pending further investigations. Blood volume measured with chromium51-tagged red blood cells showed that the blood volume and red cell mass were below the normal range. The stools were collected over a five day period and the measured red 414

After these studies, in January 1970, after transfusion of fresh blood, the child was explored through a transverse upper abdominal incision. The entire gastrointestinal tract was studded with hemangiomas measuring 0.2 to 2.0 cm in diameter. Hemangiomas acted as lead points for two areas of intussusception in the ileum. (Figure 4.) The appendix and colon were studded with lesions. Through a large anterior gastrotomy the lesions within the wall of the stomach were identified, grasped by hemostats, excised, and oversewn with 3-O chronic catgut. Several lesions were clamped and suture-ligated through a base. When possible, lesions were drawn out into the wound to facilitate excision. Lesions were palpable in the first and second portion of the duodenum, but were not surgically excised. Wedge resection of the larger hemangiomas in the jejunum and ileum was carried out through enterotomies in approximately ten sites. After resection the bowel was intussuscepted to the exterior and all available hemangiomas were excised, suture-ligated, or oversewn. More superficial lesions were treated by a serosal incision, extrusion of the lesion through the incision, and suture ligation. By these various means approximately 150 hemangiomas were removed. The lower ileum showed such a massive congregation of hemangiomas that it was elected to excise one segment of it comprising perhaps 15 to 20 per cent of the small bowel. This was resected and almost 100 lesions in the wall were counted in the open specimen by a member of the operating team. The bowel was joined by end to end anastomosis using interrupted 5-O silk and bringThe American Journal of Surgery

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ing the wall together in an abutting manner. The appendix, which contained three hemangiomas, was removed. The small bowel contained gross blood. The colon seemed to be relatively free of obvious bleeding. A few lesions were excised from the colon because of their large size and the risk that they might bleed into either the peritoneal cavity or the colon. On the second postoperative day bleeding from the stomach developed. The hematocrit fell from 42 to 22 per cent. Four units of cryoprecipitate as well as some whole blood was given. She responded well to this and made a very satisfactory recovery. Serum fibrinogen, one week postoperatively, was 99 mg per cent. She has had no gross bleeding since discharge and has maintained normal hemoglobin levels. Surgical Management

should include a very thorough study of the coagulation mechanisms. When operative intervention is planned, the surgeon should prepare himself and hie patients for a lengthy procedure. Clearly, when the lesions are few in number, excision can be undertaken simply. With multiple lesions, the procedure must be planned carefully to minimize trauma and subsequent risks to the patient. The following methods of treating the hemangiomas were employed in one or both of the patients : 1. Excision of a segment of bowel with end to end anastomosis. Multiple lesions in a limited area justify this procedure if adequate bowel remains. 2. Enterotomy with wedge excision and transverse closure. Blood loss was minimized by controlling the blood supply with umbilical tape around the bowel held as an aneurysm tourniquet. 3. Intussusception to ,the exterior. (Figure 5.) Each site of wedge excision permitted intussuscep tion of the bowel from above or below to expose lesions. Wide-based hemangiomas were clamped and excised and the bases oversewn. Smaller hemangiomas permitted simple traction snd suture ligation of the base. 4. Serosal incision with extrusion of the lesion. Many of the smaller hemangiomas were extruded through such an opening and clamped. The base was ligated and the serosa approximated with fine silk. 5. Transfixion ,or suture ligation through the serosa. This last method was used in the case of very small hemangiomas. In the first patient, many of the hemangiomas appeared at the sites of previous ligations. Method 4 is probably almost as fast and may be more effective. Electrocoagulation was avoided within the bowel because of the rimskof subsequent bleeding and perInitial

investigations

Volume 121, April1971

Figure 4. Case II. lntussusception ous hemangiomas.

of the ileum due to cavern-

foration. In the second patient, there were ten enterotomy sites for wedge excision or intussusception of the bowel to remove hemangiomas. At each site approximately one dozen hemangiomas could be reached and dealt with. The fourth method, serosal incision, was used for at least fifty lesions. As many as 100 hemangiomas of varying sizes were removed. In addition, small hemangiomas could be seen within the mesentery, the retroperitoneal tissues, and the abdominal wall. Pruzanski [11] reported on an eighteen year old man who was explored for gastrointestinal bleeding and had approximately fifty hemangiomas excised through multiple enterotomies. This patient also showed two areas of intussusception. Copple and Kingsbury [12] described a case of excision of two hemangiomas, and Rickman [6] reported on a child with a hemangioma on one hand in whom intestinal bleeding developed. He found only three small bowel hemangiomas, but in the photographs

Figure 5. Case II. Method of treatment consisting of intussusception to the exterior and clamping w.ith excision and oversewing. A site of wedge excision is seen on the right. 415

Mellish

they resemble the lesions in our patient. Weinstein, Moertel, and Waugh [13] reported on a nineteen year old woman with multiple hemangiomatous lesions of the gastrointestinal tract and other visceral hemangiomas. Their patient had bleeding, and had nine of the largest hemangiomas excised. The follow-up study suggested that some gastrointestinal bleeding was still occurring. Not all hemangiomas of the bowel lead to hemorrhage [3,4,14,15]. Although steroids and radiation may occasionally be useful, probably the only effective treatment for this complication is surgery. Coagulation Defects

Kasabach and Merritt [16] in 1940 first drew attention to platelet trapping in large hemangiomas. By 1958 Sherz, Jouro and Geppert [17’] were able to collect fourteen case reports, and since then further instances have been described [18-201. One author [al] observed that thrombopenia was principally associated with large single cavernous hemangiomas. He reported two cases of neonatal hemangiomatosis, one with severe thrombopenia. Sequestration of platelets in giant hemangiomas has been proved with radioisotope-labeled platelets [22,23]. Surgical removal of cavernous lesions has possibly cured thrombopenia in some. instances [24] (case 2). Radiation therapy has apparently been effective in other [18,20,25], but spontaneous remission has occurred [I?‘]. There was no evidence of coagulation defects in case 1, although excessive consumption might be assumed on the basis of the extensive continued blood loss. In case 2, the overriding problem seems to have been the acquired fibrinogen defect. The thrombopenia at birth disappeared after excision of the giant cavernous hemangioma of the back. Whether this can be claimed as a causal relationship is open to speculation. Blix and Aas [26] described thrombocytopenia and fibrinogen deficiency occurring in the same patient with a giant hemangioma. Verstraete et al [19] reviewed the subject of excessive consumption of blood coagulation components, and added a case of giant hemangioma with generalized bleeding due to deficiency of platelets and fibrinogen. Case 2 appears to be the first report of generalized hemangiomatosis in a newborn infant who survived thrombopenia, fibrinogen deficEency, and excision of over 200 hemangiomas from the intestinal tract. The use of 1131-labeled fibrinogen to determine possible sites of sequestration has not been reported before in a patient with multiple hemangiomas. The eight infants included by Holden and 416

Alexander [21] in the category, “diffuse neonatal all died. Because they showed hemangiomatosis,” lung, heart, and brain involvement, this may be a specific entity. Measurement of split products of fibrin should be considered [9]. In case 2, two estimations yielded negative findings. This test should not be interpreted as an isolated value [IO], but may prove useful for complete investigation. The need for careful coagulation studies in patients with hemangiomas is clear. Pathology

Both patients showed multiple angiomatous malformations throughout the gastrointestinal tract. One patient had a few surface lesions and the other patient had hundreds of lesions on the body surface and in other tissues. None of the lesions was malignant. They should probably be considered hamartomatous malformations. A difficult therapeutic aspect of the lesions in the first patient was their apparent spontaneous reappearance in areas that had ‘previously been treated. Microscopic examination would probably have revealed them. The excised lesions fit the description of cavernous hemangiomas. The walls of the vascular spaces were lined with flattened endothelial cells. Numerous septa divided the larger vascular spaces and smo’oth muscle could be seen in the walls and in the septa. Hemangiomas and hemangiomatous syndromes do not lend themselves to simple classification. A review of attempts to cl,assify these lesions suggests that there is still some confusion. Wood’s classification [2] ‘of benign tumors arising from blood vessels in the intestines is as follows: (1) cavernous hemangiomas ; (2) capillary hemangioma ; (3) hemangiomatosis ; (4) hemangiopericytoma ; (5) multiple phl’ebectasis. This agrees closely with Han(sen’s [3] adaptation of the Kaisjer-Oberndorff classification. According to Gentry, Dockerty, and Clagett [4], multiple phlebectasia is the most common pathologic variety. The lesions are usually very small and hemorrhage is uncommon. This category includes the telangiectasias of the bowel or OslerWeber-Rendu disease. Our patients would conveniently fit into category 3. Hansen [3] claimed that only ‘eight clearcut cases of this have been reported. This entity should probably be separated from “diffuse neonatal hemangi,omatosis” as recently described by Holden and Alexander [21]. They made this diagnosis on the basis of the following criteria : (1) The patient was recognized in the neonatal period to have The American

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visceral hemangiomas. (2) Three or more organ systems were affected by the hemangiomas. (3) The hemangiomas were not malignant. They wrote that “the lesions of this particular congenital defect are vascular hamartomas possibly associated with a pericyte deficiency in the vessel wall.” They noted the presence of ,thrombocytopenia in one of their cases and attempted steroid therapy without success. The finding of literally hundreds of hemangiomas throughout the gastrointestinal tract in both of these cases justifies the use of the term, hemangiomatosis of the gastrointestinal tract.

Acknowledgment: I would like to thank C. Everett Koop, MD, for permission to publish the case from the surgical service of the Children’s Hospital of Philadelphia. I also wi,sh to express a debt of gratitude to Harry C. Bishop, MD, and Charles L. Minor, MD, who continued the care of case 1 and carried out three of the operations. References 1. Shepard 2.

3. 4.

5. 6. 7.

8.

9. 10. 11. 12.

JA: Angiomatous conditions of the gastrointestinal tract. Brit J Surg 40: 409, 1953. Wood DA: Tumors of the intestines. Atlas of Tumor Pathology, sect 6, fast 22. Washington DC, Armed Forces Institute of Pathology, 1967. Hansen PS: Hemangioma of the small intestine. Amer J Clin Path 18: 14, 1948. Gentry RW, Dockerty MB, Clagett OT: Vascular malformations and vascular tumors of the gastrointestinal tract. Surg Gynec Obstet 88: 281, 1949. Ruiz-Moreno F: Hemangiomatosis of the colon: report of a case (Mexico City). Dis Colon Rectum 5: 453, 1962. Rickham PP: A case of hemangiomatosis of the small intestine. Brit J Surg 39: 462, 1952. Zarem HA, Edgerton MT: Induced resolution of cavernous hemangiomas following prednisone therapy. Plast Reconstr Surg 39: 76, 1967. Fost NC, Esterly NB: Successful treatment of juvenile hemangiomas with prednisone. J Pediat 72: 351, 1968. Stiehm ER, Clatanoff DV: Split products of fibrin in the serum of newborns. Pediatrics 43: 770, 1969. Nathan DS, Lubin BH: Significance of split products of fibrin in serum of newborns. Pediatrics 43: 758, 1969. Pruzanski W: Intestinal and cutaneous hemangiomatosis: report of a case Amer J Digest Dis 8: 200, 1963. Copple P, Kingsbury R: Hemangiomas of the small bowel in children. J Pediat 59: 243, 1961.

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Tract

13. Weinstein EC, Moertel CG, Waugh JM: lntussuscepting hemangiomas of the gastrointestinal tract. Report of a case and review of the literature. Ann Surg 157:

265, 1963. 14. Dwyer W, Steinlauf 15. 16. 17.

18.

19.

Summary

The case histories of two children with multiple gastrointestinal hemangiomas, surface hemangiomas, and severe gastrointestinal bleeding are presented. Each child underwent resection of approximately 200 hemangiomas of the bowel. The surgical management, associated coagulation problems, and pathologic considerations are discussed. The children are alive and well twelve and six years after initial treatment, justifying the aggressive surgical treatment and cautious optimism for their future.

Hemangiomas

20.

21. 22.

23.

24.

P: Surgical implications of intestinal hemangiomas. Postgrad Med 310: 330, 1964. Burman D, Mansell P,Warin R: Military heamagniomata in the newborn. Arch Dis Child 42: 193. 1967. Kasabach HH, Merritt KK: Capillary hemangioma with extensive purpura. Amer J Dis Child 59: 1063, 1940. Scherz RG, Jouro JM, Geppert LJ: Giant hemantioendothelioma with associated thrombocytopenia. J Pediat 52: 212, 1958. James DH Jr, Tuttle AH: Congenital hemangioma with thrombocytopenia. J Pediat 59: 234, 1961. Verstraete M. Vermvlen C. Vermvlen J, Vandenbrouke J: Excessive’ consumption of blood .coagulation components as a cause of hemorrhagic diathesis. Amer J Med 38: 899, 1965. Wacksman S, Flessa HC, Glueck HI, Will JJ: Coagulation defects and giant cavernous hemangioma. Amer J Dis Child 111: 71, 1966. Holden KR, Alexander F: Diffuse neonatal hemangiomatosis. Pediatrics 46: 411, 1970. Kontras SB, Green OC, King L, Duran RJ: Giant hemangioma with thrombocytopenia. Case report with suriival and sequestration -studies of platelets labeled with CP’. Amer J Dis Child 105: 188. 1963. Brizel HE, Giovanni, R: Giant hemangioma with thrombocytopenia. Radio-isotopic demonstration of platelet sequestration. Blood 26: 751, 1965. lnglefield JT Jr, Tisdale PD, Fairchild JP: A case of hemangioma with thrombocytopenia in the newborn infant treated by total excision. J Pediat 59: 238,

1961. 25. Williams OK, VanBuskirk

26.

FW, Burns S, Mellish RWP: Giant hemangioendothelioma with thrombocytopenia and hypofibrinogenemia. Amer J Roentgen01 106: 204,1969. Blix S, Aas K: Giant hemangioma, thrombocytopenia, fibrogenopenia and fibrinolytic activity. Acta Med

Stand 169: 63, 1961.

Discussion ALBERT C. MACKAY (Burlington, Vt) : Two points come to mind. I have seen only one patient, an adult, who could possibly fall into this category. In this case, we were not faced with anywhere near the problem present in these two children who required repeated observation and laparotomy with control of bleeding by various means. I am not sure we are dealing with the same clinical syndrome when present in a patient sixty-two years of age, as is the case in my patient. It is worth calling attention to the fact that Dr Mellish has underlined some useful tools that may be used when confronted with this problem, the first of which is a method of accurately measuring the blood loss from the gastrointestinal tract. This is particularly necessary when there are multiple other large hemangiomatous lesions of the body that might cause red cell disappearance. Secondly, there is the delineation of the fibrinogen defect, which allowed him to undertake the considerable problem of removing some 250 lesions from this child. As Dr Mellish has stated, this is likely not the end of the story, and continued application and observation will be necessary. I commend the doctor for his dedication and aggressiveness in helping this child. 417