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Intestinal Absorptive Capacity, Intestinal Permeability and Jejunal Gut 1995; 37: 623-629 623 Intestinal absorptive capacity, intestinal permeability and jejunal histology in HIV and their relation to diarrhoea Gut: first published as 10.1136/gut.37.5.623 on 1 November 1995. Downloaded from J Keating, I Bjarnason, S Somasundaram, A Macpherson, N Francis, A B Price, D Sharpstone, J Smithson, I S Menzies, B G Gazzard Abstract various stages and correlated the findings with Intestinal function is poorly defined in symptoms of diarrhoea, weight loss, degree of patients with HIV infection. Absorptive immune suppression, and jejunal morphology. capacity and intestinal permeability were Patients with untreated coeliac disease have assessed using 3-O-methyl-D-glucose, been used for comparison to enable functional- D-xylose, L-rhamnose, and lactulose in 88 morphometric interpretation of results in HIV HIV infected patients and the findings patients with malabsorption. were correlated with the degree of immunosuppression (CD4 counts), diar- rhoea, wasting, intestinal pathogen status, Subjects and methods and histomorphometric analysis ofjejunal biopsy samples. Malabsorption of 3-0- SUBJECTS methyl-D-glucose and D-xylose was Fifty seven healthy volunteers (21 women) prevalent in all groups of patients with acted as controls for the intestinal absorption- AIDS but not in asymptomatic, well permeability test (mean (SD) age 33 (7) patients with HIV. Malabsorption corre- years). Controls comprised 47 healthy, mainly lated significantly (r=0.34-0-56, p<0005) medical and health service staff recruited for a with the degree of immune suppression number of previous studies conducted at and with body mass index. Increased Northwick Park Hospital and King's College intestinal permeability was found in all Hospital and 10 men recruited from Chelsea subgroups of patients. The changes in Westminster Hospital during this study. None absorption-permeability were of compar- were at high risk for the HIV infection but they able severity to those found in were not tested serologically before this study patients http://gut.bmj.com/ Departments of with untreated coeliac disease. Jejunal or subsequently. Medicine, histology, however, showed only mild Eighty eight HIV positive male homosexual Gastroenterology, Genitourinary changes in the villus height/crypt depth patients were studied (mean (SD) age 39 (9) Medicine, and ratio as compared with subtotal villus years). HIV was confirmed by both enzyme Histopathology, atrophy in coeliac disease. Malabsorption linked immunosorbent assay and western blot Chelsea and Westminster Hospital, and increased intestinal permeability are analysis. This group comprised 25 consecu- common in AIDS patients. Malabsorp- tive, well patients with HIV (out of 52 (48%) London on September 25, 2021 by guest. Protected copyright. J Keating tion, which has nutritional implications, invited to participate) who had not had an N Francis D Sharpstone relates more to immune suppression than AIDS defining illness and 22 (out of43 (51%)) J Smithson jejunal morphological changes. well patients with AIDS seeing a single physi- B G Gazzard (Gut 1995; 37: 623-629) cian in the Genitourinary Medicine outpatient department of Chelsea and Westminster Department of Keywords: HIV, AIDS, intestinal permeability, Hospital. Patients who declined to participate Histopathology, intestinal function, intestinal infection, intestinal Northwick Park absorption. in these studies did not differ significantly Hospital, London (p>0.4) from those studied in respect of age, A B Price duration of AIDS, CD4 counts, body mass Deparment of index, or serum albumin. The remainder com- Chemical Pathology, Patients infected with HIV may develop diar- prised 34 consecutive inpatients with AIDS St Thomas's Hospital, London rhoea, weight loss, and wasting but the preva- admitted to Chelsea and Westminster Hospital I S Menzies lence, severity, cause, and contribution of for gastrointestinal investigation who met the malabsorption to these symptoms is controver- inclusion criteria (HIV positive, male homo- Department of Clinical Biochemistry, King's sial.'-6 Some workers suggest that malabsorp- sexuals) and seven inpatients who were wasted College School of tion is infrequent, mild, and of little clinical but did not have gastrointestinal symptoms. Medicine and importance2 while others have reported severe Patients were specifically excluded if they had Dentistry, London malabsorption in patients with AIDS associ- received a treatment course of antibiotics I Bjarnason S Somasundaram ated with cryptosporidial diarrhoea which is (including antimicrobial drugs) other than for A Macpherson purported to correlate to the degree of villus Pneumocystis carinii prophylaxis in the preced- Correspondence to: atrophy.' It is nevertheless unclear when, in ing four weeks or if they required opioids for Dr I Bjamason, Department the natural history of HIV, disease malabsorp- control of diarrhoea. of Clinical Biochemistry, King's College School of tion becomes evident and how it interrelates According to the revised classification Medicine and Dentistry, with symptoms of weight loss and diarrhoea. system of the Centres for Disease Control,7 Bessemer Road, London SE5 9PJ. We studied intestinal function with respect and taking into account the European modifi- Accepted for publication to absorption and permeability markers in a cation ofthis classification,8 25 patients were at 23 March 1995 large group of patients with HIV infection at stage 2 - asymptomatic and without an AIDS 624 Keating, Bjarnason, Somasundaram, Macpherson, Francis, Price, Sharpstone, Smithson, Menzies, Gazzard TABLE I Demographic details ofpatients infected by HIV (values median (range)) diagnosed on the basis of significant diarrhoea AIDS and weight loss with a jejunal biopsy specimen showing subtotal villus atrophy, and all Pathogen Pathogen -ve +ve responded to a gluten free diet. Gut: first published as 10.1136/gut.37.5.623 on 1 November 1995. Downloaded from HIV (well) Well Wasted diarrhoea diarrhoea These studies were approved by the local No of patients 25 22 7 7 27 ethical committees of Camberwell and Age (y) 37 (25-54) 39 (27-48) 36 (32-60) 39 (33-50) 35 (22-50) Westminster Health Authorities and all Duration of AIDS (mth)* - 11 (3-94) 6 (4-26) 15 (7-20) 23 (3-46) patients CD4 countst 295 (4-555) 67 (8-171) 40 (14-67) 18 (2-44) 29 (5-204) gave informed consent. Body mass indext 24 (18-28) 21 (18-27) 16 (14-19) 19 (18-21) 18 (14-23) Serum albumin§ 39 (19-43) 37 (21-49) 26 (14-47) 32 (26-38) 33 (19-44) *From the time of an AIDS defining illness. There was no significant difference (p>0 34) in the INVESTIGATIONS duration of AIDS between the subgroups. The AIDS patients underwent a standard tLower limit of normal is 600. HIV well patients had significantly (p<0 025) greater CD4 counts than patients with AIDS apart from wasted AIDS patients (p=0 18). There was no diagnostic gastrointestinal protocol which has significant difference between the subgroups of patients with AIDS (p>0 09). been detailed previously.9 10 Briefly, each tLower limit of normal is 20. The HIV well patients had significantly (p<0 02) higher BMI than the patients with AIDS apart from the AIDS well patients (p=0.08). was investigated by six stool examinations with §Lower normal limit is 35 g/l. HIV well patients differed significantly (p<0 05) from wasted and light microscopy and culture, gastroduo- pathogen positive patients with AIDS, but there was otherwise no significant difference between the various subgroups. denoscopy with duodenal aspiration and low duodenal (part 3) biopsy specimens, and sigmoidoscopy with rectal biopsy specimens. defining illness (infection with P carinii, Well, stage 2 HIV patients had the stool Candida albicans oesophagitis, etc). All the examinations but not the endoscopies. remaining 63 patients were stage 4 and had Body mass index (BMI: normal greater than AIDS (all but one had CD4 counts below 20) was calculated as weight (kg)/height2 200X106/1). These patients were further sub- (m) . CD4 counts were assessed by flow classified clinically and on the basis of cytometry and expressed as number of intestinal pathogen status as follows: cellsX 106/1. (i) AIDS well- 22 patients were asymptomatic with no history of weight loss or diarrhoea. (ii) AIDS wasted - seven patients who had JEJUNAL BIOPSY SPECIMENS AND greater than 10% weight loss in the preceding MORPHOMETRIC ANALYSES month without any diarrhoea. Five had Thirty six stage 4 patients with AIDS, and all recently suffered from opportunistic infections the patients with coeliac disease, underwent (P carinii (n=4) and cytomegalovirus (n= 1)). jejunal biopsy (Crosby capsule) just distal to Two had Kaposi's sarcoma. the ligament of Treitz. Fifteen were from the (iii) Thirty four patients had had diarrhoea AIDS well group and 21 with pathogen (more than three liquid motions a day, for over positive (n=17) or pathogen negative (n=4) http://gut.bmj.com/ a month). After investigation, detailed below, diarrhoea. Morphometric analyses of jejunal these were further separated into a group of biopsy samples was carried out by interactive seven in whom no intestinal pathogens were image analyses (Joyce-Loebl magiscan) as found (pathogen negative group) and the previously described.12 The histological slides remaining 27 who had cryptosporidia (n= 17), and morphometric analyses was shared microsporidia (n=6), or both (n=4). equally between two histopathologist neither Demographic details of the HIV infected of whom had any knowledge of the diagnostic on September 25, 2021 by guest. Protected copyright. patients are shown in Table I. categories of the patients. An internal quality Most of the patients were on drug treat- control showed an interobserver difference of ment. Those with CD4 counts below 200 less than 8% for the villus height and crypt received treatment with dapsone (100 mg/d), depth measurements. Mucosal height was pentamidine aerosol (300 mg/every third measured as the distance between muscularis week) or co-trimoxazole (960 mg twice a day, mucosa and tips of well oriented, vertically three times per week) for P carinii prophylaxis.
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