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The watermelon stomach: clinical presentation, diagnosis, and treatment
THE AMERICAN JOURNAL OF GASTROENTEROLOGY Copyright © 1998 by Am. Coll. of Gastroenterology Published by Elsevier Science Inc.
Vol. 93, No. 6, 1998 ISSN 0002-9270/98/$19.00 PII S0002-9270(98)00152-X
The Watermelon Stomach: Clinical Presentation, Diagnosis, and Treatment Jeffrey E. Gretz, M.D., Ph.D., and Sami R. Achem, M.D., F.A.C.P., F.A.C.G. University of Florida, Health Science Center/Jacksonville, and Mayo Clinic, Jacksonville, Florida
The watermelon stomach syndrome is an increasingly recognized cause of persistent acute or occult gastrointestinal bleeding, typically in elderly women. This disorder often presents with severe iron deficiency anemia, and a variety of associated conditions including autoimmune disease, cirrhosis, achlorhydria, and hypochlorhydria. Diagnosis is made by the characteristic endoscopic appearance of visible linear watermelon-like vascular stripes in the antrum. Histology confirms the vascular nature of this disorder, showing dilated and thrombosed capillaries in the lamina propria, associated with reactive fibromuscular hyperplasia. The optimum treatment of choice is not known. Several treatment options, including surgical antrectomy, and endoscopic photocoagulation with Nd:Yag laser, heater probe therapy, and bipolar electrocautery, have yielded excellent results. Pharmacological agents have also been used to treat selected numbers of patients, most of which comprise a small number of case reports. (Am J Gastroenterol 1998; 93:890 – 895. © 1998 by Am. Coll. of Gastroenterology)
columns collectively resemble in appearance the stripes of a watermelon, in 1984, Jabbari et al. coined the term of “watermelon stomach” to refer to this condition. Using Medline search terms that include gastric antral vascular ectasia and watermelon stomach, a search from 1962 to 1996 of the English language published papers have yielded the following review of this syndrome’s clinical, endoscopic, and pathological features, along with the current surgical and nonsurgical treatment modalities. CLINICAL PRESENTATION Watermelon stomach was considered an exotic rarity, having been recognized in only three of 10,000 endoscopy cases (4). In current series it is increasingly noted as a cause of chronic gastrointestinal blood loss (5, 6). The syndrome is more common in elderly women. A total of 164 patients with a clinical diagnosis of watermelon stomach were identified in our review. Of the 164 patients, 125 were women (76%), with a mean age of 69.1 yr (range 42– 89 yr). In the largest consecutive series (7) of patients collected from a single institution (45 patients), 71% were female, with a mean age of 73 yr (range 53– 89 yr). The average age of male patients was 68 yr (range 40 – 81 yr). The clinical presentation of watermelon stomach is summarized in Table 1. Most patients come to medical attention for evaluation of occult bleeding and severe and persistent iron deficiency anemia. Of the 164 patients identified with the clinical diagnosis of watermelon stomach, 144 of 164 (88%) presented with iron deficiency anemia, 68 of 164 (42%) presented with an occult gastrointestinal bleed or heme-positive stool, 24 of 164 (15%) presented with melena, five of 164 (3%) with hematemesis, and two of 164 (1.2%) with hematochezia. Gostout et al. (7) reported that most patients (89%) came to medical attention for evaluation of occult bleeding and severe and persistent iron deficiency anemia. Although blood loss rarely exceeds 250 mg/day, iron replacement usually fails to maintain hemoglobin at the normal level (8). Transfusion-dependent gastrointestinal bleeding was noted in 62% of the patients, with a mean 10 units (range 2–50 units) transfusion requirement over a 12-month period. Other case reports have reported similar findings (2, 4, 9, 10).
INTRODUCTION Gastric antral vascular ectasia is a rare and often misdiagnosed cause of recurrent upper gastrointestinal bleeding. This disorder was initially described in 1953 by Rider et al. (1), as an unusual case of a 62-yr-old white woman with anemia and occult gastrointestinal blood loss, whose subtotal gastrectomy surgical specimen was found to have “an erosive type of atrophic gastritis with marked veno-capillary ectasia.” In 1979, Wheeler et al. reported on two patients who presented with iron deficiency anemia, who bled from curious vascular lesions whose appearance being somewhat similar to “angiodysplasia of the colon” (2). In 1984, Lee et al. described two patients with iron deficiency anemia, whose upper endoscopic examinations revealed diffuse red antral speckling with the “appearance of dilated blood vessels” (3). The diagnostic hallmark of gastric antral vascular ectasia is based on endoscopic features: visible columns of vessels transversing the antrum in longitudinal folds and converging in the pylorus. Because the longitudinal red Received June 27, 1997; accepted Mar. 6, 1998. 890
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TABLE 1 Clinical Presentation of Watermelon Stomach* (n 5 164 patients) Iron deficiency anemia Heme positivity Melena Hematemesis Hematochezia
88% 42% 15% 3% 1%
* Percentages do not add up to 100% because many patients had two or more clinical presentations. TABLE 2 Commonly Associated Clinical Conditions Raynauld’s phenomenon Sclerodactyly Atrophic gastritis Achlorhydria Hypochlorhydria Primary biliary cirrhosis Hypothyroidism Diabetes mellitus Autoimmune liver disease Cirrhosis Portal hypertension Chronic renal failure Cardiovascular heart disease
ETIOLOGY AND ASSOCIATED CONDITIONS The etiology of watermelon stomach remains unknown; this disorder has been found in association with several clinical conditions detailed in Table 2. In Gostout’s series (7), 28 of 45 patients (62%) had autoimmune and connective tissue disorders. The most common associated disorders involved Raynaud’s phenomenon in 14 of 45 patients (31%), and sclerodactyly in 8 of 45 patients (18%). Additionally, in patients in whom biopsies where obtained, atrophic gastritis occurred in 19 of 19 (100%), and hypergastrinemia was noted in 25 of 33 of patients (76%) tested. The mean serum gastrin value was 2345 pg/ml (nl 0 –200), with a range of 240 – 6800 pg/ml. Of the 25 patients with elevated gastrin level, 14 of 25 (56%) had a history of vitamin B-12 deficiency, and carried a diagnosis of pernicious anemia as a result of abnormal Schilling’s tests. Other commonly associated autoimmune conditions are listed in Table 2 and include hypothyroidism (7), primary biliary cirrhosis (7, 11), diabetes mellitus (7), and autoimmune liver disease (7). Nonautoimmune conditions frequently associated with watermelon stomach include up to a 60% incidence of cirrhosis (12–14), portal hypertension (6, 15–18), chronic renal failure (7, 19), hypertension (19), cardiovascular heart disease (7), achlorhydria, and severe hypochlorhydria (13). DIAGNOSIS The diagnosis of watermelon stomach is based on the characteristic endoscopic appearance as shown in Figure 1.
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Jabbari et al. initially described the typical lesions as longitudinal rugal folds traversing the antrum and converging on the pylorus, each containing a visible convoluted column of vessels, the aggregate resembling the stripes on a watermelon (4). Recently, Gostout et al. (7) have reported a spectrum of four endoscopic patterns in watermelon stomach: a) raised convoluted ridges with overlying vascular ectasia, b) the same pattern described in a) but with a flat appearance, c) a mixed pattern of flat and raised “stripes”, and d) diffuse scattered vascular lesions. The majority of cases (89%) present with either raised or flat stripes of ectatic vascular tissue, whereas the diffusely scattered lesions accounted for the remaining 11%. Although these lesions are confined to the antrum, 27% of the patients may have proximal gastric involvement, typically in the presence of a diaphragmatic hernia. The endoscopic appearance of watermelon stomach can resemble portal hypertensive gastropathy. The following characteristics can help to distinguish these two clinical entities: a) watermelon stomach occurs most often in the absence of portal hypertension; b) watermelon stomach has a distinctive endoscopic appearance of erythematous longitudinal rugal folds transversing the antrum and converging on the pylorus, whereas portal hypertensive gastropathy has classically been described as a diffuse mosaic pattern or scarlatina rash located in the proximal stomach; c) watermelon stomach usually presents with a worse Child-Pugh score, a greater degree of anemia and digestive blood loss in comparison with portal hypertensive gastropathy; d) both mucosal abnormalities and bleeding associated with watermelon stomach predictably responds well to endoscopic coagulation or surgical antrectomy; in contrast, portal hypertensive gastropathy responds best to medical or surgical portal decompression (20, 21). Recent reports indicate that endoscopic ultrasound may also add to the distinguishing features between these two entities. In watermelon stomach, a thickened antral wall ,1 cm in some areas (22), with a spongy appearance of the mucosa and submucosa, is observed (23, 24), whereas in patients with portal hypertensive gastropathy, the gastric wall is diffusely thickened, with evidence of dilated veins (23). Other imaging modalities such as barium studies, computed tomography (CT), and angiographic studies are of no diagnostic value. Occasional reports have shown nonspecific findings such as persistent antral folds on barium study (25), focal thickening of prepyloric antral wall by CT imaging (22, 26), and hypervascularity of the gastric antrum by angiography (27, 28). HISTOPATHOLOGY The histopathological findings are sufficient to allow the diagnosis of watermelon stomach. Recent reports have demonstrated that endoscopic pinch biopsies are specific to differentiate between watermelon stomach and several other common antral entities such as portal hypertensive gastropa-
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AJG – Vol. 93, No. 6, 1998 characteristic of watermelon stomach, distinguishing this syndrome from normals, acute gastritis, and atrophic gastritis (20, 30). A study by Suit et al. compared the histological and morphological finding of endoscopic pinch biopsies in patients with watermelon stomach versus normals, chronic gastritis, atrophic gastritis, and ulcers. The features that most distinguished watermelon stomach from other conditions were: a) an increase in mean blood vessel crosssectional area, b) intravascular fibrin thrombi, and c) fibromuscular hyperplasia (29). Surgical resected specimens demonstrate additional features such as thickened mucosa and tortuous submucosal venous channels running in a longitudinal direction toward the pylorus (2, 4, 14, 32, 33). PATHOGENESIS
FIG. 1. The archetypical endoscopic appearance of the gastric antral lesion (from Ref. 3, copyright permission granted by W.B. Saunders and Company).
thy, acute gastritis, and chronic atrophic gastritis. The typical appearance of watermelon stomach consists of hypertrophy of the antral mucosa, dilation of mucosal capillaries with focal thrombosis, and fibromuscular hyperplasia of the lamina propria (4, 7, 13, 23, 27, 29–31) as shown in Figure 2. Additionally, spindle cell proliferation into the mucosa is
The pathogenesis of watermelon stomach is unknown. It has been proposed that traumatic gastric peristalsis causes prolapse of the antral mucosa with consequent elongation and ectasia of the mucosal vessels (4, 29, 34). These authors argue that vigorous antral contractions expose the antrum to the greatest trauma during strong contractions. Additional support for a traumatic etiology for watermelon stomach comes from histologic findings. Vascular ectasia and fibromuscular obliteration of the lamina propria, both characteristic of watermelon stomach, are common to other gastrointestinal lesions known to associated with trauma and mucosal prolapse, such as stomal sites, solitary rectal ulcer
FIG. 2. The microscopic features of watermelon stomach. Superficial hyperplastic gastric antral mucosa with dilated capillaries and thrombosis.
AJG – June 1998 syndrome, and prolapsed hemorrhoids (29). Others have proposed that the observed vessels represent exuberant mucosal and submucosal collaterals (35). The association of cirrhosis and portal hypertension in nearly 50% of the reported cases of watermelon stomach suggests that this lesion is acquired in response to obstruction or hypertension of mesenteric circulation. This proposal has been significantly weakened by the following three observations: a) there are normal angiographic studies in patients with watermelon stomach, b) the incidence of watermelon stomach in cirrhotic patients is rare, c) half of patients with watermelon stomach do not have cirrhosis. There is no satisfactory explanation for the tendency of these lesions to bleed. Acute inflammatory changes in the gastric mucosa are rarely found. Gastric acid appears to be of no importance, inasmuch as there is often hypo- or achlorhydria in many of these patients. Local factors may contribute to the development of this lesion. Two recent studies analyzed the surgically resected antrum of patients with watermelon stomach by immunohistochemical and electron microscopic studies. These authors revealed extraepithelial and intraepithelial neuroendocrine cell proliferation. Staining for a wide range of neural and endocrine markers, the authors demonstrated that these cells contain large quantities of 5-hydroxytryptamine and vasoactive intestinal polypeptide. These findings suggest that locally released neurotransmitters may account for local vasodilation and hence a propensity to bleed (8, 36). In addition, the presence of microthrombi in mucosal vessels suggests that capillary thrombosis may cause focal ischemia, which might be the main instigator of occult bleeding (14).
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compared Nd:Yag laser treatment to argon laser therapy in seven transfusion dependent patients with watermelon stomach. Although a small study, they concluded that the Nd:yag laser requires fewer treatments sessions (2.33 6 0.27 vs 5.75 6 0.89), than the argon laser to obliterate the lesions. Similar good results have been obtained in a limited number of patients (13 cases) using a heater probe unit (15, 43). Endoscopic improvement was evident in 12 of 13 patients (93%), with only mild anemia being reported in two of 13 (16%), over a mean follow-up period of 20.9 months (range 8 –50 months). Experience with bipolar electrocoagulation is limited to a case report. Binmoeller et al. (44) successfully treated a patient who, after four sessions, had almost complete resolution of visible vessel disease and no further bleeding over a follow-up period of 7 months. Additionally, Rose (45) reported significant reduction in blood transfusion requirements, in a series of seven patients, via multiple endoscopic sclerotherapy injections of absolute alcohol into the submucosa of “diffuse antral anomalies” that appeared as red “tiger stripes.” Although endoscopic laser treatment seems to offer an effective control of hemorrhage, it requires expensive technology not widely available. Further studies including larger numbers of patients with more affordable tools (heater probe) are sorely needed. SURGICAL THERAPY
The optimal treatment of choice for watermelon stomach is not known. Therapy depends on the rate of blood loss. Conservative therapy utilizing oral or parenteral iron substitutes and occasional blood transfusions may be sufficient in individual cases. If such measures fail, several treatment modalities have been proposed including surgical, endoscopic, and pharmacologic approaches.
Surgical antrectomy with Billroth I anastomosis has been the treatment used in 37 of 42 (88%) reported surgical cases. In 36 of these cases for which data is available, no further bleeding was noted in 36 of 36 patients (100%) over a follow-up period ranging from 1 to 24 months (Table 3). Five additional surgical cases reported in the literature have employed a partial gastrectomy with Roux-en-Y (33), total gastrectomy for diffuse gastric bleeding (46), total gastrectomy with esophagojejunostomy for an incidental gastric carcinoma (47), subtotal gastrectomy with Billroth II anastomosis (37), and antrectomy with vagotomy (26). Antrectomy clearly offers excellent definitive therapy; however, operative mortality is reported at a rate of 7.4% for this operation (13).
ENDOSCOPIC THERAPY
PHARMACOLOGICAL THERAPY
Endoscopic approaches have employed Nd:Yag laser, argon laser, heater probe therapy, bipolar electrocautery, and endoscopic sclerotherapy. Excellent results have been reported with Nd:Yag laser in three large series comprising a total of 73 patients (7, 10, 19). In most of these cases, after 3– 4 laser sessions over a period of 4 –12 months, resolution of visible disease and anemia and elimination of blood transfusions requirements were successfully accomplished with a follow-up of #6 yr. Review of the literature has yielded 28 additional cases, with similar excellent results using laser therapy (11, 23, 35, 37– 41) Bjorkman et al. (42),
A variety of pharmacological agents have been used to treat selected patients with watermelon stomach: prednisone (4, 27, 46), prednisolone (9, 28, 34, 48, 49), estrogenprogesterone preparation (28), alfa-interferon (50), and the serotonin antagonist cyproheptadine (51). The precise mechanism of how steroids control bleeding is not known; it has been shown that corticosteroids maintain vascular tone and heighten vascular sensitivity to vasoconstrictive agents (9). Eight patients have been treated with either prednisone or prednisolone for gastrointestinal bleeding caused by watermelon stomach, five of eight
TREATMENT OPTIONS
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TABLE 3 Reported Surgical Treatments for Watermelon Stomach
Ref.
Procedure
1 2 6 7 8 25 27 27 30 32 34 34 36 37 52 53 54 37
antrectomy 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 subtotal gastrectomy and Billroth II anastomosis partial gastrectomy and Roux-en-Y total gastrectomy total gastrectomy and esophagojejunostomy antrectomy with vagotomy
33 46 47 26 Total
No. (n) of Patients
Follow-Up (months)
Further Bleeding (Y/N)
1 4 3 1 1 1 3 8 5 2 1 1 1 1 1 1 2 1
14 8–24 n/a n/a 3 16 13–21 n/a n/a 6–18 6 n/a 12 n/a 1 18 6–24 n/a
N N N n/a N N N N N N N N N N N N N n/a
1
3
N
1 1
22 n/a
Y n/a
1
3
N
42
n/a 5 No data available. Y/N 5 Yes/No.
(62%) had complete resolution of further bleeding episodes over a follow-up period of 1–5 yr (9, 27, 28, 48). One patient continued to have occult bleeding, but her anemia was controlled (4). The remaining two patients who failed steroid therapy were treated with antrectomy (34) and Nd:Yag laser therapy (19). One patient whose bleeding was controlled on prednisolone suffered from hyperglycemia. She was switched and maintained on 30 mg of ethinyl estradiol and 1.5 mg of norethisterone daily taken for 3 wk each month (28). Previous studies have suggested a potential role of 5-hydroxytryptamine to induce gastrointestinal bleeding in watermelon stomach (8, 36). Using this information, Pina Cabral et al. (51) reported that the serotonin antagonist cypro-heptadine at 4 mg t.i.d. improved endoscopic visible disease and eliminated further gastrointestinal bleeding in one patient over a 12-month period. Disdier et al. (50) reported one patient with watermelon stomach and hepatitis C who was treated with alfa-interferon at 3 M.U. subcutaneously three times/wk for 5 months, with complete resolution of viremia, endoscopically visible disease, and increasing hemoglobin level over this time. The mechanism by which resolution of vascular gastropathy occurs during treatment with alfa-interferon is
not known. Three hypotheses could be advanced: a directed antifibrotic effect of alfa-interferon on watermelon stomachassociated perivascular fibrohyalinosis, an antiviral effect of alfa-interferon on HCV, and an alfa-interferon-induced improvement of hepatic function (50). CONCLUSION The watermelon stomach syndrome is an increasingly recognized cause of persistent acute or occult gastrointestinal bleeding, typically in elderly women. This disorder presents with severe iron deficiency anemia and occult or overt gastrointestinal bleeding. The patients with watermelon stomach may have a variety of associated disorders, which include autoimmune disease, cirrhosis, achlorhydria, and hypochlorhydria. Diagnosis is made by the characteristic endoscopic appearance of visible linear watermelonlike vascular stripes in the antrum. Histology confirms the vascular nature of this disorder, showing dilated and thrombosed capillaries in the lamina propria associated with reactive fibromuscular hyperplasia. The optimal treatment is not known. Several treatment modalities, including surgical antrectomy, endoscopic photocoagulation with Nd:Yag laser, heater probe therapy, and bipolar electrocautery, have yielded excellent results. Pharmacological agents have also been used to treat selected patients with watermelon stomach; unfortunately, most of these reports comprise small numbers of cases. To date, no clinical trials have been reported directly comparing the various therapeutic or pharmacologic options. Future research in this area is needed to better understand the etiology, pathogenesis, and natural history of this vascular antral lesion. Reprints requests and correspondence: Sami R. Achem, M.D., F.A.C.P., F.A.C.G., Mayo Clinic, Jacksonville, Gastroenterology Division, 4600 San Pablo Road, Jacksonville, FL 32224.
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AJG – June 1998 11. Tsai HH, Smith J, Danesh BJ. Successful control of bleeding from gastric antral vascular ectasia (watermelon stomach) by laser photocoagulation. Gut 1991;32:93– 4. 12. Lee FI, Costello F, Flanagan N, et al. Diffuse antral vascular ectasia. Gastrointestinal Endoscopy 1984;30:87–90. 13. Borsch G. Diffuse antral vascular ectasia: The “watermelon stomach” revised. Am J Gastroenterol 1987;82:1333– 4. 14. Arendt T, Barten M, Lakner V, et al. Diffuse gastric antra vascular ectasia: Cause of chronic gastrointestinal blood loss. Endoscopy 1987; 19:218 –20. 15. Kamberoglou D, Kakkak M, Bennett JR. Case of watermelon stomach successfully treated by heat probe electrocoagulation. Gut 1992;33: 964. 16. Zuckerman GR, Cornette GL, Clouse RE, et al. Upper gastrointestinal bleeding in patients with chronic renal failure. Ann Intern Med 1985; 102:588 –92. 17. Dave P, Romeu J, Antonelli A, et al. Gastrointestinal telangiectasia: A source of bleeding in patients receiving hemodialysis. Arch Intern Med 1984;114:1781–3. 18. Cunningham JT: Gastric telangiectasias in chronic hemodialysis patients: A report of six cases. Gastroenterology 1981;81:1131–3. 19. Liberski SM, McGarrity TJ, Hartle RJ, et al. The watermelon stomach: Long-term outcome in patients treated with Nd:Yag laser therapy. Gastrointestinal Endoscopy 1994;40:584 –7. 20. Payen JL, Cales P, Voigt JJ, et al. Severe portal hypertensive gastropathy and antral vascular ectasia are distinct entities in patients with cirrhosis. Gastroenterology 1995;108:138 – 44. 21. Viggiano TR, Gostout CJ. Portal hypertensive intestinal vasculopathy: A review of the clinical, endoscopic, and histopathologic features. Am J Gastroenterol 1992;87:944 –54. 22. Barnard GF, Colby JM, Saltzman JR, et al. Endoscopic ultrasound appearance of watermelon stomach. Abdom Imag 1995;20:26 – 8. 23. Parente F, Petrillo M, Vago L, et al. The watermelon stomach: Clinical, endoscopic, endosonographic, and therapeutic aspects in three cases. Endoscopy 1995;27:203– 6. 24. Avundak C, Hampf F. Endoscopic ultrasound in the diagnosis of watermelon stomach. J Clin Gastroenterology 1996;22:104 – 6. 25. Gilinsky NH, Giles OA, O’Conner WN. Gastric antral vascular ectasia (“watermelon stomach”): First bleeding after aortic valve replacement. J Clin Gastroenterol 1987;9:612–5. 26. Urban BA, Jones B, Fishman EK, et al. Gastric antral vascular ectasia (“watermelon stomach”): Radiologic findings. Radiology 1991;178: 517– 8. 27. Kruger R, Ryan ME, Dickson KB, et al. Diffuse vascular ectasia of the gastric antrum. Am J Gastroenterol 1987;82:421– 6. 28. Moss SF, Ghosh P, Thomas DM, et al. Gastric antral vascular ectasia: Maintenance treatment with oestrogen-progesterone. Gut 1992;33:715–7. 29. Suit PF, Petras RE, Bauer TW, et al. Gastric antral vascular ectasia. A histologic and morphometric study of “the watermelon stomach”. Am J Surg Pathol 1987;11:750 –7. 30. Gilliam JH III, Geisinger KR, Wu WC, et al. Endoscopic biopsy is diagnostic in gastric antral vascular ectasia. Digest Dis Sci 1989;34: 885– 8. 31. Wolf DC, Brooks WS. Antral vascular ectasia of cirrhosis: Endoscopic laser therapy. Gastrointest Endosc 1986;32:139 – 40.
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32. Tovey FI. Gastric antral vascular ectasia: The watermelon stomach. Gastroenterology 1985;88:1293. 33. Gardiner GW, Murray D, Prokipchuk EJ. Watermelon stomach, or antral gastritis. J Clin Path 1985;85:1317– 8. 34. Rawlinson WD, Barr GD, Lin BPC. Antral vascular ectasia—the “watermelon” stomach. Med J Australia 1986;144:709 –11. 35. Frager JD, Brandt LJ, Frank MS, et al. Treatment of a patient with watermelon stomach using transendoscopic laser photocoagulation. Gastrointest Endosc 1988;34:134 –7. 36. Lowes JR, Rode J. Neuroendocrine cell proliferations in gastric antral vascular ectasia. Gastroenterology 1989;97:207–12. 37. Watson M, Hally RJ, McCue PA, et al. Gastric antral vascular ectasia (watermelon stomach) in patients with systemic sclerosis. Arthritis Rheum 1996;39:341– 6. 38. Potamiano S, Carter CR, Anerson JR. Endoscopic laser treatment of diffuse gastric antral vascular ectasia. Gut 1994;35:461–3. 39. Scolapio JS, Matteson EL. The watermelon stomach in scleroderma. Arthrit Rheumotol 1993;36:724 –5. 40. Labenz J, Borsch G. Bleeding watermelon stomach treated by Nd-Yag laser photocoagulation. Endoscopy 1993;25:240 –2. 41. Brennan FN, Cowen AE, Laurence BH. Successful treatment of two patients with gastric antral vascular ectasia “watermelon stomach” using endoscopic Nd-Yag laser therapy. Aust NZ J Med 1991;21:439 – 41. 42. Bjorkman DJ, Buchi KN. Endoscopies laser therapy of the watermelon stomach. Lasers Surg Med 1992;12:478 – 81. 43. Petrini JL Jr, Johnston JH. Heater proble treatment for antral vascular ectasia. Gastrointest Endos 1989;35:324 – 8. 44. Binmoeller KF, Katon RM. Bipolar electrocoagulation for watermelon stomach. Gastrointest Endosc 1990;36:399 – 402. 45. Rose JDR. Endoscopic injection of alcohol for bleeding from gastroduodenal vascular anomalies. Br Med J 1987;295:93– 4. 46. Cales P, Voigt JL, Payen JL, et al. Diffuse vascular ectasia of the antrum, duodenum, and jejunum in a patient with nodular regenerative hyperplasia. Lack of response to portosystemic shunt or gastrectomy. Gut 1993;34:558 – 61. 47. Berk T, Slemmer JR, Friedman LS. Gastric antral vascular ectasia associated with gastric carcinoma. Am J Gastroenterol 1991;86:768 – 70. 48. Bhowmick BK. Watermelon stomach treated with oral corticosteroid. J R Soc Med 1993;86:52. 49. Suzuki T, Hirano M, Oka H. Long-term corticosteroid therapy for gastric antral vascular ectasia. Am J Gastroenterol 1996;91:1873– 4. 50. Disdier P, Schleinitz N, Perreard M, et al. Dramatic improvement of watermelon stomach with alfa-interferon. Am J Gastroenterol 1995; 90:1009 –10. 51. Pina Cabral JE, Pontes JM, Toste M, et al. Watermelon stomach: Treatment with a serotonin antagonist. Am J Gastroenterol 1991;86: 927– 8. 52. Tanaka T, Mori Y, Morishita Y, et al. Gastric antral vascular ectasia. Human Pathol 1991;22:1053–5. 53. Gouldesbrough DR, Pell ACH. Gastric antral vascular ectasia: A problem of recognition and diagnosis. Gut 1991;32:954 –5. 54. Manolios N, Eliades C, Duncombe V, et al. Scleroderma and watermelon stomach. J Rheumatol 1996;23:776 – 8.
Vol. 93, No. 6, 1998 ISSN 0002-9270/98/$19.00 PII S0002-9270(98)00152-X
The Watermelon Stomach: Clinical Presentation, Diagnosis, and Treatment Jeffrey E. Gretz, M.D., Ph.D., and Sami R. Achem, M.D., F.A.C.P., F.A.C.G. University of Florida, Health Science Center/Jacksonville, and Mayo Clinic, Jacksonville, Florida
The watermelon stomach syndrome is an increasingly recognized cause of persistent acute or occult gastrointestinal bleeding, typically in elderly women. This disorder often presents with severe iron deficiency anemia, and a variety of associated conditions including autoimmune disease, cirrhosis, achlorhydria, and hypochlorhydria. Diagnosis is made by the characteristic endoscopic appearance of visible linear watermelon-like vascular stripes in the antrum. Histology confirms the vascular nature of this disorder, showing dilated and thrombosed capillaries in the lamina propria, associated with reactive fibromuscular hyperplasia. The optimum treatment of choice is not known. Several treatment options, including surgical antrectomy, and endoscopic photocoagulation with Nd:Yag laser, heater probe therapy, and bipolar electrocautery, have yielded excellent results. Pharmacological agents have also been used to treat selected numbers of patients, most of which comprise a small number of case reports. (Am J Gastroenterol 1998; 93:890 – 895. © 1998 by Am. Coll. of Gastroenterology)
columns collectively resemble in appearance the stripes of a watermelon, in 1984, Jabbari et al. coined the term of “watermelon stomach” to refer to this condition. Using Medline search terms that include gastric antral vascular ectasia and watermelon stomach, a search from 1962 to 1996 of the English language published papers have yielded the following review of this syndrome’s clinical, endoscopic, and pathological features, along with the current surgical and nonsurgical treatment modalities. CLINICAL PRESENTATION Watermelon stomach was considered an exotic rarity, having been recognized in only three of 10,000 endoscopy cases (4). In current series it is increasingly noted as a cause of chronic gastrointestinal blood loss (5, 6). The syndrome is more common in elderly women. A total of 164 patients with a clinical diagnosis of watermelon stomach were identified in our review. Of the 164 patients, 125 were women (76%), with a mean age of 69.1 yr (range 42– 89 yr). In the largest consecutive series (7) of patients collected from a single institution (45 patients), 71% were female, with a mean age of 73 yr (range 53– 89 yr). The average age of male patients was 68 yr (range 40 – 81 yr). The clinical presentation of watermelon stomach is summarized in Table 1. Most patients come to medical attention for evaluation of occult bleeding and severe and persistent iron deficiency anemia. Of the 164 patients identified with the clinical diagnosis of watermelon stomach, 144 of 164 (88%) presented with iron deficiency anemia, 68 of 164 (42%) presented with an occult gastrointestinal bleed or heme-positive stool, 24 of 164 (15%) presented with melena, five of 164 (3%) with hematemesis, and two of 164 (1.2%) with hematochezia. Gostout et al. (7) reported that most patients (89%) came to medical attention for evaluation of occult bleeding and severe and persistent iron deficiency anemia. Although blood loss rarely exceeds 250 mg/day, iron replacement usually fails to maintain hemoglobin at the normal level (8). Transfusion-dependent gastrointestinal bleeding was noted in 62% of the patients, with a mean 10 units (range 2–50 units) transfusion requirement over a 12-month period. Other case reports have reported similar findings (2, 4, 9, 10).
INTRODUCTION Gastric antral vascular ectasia is a rare and often misdiagnosed cause of recurrent upper gastrointestinal bleeding. This disorder was initially described in 1953 by Rider et al. (1), as an unusual case of a 62-yr-old white woman with anemia and occult gastrointestinal blood loss, whose subtotal gastrectomy surgical specimen was found to have “an erosive type of atrophic gastritis with marked veno-capillary ectasia.” In 1979, Wheeler et al. reported on two patients who presented with iron deficiency anemia, who bled from curious vascular lesions whose appearance being somewhat similar to “angiodysplasia of the colon” (2). In 1984, Lee et al. described two patients with iron deficiency anemia, whose upper endoscopic examinations revealed diffuse red antral speckling with the “appearance of dilated blood vessels” (3). The diagnostic hallmark of gastric antral vascular ectasia is based on endoscopic features: visible columns of vessels transversing the antrum in longitudinal folds and converging in the pylorus. Because the longitudinal red Received June 27, 1997; accepted Mar. 6, 1998. 890
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TABLE 1 Clinical Presentation of Watermelon Stomach* (n 5 164 patients) Iron deficiency anemia Heme positivity Melena Hematemesis Hematochezia
88% 42% 15% 3% 1%
* Percentages do not add up to 100% because many patients had two or more clinical presentations. TABLE 2 Commonly Associated Clinical Conditions Raynauld’s phenomenon Sclerodactyly Atrophic gastritis Achlorhydria Hypochlorhydria Primary biliary cirrhosis Hypothyroidism Diabetes mellitus Autoimmune liver disease Cirrhosis Portal hypertension Chronic renal failure Cardiovascular heart disease
ETIOLOGY AND ASSOCIATED CONDITIONS The etiology of watermelon stomach remains unknown; this disorder has been found in association with several clinical conditions detailed in Table 2. In Gostout’s series (7), 28 of 45 patients (62%) had autoimmune and connective tissue disorders. The most common associated disorders involved Raynaud’s phenomenon in 14 of 45 patients (31%), and sclerodactyly in 8 of 45 patients (18%). Additionally, in patients in whom biopsies where obtained, atrophic gastritis occurred in 19 of 19 (100%), and hypergastrinemia was noted in 25 of 33 of patients (76%) tested. The mean serum gastrin value was 2345 pg/ml (nl 0 –200), with a range of 240 – 6800 pg/ml. Of the 25 patients with elevated gastrin level, 14 of 25 (56%) had a history of vitamin B-12 deficiency, and carried a diagnosis of pernicious anemia as a result of abnormal Schilling’s tests. Other commonly associated autoimmune conditions are listed in Table 2 and include hypothyroidism (7), primary biliary cirrhosis (7, 11), diabetes mellitus (7), and autoimmune liver disease (7). Nonautoimmune conditions frequently associated with watermelon stomach include up to a 60% incidence of cirrhosis (12–14), portal hypertension (6, 15–18), chronic renal failure (7, 19), hypertension (19), cardiovascular heart disease (7), achlorhydria, and severe hypochlorhydria (13). DIAGNOSIS The diagnosis of watermelon stomach is based on the characteristic endoscopic appearance as shown in Figure 1.
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Jabbari et al. initially described the typical lesions as longitudinal rugal folds traversing the antrum and converging on the pylorus, each containing a visible convoluted column of vessels, the aggregate resembling the stripes on a watermelon (4). Recently, Gostout et al. (7) have reported a spectrum of four endoscopic patterns in watermelon stomach: a) raised convoluted ridges with overlying vascular ectasia, b) the same pattern described in a) but with a flat appearance, c) a mixed pattern of flat and raised “stripes”, and d) diffuse scattered vascular lesions. The majority of cases (89%) present with either raised or flat stripes of ectatic vascular tissue, whereas the diffusely scattered lesions accounted for the remaining 11%. Although these lesions are confined to the antrum, 27% of the patients may have proximal gastric involvement, typically in the presence of a diaphragmatic hernia. The endoscopic appearance of watermelon stomach can resemble portal hypertensive gastropathy. The following characteristics can help to distinguish these two clinical entities: a) watermelon stomach occurs most often in the absence of portal hypertension; b) watermelon stomach has a distinctive endoscopic appearance of erythematous longitudinal rugal folds transversing the antrum and converging on the pylorus, whereas portal hypertensive gastropathy has classically been described as a diffuse mosaic pattern or scarlatina rash located in the proximal stomach; c) watermelon stomach usually presents with a worse Child-Pugh score, a greater degree of anemia and digestive blood loss in comparison with portal hypertensive gastropathy; d) both mucosal abnormalities and bleeding associated with watermelon stomach predictably responds well to endoscopic coagulation or surgical antrectomy; in contrast, portal hypertensive gastropathy responds best to medical or surgical portal decompression (20, 21). Recent reports indicate that endoscopic ultrasound may also add to the distinguishing features between these two entities. In watermelon stomach, a thickened antral wall ,1 cm in some areas (22), with a spongy appearance of the mucosa and submucosa, is observed (23, 24), whereas in patients with portal hypertensive gastropathy, the gastric wall is diffusely thickened, with evidence of dilated veins (23). Other imaging modalities such as barium studies, computed tomography (CT), and angiographic studies are of no diagnostic value. Occasional reports have shown nonspecific findings such as persistent antral folds on barium study (25), focal thickening of prepyloric antral wall by CT imaging (22, 26), and hypervascularity of the gastric antrum by angiography (27, 28). HISTOPATHOLOGY The histopathological findings are sufficient to allow the diagnosis of watermelon stomach. Recent reports have demonstrated that endoscopic pinch biopsies are specific to differentiate between watermelon stomach and several other common antral entities such as portal hypertensive gastropa-
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AJG – Vol. 93, No. 6, 1998 characteristic of watermelon stomach, distinguishing this syndrome from normals, acute gastritis, and atrophic gastritis (20, 30). A study by Suit et al. compared the histological and morphological finding of endoscopic pinch biopsies in patients with watermelon stomach versus normals, chronic gastritis, atrophic gastritis, and ulcers. The features that most distinguished watermelon stomach from other conditions were: a) an increase in mean blood vessel crosssectional area, b) intravascular fibrin thrombi, and c) fibromuscular hyperplasia (29). Surgical resected specimens demonstrate additional features such as thickened mucosa and tortuous submucosal venous channels running in a longitudinal direction toward the pylorus (2, 4, 14, 32, 33). PATHOGENESIS
FIG. 1. The archetypical endoscopic appearance of the gastric antral lesion (from Ref. 3, copyright permission granted by W.B. Saunders and Company).
thy, acute gastritis, and chronic atrophic gastritis. The typical appearance of watermelon stomach consists of hypertrophy of the antral mucosa, dilation of mucosal capillaries with focal thrombosis, and fibromuscular hyperplasia of the lamina propria (4, 7, 13, 23, 27, 29–31) as shown in Figure 2. Additionally, spindle cell proliferation into the mucosa is
The pathogenesis of watermelon stomach is unknown. It has been proposed that traumatic gastric peristalsis causes prolapse of the antral mucosa with consequent elongation and ectasia of the mucosal vessels (4, 29, 34). These authors argue that vigorous antral contractions expose the antrum to the greatest trauma during strong contractions. Additional support for a traumatic etiology for watermelon stomach comes from histologic findings. Vascular ectasia and fibromuscular obliteration of the lamina propria, both characteristic of watermelon stomach, are common to other gastrointestinal lesions known to associated with trauma and mucosal prolapse, such as stomal sites, solitary rectal ulcer
FIG. 2. The microscopic features of watermelon stomach. Superficial hyperplastic gastric antral mucosa with dilated capillaries and thrombosis.
AJG – June 1998 syndrome, and prolapsed hemorrhoids (29). Others have proposed that the observed vessels represent exuberant mucosal and submucosal collaterals (35). The association of cirrhosis and portal hypertension in nearly 50% of the reported cases of watermelon stomach suggests that this lesion is acquired in response to obstruction or hypertension of mesenteric circulation. This proposal has been significantly weakened by the following three observations: a) there are normal angiographic studies in patients with watermelon stomach, b) the incidence of watermelon stomach in cirrhotic patients is rare, c) half of patients with watermelon stomach do not have cirrhosis. There is no satisfactory explanation for the tendency of these lesions to bleed. Acute inflammatory changes in the gastric mucosa are rarely found. Gastric acid appears to be of no importance, inasmuch as there is often hypo- or achlorhydria in many of these patients. Local factors may contribute to the development of this lesion. Two recent studies analyzed the surgically resected antrum of patients with watermelon stomach by immunohistochemical and electron microscopic studies. These authors revealed extraepithelial and intraepithelial neuroendocrine cell proliferation. Staining for a wide range of neural and endocrine markers, the authors demonstrated that these cells contain large quantities of 5-hydroxytryptamine and vasoactive intestinal polypeptide. These findings suggest that locally released neurotransmitters may account for local vasodilation and hence a propensity to bleed (8, 36). In addition, the presence of microthrombi in mucosal vessels suggests that capillary thrombosis may cause focal ischemia, which might be the main instigator of occult bleeding (14).
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compared Nd:Yag laser treatment to argon laser therapy in seven transfusion dependent patients with watermelon stomach. Although a small study, they concluded that the Nd:yag laser requires fewer treatments sessions (2.33 6 0.27 vs 5.75 6 0.89), than the argon laser to obliterate the lesions. Similar good results have been obtained in a limited number of patients (13 cases) using a heater probe unit (15, 43). Endoscopic improvement was evident in 12 of 13 patients (93%), with only mild anemia being reported in two of 13 (16%), over a mean follow-up period of 20.9 months (range 8 –50 months). Experience with bipolar electrocoagulation is limited to a case report. Binmoeller et al. (44) successfully treated a patient who, after four sessions, had almost complete resolution of visible vessel disease and no further bleeding over a follow-up period of 7 months. Additionally, Rose (45) reported significant reduction in blood transfusion requirements, in a series of seven patients, via multiple endoscopic sclerotherapy injections of absolute alcohol into the submucosa of “diffuse antral anomalies” that appeared as red “tiger stripes.” Although endoscopic laser treatment seems to offer an effective control of hemorrhage, it requires expensive technology not widely available. Further studies including larger numbers of patients with more affordable tools (heater probe) are sorely needed. SURGICAL THERAPY
The optimal treatment of choice for watermelon stomach is not known. Therapy depends on the rate of blood loss. Conservative therapy utilizing oral or parenteral iron substitutes and occasional blood transfusions may be sufficient in individual cases. If such measures fail, several treatment modalities have been proposed including surgical, endoscopic, and pharmacologic approaches.
Surgical antrectomy with Billroth I anastomosis has been the treatment used in 37 of 42 (88%) reported surgical cases. In 36 of these cases for which data is available, no further bleeding was noted in 36 of 36 patients (100%) over a follow-up period ranging from 1 to 24 months (Table 3). Five additional surgical cases reported in the literature have employed a partial gastrectomy with Roux-en-Y (33), total gastrectomy for diffuse gastric bleeding (46), total gastrectomy with esophagojejunostomy for an incidental gastric carcinoma (47), subtotal gastrectomy with Billroth II anastomosis (37), and antrectomy with vagotomy (26). Antrectomy clearly offers excellent definitive therapy; however, operative mortality is reported at a rate of 7.4% for this operation (13).
ENDOSCOPIC THERAPY
PHARMACOLOGICAL THERAPY
Endoscopic approaches have employed Nd:Yag laser, argon laser, heater probe therapy, bipolar electrocautery, and endoscopic sclerotherapy. Excellent results have been reported with Nd:Yag laser in three large series comprising a total of 73 patients (7, 10, 19). In most of these cases, after 3– 4 laser sessions over a period of 4 –12 months, resolution of visible disease and anemia and elimination of blood transfusions requirements were successfully accomplished with a follow-up of #6 yr. Review of the literature has yielded 28 additional cases, with similar excellent results using laser therapy (11, 23, 35, 37– 41) Bjorkman et al. (42),
A variety of pharmacological agents have been used to treat selected patients with watermelon stomach: prednisone (4, 27, 46), prednisolone (9, 28, 34, 48, 49), estrogenprogesterone preparation (28), alfa-interferon (50), and the serotonin antagonist cyproheptadine (51). The precise mechanism of how steroids control bleeding is not known; it has been shown that corticosteroids maintain vascular tone and heighten vascular sensitivity to vasoconstrictive agents (9). Eight patients have been treated with either prednisone or prednisolone for gastrointestinal bleeding caused by watermelon stomach, five of eight
TREATMENT OPTIONS
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TABLE 3 Reported Surgical Treatments for Watermelon Stomach
Ref.
Procedure
1 2 6 7 8 25 27 27 30 32 34 34 36 37 52 53 54 37
antrectomy 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 subtotal gastrectomy and Billroth II anastomosis partial gastrectomy and Roux-en-Y total gastrectomy total gastrectomy and esophagojejunostomy antrectomy with vagotomy
33 46 47 26 Total
No. (n) of Patients
Follow-Up (months)
Further Bleeding (Y/N)
1 4 3 1 1 1 3 8 5 2 1 1 1 1 1 1 2 1
14 8–24 n/a n/a 3 16 13–21 n/a n/a 6–18 6 n/a 12 n/a 1 18 6–24 n/a
N N N n/a N N N N N N N N N N N N N n/a
1
3
N
1 1
22 n/a
Y n/a
1
3
N
42
n/a 5 No data available. Y/N 5 Yes/No.
(62%) had complete resolution of further bleeding episodes over a follow-up period of 1–5 yr (9, 27, 28, 48). One patient continued to have occult bleeding, but her anemia was controlled (4). The remaining two patients who failed steroid therapy were treated with antrectomy (34) and Nd:Yag laser therapy (19). One patient whose bleeding was controlled on prednisolone suffered from hyperglycemia. She was switched and maintained on 30 mg of ethinyl estradiol and 1.5 mg of norethisterone daily taken for 3 wk each month (28). Previous studies have suggested a potential role of 5-hydroxytryptamine to induce gastrointestinal bleeding in watermelon stomach (8, 36). Using this information, Pina Cabral et al. (51) reported that the serotonin antagonist cypro-heptadine at 4 mg t.i.d. improved endoscopic visible disease and eliminated further gastrointestinal bleeding in one patient over a 12-month period. Disdier et al. (50) reported one patient with watermelon stomach and hepatitis C who was treated with alfa-interferon at 3 M.U. subcutaneously three times/wk for 5 months, with complete resolution of viremia, endoscopically visible disease, and increasing hemoglobin level over this time. The mechanism by which resolution of vascular gastropathy occurs during treatment with alfa-interferon is
not known. Three hypotheses could be advanced: a directed antifibrotic effect of alfa-interferon on watermelon stomachassociated perivascular fibrohyalinosis, an antiviral effect of alfa-interferon on HCV, and an alfa-interferon-induced improvement of hepatic function (50). CONCLUSION The watermelon stomach syndrome is an increasingly recognized cause of persistent acute or occult gastrointestinal bleeding, typically in elderly women. This disorder presents with severe iron deficiency anemia and occult or overt gastrointestinal bleeding. The patients with watermelon stomach may have a variety of associated disorders, which include autoimmune disease, cirrhosis, achlorhydria, and hypochlorhydria. Diagnosis is made by the characteristic endoscopic appearance of visible linear watermelonlike vascular stripes in the antrum. Histology confirms the vascular nature of this disorder, showing dilated and thrombosed capillaries in the lamina propria associated with reactive fibromuscular hyperplasia. The optimal treatment is not known. Several treatment modalities, including surgical antrectomy, endoscopic photocoagulation with Nd:Yag laser, heater probe therapy, and bipolar electrocautery, have yielded excellent results. Pharmacological agents have also been used to treat selected patients with watermelon stomach; unfortunately, most of these reports comprise small numbers of cases. To date, no clinical trials have been reported directly comparing the various therapeutic or pharmacologic options. Future research in this area is needed to better understand the etiology, pathogenesis, and natural history of this vascular antral lesion. Reprints requests and correspondence: Sami R. Achem, M.D., F.A.C.P., F.A.C.G., Mayo Clinic, Jacksonville, Gastroenterology Division, 4600 San Pablo Road, Jacksonville, FL 32224.
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