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Intestinal Permeability in Patients with Coeliac Disease and Relatives of Patients with Coeliac Disease Gut: First Published As 10.1136/Gut.34.3.354 on 1 March 1993

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Intestinal Permeability in Patients with Coeliac Disease and Relatives of Patients with Coeliac Disease Gut: First Published As 10.1136/Gut.34.3.354 on 1 March 1993 354 Gut 1993; 34: 354-357 Intestinal permeability in patients with coeliac disease and relatives of patients with coeliac disease Gut: first published as 10.1136/gut.34.3.354 on 1 March 1993. Downloaded from R M van Elburg, J J Uil, C J J Mulder, H S A Heymans Abstract related to constitutional factors in people The functional integrity of the small bowel is susceptible to coeliac disease and may detect impaired in coeliac disease. Intestinal per- latent coeliac disease. The sugar absorption meability, as measured by the sugar absorption test may therefore be helpful in family studies test probably reflects this phenomenon. In the of coeliac disease. sugar absorption test a solution of lactulose (Gut 1993; 34: 354-357) and mannitol was given to the fasting patient and the lactulose/mannitol ratio measured in urine collected over a period offive hours. The The incidence of coeliac disease is not decreas- sugar absorption test was performed in nine ing, but the clinical picture is changing from the patients with coeliac disease with an abnormal classic form in very young children towards the jejunum on histological examination, 10 rela- atypical form in school age children and adoles- tives of patients with coeliac disease with cents.' It has been suggested that this delay in aspecific symptoms but no villous atrophy, the development of symptomatic coeliac disease six patients with aspecific gastrointestinal could be the result of the prolonged period of symptoms but no villous atrophy, and 22 breast feeding and subsequent delayed intro- healthy controls to determine whether func- duction of and exposure to gluten.2 Maki et al' tional integrity is different in these groups. described four patients with so called latent The lactulose/mannitol ratio (mean (SEM) is coeliac disease, who developed coeliac disease 2 Department of significantly higher in both coeliac disease to 9 years after histological examination of the Paediatrics, University (0.243 (0.034), p<0 0001)) and relatives of small bowel was normal on a diet containing Hospital of Groningen, patients with coeliac disease (0.158 (0.040), gluten. Groningen R M van Elburg p<0 005)) v' both healthy controls (0.043 IgA antibodies detected against reticulin and H S A Heymans (0.006)) and patients with aspecific gastro- endomysium were shown in 12% of the family intestinal symptoms (0.040 (0.011)). The members; accompanied by villous atrophy in 9% http://gut.bmj.com/ Department of Internal Medicine, lactulose/mannitol ratio in relatives of coeliac and without villous atrophy in 3%.' It remains Riinstate Hospital, disease patients was significantly lower than in to be seen whether the latter group with a low Arnhem, The the coeliac disease patient group (p=0.04). grade immunological reaction preceding coeliac Netherlands The JJ Uil lactulose/mannitol ratio was the same disease should be considered as another example C J J Mulder in healthy controls and patients with aspecific oflatent coeliac disease. This low grade immuno- Correspondence to: gastrointestinal symptoms. It is concluded that logical reaction could be the reflection of a pre- R M van Elburg, the sugar absorption test is a sensitive test that existent change in the barrier function of the on September 30, 2021 by guest. Protected copyright. Department of Paediatrics, University distinguishes between patients with coeliac small intestinal mucosa. In some of the patients Hospital of Groningen, disease and healthy controls. The explanation with latent coeliac disease minor histological PO Box 30 001, 9700 RB Gironingen, The Netherlands for the increased permeability in relatives of changes, such as an increased lymphocyte count, Accepted for publication patients with coeliac disease is uncertain. were found before they developed IgA anti- 28 July 1992 Increased intestinal permeability may be bodies and coeliac disease.I Two of the four patients with latent coeliac disease were related TABLE I Characteristics ofpatient groups in the first degree to patients with coeliac disease. In first degree relatives, asymptomatic patients Relatives of Aspecific with coeliac disease have been described with a Healthy Coeliac coeliac disease gastrointestinal controls disease patients svmptoms prevalence as high as 10%.) Whether these Group (n=22) (n=9) (n= 10) (n=6) patients can also be considered to have had latent Intestinal biopsy Not done Villous No villous No villous coeliac disease is unknown. Usually they have atrophy atrophy atrophy not been investigated previously because of a Gastrointestinal No Some Some Yes symptoms lack of symptoms. Relatives with coeliac No Some Yes No In other immunological gastrointestinal disease diseases such as food allergy, it has been suggested that disturbances in the functional TABLE II Mean (SEM) lactulose, mannitol, and lactulose/mannitol ratio in healthv controls, integrity, responsible for the barrier function of coeliac disease patients, relatives ofcoeliac disease patients, and patients with aspecific the small bowel mucosa, could play a role in gastrointestinal symptoms the development of clinical symptoms. In 'full blown' coeliac disease, the histology of the Coeliac Relatives of Aspecific Healthy disease coeliac disease gastrointestinal mucosal structure, as well as the functional controls patients patients symptoms integrity of the small bowel mucosa, are (roup (n --22) (n 9) (n= 10) (n =6) impaired."' If latent coeliac disease is a precurser Lactulosc 24-3(3-1) 138X6t(29 1) 78 5*(9 3) 250 (6 3) of coeliac disease itself, the functional integrity Mannitol 585-7 (34 7) 627.4 (107 8) 612 2 (54 9) 634-5 (66 2) I/M ratio 0-043 (0(006) 0(243t (0 034) 0 158* (0 040) 0(040 (0(011) of the small bowel could already be altered before gross histological abnormalities are found. *pp0005; t= p<(00OOl zv healthy controls (Mann Whitney U test). Intestinal permeability, as measured by the Intestinalpermeability in patients with coeliac disease and relatives ofpatients with coeliac disease 355 1 ethical reasons intestinal biopsies were not per- formed in healthy controls. * * M + 2SD ! Gut: first published as 10.1136/gut.34.3.354 on 1 March 1993. Downloaded from 01 Methods I After an overnight fast the patient emptied his or E: a) her bladder and drank a solution containing 2 g Ca)° 0 0 mannitol, 5 g lactulose and 40 g sucrose, made up to 100 ml with demineralised water, to give an -J osmolality of approximately 1 650 mosm/l. For the first 2 hours after drinking the test fluid, no 0001 food or fluid was allowed and all the urine passed 4)ci X< in the 5 hours after they had drunk the test fluid was collected. Chlorohexidine digluconate 20% e n r (0 5 ml) was added to the urine as a preservative. The urine volume was measured and aliquots Patients (groups) were stored frozen at 20°C. To calculate the Figure: Individuial lactuloselmannitol ratio of22 healthy controls, nine coeliac disease patients, 10 relatives ofcoeliac lactulose/mannitol ratio samples were analysed disease patients and six patients with aspecific gastrointestinal for lactulose and mannitol by gas chromato- symptoms. The horizontal line represents the upper limit ofthe graphy as previously described. lactuloselmannitol ratio in healthy controls (mean +2 SD). STATISTICAL ANALYSIS sugar absorption test, is considered to reflect The non-parametric Mann-Whitney U test was functional integrity. It is suggested that the used for statistical analysis of the data. A p value passive absorption of molecules 0 5 nm - for <0 05 was considered statistically significant. example lactulose - is increased by oedema, mucosal inflammation, and villous atrophy whereas the absorption of molecules <0 5 nm - Results for example mannitol - is unchanged or im- The mean lactulose/mannitol ratio in urine from paired. The urinary lactulose/mannitol ratio is the four groups is summarised in Table II. said to provide a sensitive non-invasive index The lactulose/mannitol ratio in coeliac disease of the functional integrity of the small bowel patients is significantly higher than in both the mucosa.7 8 healthy controls (p<0-0001) and in patients with This study aimed to determine if intestinal aspecific gastrointestinal symptoms (p=0002). http://gut.bmj.com/ permeability, as assessed by the sugar absorption The lactulose/mannitol ratio in relatives of test, is different in relatives of coeliac disease coeliac disease patients is significantly lower than patients compared with coeliac disease patients, in coeliac disease patients (p=0-04) but signific- healthy controls, and patients not related to antly higher than that in either healthy controls coeliac disease patients, with aspecific gastro- (p<0-0001) and patients with aspecific gastro- intestinal symptoms in which coeliac disease was intestinal symptoms (p=0002). The lactulose/ excluded by intestinal biopsy investigation. mannitol ratio is not significantly different in on September 30, 2021 by guest. Protected copyright. healthy controls and patients with aspecific gastrointestinal symptoms (p= 0 74). Patients The mean levels ofmannitol excretion in urine The group characteristics are summarised in in the four groups are summarised in Table II. Table I. Nine patients with moderate to severe The differences between the groups are not villous atrophy shown by intestinal biopsy significant. The mean levels of urinary lactulose specimen were classified as having coeliac excretion in the four groups are summarised in disease. These patients were either newly Table II. The differences between the groups diagnosed or in partial remission and were not are generally similar to the differences in adhering to a gluten free diet. Ten patients were the lactulose/mannitol ratio. The differences first degree relatives of (biopsy proved) coeliac between coeliac disease patients and relatives of disease patients, of whom seven had aspecific coeliac disease patients, however, can only be gastrointestinal symptoms such as malaise, seen in the lactulose/mannitol ratio (p=0 04) abdominal cramps, or abnormal stools, while and not in the urinary lactulose excretion alone three had no symptoms at all.
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