arteriovenous malformations of the gastrointestinal tract

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ClinicalRadiology (1981) 32, 623-628 0009-9260/81/01480623502.00 © 1981 Royal College of Radiologists Arteriovenous Malformations of the Gastrointestinal Tract S. FATAAR*, P. MORTON and A. SCHULMAN Department o/Diagnostic Radiology, Groote Schuur Hospital/University of Cape Town, Observatory, Cape Town, South Africa Congenital arteriovenous malformations of bowel occurring as solitary or multiple lesions may cause obscure gastrointestinal bleeding with negative radiological and endoscopic studies. These malformations may be missed at laparotomy and selective visceral angiography is essential for localisation and to assess the extent of the lesions. An immediate post-resection radiograph with barium injection into the arteries is recommended to assess the completeness of the resection before abdominal closure. There is a need, when discussing vascular malformations of the bowel, to distinguish the acquired degenerative colonic lesions from the congenital arteriovenous malformations which are more common in the small bowel. Arteriovenous malformations (AVM) of bowel are rare causes of both acute and chronic gastrointestinal haemorrhage. The nomenclature in the past four decades has been confusing and includes the terms telangiectasia (Gentry et al., 1949), angioma (Shep- herd, 1953), haemangioma (Taylor and Torrance, 1974; Morson and Dawson, 1979) and arteriovenous malformation (Klein et al., 1971; Alfidi et al., 1971; Cooperman et al., 1972; Crichlow et al., 1975 ; Moore et al., 1976). With the increasing use of angiography over the past 20 years in the assessment of gastro- intestinal bleeding, AVM have been more frequently recognised. However, confusion may arise with the right colonic lesions referred to as angiodysplasia (Baum et al., 1977) or vascular ectasia (Boley et al., 1977) which clinicopathologically are acquired conditions in the elderly and should be regarded separately. The following five cases illustrate the angiographic spectrum of the AVM of bowel which are congenital in origin. Patient 3 has already been documented (GoMin et al., 1979). CASE REPORTS Patient 1. A 54-year-old male presented with the passage of a large amount of fresh blood rectally. He was shocked and, with a haemoglobin of 8.5 g/dl, required five units of blood for resuscitation. He had been completely well before this admission. General examination was non-contributory. Barium meal, barium enema and gastroscopy were normal as was the blood-clotting profile. Superior mesenteric angio- graphy revealed an AVM of the proximal jejunum (Figs la, b). Coeliac and inferior mesenterie angiograms were normal. *Correspondence address: Dr S. Fataar, Department of Diagnostic Radiology, Groote Schuur Hospital, Observatory, Cape Town 7925, South Africa. At laparotomy, the jejunum appeared normal even with transillumination. 55 cm of proximal jejunum was resected as well as a 3 cm turnout in the mid-ileal region. The patient remained well over the next year. On histology many large blood vessels of both arterial and venous types were found throughout the bowel wall with no evidence of malignant change. The ileal nodule contained interlacing bundles of dense collagen with a low degree of cellularity and was regarded as a leiomyoma which had undergone collagenisation. Patient 2. A 64-year-old female presented after moderately large rectal bleeds on three occasions in five months. On each occasion blood transfusions were necessary. Ten years earlier she had had a similar episode of bleeding following which a haemorrhoidectomy was performed as no other cause was found. On examination she was generally well, but had an ejection systolic murmur over the aortic valve area. Her Hb was 9.7 g/dl. Barium meal, barium enema and colonoscopy were all normal. Suoerior mesenteric angiography revealed an AVM of the mid-to-distal transverse colon (Figs 2a, b). At laparotomy the abnormal vessels were easily seen and the distal transverse colon was reseeted. The patient has remained well since surgery. Histology revealed dilated vascular channels resembling arteries and veins in the submucosa and serosa. There was evidence of thrombosis in both vessel types. There was no evidence of ulceration in the resected specimen. Patient 3. A 44-year-old male had a history of several previous admissions over the past two years to a neighbouring hospital for recurrent melaena and iron deficiency anaemia, requiring blood transfusions on each occasion. He presented again with anaemia and melaena stools. His Hb was 5.2 g/dl. Barium meal and barium enema were normal. Gastroscopy on two occasions, including jejunoscopy into the proximal 26 cm of jejunum, and colonoseopy revealed no cause for the bleeding. A technetium scan for Meckel's diverticulum was negative. Angiography established the presence of a duo- denojejunal AVM (Figs 3a, b). The eoeliae, gastroduodenal and inferior mesenteric angiograms were normal. Following refusal of surgery the patient had five further episodes of bleeding. At eventual laparotomy the third and fourth parts of the duodenum and 15 em of jejunum, all of which appeared macroscopically normal, were resected. The extent of the resection was determined from the angiogram. The patient

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Page 1: Arteriovenous malformations of the gastrointestinal tract

ClinicalRadiology (1981) 32, 623-628 0009-9260/81/01480623502.00 © 1981 Royal College of Radiologists

Arteriovenous Malformations of the Gastrointestinal Tract S. FATAAR*, P. M O R T O N and A. S C H U L M A N

Department o/Diagnostic Radiology, Groote Schuur Hospital/University o f Cape Town, Observatory, Cape Town, South Africa

Congenital ar ter iovenous mal fo rmat ions o f bowel occurring as solitary or mul t ip le lesions may cause obscure gastrointestinal bleeding wi th negative radiological and endoscopic studies. These mal format ions may be missed at l apa ro tomy and selective visceral angiography is essential for local isat ion and to assess the ex ten t o f the lesions. An immedia te post-resect ion radiograph wi th bar ium inject ion into the arteries is r e c o m m e n d e d to assess the completeness o f the resect ion before abdominal closure. There is a need, when discussing vascular mal format ions o f the bowel , to distinguish the acquired degenerative colonic lesions f rom the congeni tal ar ter iovenous mal format ions which are more c o m m o n in the small bowel .

Arter iovenous mal format ions (AVM) o f bowel are rare causes of bo th acute and chronic gastrointest inal haemorrhage. The nomenc la tu re in the past four decades has been confusing and includes the terms telangiectasia (Gent ry et al., 1949), angioma (Shep- herd, 1953), haemangioma (Taylor and Torrance , 1974; Morson and Dawson, 1979) and ar ter iovenous mal format ion (Klein et al., 1971; Alf idi et al., 1971; Cooperman et al., 1972; Crichlow et al., 1975 ; Moore et al., 1976). With the increasing use o f angiography over the past 20 years in the assessment o f gastro- intestinal bleeding, AVM have been more f requent ly recognised. However , confus ion may arise wi th the right colonic lesions referred to as angiodysplasia (Baum et al., 1977) or vascular ectasia (Boley et al., 1977) which cl inicopathological ly are acquired condi t ions in the elderly and should be regarded separately. The fol lowing five cases il lustrate the angiographic spec t rum o f the A V M of bowel which are congeni tal in origin. Pat ient 3 has already been documen ted (GoMin et al., 1979).

CASE REPORTS

Patient 1. A 54-year-old male presented with the passage of a large amount of fresh blood rectally. He was shocked and, with a haemoglobin of 8.5 g/dl, required five units of blood for resuscitation. He had been completely well before this admission. General examination was non-contributory. Barium meal, barium enema and gastroscopy were normal as was the blood-clotting profile. Superior mesenteric angio- graphy revealed an AVM of the proximal jejunum (Figs la, b). Coeliac and inferior mesenterie angiograms were normal.

*Correspondence address: Dr S. Fataar, Department of Diagnostic Radiology, Groote Schuur Hospital, Observatory, Cape Town 7925, South Africa.

At laparotomy, the jejunum appeared normal even with transillumination. 55 cm of proximal jejunum was resected as well as a 3 cm turnout in the mid-ileal region. The patient remained well over the next year. On histology many large blood vessels of both arterial and venous types were found throughout the bowel wall with no evidence of malignant change. The ileal nodule contained interlacing bundles of dense collagen with a low degree of cellularity and was regarded as a leiomyoma which had undergone collagenisation.

Patient 2. A 64-year-old female presented after moderately large rectal bleeds on three occasions in five months. On each occasion blood transfusions were necessary. Ten years earlier she had had a similar episode of bleeding following which a haemorrhoidectomy was performed as no other cause was found. On examination she was generally well, but had an ejection systolic murmur over the aortic valve area. Her Hb was 9.7 g/dl. Barium meal, barium enema and colonoscopy were all normal. Suoerior mesenteric angiography revealed an AVM of the mid-to-distal transverse colon (Figs 2a, b). At laparotomy the abnormal vessels were easily seen and the distal transverse colon was reseeted. The patient has remained well since surgery. Histology revealed dilated vascular channels resembling arteries and veins in the submucosa and serosa. There was evidence of thrombosis in both vessel types. There was no evidence of ulceration in the resected specimen.

Patient 3. A 44-year-old male had a history of several previous admissions over the past two years to a neighbouring hospital for recurrent melaena and iron deficiency anaemia, requiring blood transfusions on each occasion. He presented again with anaemia and melaena stools. His Hb was 5.2 g/dl. Barium meal and barium enema were normal. Gastroscopy on two occasions, including jejunoscopy into the proximal 26 cm of jejunum, and colonoseopy revealed no cause for the bleeding. A technetium scan for Meckel's diverticulum was negative. Angiography established the presence of a duo- denojejunal AVM (Figs 3a, b). The eoeliae, gastroduodenal and inferior mesenteric angiograms were normal. Following refusal of surgery the patient had five further episodes of bleeding. At eventual laparotomy the third and fourth parts of the duodenum and 15 em of jejunum, all of which appeared macroscopically normal, were resected. The extent of the resection was determined from the angiogram. The patient

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624 C L I N I C A L R A D I O L O G Y

Fig. la - Patient 1. Superior mesenteric angiogram. The first five jejunal arteries (arrows) are dilated and supply an abun- dant meshwork o f peripheral vessels.

was well post-operatively and a repeat superior mesenteric angiogram a year later was normal. On histology there were dilated submucosal channels resembling veins and arteries. A few engorged, p rominen t capillaries were present in the lamina propria.

Fig. lb - Patient 1. Superior mesenteric angiogram. Capillary phase reveals contrast med ium persistence in the dilated vascular channels. Venous filling was normal.

Patient 4. A 57-year-old female was transferred from a rural hospital where she had had a vagotomy and pyloroplasty for presumed haemorrhagic gastritis causing massive gastro- intestinal bleeding. Despite the surgery she continued bleeding and was admit ted here a week later where resuscitat ion was

Fig. 2a - Patient 2. Superior mesenter ic angiogram. The middle colic artery (arrows) is dilated and supplies prominent , to r tuous arteries to the distal transverse colon. There is no early venous filling.

Fig. 2b - Patient 2. Superior mesenteric angiogram. Dilated, to r tuous veins drain into the dense middle colic vein (arrow- heads) which persisted late into the venous phase. Superior mesenteric vein is well seen (arrow).

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AV M A L F O R M A T I O N S O F T H E GI T R A C T 625

Fig. 3a - Patient 3. Superior mesenteric angiogram. Dense blushing of the duodenoje junal area (arrowheads) with early portal vein filling (arrow) in the late arterial phase. (Courtesy of South African Medical Journal.)

Fig. 3b - Patient 3. Selective angiogram of first jejunal artery. There is extravasat ion o f contrast due to rupture of the abnormal vascular spaces. Early portal vein filling is again noted. (Courtesy of South African Medical Journal.)

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626 CLINICAL RADIOLOGY

followed by gastroscopy which confirmed the presence of severe gastritis with a shallow erosion on the greater curve. She remained stable for a week, but then had another episode of bleeding. On repeat gastroscopy no active bleeding could be detected from the stomach or duodenum. Coeliac, mesen- teric and pancreaticoduodenal angiograms were normal. Because of persistent bleeding requiring transfusion, a lapar- otomy was performed and dilated, ectatic veins, due to an AVM, were found from the third part of duodenum to the duodenojejunal flexure. This segment of duodenum and jejunum was resected. Post-operatively the patient became septicaemic and at laparotomy a week later there was gross peritoneal soiling from disruption of the anastomosis. After repafr and drainage, the course was complicated by renal failure, with death a week later. Histology of the resected bowel revealed large and small vascular channels with features of arteries and veins and evidence of intimal proliferation. The mucosal surface over the vascular area showed evidence of superficial ulceration. On retrospective assessment of the angiograms, it was still not possible to detect the malformation.

Patient 5. A 22-year-old female presented with chronic anaemia and gastrointestinal bleeding requiring regular trans- fusions of blood over three years. She had no family history of note and had not experienced any significant epistaxis in the past. Examination revealed a small telangiectatie focus on

Fig. 4a - Patient 5. Superior mesenteric angiogram. Prominent superior mesenteric artery (arrowhead) sup- plies small ectatic tufts in bowel (white arrows). There is dense, early filling of the superior mesenteric and portal veins (black arrow) which emptied rapidly.

the lower lip and left cheek. Apart from moderate hepato. splenomegaly, the rest of the examination was normal. Her stool was repeatedly strongly positive for occult blood and her haemoglobin was 4 g/dl. An isotope scan for Meckel's diverticulum was negative as were endoscopy of the upper gastrointestinal tract, barium meal and follow-through, barium enema and colonoscopy. Aortography and selective coeliac and superior mesenteric angiography revealed features compatible with hereditary haemorrhagic telangiectasia (Figs 4a, b). At laparotomy multiple, dilated, small serosal and mucosal vessels could be seen from 45 cm from the duo. denojejunal flexure down to 100cm from the terminal ileum. This abnormal segment of small bowel was resected and the patient remained well post-operatively. A year later there was neither melaena nor malabsorption. Her Hb was 14.4 g/dl and her weight had increased by 4 kg. Histology of the resected specimen revealed abnormal dilated vessels throughout the bowel wall. Many vessels were thick-walled and the features were of a hamartomatous nature compatible with hereditary haemorrhagic telangiectasia.

DISCUSSION

Since angiography began to be used in the 1960s for the de t ec t i on o f gastrointes t inal bleeding

(Margulis et al., 1960; Boijsen and Reu te r , 1967)

Fig. 4b - Patient 5. Splenic angiogram. Ectatic vascular foci are seen throughout the spleen. Similar changes were noted in the liver.

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A V M A L F O R M A T I O N S O F T H E G I T R A C T 627

vascular malformations have been recognised on angiograPhY as a cause of either acute upper or lower gastrointestinal bleeding or chronic unexplained melaena. On reviewing some of the earlier reported cases of vascular malformations of the gastrointestinal tract, it is obvious that many of the lesions illustrated are of both the acquired and congenital types (Reuter and Redman, 1977; Cooperman e t al., 1972; Alfidi et al., 1971 ; Sheedy e ta l . , 1975). As a result of work by Baum et al. (1977) and Boley et al. (1977) the acquired malformation affecting especially the right colon has been well defined, but there is a need to separate this from congenital AVM of bowel. The acquired lesion has a typical angiographic appearance, namely a dense draining vein appearing early with persistent opacification late into the venous phase. The lesion may also have a vascular tuft and occasion- ally one may see active bleeding.

Shepherd (1953) has indicated the difficulty in differentiating congenital vascular malformations (hamartomas) from angiomas (benign neoplasms) on histological grounds and concludes that it is highly likely that most of these lesions are congenital and we are calling them arteriovenous malformations. This concept is supported by Moore e t al. (1976) who identified three distinct groups of patients based on the clinical, angiographic and histological features. Their first group is the acquired variety with localised lesions affecting the right colon in patients with an average age of 63 years. The other two groups involve younger patients and are congenital AVM.

Malan and Puglionisi (1964, 1965) have a complex classification for the congenital vascular malforma- tions affecting the periphery, but their basic aetio- logical hypothesis may be applied to bowel. There is probably a breakdown in the normal resorption of the primitive capillary rete linking the arterial and venous trunks. The severity of arteriovenous shunting will be determined by the size of the remaining channels which may be lined by only a single layer of endothelial cells and may, in their more usual sub- mucosal location, be close to the bowel lumen so that bleeding readily occurs. Gastrointestinal haemorrhage may be acute (Patients 1,2 and 4) or chronic (Patients 3 and 5). Other complications are less common and include intussusception or obstruction due to a mass effect (Gentry e t al., 1949; Shepherd, 1953). Lesions are commonest in the small bowel, followed by colon, rectum and anus (Gentry e t al., 1949). The stomach, duodenum, oesophagus and appendix are less commonly affected. The lesions are usually solitary, but may be multiple involving only the intes- tine or many organs and tissues throughout the body. The presence of vascular lesions on the skin or the mucous membranes is of great value in suggesting the

diagnosis of hereditary haemorrhagic telangiectasia especially where a family history is present. In our patient (Number 5), the small stellate lesion on the cheek and purpuric spot on the lip assumed retrospec- tive significance only after the angiographic diagnosis. She was unusual also in that a family history was absent and she had never had any epistaxis.

Typically, in bleeding from gastrointestinal AVM, all routine upper and lower gastrointestinal radiological and endoscopic studies are normal. Occasionally a plain radiograph of the abdomen may reveal phlebo- liths in the vascular channels of extensive cavernous lesions especially in the rectosigmoid region (Morson and Dawson, 1979). They may reveal a sinuous, plexi- form pattern on barium enema which may alter in appearance on supine and erect projections (Van Niekerk, 1980). Occasionally, a purple discoloration of the mucosa may be detected on endoscopy but this is unusual and extensive lesions may be missed even at laparotomy when transillumination may be of no value (Patient 1) (Moore et al., 1976). Our small series is unusual in that two of the localised lesions were readily seen at laparotomy (Patients 2 and 4), including one that was missed at angiography. Patients 1 and 3 emphasise the need for preoperative angio- graphy to establish both the presence and the extent of the lesions as neither was visible at laparotomy.

The angiographic features of AVM faithfully reproduce the abnormal vascular channels seen histo- logically. The meshwork of dilated vessels (Patients 1 and 2) is often supplied by dilated arteries which may be tortuous. Enlarged veins accompany these arteries, the size being determined by the extent of the abnormal channels and the degree of shunting. The latter will also determine the timing and the extent of venous opacification.

Thus venous filling may be rapid (Patients 3 and 5) with opacification in the arterial phase, or it may be normal (Patients 1 and 2) and either of these situa- tions may be associated with prolonged venous drainage due to slow flow in the vascular pools. Rapid shunting may result in early venous filling and clearing (Patient 5) even when no other abnormality is detected. Mucosal blushing may be intense (Patient 3) while extravasation of contrast is unusual except when bleeding is active and severe. Very rarely, some of these features may be mimicked by a leiomyosarcoma, carcinoid or caecal carcinoma, but these should be obvious on barium studies or at laparotomy (Alfidi et al., 1971).

In the assessment of these patients all major arteries (coeliac, superior and inferior mesenteric arteries) should be injected as the lesions may be multiple (Gentry et al., 1949;Moore etal . , 1976;Alifldi, 1971). Moore et al. (1976) recommend subselective arterio-

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628 CLINICAL RADIOLOGY

graphy and magnification techniques and it is possible that this would have enabled detection of the AVM in Patient 4. Another explanation in this patient is that the lesion was a purely venous malformation with no arterial supply, but both venous and arterial elements were identified on histology.

Pre-operative angiography would also allow diagnosis of multiple lesions which may determine resectability of the lesions. Intra-operative angiography has been recommended (Alfidi et al., 1971) but has not proved popular and there is always a risk of mesenteric ischaemia in these studies (Crichlow et al., 1975). More useful is a radiograph following the injection of barium into the arteries of the resected specimen to assess the completeness of resection of the AVM (Moore et al., 1976; Sheedy et al., 1975).

When leiomyomas or other tumours or a Meckel's diverticulum are detected during angiography or laparotomy, then these should also be removed as any of these may be a source of bleeding (Patient 1).

Hereditary haemorrhagic telangiectasia represents the severest form of arteriovenous malformation with involvement of multiple systems, usually occurring as a familial disease with Mendelian recessive trans- mission. In patients presenting with gastrointestinal haemorrhage from an obscure cause a family history with recurrent epistaxis from a young age would suggest this possibility while the presence of cutaneous or mucosal telangiectatic foci would strengthen the diagnosis. Our patient was unusual in that there was no family history and only very small vascular lesions were noted on her cheek and lip. It is also unusual for the gastrointestinal haemorrhage to be so severe in such a young patient. Th6 angiographic features are diagnostic and have been detailed by Halpern et al. (1968). In our patient the abnormal vascular opacifi- cation (Fig. 4a) with early filling and rapid emptying of the veins was probably due to conglomerate masses of angiectasia with rapid shunting of blood through them. Similar multiple foci accounted for the diffuse small accumulations of contrast medium in the liver and spleen (Fig. 4b). At laparotomy these lesions were all visible as foci of dilated vessels.

Acknowledgements. We wish to thank Mrs J. Tuft for the photographic assistance and Mrs A. van de Vijver and Miss B. Neumann for the typing.

REFERENCES

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