Fu-Jing Lv, Xiao-Lan Luo, Rui Jin, Hui-Guo Ding, Department of Digestive Diseases, Beijing You’an Hospital, Capital Medical University, Beijing 100069, China
Xin Meng, Pathology Department, Beijing You’an Hospital, Capital Medical University, Beijing 100069, China
Shu-Tian Zhang, Department of Digestive Diseases, Beijing Friendship Hospital, Capital Medical University, Beijing 100050, China
Correspondence to: Dr. Shu-Tian Zhang, Department of Digestive Diseases, Beijing Friendship Hospital, Capital Medical University, 95 Yong An Road, Xuanwu District, Beijing 100050, China. email@example.com
Telephone: +86-10-63138339 Fax: +86-10-63020006
Received: June 19, 2007 Revised: August 17, 2007
AIM: To compare the prevalence of H pylori infection, peptic ulcer, cytomegalovirus (CMV) infection and Candida esophagitis in human immunodeficiency virus (HIV)-positive and HIV-negative patients, and evaluate the impact of CD4 lymphocyte on H pylori and opportunistic infections.
METHODS: A total of 151 patients (122 HIV-positive and 29 HIV-negative) with gastrointestinal symptoms were examined by upper endoscopy and biopsy. Samples were assessed to determine the prevalence of H pylori infection, CMV, candida esophagitis and histologic chronic gastritis.
prevalence of H pylori was less common in HIV-positive patients
(22.1%) than in HIV-negative controls (44.8%; P < 0.05), and the
prevalence of H pylori displayed a direct correlation with CD4 count
stratification in HIV-positive patients. In comparison with
HIV-negative group, HIV-positive patients had a lower incidence of
peptic ulcer (20.7% vs 4.1%; P < 0.01), but a higher prevalence of
chronic atrophy gastritis (6.9% vs 24.6%; P < 0.05),
Candida esophagitis and CMV infection. Unlike
HIV-negative group, H pylori infection had a close relationship to
chronic active gastritis (P < 0.05). In HIV-positive patients,
chronic active gastritis was not significantly different between
CONCLUSION: The lower prevalence of H pylori infection and peptic ulcer in HIV-positive patients with gastrointestinal symptoms suggests a different mechanism of peptic ulcerogenesis and a different role of H pylori infection in chronic active gastritis and peptic ulcer. The pathogen of chronic active gastritis in HIV-positive patients may be different from the general population that is closely related to H pylori infection.
© 2007 WJG. All rights reserved.
Key words: Human immunodeficiency virus; Endoscopy; Cytomegalovirus; Candida esophagitis; H pylori; Peptic ulcer; Chronic gastritis
Lv FJ, Luo XL, Meng X, Jin R, Ding HG, Zhang ST. A low prevalence of H pylori and endoscopic findings in HIV-positive Chinese patients with gastrointestinal symptoms. World J Gastroenterol 2007; 13(41): 5492-5496
H pylori has been extensively studied and proven to be the main cause of chronic gastritis and peptic ulcer in the HIV-negative population[1,2]. The reported prevalence of H pylori in unselected populations ranges from 32% to 65%[3-6]. Over 90% patients with chronic active gastritis showed an evidence of H pylori infection[3,4,7], and 70%-100% of those patients had peptic ulcer disease[1,5,7].
In contrast, the prevalence of H pylori infection in patients infected with HIV has been reported to be remarkably low[8-11]. Reasons for these lower rates of H pylori infection remain unclear. Other studies showed that H pylori infection is similar in both HIV-positive and HIV-negative patients[12,13]. Patients infected with HIV, with or without acquired immune deficiency syndrome (AIDS), have a high incidence (50%-90%) of upper gastrointestinal symptoms. The immune deficiencies caused by HIV give rise to many different gastrointestinal opportunistic infections, such as cytomegalovirus (CMV) infection and fungal esophagitis[15,16].
The aims of our study are to assess the prevalence of H pylori infection and the association with histological chronic active gastritis in HIV-positive patients with gastrointestinal symptoms. The impact of CD4+ count on the prevalence of H pylori, gastric CMV infection and Candida esophagitis was also evaluated.
MATERIALS AND METHODS
The study was carried out at Beijing You’an Hospital, Capital Medical University, Beijing, the largest referral center for management of HIV infection and HIV-related complications in China, from January 2003 to March 2006. Endoscopy was performed in 151 patients for gastrointestinal symptoms such as abdominal pain, dyspepsia, diarrhea, nausea, vomiting, gastrointestinal bleeding, and odynophagia or dysphagia.
The study groups consisted of 122 HIV-positive patients (49 males and 73 females; mean age 40.8 ± 7.9, range 26-60 years) and 29 age-matched HIV-negative patients (15 males and 14 females; mean age 49.5 ± 12.7, range 28-77 years) as control groups. The absolute CD4+ lymphocyte count of HIV-positive patients at the time of endoscopic examination was measured with FACS Count Reagents (BD Company, USA). Patients all gave their consent before undergoing endoscopy, and the symptoms, consumption of medications within one month, including antibiotics, proton pump inhibitors were also recorded.
Endoscopy, diagnosis and histology
Video-endoscopes (Olympus XQ240, Tokyo, Japan) were used for the procedure. All patients underwent three biopsies from the lesser and greater curvature of the gastric antrum and lesser curvature of lower body, one for Rapid Urease Test (RUT) and two for histology. Additional biopsies were obtained from endoscopic lesions such as ulceration. The biopsy specimens were placed in 10% formaldehyde at the time of endoscopy and stained with hematoxylin-eosin, Warthin-Starry stains for histologic chronic gastritis and H pylori infection, and immunocytochemical techniques were performed for CMV infection (Monoclonal Mouse Anti-Human Cytomegalovirus, Dako). The H pylori infection was diagnosed by positive identification of both the organism on histology (Warthin-Starry) and RUT. The histologic gastritis was diagnosed according to the Sydney criteria. Specimens were reviewed by only one pathologist who was blind to the status of those patients in present study.
The Candida esophagitis was diagnosed by sheathed brush cytology from endoscopic lesions, and gross appearance of mucosal presented with white plaques. Specimens obtained by sheathed brush should be smeared onto slides for fungi.
Chi-square test or Fisher exact probability tests were used to compare the prevalence of H pylori, CMV infection, Candida esophagitis, and peptic ulcer between HIV-positive patients, control groups, and HIV-infected patients with higher and lower CD4+ counts and the use of antibiotics and proton pump inhibitors. Independent sample t test was used to compare the age and sex between the HIV-positive and control groups. A value of P < 0.05 was regarded as statistically significant.
The patient data and the prevalence of H
pylori and endoscopic findings in HIV-positive patients and
HIV-negative patients are shown in
Table 1. The gastrointestinal
symptoms of HIV-positive patients were mostly nonspecific, such as
diarrhea, dyspepsia, abdominal pain, nausea, vomiting, and odynophagia or dysphagia. Only the occurrence of symptoms of
diarrhea, odynophagia, and dysphagia in HIV-positive patients was
significantly higher than that of control group (P < 0.05).
The prevalence of H pylori infection was significantly lower
in the HIV-positive group than that of HIV-negative control group
(27/122; 22.1% vs 13/29; 44.8%, P < 0.05). Endoscopic
examination revealed more patients with peptic ulcer in HIV-negative
group than in HIV-positive group (6/29; 20.7% vs 5/122; 4.1%,
P < 0.01). More histologic chronic atrophy gastritis was
found in HIV-positive patients than in HIV-negative group (30/122;
24.6% vs 2/29; 6.9%, P < 0.05). Opportunistic
infection by CMV was noted in 4.9% (6/122) HIV-positive patients but
none in the HIV-negative group (P = 0.49). The incidence of
Candida esophagitis in HIV-positive patients (19/122; 15.6%) was
significantly higher than that of HIV-negative patients
infection was less common in those with CD4+ counts <
200/mL than those with CD4+
counts > 200/mL in HIV-positive patients
(8/57; 14.0% vs 19/65; 29.2%, P < 0.05).
Interestingly, the prevalence of H Pylori infection
Histological examination revealed less chronic
active gastritis in HIV-positive patients than in HIV-negative
control group (24/122; 19.7% vs 9/29; 31%, P = NS),
but the difference was not statistically significant. The
relationship of H pylori infection with chronic active
gastritis was evaluated in HIV-positive and HIV-negative patients
(Table 4). In HIV-negative group, the incidence of chronic active
gastritis was significantly higher in those with H pylori
infection (61.5%) than those without (6.3%;
The relationship in H pylori and CMV infection and peptic ulcer was evaluated between the two groups of patients. Peptic ulcer was detected in five HIV-positive patients, one of whom (20%) was positive for H pylori infection and one (20%) for CMV infection. In HIV-negative group, six patients were diagnosed as having peptic ulcer, four (67%) as H pylori infection and none as CMV infection.
The previous use of antibiotics and proton pump inhibitor was also evaluated between HIV-positive and HIV-negative patients (47/122; 38.5% vs 3/29; 10.3%, P < 0.01 and 3/122; 2.5% vs 4/29; 13.8%, P < 0.05, respectively) (Table 1). If CD4+ count was taken into consideration, the use of all kinds of antibiotics in HIV-positive patients with CD4+ counts < 100/mL was not significantly different in those with CD4+ counts > 100/µL (18/37; 48.6% vs 29/85; 34.1%, P = 0.13) (Table 3). Those antibiotics mainly included Sulfonamides, penicillins and quinolones. None of the patients took NSAIDs, aspirin or steroid before endoscopic examination.
The HIV-positive patients in this study were usually concomitant with HCV and/or HBV infection which was more significantly frequent than in HIV-negative patients (102/122; 83.6% vs 2/29; 6.9%, P < 0.01). Nine patients with esophagogastric varices (7.4%) and 3 patients with portal hypertensive gastropathy (2.5%) in HIV-positive group were also found by endoscopic examination.
In the present study, we found that the majority of gastrointestinal symptoms of HIV-positive patients at our hospital were similar to that of HIV-negative group. In comparison with HIV-negative group, the symptoms of diarrhea, odynophagia, and dysphagia were significantly more in HIV-positive patients (P < 0.05). Several previous studies[16,18-19] revealed that more than 71% of AIDS patients who present with dysphagia and odynophagia have endoscopic evidence of esophageal candidiasis. Our result showed a high infection rate of Candida esophagitis in HIV-positive patients (19/122; 15.6%), which may be a possible explanation. Studies showed that the incidence of Cryptosporidium infection has been estimated to be 16%-33% in the AIDS patients in north America with chronic diarrhea[20,21]. In developing countries, the infection of Cryptosporidium was 55% among AIDS patients. The etiological factor of diarrhea in HIV-positive patients in our study was not evaluated.
The prevalence of H pylori infection in HIV-positive patients at our hospital was significantly lower than that in HIV-negative control group. Our results were in agreement with some previous reports[8-11]. The reason of lower prevalence of H pylori infection may be lack of CD4+ cells, use of antibiotics and proton pump inhibitor, decreased acid secretion, or competitive inhibition by other pathogens in HIV-positive patients.
According to previous reports, CD4+ lymphocytes were reported to be involved[23-25] in the pathogenesis of H pylori-related gastritis or ulcer. It is well known that CD4+ cells play a role in inducing gastritis and this gastritis might be a mechanism by which H pylori colonization is enhanced. Patients with HIV infection and a low CD4+ count would then lose this mechanism by which H pylori colonization is sustained, and infection intensity would diminish. In addition, the T-cell response to the organism could serve to induce tissue and epithelial damage. In AIDS patients, the decreased T-cell would induce a decreased incidence of H pylori gastritis. In our results, a stratification of cases on the basis of CD4+ count has shown a decrease of H pylori infection with the progression of HIV-related disease, and histological examination revealed less chronic active gastritis in HIV-positive patients than in HIV-negative control group (19.7% vs 31%). H pylori infection was closely related to chronic active gastritis in HIV-negative group (P < 0.05), but not in HIV-positive patients, indicating that other pathogens might exist , such as CMV and Cryptosporidium infection.
An impairment of H pylori colonization environment might result from a progressive atrophic involution of the gastric mucosa with secondary decreased acid secretion in HIV-positive patients, which represents an altered intragastric environment[28,29]. In our results, histologic chronic atrophy gastritis in HIV-positive patients was significantly higher than in HIV-negative group (30/122; 24.6% vs 2/29; 6.9%, P < 0.05), which might be result of gastric secretory failure in HIV infection patients. The impaired acid secretion may allow subsequent gastric bacterial overgrowth and provide a less suitable environment or competitive inhibition for H pylori colonization.
An altered intragastric environment might also result from frequent use of antibiotics against apportunistic infections in patients at an advanced stage of HIV infection. In comparison with HIV-negative group, HIV-positive group had a more frequent use of antibiotics. In HIV-positive patients, previous use of antibiotics with CD4+ counts < 100/mL was not significantly different from that of CD4+ counts > 100/mL (P = 0.13)，but the prevalence of H pylori infection showed significant difference. In our patients, the antibiotics most frequently used was trimetoprim-sulfa, usually for treatment or prophylaxis against pneumocystis in HIV-positive patients, and monotherapy of antibiotics has been proven to inhibit rather than eradicate H pylori. Therefore, current prophylaxis has been excluded from evaluation of eradicating the microorganism. Previous use of proton pump inhibitors might alter intragastric environment and therefore influence the prevalence of H pylori infection. In the present study, the HIV-negative control group took proton pump inhibitors more frequently than HIV-positive group (13.8% vs 2.5%, P < 0.05), which further proved the lower prevalence of H pylori infection in HIV-positive patients.
In this study, all 122 HIV-positive patients with gastrointestinal symptoms, only 4.1% had peptic ulcer, but 20.7% in HIV-negative group. This might explain that the low prevalence of H pylori infection result in the lower incidence of ulcers among HIV-positive patients. On the other hand, decreased acid secretion in HIV-positive patients plays a role in the lower incidence of peptic ulcer. According to previous reports, CMV-associated peptic ulcer disease was highly prevalent and CMV was the only organism significantly associated with gastroduodenal ulcers in HIV-positive patients, and H pylori was an uncommon cause of peptic ulcer[11,32]. In our study, among the 5 patients with peptic ulcer in HIV-positive group, only one proved to have CMV infection, which was lower according to previous studies[11,32]. The inadequate biopsies in the present study may be a possible explanation. According to literature, histological changes of CMV infection are patchy in distribution, however, and the single biopsy sensitivity for ulcerative lesions has been reported to be as low as 13%. Therefore, at least 8-10 biopsies of suspicious lesions are recommended.
Candida esophagitis is one of the most common opportunistic infections in patients with AIDS. Our study showed that the Candida esophagitis was significantly higher in HIV-positive patients with CD4+ count below 200/mL, and the average CD4+ counts with Candida esophagitis was 116.47 ± 133.08/mL. According to previous studies, the CMV infection is also a common opportunistic pathogen in HIV-positive patients with a low CD4+ count and is one of the main causes of gastrointestinal ulcer in AIDS patients[11,33]. The incidence of CMV infection in HIV-positive patients (4.9%) in our study was lower than previous reports. The incorrect location of biopsy may be another possible reason. According to literature review, gastric CMV infections are usually seen in the fundus with contiguous involvement of the esophagus and gastroesophageal junction, and the distal stomach and antrum are less commonly involved[35,36]. In the present study, the biopsy specimens were usually obtained from gastric antrum and lower body, therefore might lower the incidence of CMV infection in our patients.
The HIV-positive patients in the present study, mainly from Henan Province of China, infected through illegal blood plasma collection, and usually coinfected with HCV and/or HBV infection (83.6%). Endoscopic examination also revealed findings such as esophagogastric varices and portal hypertensive gastropathy, which were significantly different from previous reports.
In summary, we have found that a lower prevalence of H pylori infection and peptic ulcer in HIV-positive patients with gastrointestinal symptoms than that of HIV-negative patients with similar symptoms. The mechanism of chronic active gastritis in HIV-positive patients may be different from HIV-negative group that was closely related to H pylori infection. Various opportunistic infections (especially Candida esophagitis) of upper gastrointestinal tract likely occur in HIV-positive patients with a CD4+ count less than 200/mL.
Helicobacter pylori has been proven to be the main cause of chronic gastritis and peptic ulcer in the HIV-negative population. The role and prevalence of H pylori infection might be different in the HIV infected patients.
The immune deficiencies caused by HIV give rise to many different gastrointestinal opportunistic infections, and the prevalence of H pylori infection in patients infected with HIV is remarkably low.
Innovations and breakthroughs
It is the first report to characterize the prevalence and role of H pylori infection in chronic active gastritis and peptic ulcer in HIV-positive patients infected through illegal blood plasma collection in China, who are usually coinfected with HCV and/or HBV. The pathogen of chronic active gastritis in HIV-positive patients may be different from the general population that was closely related to H pylori infection.
This observation might be of potential value in HIV-positive patients with gastrointestinal symptoms.
The authors compared the prevalence of H pylori infection, peptic ulcer, cytomegalovirus (CMV) infection and Candida esophagitis in human immunodeficiency virus(HIV)-positive and HIV-negative patients. The lower prevalence of H pylori infection and peptic ulcer in HIV-positive patients with gastrointestinal symptoms suggests a different mechanism of peptic ulcerogenesis and a different role of H pylori infection in chronic active gastritis and peptic ulcer.
1 Carrick J, Lee A, Hazell S, Ralston M, Daskalopoulos G. Campylobacter pylori, duodenal ulcer, and gastric metaplasia: possible role of functional heterotopic tissue in ulcerogenesis. Gut 1989; 30: 790-797 PubMed
2 Suzuki H, Hibi T, Marshall BJ. Helicobacter pylori: present status and future prospects in Japan. J Gastroenterol 2007; 42: 1-15 PubMed
3 Li YY, Hu PJ, Du GG, Hazell SL. The prevalence of Helicobacter pylori infection in the Peoples Republic of China. Am J Gastroenterol 1991; 86: 446-449 PubMed
4 Dooley CP, Cohen H, Fitzgibbons PL, Bauer M, Appleman MD, Perez-Perez GI, Blaser MJ. Prevalence of Helicobacter pylori infection and histologic gastritis in asymptomatic persons. N Engl J Med 1989; 321: 1562- 1566 PubMed
5 Peterson WL. Helicobacter pylori and peptic ulcer disease. N Engl J Med 1991; 324: 1043-1048 PubMed
6 Taylor DE, Hargreaves JA, Ng LK, Sherbaniuk RW, Jewell LD. Isolation and characterization of Campylobacter pyloridis from gastric biopsies. Am J Clin Pathol 1987; 87: 49-54 PubMed
7 Blaser MJ. Helicobacter pylori: its role in disease. Clin Infect Dis 1992; 15: 386-391 PubMed
8 Panos GZ, Xirouchakis E, Tzias V, Charatsis G, Bliziotis IA, Doulgeroglou V, Margetis N, Falagas ME. Helicobacter pylori infection in symptomatic HIV-seropositive and -seronegative patients: a case-control study. AIDS Res Hum Retroviruses 2007; 23: 709-712 PubMed
9 Lichterfeld M, Lorenz C, Nischalke HD, Scheurlen C, Sauerbruch T, Rockstroh JK. Decreased prevalence of Helicobacter pylori infection in HIV patients with AIDS defining diseases. Z Gastroenterol 2002; 40: 11-14 PubMed
10 Cacciarelli AG, Marano BJ Jr, Gualtieri NM, Zuretti AR, Torres RA, Starpoli AA, Robilotti JG Jr. Lower Helicobacter pylori infection and peptic ulcer disease prevalence in patients with AIDS and suppressed CD4 counts. Am J Gastroenterol 1996; 91: 1783-1784 PubMed
11 Chiu HM, Wu MS, Hung CC, Shun CT, Lin JT. Low prevalence of Helicobacter pylori but high prevalence of cytomegalovirus-associated peptic ulcer disease in AIDS patients: Comparative study of symptomatic subjects evaluated by endoscopy and CD4 counts. J Gastroenterol Hepatol 2004; 19: 423-428 PubMed
12 Sud A, Ray P, Bhasin DK, Wanchu A, Bambery P, Singh S. Helicobacter pylori in Indian HIV infected patients. Trop Gastroenterol 2002; 23: 79-81 PubMed
13 Olmos M, Araya V, Pskorz E, Quesada EC, Concetti H, Perez H, Cahn P. Coinfection: Helicobacter pylori/human immunodeficiency virus. Dig Dis Sci 2004; 49: 1836-1839 PubMed
14 Francis ND, Logan RP, Walker MM, Polson RJ, Boylston AW, Pinching AJ, Harris JR, Baron JH. Campylobacter pylori in the upper gastrointestinal tract of patients with HIV-1 infection. J Clin Pathol 1990; 43: 60-62 PubMed
15 Francis ND, Boylston AW, Roberts AH, Parkin JM, Pinching AJ. Cytomegalovirus infection in gastrointestinal tracts of patients infected with HIV-1 or AIDS. J Clin Pathol 1989; 42: 1055-1064 PubMed
16 Dieterich DT, Wilcox CM. Diagnosis and treatment of esophageal diseases associated with HIV infection. Practice Parameters Committee of the American College of Gastroenterology. Am J Gastroenterol 1996; 91: 2265-2269 PubMed
17 Price AB. The Sydney System: histological division. J Gastroenterol Hepatol 1991; 6: 209-222 PubMed
18 Bonacini M, Young T, Laine L. The causes of esophageal symptoms in human immunodeficiency virus infection. A prospective study of 110 patients. Arch Intern Med 1991; 151: 1567-1572 PubMed
19 Bonacini M, Laine L, Gal AA, Lee MH, Martin SE, Strigle S. Prospective evaluation of blind brushing of the esophagus for Candida esophagitis in patients with human immunodeficiency virus infection. Am J Gastroenterol 1990; 85: 385-389 PubMed
20 Rossi P, Rivasi F, Codeluppi M, Catania A, Tamburrini A, Righi E, Pozio E. Gastric involvement in AIDS associated cryptosporidiosis. Gut 1998; 43: 476-477 PubMed
21 Lumadue JA, Manabe YC, Moore RD, Belitsos PC, Sears CL, Clark DP. A clinicopathologic analysis of AIDS- related cryptosporidiosis. AIDS 1998; 12: 2459-2466 PubMed
22 Wyatt SH, Fishman EK. The acute abdomen in individuals with AIDS. Radiol Clin North Am 1994; 32: 1023- 1043 PubMed
23 Seifarth C, Funk A, Reich K, Dahne I, Classen M, Deusch K. Selective increase of CD4+ and CD25+ T cells but not of gamma delta T cells in H. pylori associated gastritis. Adv Exp Med Biol 1995; 371B: 931-934 PubMed
24 Bamford KB, Fan X, Crowe SE, Leary JF, Gourley WK, Luthra GK, Brooks EG, Graham DY, Reyes VE, Ernst PB. Lymphocytes in the human gastric mucosa during Helicobacter pylori have a T helper cell 1 phenotype. Gastroenterology 1998; 114: 482-492 PubMed
25 Edwards PD, Carrick J, Turner J, Lee A, Mitchell H, Cooper DA. Helicobacter pylori-associated gastritis is rare in AIDS: antibiotic effect or a consequence of immunodeficiency? Am J Gastroenterol 1991; 86: 1761-1764 PubMed
26 Bontems P, Robert F, Van Gossum A, Cadranel S, Mascart F. Helicobacter pylori modulation of gastric and duodenal mucosal T cell cytokine secretions in children compared with adults. Helicobacter 2003; 8: 216-226 PubMed
27 Fabris P, Pilotto A, Bozzola L, Tositti G, Soffiati G, Manfrin V, de Lalla F. Serum pepsinogen and gastrin levels in HIV-positive patients: relationship with CD4+ cell count and Helicobacter pylori infection. Aliment Pharmacol Ther 2002; 16: 807-811 PubMed
28 Lake-Bakaar G, Quadros E, Beidas S, Elsakr M, Tom W, Wilson DE, Dincsoy HP, Cohen P, Straus EW. Gastric secretory failure in patients with the acquired immunodeficiency syndrome (AIDS). Ann Intern Med 1988; 109: 502-504 PubMed
29 Biasco G, Miglioli M, Barbara L, Corinaldesi R, di Febo G. Omeprazole, Helicobacter pylori, gastritis, and duodenal ulcer. Lancet 1989; 2: 1403 PubMed
30 Pavicic MJ, Namavar F, Verboom T, van Winkelhoff AJ, De Graaff J. In vitro susceptibility of Helicobacter pylori to several antimicrobial combinations. Antimicrob Agents Chemother 1993; 37: 1184-1186 PubMed
31 Peterson WL, Graham DY, Marshall B, Blaser MJ, Genta RM, Klein PD, Stratton CW, Drnec J, Prokocimer P, Siepman N. Clarithromycin as monotherapy for eradication of Helicobacter pylori: a randomized, double-blind trial. Am J Gastroenterol 1993; 88: 1860-1864 PubMed
32 Varsky CG, Correa MC, Sarmiento N, Bonfanti M, Peluffo G, Dutack A, Maciel O, Capece P, Valentinuzzi G, Weinstock D. Prevalence and etiology of gastroduodenal ulcer in HIV-positive patients: a comparative study of 497 symptomatic subjects evaluated by endoscopy. Am J Gastroenterol 1998; 93: 935-940 PubMed
33 Goodgame RW, Genta RM, Estrada R, Demmler G, Buffone G. Frequency of positive tests for cytomegalovirus in AIDS patients: endoscopic lesions compared with normal mucosa. Am J Gastroenterol 1993; 88: 338-343 PubMed
34 Quinn TC. Clinical approach to intestinal infections in homosexual men. Med Clin North Am 1986; 70: 611-634 PubMed
35 Stoane JM, Haller JO, Orentlicher RJ. The gastrointestinal manifestations of pediatric AIDS. Radiol Clin North Am 1996; 34: 779-790 PubMed
36 Wyatt SH, Fishman EK. The acute abdomen in individuals with AIDS. Radiol Clin North Am 1994; 32: 1023- 1043 PubMed
S- Editor Zhu LH L- Editor Ma JY E- Editor Liu Y