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Malabsorption associated with diarrhea

and intestinal infections13


Irwin H. Rosenberg,4 M.D., Noel W. Solomons,5 M.D., and Roberto E. Schneider,6 M.D.

ABSTRACT An episode of diarrhea causes weight loss and a temporary cessation of growth
in infants and children. Diarrhea is accompanied by malabsorption of sugars, nitrogen, fats, and
micronutrients. The mechanisms by which acute diarrheal disease produce malabsorption have
not been studied carefully. The nutritional costs of malabsorption may pose a major threat if
diarrhea becomes chronic or recurrent. The hydrogen breath test for carbohydrate malabsorption
does not require intubation or blood drawing and can be used in children to help clarify the
importance of carbohydrate intolerance in the duration and perpetuation of acute diarrhea and

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intestinal bacterial overgrowth. Am. J. Clin. Nutr. 30: 1248-1253, 1977.

Diarrhea may well be the commonest dis- sorption, and we will examine the possible
ease/symptom in the world. In Central mechanisms by which infectious diarrhea
America a majority of childhood deaths are may produce a transient but significant mal-
associated with diarrhea (1). Morbidity absorption syndrome. Finally, we will dis-
from diarrheal disease must be measured cuss some of the possible nutritional impli-
not only in terms of the life-threatening ef- cations of malabsorption in diarrheal dis-
fects of water and electrolyte loss, dehydra- ease.
tion, and sepsis but also in terms of the
impact on growth and nutrition in children Malabsorption of nutrients
under the age of 5. It is well documented
that an episode of acute diarrhea results in a Table 1 presents a listing of the nutrients
drop in weight and a temporary cessation of the malabsorption of which has been docu-
growth in infants and children (2). Several mented in man in association with diarrheal
factors are involved in this detrimental ef- disease or intestinal infection. The largest
fect on nutritional status of the child. These number of studies are referable to malab-
factors include withdrawal of food, shift of sorption of sugars (3-15) and fats (4, 6, 16).
food from a more nutritious diet to one of Considering that sugars represent the end
starchy gruels, the nutritional costs of infec- product of digestion of starches, the com-
tion, and the impact of diarrheal disease on monest source of dietary calories in most of
the absorption and utilization of nutrients.
We will examine the evidence for the tem- ‘From the University of Chicago Pritzker School of
porary malabsorption syndrome which oc- Medicine and the Institute of Nutrition of Central
curs in association with diarrheal disease America and Panama.
2Supported in part by the Women’s Program of the
and evaluate the scope of this problem
Gastrointestinal Research Foundation.
based on published reports. The other fac- 2Address reprint requests to: Irwin H. Rosenberg,
tors which influence the effect of infectious M.D., Professor of Medicine, University of Chicago
diarrhea on nutritional status are discussed Pritzker School of Medicine, 950 East 59th Street,
Chicago, Illinois 60637.
elsewhere.
Professor of Medicine, Head, Section of Gastroen-
We will first examine the scope of the terology, University of Chicago Pritzker School of
problem by reviewing the evidence that nu- Medicine, Chicago, Illinois 60637 5Faculty Fel-
trient malabsorption exists in acute diar- low of the Josiah Macy Jr. Foundation; holds a Future
rheal disease and the documentation of indi- Leader’s Award of the Nutrition Foundation. Univer-
sity of Chicago Pritzker School of Medicine, Chicago,
vidual nutrient malabsorption. We will ex-
Illinois 60637. 6Division de Biomedica, Institute
plore the regularity with which diarrheal dis- of Nutrition of Central America and Panama, Guata-
ease of different etiologies produces malab- mala City, Guatamala.

1248 The American Journal of Clinical Nutrition 30: AUGUST 1977, pp. 1248-1253. Printed in U.S.A.
MALABSORPTION, DIARRHEA, AND INTESTINAL INFECTIONS 1249

TABLE 1 disaccharides. Second, intestinal lactase is


Nutrient malabsorption in acute diarrheal disease the most sensitive of the intestinal disac-
Nutrient Reference charidases to infectious, toxic, or metabolic
injury, and therefore lactose malabsorption
Sugar
Monosaccharides (glucose, 3-15 is one of the more sensitive indicators of
xylose) mild intestinal insult. Lipshitz and col-
Disaccharides (lactose) 6, 8, 12-15, 17 leagues studied 50 Mexican infants with se-
Nitrogen, protein, amino acids 18, 19
vere diarrhea and found 46% with lactose
Fat 4, 6, 16
Vitamins intolerance, 10% intolerant to other disac-
B,2 4, 7, 20-22 charidases, and 6% who could not tolerate
Folate 7, 23 monosaccharides (13-15). Sugar malab-
Vitamin A 24, 25 sorption, they suggest, may not only worsen
Minerals and trace elements 26, 27
diarrheal symptoms but may also contribute
substantially to the perpetuation and
the world, the potential impact of diarrheal worsening of bacterial overgrowth. The
disease on energy use is emphasized here. problem of repeated blood tests to docu-

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Indeed, preliminary results from a detailed ment lactose malabsorption in small chil-
study in Guatemala indicate that moderate dren with diarrheal disease has precluded
diarrhea may result in an increased calorie
extensive study of the problem of transient
loss in stool of 500 to 600 cal/day. lactose malabsorption, but with the more
Solid evidence exists also for nitrogen,
newly developed noninvasive breath tests
amino acid, and protein malabsorption (18, based upon elevations in breath hydrogen in
1 9) . In certain types of diarrheal disease, sugar malabsorption (28), it is likely that the
there is loss of excessive protein from the severity and duration of the problem of lac-
gastrointestinal tract by protein-losing en- tose intolerance with acute diarrheal disease
teropathy (3). Extensive studies of vitamin
will be more fully elucidated.
and trace element absorption are not availa-
ble, but documentation of malabsorption of Categories of infection associated with
vitamin B12 is regular in studies of patients malabsorption
with intestinal infection (4, 7, 20-22), and
the isolated reports of the malabsorption of Table 2 presents the problem of malab-
folate (7, 23) and vitamin A (24, 25) sug- sorption in diarrheal disease from the stand-
gest that malabsorption of both water- and
fat-soluble vitamins occurs with diarrhea. TABLE 2
Positive association of malabsorption and infection in
Excessive loss of magnesium has been seen
man
in acute enteritis (26), but definitely im-
paired absorption of this mineral has not Infection Reference

been documented. Animal models of infec- Bacterial enteritis


tious diarrhea have shown malabsorption of Salmonella 20
Shigella
trace elements such as zinc (27), but such
Vibrio cholerae 7
studies have not yet been performed in man. Viral enteritis
We call special attention to the problem Norwalk agent 5, 6
Qf sugar malabsorption in acute diarrheal Nonspecific gastroenteritis 4, 7, 29
disease. The work of Dr. Torres-Pinedo and Protozoal enteritis
Giardia lamblia 32
his associates (10, 11) has elegantly docu-
Coccidiosis 16, 30, 31
mented the severity of glucose malabsorp- Parasitic Infestation
tion in children with acute diarrheal disease. Hookworm 35, 36
Malabsorption has been confirmed in a wide Fish tapeworm 21, 22
Ascariasis 24, 25, 34
variety of enteritis, using the nondietary
Strongyloidiasis 37
pentose, xylose, as the test sugar. Malab- Systemic disorders
sorption of lactose is a problem of special Measles 3
importance for two reasons. First, this Tuberculosis 8, 18
sugar, which is the major carbohydrate in Systemic bacterial sepsis 25
Streptococcal infections 17
milk, is the most poorly absorbed of all
1250 ROSENBERG ET AL.

point of different etiologies. This table em- blood loss and iron deficit seen in hook-
phasizes the observation that whenever in- worm and schistosomal infestation.
testinal infection is sufficiently severe to
produce diarrhea, malabsorption also re- Pathogenesis of malabsorption in patients
suits. Thus, diarrheal disease and intestinal with diarrheal disease
infection associated with bacterial enteritis
(7, 20), viral enteritis (3, 5, 6), nonspecific The mechanism by which acute diarrheal
gastroenteritis (4, 7, 29), and protozoal (16, disease produces malabsorption has not
30-32) and parasitic infections (21 22, 24,
,
been studied carefully. However, the les-
25, 33-35) have all been documented to be sons learned from studies of chronic intes-
associated with malabsorption. Indeed, cer- tinal bacterial overgrowth, protein-calorie
tam systemic disorders not directly involving malnutrition, and other forms of more per-
the intestine have been shown to produce sistent intestinal mucosal damage may well
some element of malabsorption particularly, be applied to an evaluation of the mecha-
if not exclusively, when systemic infection nisms of malabsorption in acute diarrheal
results in a transient diarrheal syndrome (8, disease. The framework of possible mecha-

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17, 18, 23, 25). nisms is presented in Table 3. Malabsorp-
Some of the studies of xylose and folic tion could occur because of events in the
acid absorption by Lindenbaum (7) in pa- lumen of the intestine which interfere with
tients with cholera and related diarrheal dis- normal digestive and absorptive processes.
ease are instructive for their documentation Of these processes the one which is perhaps
of the finite period of malabsorption which most susceptible to interference is the im-
may be associated with acute bacterial diar- portant process of micelle formation, which
rheas. Similarly, the transient nature of is dependent upon a normal bile acid metab-
acute viral infection-induced malabsorption olism and which is required for the normal
has been well reviewed by Blacklow and his absorption of dietary fat (42). We are not
associates in the case of experimental viral sure whether transient proximal intestinal
infection with the Norwalk agent (6). In bacterial overgrowth occurs in all cases of
these studies, transient malabsorption was acute diarrheal disease, but it is likely from
observed even in infected patients who the studies in Guatemala that transient in-
failed to manifest clinical diarrhea. testinal bacterial overgrowth is common un-
The evidence for malabsorption in proto- der these circumstances (43). Deconjuga-
zoal and other parasitic infection is conflict- tion of bile salts in the proximal intestine in
ing. Transient malabsorption due to Giardia the presence of abnormal bacterial over-
infection with invasion of the intestinal mu- growth is well documented (44), and this
cosa is clearly documented (32). On the mechanism could interfere with the intes-
other hand, milder forms of acute giardiasis tinal absorption of fat.
have been studied and malabsorption has Other detrimental effects of proximal
not been found (33). Similarly, there are
TABLE 3
reports of some degree of malabsorption Malabsorption in diarrheal disease: pathogenetic
with Ascaris (24, 25, 34), hookworm (35, factors
36), and other parasitic infections of the
Framework of possible mechanisms
gastrointestinal tract (2). In a recent study
A. Intraluminal events
in rural Guatemala, mild to moderate intes-
1. Bacterial overgrowth
tinal parasitic infestation was not related to a. competition
ability to absorb calories, nitrogen, and fat b. metabolism (fermentation)
from a mixed diet (R. Schneider, personal c. gas
d. short chain fatty acids
communication).
e. bile acids
The balance of evidence seems to indicate
2. Osmotic effects
that malabsorption with intestinal parasites B. Cellular events
is irregular and mild and that the nutritional 1. Pharmacotoxic
importance of such malabsorption is uncer- 2. Cytotoxic
tain (33, 38-41), except in the case of the C. Villous abnormalities
MALABSORPTION, DIARRHEA, AND INTESTINAL INFECTIONS 1251

bacterial overgrowth have been observed. defects in intestinal absorption Cytotoxic


.

The bacterial mass is capable of competing effects of intestinal infection might be pro-
with the host for the uptake of ingested duced not only by bacterial toxins but also
nutrients; this phenomenon is well de- by metabolites of endogenous or exogenous
scribed in the case of vitamin B12 (45). Fur- materials.
thermore, the effects of bacterial metabo- Acute intestinal infection from a variety
lism of ingested nutrients may be important. of causes may be associated with morpho-
Bacterial fermentation of sugars occurs with logical and even villous abnormalities of the
production of gas and short-chain fatty acids intestinal mucosa similar to those associated
(46), both of which are capable of produc- with more severe chronic forms of malab-
ing gastrointestinal symptoms and increased sorption. There is often a marked loss of
water loss. Deconjugated bile acids them- absorbing surface. Such morphological ab-
selves may be irritating to the intestinal mu- normalities may reflect the toxin elabora-
cosa and may contribute to diarrhea by their tion of the offending organism, and there
own cathartic effects (47). Furthermore, may be direct invasion of the mucosa.
failure to digest and absorb sugars such as

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lactose or sucrose or the oligosaccharide Impact of infection-associated
products of starch digestion may result in an malabsorption on nutritional status
increased osmotic load in the gastrointes-
tinal lumen and thereby contribute to diar- A great deal of work is left to be done on
rhea with secondary effects on vitamin and assessment of the nutritional impact of the
micronutrient absorption. Finally, the cor- malabsorption which is associated with
relation between carbohydrate malabsorp- acute diarrheal disease. Obviously, the se-
tion and bacterial counts in the intestine, verity of the nutritional deficit is related to
reported previously (13), suggests that car- the duration and magnitude of the malab-
bohydrate malabsorption may contribute to, sorption in each individual situation. In fact,
as well as result from, bacterial contamina- the costs of malabsorption in diarrheal dis-
tion of the gut. ease rarely pose a major threat to nutri-
The second major category of pathogen- tional status unless diarrhea becomes
esis relates to the intestinal epithelium and chronic or recurrent. Then, the downward
its response to toxins from the lumen of the spiral of food withdrawal, malnutrition,
intestine. Such toxins can be categorized in diarrhea, malabsorption, etc., threatens
two general groups: the pharmacotoxic life. A certain percentage of children with
agents, which produce an abnormality of acute diarrheah disease of nonspecific cause
intestinal epithelial function without pro- have persistent carbohydrate intolerance
ducing a morphological change, and the cy- and therefore undergo a much more severe
totoxic agents, which cause damage with or and prolonged nutritional deficit. Coello-
without invasion of the intestinal epithe- Ramirez and Lipshitz reported that 18% of
hum. An example of the former is cholera 403 Mexican children with diarrhea had
toxin (48) and an example of the latter is persistent diarrhea and carbohydrate intol-
Shigella toxin (49). Current evidence indi- erance (13). Lindenbaum found that 18 of
cates that the pharmacotoxins such as chol- 52 patients with diarrhea in Bangladesh
era enterotoxin do not affect intestinal ab- failed to recover normal absorption within 2
sorption of sugars and amino acids. Indeed, weeks (7). New noninvasive techniques of
the fact that sugar absorption is intact in assessing bacterial overgrowth and carbohy-
cholera is used as the basis for oral therapy drate intolerance promise to add greatly to
with solutions containing glucose. However, our ability to study the costs and causes of
the effect of such toxins on net fluid excre- chronic diarrhea. The recently described hy-
tion may very well influence the absorption drogen breath test for carbohydrate malab-
and disposition of water-soluble nutrients sorption which is performed in children
such as folic acid. Shigella toxin contributes without intubation or blood drawing (36)
to a cytotoxic effect which interrupts normal should clarify the importance of carbohy-
intestinal epithehial processes, resulting in drate intolerance in the duration and per-
1252 ROSENBERG ET AL.

petuation of acute diarrhea and bacterial TORRES-PINEDO. Studies on the mechanism of

overgrowth. Coupled with the bile salt sugar malabsorption in infantile infectious diar-
rhea. Am. J. Clin. Nutr. 25: 1248, 1972.
breath test of bacterial overgrowth (50),
12. LUCKING, T., AND R. GRUTFNER. Chronische
which can now be performed with nonradio- Diarrhoe und schweres Inalabsorptionssyndrom
active ‘3C rather than ‘4C (51), thus obviat- im Sauglingsalter nach Infektion mit Dyspepsre-
ing any hazard in infants and children, such cole. Monatsschr. Kinderheilk. 121: 376, 1973.
tests will permit assessment of the relative 13. COELLO-RAMIREZ, P., AND F. LIPSHITZ. Enteric
microflora and carbohydrate intolerance in infants
importance of carbohydrate fermentation, with diarrhea. Pediatrics 49: 233, 1972.
bacterial overgrowth, and bile salt metabo- 14. LIPSHITZ, F., P. COELLO-RAMIREZ AND G. GU-
lism in the chronicity of childhood diarrhea. TIERREZ-TOPETE. Monosaccharide intolerance and
The hydrogen breath test also promises to hypoglycemia in infantswith diarrhea. I. Clinical
course of 23 infants. J. Pediatr. 77: 595, 1970.
be useful in assessing our ability to intervene
15. LIPSHITZ, F., P. COELLO-RAMIREZ AND G. GU-
with high-calorie nutritional diets early in TIERREZ-T0PETE. Monosaccharide intolerance and
the course of childhood diarrhea before fur- hypoglycemia in infants with diarrhea. II. Meta-
ther nutritional deficit is added to that which bolic studies in 23 infants. J. Pediatr. 77: 604,
so often underlies the diarrheal episode. U 1970. *

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16. BRANDBORG, L.L., S. B. GOLDBERG AND W. C.
BREIDENBACH. Human coccidiosis - a possible
References cause of malabsorption. The life cycle in small
bowel mucosal biopsies as a diagnostic feature.
1. SCRIMSHAW, N. S., C. E. TAYLOR AND J. E. GOR- New Engl. J. Med. 283: 1306, 1970.
DON. Interactions of nutrition and infection. WHO 17. INAGA, T. Absorption of lactose and its disorder
Monograph Ser. No. 57, Geneva: World Health by streptococcal infections. Acta. Paediat. Jpn.
Organization, 1968. 69: 926, 1965.
2. MATA, L. J., J. J. URRU1-rIA, C. ALBERTAZZI, 0. 18. COOK, G. C. Effect of systemic infections on gly-
PELLECER AND E. ARELLANO. Influence of recur- cylglycine absorption rate from the human je-
rent infections on nutrition and growth of children junumin vivo. Brit. J. Nutr. 32: 163, 1974.
in Guatemala. Am. J. Clin. Nutr. 25: 1267, 1972. 19. GHADIMI, H., S. KAMAR AND F. ABACI. Endoge-
3. DOSSETOR, J. F. B., AND H. C. WHITrLE. Protein- nous amino acid loss and its significance in infan-
losing enteropathy and malabsorption in acute tile diarrhea. Pediatr. Res. 7: 161, 1973.
measles enteritis. Brit. Med. J. 2: 592, 1975. 20. GIANNELLA, R. A., S. A. BROITMAN AND N.
4. BUTLER, T., F. G. MIDDLETON, D. L. EARNEST ZAMCHECK. Salmonella enteritis. II. Fulminant
AND G. T. STRICKLAND. Chronic and recurrent diarrhea in and effects on the small intestine. Am.
diarrhea in American servicemen in Vietnam. An J. Digest. Diseases 16: 1007, 1971.
evaluation of etiology and small bowel structure 21. PALvA, I. Vitamin B,2 deficiency in fish tapeworm
and function. Arch. Internal Med. 132: 373, carriers. A clinical and laboratory study. Acta
1973. Med. Scand. 171(Suppl. 374): 1, 1962.
5. SCHREIBER, D. S., N. R. BLACKLOW AND J. S. 22. NYBERG, W., AND M. SAARNI. Calculation on the
TRIER. The mucosal lesion of the proximal small dynamics of vitamin B,2 in fish tapeworm carriers
intestine in acute infectious nonbacterial gastroen- spontaneously recovered from vitamin B,2 defi-
teritis. New EngI. J. Med. 288: 1318, 1973. ciency. Acta Med. Scand. 175(Suppl. 412): 65,
6. BLACKLOW, N. R., R. DOLIN, D. S. FEDSON, H. 1964. S

DUPONT, R. S. NORTHRUP, R. B. HORNICK AND 23. MATOTH, Y., R. ZAMR, S. BASR-SHANI AND N.
R. M. CHANOCK. Acute infectious nonbacterial GROSSOWICZ. Studies on folic acid in infancy. II.
gastroenteritis: etiology and pathogenesis. Ann. Folic and folinic acid blood levels in infants with
Internal Med. 76: 993, 1972. diarrhea, malnutrition, and infection. Pediatrics
7. LINDENBAUM, J. Malabsorption during and after 33: 694, 1964.
recovery from acute intestinal infection. Brit. 24. SIVAKUMAR, B., AND V. REDDY. Absorption of
Med. J. 2: 326, 1965. vitamin A in children with ascariasis. J. Trop.
8. COOK, G. C. Glucose absorption kinetics in Zam- Med. Hyg. 78: 114, 1975.
bian African patients with and without systemic 25. SIVAKUMAR, B., AND V. REDDY. Absorption of
bacterial infections. Gut 12: 1001, 1971. labelled vitamin A in children during infection.
9. EINSTEIN, L. P., D. M. MACKAY AND I. H. Ro- Brit. J. Nutr. 27: 299, 1972.
SENBERG. Pediatric xylose malabsorption in East 26. BACK, E. H., R. D. MONTGOMERY AND E. E.
Pakistan: correlation with age, growth retardation, WARD. Neurological manifestations of magnesium
and weanling diarrhea. Am. J. Clin. Nutr. 25: deficiency in infantile gastro-enteritis and malnu-
1230, 1972. trition. Arch. Diseases Childhood 37: 106, 1962.
10. TORRES-PINEDO, R., C. RIVERA AND H. RODRI- 27. TURK, D. E., AND J. F. STEPHENS. Upper intes-
GUEZ. Intestinal absorptive defects associated with tinal tract infection produced by E. acervulina and
enteric infections in infants. Ann. N. Y. Acad. Sci. absorption of 6’Zn and ‘3tI-labeled oleic acid. J.
176: 284, 1971. Nutr. 93: 161, 1967.
11. LUGO-DE-RIVERA, C., H. RODRIGUEZ AND R. 28. SOLOMON, N. W., F. VITERI AND L. HAMILTON.
MALABSORPTION, DIARRHEA, AND INTESTINAL INFECTIONS 1253

Development of an interval sampling H2 breath 40. ABDALLA, A., N. GAD-EL-MAWLA, A. EL-ROOBY,


test for carbohydrate malabsorption in children. J. M. SHAKER AND N. GALIL. Studies on the malab-
Lab. Clin. Med. In press. sorption syndrome among Egyptians. I. Foecal fat
29. KING, M. J., AND R. A. JOSKE. Acute enteritis and o-xylose absorption tests in pellagra and ancy-
with temporary intestinal malabsorption. Brit. lostomiasis. J. Egypt. Med. Assoc. 46: 544, 1963.
Med. J. 1: 1324, 1960. 41. GAD-EL-MAWLA, N., A. ABDALLA AND N. GALIL.
30. BARKSDALE, W. L., AND C. F. ROUTH. Isospora Studies on the malabsorption syndrome among
hominis infections among American personnel in Egyptians. V. Foecal fat and D-xylOse absorption
the Southwest Pacific. Am. J. Trop. Med. Hyg. test in patients with ascariasis and taeniasis. J.
28: 639, 1948. Egypt. Med. Assoc. 49: 473, 1966.
31. FRENCH, J. M., J. L. WHITBY AND A. G. W. 42. ROSENBERG, I. H. Influence of intestinal bacteria
WHITFIELD. Steatorrhea in a man infected with on bile acid metabolism and fat absorption. Con-
coccidiosis (Isospora belli). Gastroenterology 47: tributions from studies of the blind-loop syn-
642, 1964. drome. Am. J. Clin. Nutr. 22: 284, 1968.
32. ZAMCHECK, N., L. C. HOSKINS, J. WINAWER, S. 43. SCHNEIDER, R. E., AND F. E. VITFRI. Luminal
A. BROITMAN AND L. S. GOrFLIEB. Histology and events of lipid absorption in protein-calorie mal-
ultrastructure of the parasite and the intestinal nourished children; relationship with nutritional
mucosa in human giardiasis; effects of atabrine recovery and diarrhea. II. Alterations in bile acid
therapy. Gastroenterology 44: 860, 1963. content of duodenal aspirates. Am. J. Clin. Nutr.

Downloaded from www.ajcn.org by guest on December 23, 2010


33. PALUMBO, P. J., H. H. SCUDMORE AND J. H. 27: 788, 1974.
THOMPSON, JR. Relationship of infestation with 44. ROSENBERG, I. H., W. G. HARDISON AND D. M.
Giardia lamblia to intestinal-malabsorption syn- BULL. Abnormal bile-salt patterns and intestinal
dromes. Proc. Mayo Clin. 37: 589, 1962. bacterial overgrowth associated with malabsorp-
34. TRIPATHY, K., E. DUQUE, 0. BOLANOS, H. Lo- tion. New Engl. J. Med. 276: 1391, 1967.
TERO AND L. G. MAYORAL. Malabsorption syn- 45. DONALDSON, R. M. Role of enteric microorga-
drome in ascariasis. Am. J. Clin. Nutr. 25: 1276, nisms in malabsorption. Federation Proc. 26:
1972. 1426, 1967.
35. SHEEHY, T. W., W. H. MERONEY, R. S. Cox, JR. 46. BOND, J. H., JR., AND M. D. LEVITr. Fate of
AND J. E. SOLER. Hookworm disease and malab- soluble carbohydrate in the colon of rats and man.
sorption. Gastroenterology 42: 148, 1962. J. Clin. Invest. 57: 1158, 1976.
36. DRAKE, S. J. Malnutrition in African adults. II. 47. HOFMANN, A. F. The syndrome of ileal disease
Effects of hookworm infestation on absorption of and the broken enterohepatic circulation: choler-
food stuffs. Brit. J. Nutr. 13: 278, 1959. heic enteropathy. Gastroenterology 52: 752,
37. MILNER, P. F., R. A. IRVINE, C. J. BARTON, G. 1967.
BRAS AND R. RICHARDS. Intestinal malabsorption 48. FIELD, M. Intestinal secretion: effect of cyclic
in Strongyloides stercoralis infestation. Gut 6: 574, AMP and its role in cholera. New EngI. J. Med.
1965. 284: 1137, 1971.
38. KOTCHER, E., M. MIRANDA, R. ESQUIVEL, A. 49. GRADY, G. F., AND G. T. KEUSCH. Pathogenesis
PENA-CHAVARRIA, D. L. DONOHUGH, C. BULDI- of bacterial diarrheas. New EngI. J. Med. 285:
ZON, A. ACOSTA AND J. L. APUY. Intestinal malab- 831, 891, 1971.
sorption and helminthic and protozoan infections 50. FROMM, H., AND A. F. HOFMANN. Breath test for
in the small intestine. Gastroenterology 50: 366, altered bile-acid metabolism. Lancet 2: 621, 1971.
1966. 51. S0L0M0NS, N., D. SCHOELLER, J. WAGONFELD, I.
39. LAYRISSE, M., N. BLUMENFELD, L. CARBONELL, Orr, I. ROSENBERG AND P. KLEIN. Validation of
J. DESENNE AND M. ROCHE. Intestinal absorption ‘3C-labeled vs ‘4C-labeled glycocholate (GC) in the
tests and biopsy of the jejunum in subjects with diagnosis of bacterial overgrowth by respiratory
heavy hookworm infection. Am. J. Trop. Med. CO2 isotopic measurements. J. Lab. Clin. Med. In
Hyg. 13: 297, 1964. press.