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J Appl Physiol 98: 2163-2168, 2005. First published January 20, 2005; doi:10.1152/japplphysiol.00761.2004
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Effect of glutamine on water and sodium absorption in human jejunum at baseline and during PGE1-induced secretion

Moïse Coëffier, Bernadette Hecketsweiler, Philippe Hecketsweiler, and Pierre Déchelotte

Appareil Digestif, Environnement et Nutrition (ADEN EA 3234), Institut Fédératif de Recherche Multidisciplinaire sur les Peptides (IFR 23), Faculté de Médecine-Pharmacie, Rouen, France

Submitted 20 July 2004 ; accepted in final form 17 January 2005


   ABSTRACT
TOP
 ABSTRACT
SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Glutamine, a major fuel for enterocytes, stimulates water and sodium absorption in animal models of secretory diarrhea, but data in humans are still limited. The aim of this study was to investigate the effect of glutamine on jejunal absorption during hypersecretion in humans. In six healthy adults, the effects of glutamine on jejunal absorption were assessed with a triple-lumen tube on two occasions, at baseline and during PGE1-induced hypersecretion (0.1 µg·kg–1·min–1) in a random order. Isoosmolar solutions containing polyethylene glycol 4000 as nonabsorbable marker were infused in the jejunum at 10 ml/min over 1-h periods: saline (sodium chloride 308 mmol/l), glucose-mannitol 45:45 mM, glucose 90 mM, alanine-glucose 45:45 mM, glutamine-glucose 45:45 mM, and glutamine 90 mM. Net absorptive and secretory fluxes were measured at steady state. At baseline, glutamine- and alanine-containing solutions induced a threefold increase of water and sodium absorption (P < 0.05); 90 mM glutamine stimulated water absorption more than 90 mM glucose (3.6 ± 0.6 vs. 1.9 ± 0.3 ml·min–1·30 cm–1, P < 0.05). PGE1-induced hypersecretion was reduced (P < 0.05) by solutions of alanine-glucose, glutamine-glucose, and glutamine 90 mM (P < 0.05) and reversed to absorption by alanine-glucose and glutamine-glucose. Glutamine and alanine absorption was nearly complete and was not influenced by PGE1. In conclusion, glutamine stimulates water and electrolyte absorption in human jejunum, even during experimental hypersecretion. In addition to the metabolic effects of glutamine, these results support the evaluation of glutamine-containing solutions for the rehydration and the nutritional support of patients with secretory diarrhea.

prostaglandins; secretory diarrhea; amino acids; oral rehydration solution

ORAL REHYDRATION THERAPY, the main way of treating dehydration due to diarrhea, is based on the cotransport of sodium with glucose (14), which is maintained in acute secretory diarrhea of diverse etiologies (e.g., Cryptosporidium parvum, cholera toxin) (30). Despite its efficacy, improvements of the glucose-based oral rehydration solution (ORS) are needed, both to enhance its efficacy and reduce the stool output and to provide a more adequate nutritional support to patients often malnourished in developing countries (25). Improvement of glucose-ORS could be achieved either by low osmolality of solutions (16, 40) or by addition of amino acids promoting intestinal transport (7).

Indeed, neutral amino acids and dipeptides are cotransported with Na+ in the intestine by carriers that are different from the glucose-galactose carrier and may thus be added to the glucose-sodium ORS. Glutamine has been identified as a potential candidate to supplement or replace glucose in ORS (7, 23, 34). It was reported that L-glutamine stimulates sodium intestinal absorption in animals by a distinct and additive mechanism to that of glucose (29) and that this promising effect was maintained to some extent in animals with experimental diarrhea (33, 37). In addition, glutamine supports the metabolism of intestinal epithelial cells both as a major fuel and as a precursor for nucleic acid synthesis (39). Finally, glutamine is a major nitrogen carrier in vivo and plays a key role in the regulation of intestinal protein turnover (9) and lipolysis (12).

We previously reported the characteristics of L-glutamine absorption in human jejunum (12). In the present study performed in healthy subjects, the effect of L-glutamine on water and electrolyte jejunal absorption was assessed by means of an intestinal infusion method and was compared with the effects of glucose and alanine, at baseline and during an experimentally induced hypersecretion achieved by intrajejunal infusion of PGE1.


   SUBJECTS AND METHODS
TOP
 ABSTRACT
 SUBJECTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Subjects.   Six healthy, normal-weight nonpregnant young adults were recruited for the study (Table 1) and were instructed to maintain their usual levels of dietary intake and physical activity at home in the days preceding each study. They received detailed information on the purpose, methods, and potential risks of the protocol and gave their written consent before the study. The study protocol had been previously reviewed and accepted by the Ethics Committee of the Rouen University Hospital.


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  		Table 1. Characteristics of the subjects and individual order of infusion

 
Materials.   Natural L-glutamine, L-alanine, D-glucose, D-mannitol, and PGE1 were obtained from Sigma (La Verpillière, France). The nasojejunal enteral tube consisted of three joined polyvinyl tubes. The upper tube was used for infusion of solutions (I); the two other tubes downward were used for aspiration of jejunal contents through a proximal (P) and a distal opening (D). The segment between I and P (mixing segment), and P and D (study segment) was 15 and 30 cm long, respectively. Tubes I and D were identifiable by fluoroscopy to facilitate adequate positioning of the device.

Solutions for enteral infusion.   All solutions were prepared with sterile water in the morning of each study by the hospital pharmacy. The composition of the solutions is given in Table 2. Ionic composition and osmolality (300 mosmol/kg) were checked and adjusted if necessary before use. A control rehydration solution with a 90 mmol/l glucose concentration was chosen, instead of 111 mmol/l, to allow the addition of high glutamine concentration without increasing markedly osmolarity; it has been reported that hypoosmolar solutions containing 90 mmol/l glucose were more efficient than solutions with 111 mmol/l glucose (16).


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  		Table 2. Composition of enterally infused solutions mmol/l

 
Perfusion protocol.   Each subject was studied twice in the morning of 2 separate days, at baseline or during hypersecretion, in a random order, with a 15-day interval between studies. After a 12-h fast, subjects were intubated through the nose after local anesthesia (lidocaine), and the tube was allowed to migrate spontaneously across the pylorus; a few (1–3) h later, the correct position of the tube was assessed by fluoroscopic examination, with the infusion opening I being 10 cm beyond the duodenojejunal junction. The infusion was then initiated through infusion opening I.

In all studies, the six tested solutions were administered through tube I as follows: the control solution (saline) was infused first to assess basal absorption rate, and then other solutions [glucose 90 mM (glc90); glucose-mannitol (glc:man); alanine-glucose (ala:glc); glutamine-glucose (gln:glc); glutamine 90 mM (gln90)] were infused in a random order (Table 1). All the solutions were maintained at 37°C during infusion, which was achieved at a constant 10 ml/min rate over 60 min by means of a calibrated pump. Each 60-min infusion period consisted of a 30-min equilibration period, followed by three successive 10-min sampling periods during which samples were aspirated simultaneously from tubes P and D and collected on ice (aspiration was achieved by gentle and regular manual suction at a rate of 0.5 ml/min for each aspiration site). Separate aliquots of each sample were immediately frozen and kept at –20°C until analysis of ions, glucose, and polyethylene glycol (PEG), respectively. Other aliquots (0.5 ml) were mixed with an equal volume of an ice-cold sulfosalicylic acid solution containing AGPA as an internal standard and centrifuged, and the resulting deproteinized supernatant was frozen until analysis of amino acid concentration.

Intestinal hypersecretion was induced by infusion of PGE1 to mimic a secretory diarrhea with a pattern of water and electrolyte secretion similar to that observed in cholera (4, 26). PGE1 (0.1 µg·kg–1·min–1 in isotonic saline, 8 ml/h) was continuously infused intrajejunally through tube I, together with the solutions tested, over the 6 h of study, by means of a calibrated syringe pump (Vial, Grenoble, France); during baseline studies, subjects received an equal load of saline. The clinical tolerance of jejunal infusions was good, and all subjects completed the study. During infusion of PGE1, two subjects experienced mild and transient abdominal cramping. All six subjects passed one to three loose stools during the infusion period, without any relevant modifications of vital signs (blood pressure, temperature, respiratory rate).

Analytical procedures.   Glucose and electrolytes were analyzed with standard automated techniques. PEG was assessed in duplicate by a turbidimetric method (18). Alanine and glutamine were assessed in luminal samples pretreated as described above by ion exchange chromatography on an amino acid autoanalyzer (Beckman, Anaheim, CA).

Calculations.   The achievement of steady state during each hour of infusion of a given solution was checked on the fact that the coefficient of variation of PEG and water fluxes, measured at the proximal and distal sampling sites, between the three consecutive 10-min sampling periods was less than 10%. At steady state, for each 10-min sampling period, water intraluminal outputs (ml/min) entering the study segment at port P (JP) and leaving the study segment at port D (JD) were calculated from measured concentrations of PEG according to standard PEG dilution equations (4, 27):


where i is the infusion rate (10 ml/min), [PEG]I the actual concentration of PEG measured in each solution, and 0.5 the rate of aspiration of luminal contents at P (see Perfusion protocol). The net water transmucosal flux (JW, ml·min–1·30 cm jejunum–1) over P-D is obtained by calculating:

Net absorptive fluxes are indicated as positive values and secretory fluxes as negative values.

For each 10-min sampling period, intraluminal outputs of electrolytes and substrates entering and leaving the segment P-D were calculated by multiplying JD or JP by the respective concentration of electrolyte or substrate measured in the same sample; the net absorptive or secretory flux was then calculated by difference, e.g., the net transmucosal flux of sodium over P-D (JNa, µmol·min–1·30 cm jejunum–1) is given by

where [Na]D and [Na]P are the Na concentration at P and D, respectively.

The cumulative absorption of glucose, alanine, and glutamine over the total length of the segments I-P-D (45 cm) was also estimated by subtracting the output of substrate remaining in the lumen at port D from the input of substrate infused at I and expressed as percentage of infused load. Because some luminal material may reflux above the infusion point, this calculation slightly underestimates in theory the actual length of gut involved in absorption and thus slightly overestimates the cumulative absorption over I-D. However, this approximation has been found to be quite valid when high infusion rates are used, as is the case in the present study (27).

Mean outputs and net fluxes over segment P-D were then calculated for each solution of each subject. Finally, the mean values for the six subjects were calculated from the mean net fluxes of each subject.

Statistical analysis.   Net fluxes between baseline and hypersecretion conditions were compared by nonparametric Wilcoxon’s test for paired data. Net fluxes between solutions at baseline or during hypersecretion were compared using Friedman and Dunn’s multiple comparison tests. Significance level was P < 0.05. The coupling ratios between absorbed sodium and substrates (e.g., glucose and glutamine) were calculated by dividing the increment in segmental sodium net absorption above control value, by the segmental absorption of the substrate, both being expressed in micromoles per minute per 30 cm.


   RESULTS
TOP
 ABSTRACT
 SUBJECTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Glutamine and alanine increase water and electrolyte absorption at basal conditions.   At baseline, a net absorption of water and electrolytes was observed (Table 3, Fig. 1). Water and electrolyte fluxes were significantly affected by administered solutions (P ≤ 0.05 for all, Friedman’s test). Solutions ala:glc, gln:glc, and gln90 induced a significant increase above control water and sodium absorption rates (Fig. 1). The glc90 solution did not stimulate significantly water absorption. The gln:glc and ala:glc solutions were the most effective and promoted water and sodium absorption threefold above control values; gln90 solution was significantly more potent than the equimolar pure glucose, glc90, solution (P < 0.05). Addition of 45 mM gln (gln:glc) or ala (ala:glc) to 45 mM glucose resulted in a twofold increase of water and sodium absorption compared with 45 mM glucose (glc:man). Chloride absorption (Table 3) was significantly increased by gln:glc and gln90 and potassium absorption by ala:glc and gln:glc solutions (both, P ≤ 0.05). Glc90 solution did not significantly affect chloride and potassium fluxes.


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  		Table 3. Net water, electrolyte, and solute fluxes in human jejunum

 


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  		Fig. 1. Water (JW, top) and sodium (JNa, bottom) net fluxes over 30 cm jejunum in 6 healthy subjects studied at baseline. Negative values denote net secretion into jejunal lumen; positive values denote net absorption from lumen. Bars represent means ± SE. The order of infusion of the solutions is given in Table 1 and their composition in Table 2. *P < 0.05 vs. saline and {dagger}P < 0.05 vs. glc90 (Dunn’s multiple comparison test). See Table 3 for other electrolyte and solute fluxes.

 
Glutamine and alanine reverse net water secretion induced by PGE1 to water absorption.   As expected, PGE1 intrajejunal infusion shifted basal water, sodium, chloride, and potassium net absorptive fluxes during infusion of saline to a secretory pattern (Table 3, Figs. 1 and 2). All tested solutions reduced water and sodium secretion to some extent (Fig. 2). However, this effect reached statistical significance only for the three amino acid-containing solutions (P ≤ 0.05, Dunn’s multiple comparison test compared with saline). Alanine-glucose and glutamine-glucose solutions even reversed net water secretion to an absorptive pattern (Fig. 2). Chloride and potassium fluxes were significantly affected by ala:glc and gln:glc solutions (Table 3).



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  		Fig. 2. Water (top) and sodium (bottom) net fluxes over 30 cm jejunum in 6 healthy subjects studied during hypersecretion induced by 0.1 µg·kg–1·min–1 intrajejunal PGE1. Negative values denote net secretion into jejunal lumen; positive values denote net absorption from lumen. Bars represent means ± SE. The order of infusion of the solutions is given in Table 1 and their composition in Table 2. *P < 0.05 vs. saline (Dunn’s multiple comparison test). See Table 3 for other electrolyte and solute fluxes.

 
PGE1 does not influence glucose, glutamine, and alanine absorption.   Glutamine was very efficiently absorbed over segment I-P and segment P-D (Table 3). Glutamine cumulative absorption over 45 cm reached 87 to 99% of infused load in the basal state. Glutamine total absorption as well as its segmental absorption over P-D (Table 3) was strongly correlated to the rate of infusion and to the output entering the study segment at port P (r = 0.99, P < 0.05), thus indicating that glutamine jejunal absorption was not saturated in this range of concentration. PGE1-induced hypersecretion did not influence the segmental absorption of glutamine infused either alone (gln90) or in combination with glucose (gln:glc) (Table 3). Alanine and glucose cumulative absorption also reached nearly 100% over 45 cm and were not significantly altered by PGE1 infusion. At baseline, coupling ratios between sodium absorption and 90 mM glucose absorption averaged 1.1:1, and those between sodium absorption and 90 mM glutamine absorption averaged 1.2:1 (not significantly different). These coupling ratios were both enhanced during hypersecretion and averaged 2.1:1 and 1.7:1, respectively (not significantly different).


   DISCUSSION
TOP
 ABSTRACT
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The present study demonstrates that glutamine is able to promote absorption more potently than glucose and that both substrates may be used in an additive way. Moreover, the stimulating effect of glutamine is maintained during an experimental stimulation of secretion mimicking a secretory diarrhea.

The intestinal infusion technique is an established method to assess water and electrolyte transport in human intestine and the effects of specific substrates, both in healthy humans (14, 15, 20) and diarrheic patients (4, 28, 41). The triple-lumen tube method used in this study is more accurate than the double-lumen tube to measure segmental fluxes (4, 27). The intrinsic limitation of the intestinal infusion technique comes from the limited length of intestine under study, which does not allow a definite extrapolation of data on the full length of intestine. However, the jejunum is a major site for intestinal absorption, and most of nutrients are absorbed up to 75% over 50 cm of jejunum (42); more specifically, glutamine is absorbed almost 70% over 30 cm jejunum (12); thus the present study on 30 cm already gives a reasonable estimate of the major part of glutamine-related water and electrolyte absorption. Hypersecretion induced by PGE1 was chosen because infusion of PGE1 in human jejunum induces a reproducible pattern of water and electrolyte secretion, which resembles much that of cholera (4, 26). Moreover, intestinal hypersecretion induced by cholera enterotoxin may be mediated in part by an increased local production of prostaglandins (2, 41). The infusion rate of PGE1 used in this study (0.1 µg·kg–1·min–1) was selected to induce a marked hypersecretion, yet without saturation of secretory pathways (38). The resulting water secretion (Fig. 2) was in the medium range of that reported in the jejunum of cholera patients (4).

The effects of glutamine on water and electrolyte absorption have been well established in experimental models. Indeed, glutamine stimulates sodium and water absorption in rabbit (1, 19, 29, 37), bovine (5, 10), porcine (2, 32, 33), or rat small intestine (24) under basal conditions and during hypersecretion. In these models, hypersecretion was induced by cholera toxin (1, 24, 37), cryptosporidiosis (2, 5, 10), rotavirus (33), or enteropathogenic Escherichia coli (29). In cholera-infected humans, glutamine in the presence of glucose reduced net water and sodium secretion to the same degree as glucose alone (41). Nevertheless, the effects of glutamine alone were not tested (41). In infants with acute noncholera diarrhea, a glutamine-enriched ORS did not provide any additional therapeutic advantage over the standard ORS, possibly because the total osmolarity of this experimental ORS was too high (34). Indeed, hypoosmolar solutions could be more efficient (17).

In the present study, the 90 mM glutamine solution stimulated sodium and water segmental absorption more potently than the 90 mM glucose solution in baseline. Because coupling ratios between sodium and both solutes are similar, this could be explained in part by a higher segmental absorption of glutamine compared with glucose (Table 3). In vitro studies with Ussing chambers have suggested that glutamine stimulates to a variable extent both electrogenic sodium absorption and electroneutral NaCl absorption (1, 29, 32). These two components of sodium transport cannot be distinguished in vivo. However, the superiority of glutamine over glucose could come in part from its ability to promote chloride absorption and consequently electroneutral NaCl absorption, whereas glucose effect is limited to the electrogenic glucose-sodium cotransport. In hypersecretion-induced conditions, gln:glc and gln90 increased water and sodium absorption compared with saline, whereas glc90 did not significantly affect fluxes. With the glutamine-glucose solution, the net water and sodium absorptive fluxes were about twofold those observed with glucose. This result confirms in vitro experiments (13, 29, 31) showing that glutamine and glucose have additive effects on sodium absorption, which reflects the existence of separate sodium-solute cocarriers for glucose and glutamine at the apical membrane of enterocytes (31), with no competitive effect of glucose on glutamine intestinal absorption (13).

The alanine-glucose ORS also stimulated water and sodium absorption, which is in accordance with previous data (24, 41). The effects of alanine-glucose and glutamine-glucose solutions on sodium absorption were almost identical, suggesting that at the tested amino acid concentration (45 mM), sodium absorption results mainly from a solute-sodium cotransport of similar capacities. It has been suggested in some experiments that alanine and glutamine may be transported by the same carrier in rat enterocytes (6), but other studies indicate that glutamine transport may be carried by several distinct Na+-dependent (A, N, Y+) and Na+-independent (L) transport systems, whereas alanine is transported mainly by the Na+-dependent ASC system (31). During a secretory diarrhea induced by cholera toxin in rats (24), an experimental ORS containing the dipeptide alanyl-glutamine was more effective than a glutamine-containing ORS on water and sodium absorption; this could be explained by a stronger effect of the dipeptide on sodium absorption compared with any constitutive single amino acid (31), by the additive effects of alanine and glutamine generated by the intraluminal hydrolysis of the dipeptide, or by the effect of a proton/dipeptide cotransport (11). Alanyl-glutamine containing ORS have not been evaluated in humans.

In the present study, an apparent stoichiometric ratio of about 1:1 for sodium-glucose and glutamine-glucose cotransport has been estimated, which is in accordance with classical experiments in rabbit ileum but probably underestimates the true absorptive glutamine:sodium ratio; other studies have suggested that a ratio of 2:1 was closer to the actual transepithelial influxes (3, 5, 13, 20, 29). Indeed, glutamine transport across intestinal brush-border membrane is only partly sodium dependent (36). Thus the actual Na+-glutamine coupling ratio is probably higher than 1.2:1 at baseline and than 1.7:1 at the hypersecretory state, because of an enhanced paracellular Na+ efflux (33).

Finally, glutamine was almost completely absorbed along the 45-cm-long jejunal segment. This confirms our previous observations that, in this range of infusion rate (27 and 54 mmol/h), glutamine absorption is ~70% over 30 cm jejunum (12). The estimated Km for glutamine absorption in human jejunum is 2.3 mmol/min, i.e., 139 mmol/h (12); thus even the highest infusion rate in the present study is far from saturating glutamine absorption. Interestingly, glutamine absorption was not affected by experimental hypersecretion (Table 3); this is in accordance with experimental studies showing maintained glucose (8) or glycine (21) absorption during cholera and with the clinical observations that glucose- or amino acid-linked sodium absorption is maintained in cholera patients (4, 28). Glucose and alanine were also almost completely absorbed, even during PGE1 infusion; only a very high PGE1 infusion rate decreased glucose absorption ~25% in other studies (26).

In conclusion, glutamine promotes sodium absorption in human jejunum both at baseline and during hypersecretion, an effect that is additive to that of glucose. Moreover, glutamine absorption is maintained during hypersecretion. Thus, in addition to its beneficial effect on intestinal fluid and electrolyte transport, glutamine could be efficiently administered to diarrheic patients via the enteral route, as a specific component of the nutritional therapy of associated malnutrition.


   FOOTNOTES
 

Address for reprint requests and other correspondence: P. Déchelotte, ADEN, IFR 23, Faculté de Médecine-Pharmacie, 22 Bd Gambetta, 76183 Rouen Cedex, France (E-mail: pierre.dechelotte{at}chu-rouen.fr)

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.


   REFERENCES
TOP
 ABSTRACT
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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