potassium transport in the small bowel - gut.bmj.com · l. a. turnberg duce similar flow rates and...

Gut, 1971, 12, 811-818

Potassium transport in the human small bowelL. A. TURNBERG

From the Manchester Royal Infirmary

SUMMARY Perfusion experiments in the small intestine of normal subjects and in the ileum ofpatients with ileostomies demonstrated that the distribution of potassium across the mucosawas compatible with a passive process for transport. In the jejunum potassium transport was shownto be markedly influenced by solvent drag and the jejunal mucosa appears to be more permeableto potassium than to sodium. This permeability was apparently unaffected by calcium in the lumenin concentrations ofbetween 1 a15 and 7.25 m-equiv/l. In the ileum potassium transport was influencedby changes in luminal sodium concentration and it is suggested that this is a passive consequenceof the change in electrical potential which the change in sodium concentration induces. The electricalpotential is thought to be a sodium diffusion potential. All the evidence thus points to a purelypassive behaviour of the small intestine towards potassium.

While intestinal transport of sodium has been thesubject of fairly intensive investigation less attentionhas been paid to potassium transport in the humansmall bowel. Indirect evidence suggests that potas-sium is distributed simply passively across themucosa of the small bowel. Thus after a meal itsconcentration in luminal contents of jejunum andileum is close to plasma concentrations (Fordtranand Locklear, 1966) and isotonic electrolyte solu-tions equilibrate in the lumen of the small bowelat a similar potassium concentration (Code,Phillips, and Swallow, 1966). Investigationssuggest that potassium transport is a purely passiveprocess in the rat (Gilman, Koelle, and Ritchie,1963) and a similar conclusion was reached byPhillips and Summerskill (1967) on the basis of small-intestinal perfusion experiments in man. The presentinvestigations were designed to confirm and extendthese observations and to study some of the factorswhich influence transport of potassium.

Methods

Normal young adult volunteers formed the majorityof the experimental subjects in these investigations.In addition, four patients who had had an ileostomyfor ulcerative colitis or Crohn's disease of the largebowel, performed between one and six years beforethis investigation, were also studied. These patientswere fit and well, had normal serum electrolyteRoceived for publication 21 July 1971.

concentrations, and the terminal ileum and ileostomywas normal so far as could be judged clinically. Thenature of the tests was fully explained beforepatients were asked if they would take part.

Perfusion studies in the normal volunteers wereperformed using a triple-lumen tube technique(Cooper, Levitan, Fordtran, and Ingelfinger, 1966).This technique has been described in detail pre-viously (Fordtran, Rector, and Carter, 1968) butbriefly the test involves the constant infusion of testsolutions into the lumen of the intestine and thesampling of luminal contents 10 and 40 cm distally.For the jejunal studies the infusion point was sitedat the duodeno-jejunal junction and for the ilealstudies at 200 cm from the teeth. The infusion ratewas 10 ml/min for most of the jejunal studies. In thestudies of the influence of water movement onpotassium transport, in which solutions of varyingtonicity were infused, it was necessary to modifythe infusion and aspiration rates and the concen-tration of electrolytes in order to achieve constantmean flow rates and mean ionic concentrations inthe test segment of jejunum. Thus, when a solutionmade hypertonic with mannitol was infused, waterentered the lumen across the mucosa in answer tothe osmotic gradient. This had the effect of increasingthe flow rate through the test segment and of de-creasing the concentration of solutes in the lumen.A hypotonic solution, from which water was rapidlyabsorbed, developed a decreased mean flow rate andan increased solute concentration. In order to pro-

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L. A. Turnbergduce similar flow rates and solute concentrationswith these two solutions it was necessary to infusethe hypertonic solutions at a slower rate (8.0 ml/min) and take samples at a faster rate from theproximal aspiration site (1.5 ml/min) than with thehypotonic solutions (14 ml/min and 1.0 ml/minrespectively). To maintain similar mean potassiumconcentrations in the test segment the hypertonicsolutions had a higher potassium concentration(8 m-equiv/l) than the hypotonic solutions (25m-equiv/l). Using this technique, mean flow ratesand electrolyte concentrations in the intestinal lumenwere similar when either a hyper- or hypotonicsolution was infused (Table I).

Solution Mean Flow Rate Mean Potassium(ml/min) Concentration (m-equiv/l)

Hypotonic 11-4 4.5Isotonic 10.0 4-7Hypertonic 10-7 5.25

Table I Mean values for flow rate through the testsegment ofjejunum andfor luminalpotassiumconcentrations during perfusion with solutions ofvarying tonicity''By changing the infusion rate and initial potassium concentrations,as described in the text, it was possible to achieve similar results withthese three solutions.

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Fig. 1. Double-lumen tube perfusion of the distal ileumthrough an ileostomy.

The studies of distal ileum in the patients withileostomies were performed using a double-lumentube perfusion technique similar to that describedby Wright, Cleveland, Tilson, and Herskovic (1969).The tube was made of two polyvinyl tubes looselyattached to each other and gently inserted throughthe ileostomy to a distance of 35 cm (Fig. 1). Testsolutions were infused at a steady rate through theopening at the tip of the tube and intestinal contentswere sampled 10 cm distal to this point through thesecond tube. This sample consisted partly of infusateand partly of intestinal fluid, which had mixed withit during passage down the intestine. The remainderof this perfusate passed down the last 25 cm of ileumand was collected in a disposable ileostomy bag. Itwas thus possible to measure electrolyte transportin the last 25 cm of ileum with this technique.Before perfusion studies were started an isotonicelectrolyte solution was infused at 15 ml/min untilthe ileal washings leaving the ileostomy becameclear. Test solutions were then infused at 9 ml/minfor a 30-minute equilibration period and continuedfor a 40-min test period. On the basis of previousexperience with triple-lumen tube perfusion experi-ments in normal subjects it was felt that theseequilibration and collection period times would besufficient to produce the necessary steady stateconditions at this infusion rate. This was validatedin two studies in which two consecutive perfusionexperiments were performed, each of 40 minutes,after an initial 30-min equilibration period. Theduplicate values for marker and potassium concen-trations were very close to each other on bothoccasions. With an infusion solution containing5 m-equiv/l potassium the potassium transport rateswere + 0.04 and - 0.01 m-equiv/hour at a meanluminal potassium concentration of 4.7 m-equiv/lfor both of the first pair of studies, and, with aninfusion solution containing 10 m-equiv/l, transportrates were -0.22 and -0.20 at mean luminalpotassium concentrations of 7-8 and 7.95 m-equiv/lrespectively for the second pair. Samples of perfusatewere taken at 1.5 ml/min from the aspiration tubewith a syringe, by hand. The fluid leaving theileostomy was also collected for 40 minutes but thetiming of this collection was delayed by eightminutes from that for the aspirated sample. Pre-liminary investigation had suggested that the peakconcentration of a bolus of infused bromsulphaleintook eight minutes to pass down the 25 cm of ileumbetween the aspiration site and the ileostomy.Three different test solutions were infused consecu-tively during each investigation.

All infusion solutions contained 5 g/l of the poorlyabsorbable marker polyethylene glycol 4000 (PEG).Polyethylene glycol concentrations were measured

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Potassium transport in the human small bowel

by the method of Hyden (1955), sodium andpotassium by flame photometry, chloride with an

EEL chloride meter, and total carbon dioxidecontent with a Natelson microgasometer. Osmolalitywas measured with an Osmette freezing pointosmometer.

Results

JEJUNUM

solvent drag is an important force in the passivetransport of potassium in the jejunum.

Influence ofcalcium on potassium transportSince it is known that calcium exerts an effect on

the passive permeability of a number of biologicalmembranes it was of some interest to study theinfluence of calcium, in different concentrations, on

potassium transport. In 14 normal subjects electro-

Influence ofpotassium concentration on absorptionThe influence of changes in luminal potassium con-

centration on net potassium transport rate was

studied in four subjects. Solutions infused contained100 m-equiv/l of sodium chloride, 30 m-equiv/lsodium bicarbonate, and 1, 5, or 10 m-equiv/l ofpotassium chloride. Small amounts of mannitolwere added to the solutions with the lower potassiumconcentrations so that each solution had a similarosmolality of 280 mOsm/kg. The results, depictedin Figure 2, show that there is a linear relationshipbetween mean luminal potassium concentration andnet potassium transport rate. At concentrationsgreater than 3.5 to 40 m-equiv/l potassium was

absorbed while at lower concentrations potassiumwas secreted into the lumen. There was no netpotassium movement into or out of the lumen atthis concentration which was similar to the serumpotassium level of between 3.8 and 5.2 m-equiv/lin these subjects. These findings suggest that potas-sium may be distributed passively across the jejunalmucosa.

Influence of solvent dragSodium transport in the human jejunum has beenshown to be markedly influenced by the directionand volume of water flowing across the mucosa

(Fordtran et al, 1968). It was of interest then to studythe influence of water movement on potassiumtransport. This was investigated in seven normalsubjects in a series of experiments in which thepotassium concentration in the lumen was heldconstant at a level similar to that in plasma whilewater was made to enter or leave the lumen across

the mucosa by changing the osmotic pressure of theperfusate. Hypotonic solutions were made by reduc-ing the concentration of electrolytes and hypertonicsolutions by adding the non-absorbable mannitol.The results, shown in Figure 3, demonstrate that ata constant potassium concentration water move-

ment had a marked influence on potassium transport.Thus potassium absorption was associated withwater absorption and secretion with water secretion.When water movement was nil, net potassiummovement also ceased. These findings suggest that

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Fig. 2. Jejunum. Relationship between potassiumtransport rates and the mean potassium concentration inthe lumen.

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Fig. 4. Jejunum. The relationship between net water and net potassium transport rates at three differentintraluminal concentrations of calcium.

lyte solutions containing 5 m-equiv/l potassiumchloride, 130 or 135 m-equiv/l sodium chloride,and 1, 5, or 10 m-equiv/l of calcium chloride wereinfused at 4.5 ml/min into the jejunum. Absorptionof potassium was variable in these studies but therewas no evidence that changing the intraluminalcalcium concentration altered potassium transport.When the mean intraluminal calcium concentra-tions were 1.15, 4.22, and 7.25 m-equiv/l potas-sium absorption rates were 0.187, 0.113, and0.117 m-equiv/hour respectively and these were notsignificantly different from each other. Watermovement in these studies varied from secretion of47 ml/hour to absorption of 107 mI/hour but thisvariation was not related to changes in luminalcalcium concentration or calcium transport rates.However, potassium movement bore a directrelationship to water movement (Figure 4). Ifpotassium transport here is a passive process, as

suggested by the results presented above, then thevariation in potassium movement shown in Figure 4is probably secondary to the variation in watermovement. The finding that the slope of the linefor this relationship is virtually identical for thestudies performed at three different concentrationsof calcium suggests that the permeability of thejejunal mucosa to potassium is also unaffected bychanges of this order in luminal calcium concen-tration.

ILEUM

Slow perfusionIn 14 normal subjects the ileum was perfused withan electrolyte solution resembling plasma incomposition. This solution was infused at the slowrate of 2.5 ml/minute so that changes in electrolyteconcentration were made more obvious by pro-longation of the contact time between mucosa andperfusate.The initial concentration of potassium was

5 m-equiv/l and after passing down the 45 cm ofileum between the infusion site and the distal endof the test segment a mean concentration of4.94 m-equiv/l was reached (Table II). Potassiumwas slowly absorbed from this solution at a meanrate of 0.14 m-equiv/hr/30 cm of ileum. Thisconcentration is near to the concentration whichwas achieved when solutions were allowed toequilibrate in the lumen (Code et al, 1966). Since itis close to plasma concentrations this equilibriumvalue suggests that potassium is distributed acrossileal mucosa by passive forces as in the jejunum.

Ileostomy perfusionThe influence of variation in luminal potassiumconcentration on potassium transport was investi-gated during perfusion of the distal ileum in fourpatients with ileostomies. All solutions had a similar

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Potassium transport in the human small bowel

Test Concentration ofK+ K+ Absorption (-) orNo. Secretion (+) (m-equlvj

Distal End ofTest Segment Mean

1 5S65 5-43 -0-072 49 49 -0093 52 52 -0-784 4-6 4-7 -0-08S 4-8 485 -0 116 4-4 455 -0 187 4-6 4-7 -0-048 4-4 455 -0159 4-4 4.5 -01010 4-6 4-7 -0-2311 655 6-0 -0-0212 4.35 4.55 -0-0613 5S1 4-92 -0-0614 5S6 5S6 +0-01Mean 4.94 4.94 -0-14

Table II Concentration ofpotassium at the distal endof the ileal test segment and the mean concentrationduring slow perfusion of the ileum for 14 subjects andpotassium transport rates

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/hr)sodium concentration of 135 m-equiv/l. The resultsof these studies, shown in Figure 5, demonstrate alinear relationship between potassium concentra-tion and transport rate. As in the jejunum, potassiumwas neither absorbed nor secreted when the luminalpotassium concentration was similar to plasmaconcentrations at 3.5 to 4.0 m-equiv/l.

This finding lends support to the suggestion thatpotassium is transported by passive forces in theilleum.

Influence of changing sodium concentration onpotassium transportSolutions containing potassium, 5 m-equiv/l, andsodium in a concentration of 25, 75, or 140 m/equiv/l,were infused into the ileum in a group of normalsubjects. Isotonicity was maintained by the additionof mannitol to solutions with low sodium concen-trations. In four experiments the electrical potentialdifference between lumen and abraded skin wasmeasured during perfusion of these solutions andin seven experiments electrolyte transport rates weremeasured. The results, shown in Figure 6, revealthat as the luminal sodium concentration waslowered from a mean concentration of 124.4 to27-4 m-equiv/l, potassium absorption increasedfrom 0.21±0.04 to 0.42±0.1 m-equiv/hour (mean+ 1 SE). This increase just fails to reach statisticalsignificance (0.05 <P < 0 1). The electrical potentialdifference increased as sodium concentration wasreduced, the lumen becoming increasingly electro-positive (Fig. 6). This change in PD, which isprobably the result of a sodium diffusion potential(Turnberg, Bieberdorf, Morawski, and Fordtran,1970), would tend to increase the passive absorption

50 100SODIUM CONCENTRATION (mEq/litre)

.25Fig. 5. Ileum. Potassiumtransport rates at differentmean intraluminal potassium

.20 concentrations in patientswith ileostomies.

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I5 intraluminal concentrations ofsodium, when potassiumconcentration was constant.Also shown are the meanvalues for the electrical PD at

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of potassium and may account for the observedincrease in absorption.

Discussion

The finding that potassium is absorbed from thejejunum and ileum when the luminal concentrationis higher than that in plasma and secreted when itis lower suggests that potassium traverses the mucosaaccording to the simple physical forces governingdiffusion of ions.

Diffusion of potassium across the mucosa fromthe lumen would appear to be an adequate mechanismfor its absorption since the concentration of potas-sium in ingested food is usually much higher thanin plasma. Thus on theoretical grounds, too, thereis no requirement for a special active transportprocess for potassium absorption.The electrical potential will influence the distribu-

tion of ions across the mucosa, but it is unlikelythat it affected potassium movement in theseexperiments since the PD was close to zero duringperfusion with solutions similar to those used here(Turnberg, Fordtran, Carter, and Rector, 1970).

Phillips and Summerskill (1967) also concludedfrom the results of their perfusion experiments thatpotassium was transported passively in the humansmall intestine. However, interpretation of theirdata is complicated by their use of perfusion solutionsin which potassium concentrations were variedreciprocally with sodium concentrations. At highpotassium concentrations sodium concentrationswere low and, as shown in the present studies inthe ileum, potassium transport is influenced by theluminal sodium concentration, as well as by thepotassium concentration. Reciprocal changes madein the concentration ofboth ions will have an additiveeffect on potassium transport, and the influence ofeach of these ionic concentration changes alonecannot be assessed. In those studies in which sodiumand potassium concentrations were not far removedfrom plasma concentrations, where the predominantfactor influencing potassium transport was thepotassium concentration, their results are morereadily interpreted as indicating a passive processfor potassium transport. The present studies, inwhich the complicating influence of variation insodium concentration was removed, confirm theseconclusions.The mechanism by which potassium absorption

is enhanced by lowering the luminal sodiumconcentration is most likely to be through the changein electrical potential which this produces. At lowsodium concentrations the lumen became moreelectropositive, probably as a result of a sodiumdiffusion potential (Turnberg et al, 1970). This change

would itself enhance the passive absorption ofpotassium ions.

Transport of potassium in the jejunum is shownhere to be markedly influenced by the movement ofwater across the mucous membrane. Thus watermoving from lumen to mucosa took potassium withit even in the absence of an electrochemical gradientwhich would make potassium diffuse across themembrane. Water flowing across the membrane isbelieved to take up small solutes in its stream andsweep them through 'pores' thought to exist in themembrane. This phenomenon of 'solvent drag' hasbeen put forward as an important mechanism forsodium absorption in the human jejunum (Fordtranet al, 1968). The present results suggest thatpotassium movement is also markedly influenced bysolvent drag.

Phillips and Summerskill (1967) suggested thatpotassium was not influenced by solvent drag in thejejunum but this conclusion was based on the resultsof experiments in which luminal potassium concen-trations were 20 m-equiv/l. At this level diffusion ofpotassium out of the lumen will predominate and islikely to swamp any effect due to solvent drag.Conclusions made about solvent drag under theseconditions are thus likely to be in error.A numerical indication of the permeability of a

membrane to an ion is given by its reflectioncoefficient (a), and the smaller a the greater thepermeability. It is possible to calculate a forpotassium from the slope of the line relatingpotassium movement to water movement inFigure 3, using the formula J. = c (1 -a)Jw(Curran and Schultz, 1968) where Js is the solutemovement, Jw the water movement, and c themean potassium concentration across the membrane.a for potassium derived in this way is 0.38 whichcompares with the value of 0.45 for sodium cal-culated by Fordtran, Rector, Ewton, Soter, andKinney (1965). Although the derivation of thesevalues may be open to question they do suggestthat the human jejunum is more permeable topotassium than to sodium. It is of interest in thisrespect that although the relative permeability of amembrane towards different ions depends on severalfactors (Diamond and Wright, 1969) the hydratedpotassium ion is somewhat smaller than the hydratedsodium ion (Ussing, 1960).Although the intracellular potassium concentra-

tion of human intestinal mucosal cells has not beenmeasured it is likely that, as in other mammals, itis higher than plasma levels (Schultz, Fuisz, andCurran, 1966). The question arises then as to howpotassium in the lumen is able to cross the mucosaso rapidly by solvent drag, when it is separatedfrom plasma by a mucosal barrier containing a high

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Potassium transport in the human small bowel 817

concentration of potassium. One possibility is thatthe pores through which the potassium equilibrateslie in the so-called tight junctions between the cellsrather than in the cell membrane itself. Evidence infavour of a similar route for the rapid flux ofpotassium across rat colonic mucosa has beenreported by Barnaby and Edmonds (1969), andsimilar suggestions have been made for the routefor passive sodium movement across rat ileum andfrog skin (Clarkson, 1967; Cereijido and Rotunno,1968). An alternative explanation is that potassiummay traverse the cell rapidly through a compartmentwhich is separated from the bulk of the intracellularpotassium.

In a variety of epithelia the permeability todifferent ions has been shown to be influenced consid-erably by the concentration ofcalcium in fluid bathingthe mucosal surface.Thus, bathing toad bladder, frogskin, frog gastric mucosa, and rabbit gallbladderwith a calcium-free medium increases their permea-bility to cations, while increasing the calciumconcentration decreases their permeability (Hays,Singer, and Malamed, 1965; Curran and Gill, 1962;Sedar and Forte, 1964; Wright and Diamond,1968). In the present investigations, changing themean luminal calcium concentration from 1*15 to7-25 m-equiv/l did not apparently alter potassiumabsorption rates nor did it clearly influence therelationship between potassium and water absorp-tion. Thus, there was no evidence to suggest thatpermeability to potassium was affected by changesin calcium concentrations over the range normallyfound in the intestine after meals (Fordtran andLocklear, 1967). This does not exclude the possibilitythat mucosal permeability is influenced by calciumconcentrations outside this range, and indeed itseems likely that if an extremely low calciumconcentration could be achieved in the immediatevicinity of the mucosal cell surface then ionpermeability would be changed. However, thisphenomenon is unlikely to be observed in vivo.Although open to criticism the assumption was

made in the studies of patients with ileostomiesthat the terminal ileum in these subjects behavedas a normal ileum, at least towards potassium. Insupport of this assumption are the results of theslow perfusion studies of ileum in the normalsubjects which fit in well with the conclusion,derived from the ileostomy perfusion experiments,that potassium is transported passively. While allthe evidence presented here suggests that potassiumtransport is a purely passive process in the smallintestine some observations suggest that this maynot always be the case. Thus potassium concentra-tions in ileostomy effluent may reach levels muchhigher than in plasma in salt-depleted patients,

suggesting the possibility that active potassiumsecretion might occur under these conditions(Clarke, Hill, and Macbeth, 1967). However, theelectrical PD across ileal mucosa has not beenreported in these circumstances and the mechanismior the high potassium concentrations cannot beascribed with certainty.

I am grateful to Mrs M. Dussart and Miss T. Bunnellfor their expert technical assistance with theseinvestigations.

I would like to thank the Research GrantsCommittee of the United Manchester Hospitalsfor financial support for most of this work. Some ofthis work was performed while the author held aresearch fellowship in the Department of InternalMedicine, Southwestern Medical School, Dallas,USA, and was supported under US Public HealthService training grant S.TOIAM5490 and researchgrant 5ROl.AM06506.

References

Barnaby, C. F., and Edmonds, C. J. (1969). Use of a miniature GMcounter and a whole body counter in the study of potassiumtransport by the colon of normal, sodium-depleted and adren-alectomized rats in vivo. J. Physiol. (Lond.), 205, 647-665.

Cereijido, M., and Rotunno, C. A. (1968). Fluxes and distribution ofsodium in frog skin. A new model. J. gen. Physiol., 51, 280,289S.

Clarke, A. M., Hill, G. L., and Macbeth, W. A. A. G. (1967). Intestinaladaptation to salt depletion in a patient with an ileostomy.Gastroenterology, 53, 444-449.

Clarkson, T. W. (1967). The transport ofsalt and water across isolatedrat ileum: evidence for at least two distinct pathways. J. gen.Physiol., 50, 695-727.

Code, C. F., Phillips, S. F., and Swallow, J. H. (1966). The finalcommon sorption fluids of small and large bowel. J. Physiol.(Lond.), 187, 42-43P.

Cooper, H., Levitan, R., Fordtran, J. S., and Ingelfinger, F. J. (1966).A method for studying absorption of water and solute fromthe human small intestine. Gastroenterology, 50, 1-7.

Curran, P. F., and Gill, J. R., Jr. (1962). The effect of calcium onsodium transport by frog skin. J. gen. Physiol., 45, 625-641.

Curran, P. F., and Schultz, S. G. (1968). Transport across membranes:general principles. In Handbook of Physiology Sect. 6,American Physiological Society, Washington, D.C. AlimentaryCanal, Vol. III, pp. 1217-1243.

Diamond, J. M., and Wright, E. M. (1969). Biological membranes:the physical basis of ion and non electrolyte selectivity. Ann.Rev. Physiol., 31, 581-646.

Fordtran, J. S., and Locklear, T. W. (1966). Ionic constituents andosmolality of gastric and small-intestinal fluids after eating.Amer. J. dig. Dis., 11, 503-521.

Fordtran, J. S., Rector, F. C., Jr., and Carter, N. W. (1968). Themechanisms of sodium absorption in the human smallintestine. J. clin. Invest., 47, 884-900.

Fordtran, J. S., Rector, F. C., Jr., Ewton, M. F., Soter, N., andKinney, J. (1965). Permeability characteristics of the humansmali intestine. J. clin. Invest., 44, 1935-1944.

Gilman, A., Koelle, E., and Ritchie, J. M. (1963). Transport ofpotassium ions in the rat's intestine. Nature (Lond.), 197, 1210-1211.

Hays, R. M., Singer, B., and Malamed, S. (1965). The effect ofcalcium withdrawal on the structure and function of the toadbladder. J. Cell Biol., 25 (3, pt 2), 195-208.

Hyden, S. (1955). A turbidometric method for the determination ofhigher polyethylene glycols in biological materials. k. Lantbr.-Hdgsk. Annlr., 22, 139-145.

Phillips, S. F., and Summerskill, W. H. J. (1967). Water and elec-



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trolyte transport during maintenance of isotonicity in humanjejunum and ileum. J. Lab. clin. Med., 70, 686-698.

Schultz, S. G., Fuisz, R. E., and Curran, P. F. (1966). Amino acidand sugar transport in rabbit ileum. J. gen. Physiol., 49, 849-866.

Sedar, A. W., and Forte, J. G. (1964). Effects of calcium depletion onthe junctional complex between oxyntic cells of gastric glands.J. Cell Biol., 22, 173-188.

Turnberg, L. A., Bieberdorf, F. A., Morawski, S. G., and Fordtran,J. S. (1970). Interrelationships ofchloride,bicarbonate,sodium,and hydrogen transport in the human ileum. J. clin. Invest.,49, 557-567.

Turnberg, L. A., Fordtran, J. S., Carter, N. W., and Rector, F. C., Jr.

(1970). Mechanism of bicarbonate absorption and its re-lationship to sodium transport in the human jejunum. J.clin. Invest., 49, 548-556.

Ussing, H. H. (1960). The Alkali Metal Ions in Biology. I. TheAlkali Metal Ions in Isolated Systems and Tissues. (Handbuchder experimentellen Pharmakologie Erg8nzungswerk, Vol. 13)p. 3. Springer. Berlin.

Wright, E. M., and Diamond, J. M. (1968). Effects of pH and poly-valent cations on the selective permeability of gall bladderepithelium to monovalent ions. Biochim. biophys. Acta (Amst.),163, 57-74.

Wright, H. K., Cleveland, J. C., Tilson, M. D., and Herskovic, T.(1969). Morphology and absorptive capacity of the ileum afterileostomy in man. Amer. J. Surg., 117, 242 245.



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