Up per gas tro in tes ti nal (UGI) bleed ing in in fants and

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1 Orig i nal Article J Chin Med Assoc 2003;66: Up per Gas tro in tes ti nal En dos copy in Children with Up per Gas tro in tes ti nal Bleeding I-Fei Huang 1 Tzee-Chung Wu 2,3 Ke-Sheng Wang 2 Betau Hwang 2,3 Kai-Sheng Hsieh 1 1 De part ment of Pe di at rics, Kaohsiung Vet erans Gen eral Hos pi tal; 2 Di vi sion of Gastroenterology and Nu tri tion, Children s Med i cal Cen ter, Tai pei Vet erans Gen eral Hos pi tal; and 3 Na tional Yang-Ming Uni ver sity School of Med i cine, Tai wan, R.O.C. Key Words endoscopy; Helicobacter pylori; superficial gastric mucosal lesions; upper gastrointestinal bleeding Up per gas tro in tes ti nal (UGI) bleed ing in in fants and chil dren is not un com mon, and it ranges in se ver ity from a wor ri some mild ep i sode to an acute panicprovoking in ci dent. Al though the var i ous clin i cal par a - digms have not changed, ad vances in en dos copy and ra di - ol ogy, as well as new ther a peu tic mo dal i ties, per mit us to pin point the cause of bleed ing more eas ily and to treat it ef fec tively. Be fore en dos copy came into com mon use, it was only pos si ble to iden tify 50% to 80% of the bleed ing Background. The pur pose of this study was to eval u ate the clin i cal pre sen ta tions and fea tures of up per gas tro in tes ti nal (UGI) en dos copy and the role of Helicobacter pylori in chil dren with UGI bleed ing. Methods. A ret ro spec tive re view was done of the med i cal re cords of 112 in fants and chil dren who pre sented with UGI bleed ing. They un der went UGI en dos copy in the Tai pei Vet erans Gen eral Hos pi tal, Tai wan be tween July 1996 and De cem ber Pa tients with hematemesis caused by swal low ing caus tic agents or for eign bod ies were ex cluded. Re sults. There were 112 pa tients in volved in this study. Clin i cal man i fes ta tions in - cluded hematemesis (77 cases, 68.8%), tarry stool (37 cases, 33%) and hematochezia (9 cases, 8%). Fifty-three patients (47.3%) had underlying dis eases, in clud ing neuromuscular def i cits (17), hepatobiliary disease (17), re nal in suf fi ciency (8), Henoch-Schonlein purpura (HSP) (3), and cow milk al lergy (3). An other 34 pa tients had a pre ced ing acute fe brile ill ness his tory. The en do scopic ap pear ances in cluded esoph a geal varices (10.7%), esophagitis or esoph a geal ul cers (30.4%), su per fi cial gas tric mucosal le sions (SGML) (44.6%), gas tric ul cers (9.8%), du o de nal ul cers (DU) (15.2%), and hem or rhagic ero sive duodenitis (2.7%). Eleven cases (9.8%) showed neg a tive find ings. There were 13 (11.6%) pa tients re ceiv ing en do scopic hemostatic ther apy. The rate of pos i tive re sults in rapid urease tests in the pa tients with out un der ly ing dis eases was 54.8%, which was sig nif i cantly higher than that of the pa tients with un der ly ing dis eases (17.1%), while Helicobacter pylori was closely re lated to pri mary DU. Conclusions. In chil dren with UGI bleed ing, UGI en dos copy pro vides an ac cu rate di ag nos tic tool and also pro vides ther a peu tic in ter ven tion when needed. SGML was the most com mon en do scopic find ing. About 30% of the in fants and chil dren with UGI bleed ing had his tory of acute fe brile ill ness. Half of the chil dren had un der ly ing dis eases. Helicobacter pylori plays a role in a sub group of chil dren with UGI bleed - ing, par tic u larly in chil dren with pri mary DU. sites, 1,2 whereas now most au thors use fiberoptic en do - scopes and re port a rate of iden ti fi ca tion of more than 80% of the bleed ing sites. 3,4 The value of cur rent pro ce dures in di ag nos tic ca pa bil i ties and in pro vid ing interventional ther apy are un de ni able; even if active bleed ing has stopped at the time of en dos copy, the pro ce dure can pro - vide im por tant in for ma tion to de ter mine if the le sion will po ten tially bleed again. 5 Based on 54 months of re search in the Tai pei Vet erans Gen eral Hos pi tal, Tai wan, this ret - Re ceived: December 10, Ac cepted: January 7, Cor re spon dence to: Tzee-Chung Wu, MD, Di vi sion of Gastroenterology and Nu tri tion, Children s Med i cal Cen ter, Tai pei Vet erans Gen eral Hos pi tal, Taipei 112, Tai wan. Fax: ; tcwu@vghtpe.gov.tw 271

2 I-Fei Huang et al. Jour nal of the Chi nese Med i cal As so ci a tion Vol. 66, No. 5 Table 1. UGI endoscopic findings in 112 children with UGI bleeding Endoscopic findings With underlyingdisease (n = 53) Without underlying disease (n = 59) p value Total patients (n = 112) Esophageal varices 12 (22.6) a (10.7) Esophagitis or esophagealulcers 17 (32.1) 17 (28.8) (30.4) Superficial gastric mucosal lesions 22 (41.5) 28 (47.5) (44.6) Gastric ulcers 3 (5.7) 8 (13.6) (9.8) Duodenal ulcers 5 (9.4) 12 (20.3) (15.2) Hemorrhagic erosive duodenitis 3 (5.7) (2.7) Negative finding 1 (1.9) 10 (16.9) (9.8) a Number in the parentheses represents the percentage; UGI = upper gastrointestinal. Table 2. The frequent underlying diseases predisposing UGI bleeding Underlying diseases ro spec tive study shows the clin i cal pre sen ta tions and causes of UGI bleed ing in chil dren. The study in ves ti gates whether the causes of UGI bleed ing dif fer from those in ci - dences in de vel oped coun tries and as sesses the role of Helicobacter pylori (H. pylori) in chil dren with UGI bleeding. METHODS UGI endoscopic findings Neuromuscular deficits (17) Esophagitis or ulcers (9) SGML (7) Duodenal ulcers (2) Hepatobiliary diseases (17) Esophageal varices (12) SGML (5) Duodenal ulcers (2) Negative finding (1) Renal insufficiency (8) Esophagitis (4) SGML (3) Gastric ulcers (2) Henoch-Schonlein Hemorrhagic erosive purpura (3) duodenitis (3) Cow milk allergy (3) SGML (3) Others (5) Esophagitis (4) SGML (4) Gastric Ulcers (1) Duodenal ulcers (1) UGI =upper gastrointestinal; SGML = superficial gastric mucosal lesions. Find ings were based on a ret ro spec tive re view of the med i cal re cords of chil dren (up to 18 years old) with UGI bleed ing who were ad mit ted at Tai pei Vet erans Gen eral Hos pi tal, Tai wan be tween July 1996 and De cem ber Those pa tients with hematemesis due to swal low ing caus - tic agents or for eign bod ies were ex cluded. To lo cal ize the site of bleeding, esophagogastroduodenoscopy (Olympus Pae di at ric Fiberscope GIF P230; Olympus Optical Co. Ltd., Tokyo, Ja pan) was per formed un der intravenous (IV) se da tion af ter vi tal signs were sta bi lized. In pa tients with gas tric or du o de nal mucosal ero sions or ul cer ations, 1 or 2 antral mu cosa were biopsied and sent for rapid urease CLO tests (Ballard Med i cal Prod ucts, Utah, U.S.A.). Statistical analysis Chi-square tests and Fisher s tests of ex act prob a bil - ity were used for sta tis ti cal com par i sons. A p value of less than 0.05 was con sid ered of sta tis ti cal sig nif i cance. RESULTS There were 112 patients analyzed in this study, 78 (69.6%) of whom were male. Their me dian age at the time of study was 6.0 y/o (rang ing from 2 months to 18 years). There were 9 pa tients un der 1 year old. Clin i cal man i fes ta - tions in cluded hematemesis (77 cases, 68.8%); tarry stool (37 cases, 33%), and hematochezia (9 cases, 8%). UGI endoscopic findings in UGI bleed ing children are shown in Ta ble 1. Fifty-three pa tients had un der ly ing diseases, including various neuromuscular diseases, hepatobiliary dis eases and mis cel la neous (Ta ble 2). Pep - tic mucosal le sions were the ma jor find ings in the re main - ing 59 patients without definite underlying diseases. Among them 34 had an acute fe brile ill ness or were with 272

3 May 2003 UGI En dos copy in Children Table 3. The positive rate of rapid urease test in 72 children with UGI bleeding Group No. (%) of patients with positive results With underlying disease Without underlying disease Total All patients 7/41 (17.1) a 17/31 (54.8) a 24/72 (33.3) Patients with DU 1/5 (20) b 8/12 (66.7) b 9/17 (52.9) a p = 0.002; b p = 0.131; DU = duodenal ulcer. Fig. 1. One uremic pa tient with gas tric ul cer bleed ing: the left im age shows ther a peu tic en dos copy with heat probe for hemostasis; the right shows a post-therapeutic pic ture. us age of antipyretics; 8 of them had vi ral enanthems, in - cluding herpangina (5) and gingivostomatitis (3). En do - scopic ap pear ance in cluded su per fi cial gas tric mucosal le - sions (SGML) (28 cases), esophagitis or ul cers (17 cases), gas tric ul cer (8 cases) and du o de nal ul cer (12 cases). Rapid urease test (CLO test) was done for 72 pa - tients. Twenty-four pa tients (33.3%) showed pos i tive re - sults (Ta ble 3). There were 46 pa tients re ceiv ing blood trans fu sions. Among the 53 pa tients with un der ly ing dis - eases, there were 31 pa tients (58.5%) hav ing blood trans - fu sions. In con trast, the blood trans fu sion rate was only 25.4% (15/59) for the patients with out un der ly ing dis - eases (p < 0.001). There were 13 (11.6%) pa tients receiving en do - scopic treat ment, in clud ing esoph a geal variceal li ga tion (EVL) (4), local in jec tion with diluted epi neph rine or sclerosants (6), and heat probe co ag u la tion (3) (Fig. 1). Of the 13 pa tients, there were 9 with un der ly ing dis eases. DISCUSSION In this study, the clin i cal pre sen ta tion of UGI bleed ing in chil dren varied in ap pear ance from coffee ground vomitus to life-threatening bleed ing. About 41% (46/112) of our pa tients had mod er ate to se vere bleed ing, and they needed blood transfusions to replenish their blood loss. Hematemesis was the most com mon clin i cal man i fes ta tion, and en do scopic ex am i na tion was proved to be an ex cel lent di ag nos tic tool; 72 of 77 pa tients with hematemesis had pos i tive en do scopic find ings, but 6 of the 46 pa tients who pre sented with tarry stool (5 cases) or hematochezia and with out hematemesis had ob scure bleed ing sources. Besides the esoph a geal varices (12 cases), which accounted for 10.7% of the bleed ing sources, pep tic mucosal le sions were the most com mon en do scopic find ings, in clud ing su per fi cial gas tric mucosal le sions, gas tric ul cers and du o de nal ul cers. These find - ings are sim i lar to those from de vel oped coun tries, where variceal bleed ing was found in 5-20% of cases 6-8 and peptic ulcer, esophagitis and gastroduodenitis occured with higher fre quency (66%). 9 In UGI bleed ing pa tients with out un der ly ing se ri ous dis eases, the causes of bleed ing in cluded H. pylori, re cent vi ral in fec tion and drugs (nonsteroidal anti-inflammatory drugs, an ti bi ot ics, ste roids, etc.), which of ten re sulted in mucosal dam age. However, except for H. pylori, the other causes were dif fi cult to trace or prove. In our se ries, there were about 30% of pa tients who, with out definite un der ly ing serious diseases, had a history of preceding acute febrile ill ness or us age of antipyretics, the ma jor en do scopic find ings were pep tic mucosal le sions. Other au thors re ported that young chil dren with UGI bleed ing had frequently had some preceding acute ill ness, and con cluded that the pep tic mucosal le sions were re lated to the fast ing state and the us age of antipyretics dur ing acute dis tress More over, our study re sults were com - patible with the peptic mu cosa pos si bly hav ing been dam aged by vi ral in fec tion; the vi ral enanthems not only ap peared on oral cavity in herpangina and gingi - vostomatitis, but also in volved the up per gas tro in tes ti nal 273

4 I-Fei Huang et al. Jour nal of the Chi nese Med i cal As so ci a tion Vol. 66, No. 5 Fig. 2. The en do scopic find ings of a pa tient with hepangina: the left shows mul ti ple dis crete ero sions over the greater cur va ture side of the body; the right shows ul cers with some hematin coat ing over the antrum. tract. The most unique en do scopic ap pear ances were the dis crete ero sions and ul cers over the stom ach and esoph - agus, sim i lar to those found in the oral cav ity (Fig. 2). The mucosal le sions in our pa tients with vi ral enanthems ill ness im proved af ter anti-acid se cre tory med i ca tions. Acute gas tric mucosal le sion (AGML) is now rec og - nized as 1 of the im por tant patho log i cal causes of UGI bleed ing. Using en dos copy, AGML may be di ag nosed if there are find ings of gas tric ero sions, hem or rhagic gas - tri tis and gastroduodenitis. 13 The le sions in en dos copy are also called erosive and/or hemorrhagic gastritis, or gastropathy by 1 classification sys tem. 14 We pre fer the term SGML, as many of our pa tients had pep tic le sions in a chronic course. There are a va ri ety of causes for SGML, such as psy cho log i cal and phys i cal stress, drugs and se ri ous or gan fail ure. In this study, we found 3 in - fants aged 2-4 months who pre sented with re peated cof - fee-ground vomiting and clinically di ag nosed as cow milk allergy. The en do scopic find ing re vealed SGML, and the gas tric mucosal bi opsy pa thol ogy showed heavy in fil tra tion of eosinophils in lamina propia. Although esophageal variceal bleeding is the most important cause of UGI bleeding in patients with hepatobiliary disease, about 30% (5/17) of our patients with underlying liver dis eases had other pep tic mucosal le sions. Esophagitis and esoph a geal ul cers were the most com mon en do scopic find ings in pa tients with un der ly ing neuromuscular def i cits not suprisingly they were at trib - uted to gastroesophageal re flux and the re main ing pep tic mucosal le sions were related to increased intracranial pres sure (IICP), stress, med i ca tions. Pa tients with chronic re nal insufficiency had peptic mucosal le sions var ied from shal low ero sions to deep ul cers (Fig. 1). The en do - scopic find ings in our chil dren with Henoch- Schonlein purpura (HSP) included gastric mucosal petechiae and hem or rhagic ero sive duodenitis, just as other stud ies re - ported H. pylori is now recognized as a cause of peptic mucosal le sions in clud ing gas tri tis, gas tric ul cers and du - o de nal ul cers. 18 In our study, the pa tients without un der - ly ing dis eases had a much higher rate of pos i tive CLO tests than those pa tients with un der ly ing dis eases, which sug gests that H. pylori in fec tion plays a sig nif i cant role in those pa tients with out un der ly ing dis eases. Ac cord ing to the lit er a ture, H. pylori can be found in more than 90% of chil dren with pri mary du o de nal ul cers. 18,19 How ever, in our study, the rate of positive CLO tests was only found in 66.7% of pa tients with pri mary du o de nal ul cer with bleed ing. This may be ex plained by re cent re ports that among pa tients with bleed ing ul cers, there were high rates of false neg a tive re sults for antral in fec tion with H. pylori when as sessed by rapid urease tests Most of our pa tients with UGI bleed ing were treated successfully with conservative man age ment, such as IV fluid, anti-acid secretory drugs and blood trans fu sions, par tic u larly in pa tients with un der ly ing dis eases. In ad di - tion, somatostatin analogues were used in those with esophageal variceal bleeding. Nevertheless, there were some pa tients (11.6%) who still needed ther a peu tic en dos - copy for hemostasis, including EVL and sclerotherapy. 5 All patients had a satisfactory hemostatic result. No pa - tient needed emergency sur gery in our study. Nev er the - less, for patients with unstable hemodynamic sta tus, the pe di at ric sur geon should be con sulted early. 23 In sum mary, UGI bleed ing is not un com mon in pe di - at ric pa tients. En do scopic ex am i na tion pro vides ex cel - lent di ag nos tic help and also pro vides ther a peu tic in ter - ven tion when needed. About 30% of the in fants and chil - dren with UGI bleed ing had his tory of acute fe brile ill - ness, and half of the chil dren had un der ly ing dis eases such as neuromuscular def i cit, hepatobiliary dis ease, and re nal insufficiency. Su per fi cial gastric mucosal lesion was the most com mon endoscopic find ing. Al though most of the bleed ing will stop spon ta ne ously, there are 274

5 May 2003 UGI En dos copy in Children some pa tients who need en do scopic hemostasis ther apy. Fur ther more, H. pylori plays a role in a sub group of chil - dren with UGI bleeding, par tic u larly in chil dren with pri - mary du o de nal ul cers. REFERENCES 1. Sherman NJ, Clatworthy HW. Gas tro in tes ti nal bleed ing in ne - o nates: a study of 94 cases. Sur gery 1967;62: Spencer R. Gas tro in tes ti nal hem or rhage in in fancy and child - hood: 476 cases. Sur gery 1964;55: Ament ME, Berquist WE, Vargas J, Perisic V. Fiberoptic up per in tes ti nal en dos copy in in fants and chil dren. Pediatr Clin North Am 1988;35: Hyams JS, Leichtner AM, Schwartz AN. Re cent ad vances in di ag no sis and treat ment of gas tro in tes ti nal hem or rhage in in - fants and chil dren. J Pediatr 1985;106: Wu TC. Bleeding pep tic ul cer. Sin ga pore Pediatr J 1999;41: Cox K, Ament ME. Up per gas tro in tes ti nal bleed ing in chil d - ren and ad o les cents. Pe di at rics 1979;63: Gleason WA, Tedesco FJ, Keating JP, Goldstein PD. Fiberoptic gas tro in tes ti nal en dos copy in in fants and chil dren. J Pediatr 1974;85: Gra ham DY, Klish WJ, Ferry GD, Sabel JS. Value of fiberoptic en dos copy in in fants and chil dren. South Med J 1978;71: Vinton NE. Gas tro in tes ti nal bleed ing in in fancy and child - hood. Gastroenterol Clin North Am 1994;23: Hsu HY, Chang MH, Wang TH, Hsu JY, Wang CY, Lin MI, et al. Acute du o de nal ul cer. Arch Dis Child 1989;64: Chen PH, Chang MH, Chuang YH, Liu YC. Acute ef fects of fe ver, fast ing and as pi rin on in fant rat gas tric mu cosa. J Formos Med Assoc 1989;88: Wu MH, Chang MH, Hsu JY. Pep tic ul cer in child hood: clin i - cal and en do scopic ob ser va tions. Acta Pediatr Sinica 1983; 24: Yakabi K, Nakamura T. Acute gastroduodenal mucosal le sion. Jpn J Clin Med 1998;56: Dohil R, Hassall E, Jevon G, Dimmick J. Gas tri tis and gastropathy of child hood. J Pediatr Gastroenterol Nutr 1999;29: Saulsbury FT. Henoch-Schonlein purpura in chil dren: re port of 100 pa tients and re view of lit er a ture. Med i cine 1999; 78: Tin CW, Wu TC, Cheng JH, Hwang BT. Gas tro in tes ti nal mani - festations and en do scopic find ings in chil dren with Henoch- Schonlein purpura. Chung-Hua Min Kuo Hsiao Erh Ko i Hsueh Hui Tsa Chih 1988;29: Kato S, Shibuya H, Naganuma H, Nakagawa H. Gas tro in tes ti - nal en dos copy in Henoch-Schonlein purpura. Eur J Pediatr 1992;151: Mac ar thur C, Saunders N, Feldman W. Helicobacter pylori, gastroduodenal dis ease and re cur rent ab dom i nal pain in chil d - ren. JAMA 1995;273: Vandenplas Y, Blecker U. Helicobacter pylori in fec tion in chil dren. Acta Paediatr 1998;87: Archinmandritis A, Tzivras M, Sougioultzis S, Papaparaskevas I, Apostolopoulos P, Avlami A, et al. Rapid urease test is less sen si tive than his tol ogy in di ag nos ing Helicobacter pylori in - fec tion in pa tients with non-variceal up per gas tro in tes ti nal bleed ing. J Gastroentero Hepatol 2000;15: Colin R, Czernichow P, Baty V, Touze I, Bra zier F, Bretagne JF, et al. Low sen si tiv ity of in va sive tests for the de tec tion of Helicobacter pylori in fec tion in pa tients with bleed ing ul cer. Gastroenterol Clin Biol 2000;24: Tu TC, Lee CL, Wu CH, Chen TK, Chen CC, Huang SH, Lee SC. Com par i son of in va sive and noninvasive tests for de tect - ing Helicobacter pylori in fec tion in bleed ing pep tic ul cers. Gastrointest Endosc 1999;49: Gershman G, Ament ME. Pe di at ric up per gas tro in tes ti nal en - dos copy: state of the art. Acta Paediatr Tai wan 1999;40: