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Journal of Pediatric Gastroenterology & Nutrition:
Original Articles: Gastroenterology

Disaccharidase Activities in Dyspeptic Children: Biochemical and Molecular Investigations of Maltase-Glucoamylase Activity

Karnsakul, Wikrom*; Luginbuehl, Ursula†; Hahn, Dagmar†; Sterchi, Erwin†; Avery, Stephen‡; Sen, Partha‡; Swallow, Dallas§; Nichols, Buford‡

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*USDA Children's Nutrition Research Center, Baylor College of Medicine, and Texas Children's Hospital, Houston, Texas, U.S.A., and Siriraj Hospital, Mahidol University, Bangkok, Thailand; †University of Bern, Bern, Switzerland; ‡USDA Children's Nutrition Research Center, Baylor College of Medicine, and Texas Children's Hospital, Houston, Texas, U.S.A.; and §University of College London, London, United Kingdom

Received March 11, 2002; accepted May 23, 2002.

Supported by the National Institutes of Health, Bethesda, MD, and in part by federal funds from the US Department of Agriculture, Agricultural Research Service, under Cooperative Agreement number 58-6250-1-003 (B.N.), and by the Swiss National Foundation number 3200-052736.97 (E.S.).

Presented at the annual meeting of the Academic Pediatric Societies, Baltimore, MD, April 29–May 1, 2001.

The contents of this publication do not necessarily reflect the views or policies of the US Department of Agriculture, nor does mention of trade names, commercial products, or organizations imply endorsement by the US or Swiss governments.

Address correspondence and reprint requests to Dr. Buford L. Nichols, Department of Pediatrics, Baylor College of Medicine, 1100 Bates Street, Houston, TX 77030–2600 (e-mail:

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Background: Maltase-glucoamylase enzyme plays an important role in starch digestion. Glucoamylase deficiency is reported to cause chronic diarrhea in infants, but its role in dyspeptic children is unknown.

Methods: Glucoamylase and other disaccharidase specific activities were assayed from duodenal biopsy specimens in 44 children aged 0.5–18 years (mean, 10 ± 5 years) undergoing endoscopy to evaluate dyspeptic symptoms. All subjects had normal duodenal histology. Intestinal organ culture was used to evaluate synthesis and processing of maltase-glucoamylase. Sequencing of the maltase-glucoamylase coding region was performed in subjects with low activity or variation of isoform in organ culture.

Results: Twenty-two of the dyspeptic children had one or more disaccharidases with low specific activity. Twelve subjects (28%) had low activity of glucoamylase. Eight subjects had low activities of glucoamylase, sucrase, and lactase. Low glucoamylase activity was not correlated with the isoform phenotype of maltase-glucoamylase as described by metabolic labeling and sodium dodecyl sulfate electrophoresis. Novel nucleotide changes were not detected in one subject with low glucoamylase activity or in two subjects with variant isoforms of maltase-glucoamylase peptides.

Conclusion: Twelve of 44 dyspeptic children had low specific activity of duodenal maltase-glucoamylase. Eight of these children had low specific activity of all measured disaccharidases.

Although carbohydrate malabsorption is not rare in children, the symptoms vary and are dependent on diet and age. The symptoms of lactase deficiency are the best understood. Unabsorbed lactose attracts fluid and electrolytes into the small intestinal lumen because of the osmotic force of the undigested sugar. Intraluminal fluid accumulation augments peristalsis and decreases small intestinal transit time. In young infants with congenital lactase deficiency, watery diarrhea develops, which responds to a lactose-free diet (1,2). In adult-type lactase deficiency, lactose malabsorption contributes to dyspeptic symptoms, crampy abdominal pain, and diarrhea, which also respond to lactose restriction (3). The symptoms of congenital sucrase deficiency (CSID) are similar to those of lactase deficiency (4). The osmolar load from unhydrolzed sucrose is the same as that of lactose. Diarrhea is a common symptom of sucrase deficiency in young infants. Dyspeptic symptoms are more common in children and adults (5). The prevalence of CSID is 0.2% in individuals of European descent and greater than 20% in Alaskan Natives (5).

The symptoms of maltase-glucoamylase (MGA) deficiency are poorly defined. Glucoamylase deficiency may cause chronic diarrhea in young children (6). Although the osmolar force of starch is less than that of sucrose or lactose because of its larger molecular weight, starch-elimination diets relieved diarrhea in the reported infants (6). The frequency of glucoamylase deficiency is unknown; however, its frequency in infants with chronic diarrhea was similar to that those with sucrase deficiency (6). Based on the finding that older children with lactase or sucrase deficiency have mainly dyspeptic symptoms, we hypothesized that MGA deficiency might also cause dyspepsia.

Studies of patients with CSID have shown posttranslational defects in sucrase synthesis and processing (7). Sucrase precursors are synthesized and initially processed in the endoplasmic reticulum as a high-mannose glycoprotein. This immature isoform is transported to the Golgi apparatus, where the molecule is transformed into a complex glycoprotein. The complex glycosylated isoform is then transported to the external surface of the apical membrane as the active and mature sucrase (7). Immunoelectron microscopy and organ culture experiments in CSID have shown that the enzyme is confined to the Golgi cistern and not processed to the apical membrane. The isoform in the Golgi is the high-mannose type of glycoprotein (7). CSID thus appears to be a result both of defective synthesis and glycoprotein processing. Variations of synthesis and processing to the apical membrane have resulted in recognition of six CSID phenotypes (5,7–9). It is assumed that mutations of the SI coding region cause the different phenotypes. To date, three different SI mutations have been identified (10–13). Because MGA has such a strong similarity to SI at gene, peptide, and processing levels, we hypothesized that MGA deficiency might also have posttranslational defects and sequence mutations similar to those in SI (7–16).

The objectives of this study were to assess the frequency of low mucosal glucoamylase activity in children with dyspepsia and to search for cDNA mutations and defective processing of MGA. Because of the frequent occurrence of dyspeptic symptoms in lactase and sucrase deficiencies, these disaccharidases were assayed in all subjects. Secondary disaccharidase deficiencies were excluded by limiting the investigation to subjects with normal mucosal histology (17). The novel observations from this investigation are the high frequency of disaccharidase deficiencies in dyspeptic children, the common occurrence of glucoamylase deficiencies in this population, and the discovery of multiple disaccharidase deficiency in many of these patients.

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Subject Selection

During two time periods, October 1999 through February 2000, and May through October 2000, all patients undergoing upper intestinal endoscopy in the Texas Children's Hospital Gastrointestinal Procedure Suite for complaints of recurrent abdominal pain, vomiting, or gastroesophageal reflux were identified as candidates for the investigation. Eighty-five patients were contacted before endoscopy for permission to obtain three additional distal duodenal biopsy specimens during the procedure. The parents of 17 patients did not consent. Twenty-six subjects were excluded because of insufficiency of biopsy size or abnormal duodenal histology. Forty-four patients became the subjects of this study. The Baylor College of Medicine Institutional Review Board approved all studies.

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Duodenal Biopsy Specimens

After obtaining routine duodenal biopsy specimens for histology, three additional duodenal biopsy specimens were obtained. Two of the duodenal biopsy specimens were immediately stored in sterile tubes, snap-frozen in liquid nitrogen, and held at −70°C for measurement of disaccharidase activity and RNA extraction for cDNA sequencing. The third duodenal biopsy specimen was placed in media for organ culture studies. Morphology of duodenal tissue from each subject was examined after hematoxylin and eosin staining of fixed sections.

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Glucoamylase and Other Disaccharidase Enzyme Assays

Forty-four duodenal biopsy specimens were sent on dry ice in six batches to one of the authors in Bern, Switzerland (U.L.) for disaccharidase measurement. All arrived frozen. Disaccharidase activities were measured by modified Dahlqvist method (18). Tissue analyses were performed in six batches. A 0.15-mol/L KCl homogenate was used to assay the hydrolysis of 2% Polycose® (Ross Laboratories, Columbus, OH), sucrose, lactose, and maltose. Glucose production was measured by glucose oxidase. Protein was measured with a bicinchoninic acid protein assay kit (Pierce Co., Rockford, IL). Enzyme specific activity was expressed as units (U), defined as moles of glucose released per minute per gram of mucosal protein at 37°C. The lower limit of normal activity of the disaccharidase enzymes was defined by the mean minus one SD derived from these assays.

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Intestinal Organ Culture, Immunoprecipitation, and Sodium Dodecyl Sulfate–Polyacrylamide Gel Electrophoresis

Fresh duodenal biopsy specimens from 20 subjects were cultured by a modification of the method of Naim et al. (14). The tissues were oriented with villus surface upward on stainless steel grids in organ culture dishes and incubated in a lucite chamber containing an atmosphere of carbon dioxide and oxygen (5/95, vol/vol) for 2 hours. The tissues were then labeled with 100 μCi of [35S]methionine and replaced in the chamber for 8 hours of radiolabeling. The radiolabeled tissues were homogenized, normalized for protein concentration, and immunoprecipitated with anti-MGA antibodies conjugated to sepharose beads and separated on sodium dodecyl sulfate–polyacrylamide gel electrophoresis (14). Duplicate duodenal biopsy specimens from four subjects were studied to test reproducibility of the intestinal organ culture assay. To identify biochemical characteristics of the isoforms (unglycosylated, high mannose, and mature glycoproteins), endoglycosidase F/GF was used to digest one of the duplicate homogenates from three additional subjects (14).

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Reverse Transcription and Polymerase Chain Reaction

Forty-four intestinal tissues were studied by the method of Nichols et al. (15,16). The frozen biopsy specimens were divided by cutting on dry ice, and RNA was extracted and applied to RNeasy spin column (Qiagen, Germany). Reverse transcription and polymerase chain reaction was performed with a kit (Stratagene, La Jolla, CA) (15,16). Polymerase chain reaction products were separated on a gel, and the amplicons were recovered using QIAquick Gel Extraction Kit (Qiagen, Chatsworth, CA). Reamplification of cDNA was performed by the same method. The final DNA products were submitted to Child Health Research Center, Department of Pediatrics, Baylor College of Medicine, for direct DNA sequencing (15).

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Data Analysis

The software from Genetics Computer Group, Inc., was accessed via the Baylor College of Medicine Molecular Biology Computation Resource (15). Sequence analysis was performed with the Genetics Computer Group programs to search for mutations or polymorphisms in our subjects (15).

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Clinical Characteristics

The Pediatric Endoscopy Database System–Clinical Outreach Research Initiative System of computer records was used to collect demographic, clinical indications for endoscopic procedures, and endoscopic findings. From October 1999 through February 2000, and from May 2000 to October 2000, 767 children underwent upper endoscopy. The most common chief complaints were abdominal pain (n = 226; 29%), reflux (n = 107; 14%), and vomiting (n = 79; 10%). Only 18 (2.3%) complained of diarrhea. For our investigation, 44 subjects were recruited from among 226 children with abdominal pain, reflux, or vomiting. Thirty-three of the study sample complained of abdominal pain, 11 of vomiting, 3 of reflux symptoms, 5 of diarrhea, and 3 of delayed gastric emptying. There were children with multiple overlapping symptoms in both the endoscopy population and study subjects. The age in the study sample ranged from 6 months to 18 years, with a mean of 10 ± 5 years. There was no gender difference, and ethnicity was predominantly white (84% white; 2% Hispanic; 5% black; and 11% others).

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Enzyme Activities

The disaccharidase specific activities in our subjects were not normally distributed. Therefore, the activities were logarithmically transformed and means ± SD were calculated from units per gram of protein. The lower limit of normal activity was defined as antilog of mean minus one SD. Our lower limit of normal values for glucoamylase, sucrase, lactase, and maltase were 33, 25, 11, and 104 U/g protein, respectively, and are comparable with those from several national laboratories (personal communications, University of Maryland School of Medicine, Division of Pediatric Gastroenterology and Nutrition; and Children's Hospital of Buffalo Gastrointestinal Laboratory). Our assays were performed on histologically normal duodenal tissues, whereas normal values from the national laboratories include histologically abnormal tissues.

We found that half of the subjects had activities of one or more disaccharidases below the lower limits of normal activity. Assays detected 12 subjects (28%) with low glucoamylase, 15 (34%) with low sucrase, and 14 (32%) with low lactase. Most had more than one low disaccharidase activity. Two subjects had isolated low glucoamylase; two had combined low glucoamylase and sucrase; eight had low glucoamylase, sucrase, and lactase; four had isolated low sucrase; four had isolated low lactase; and one had low sucrase and lactase. The enzyme activities of 12 subjects with low glucoamylase activities are shown in Table 1. Five of the children with low lactase (three with isolated low lactase and two with additional low MGA) had very high SI/L ratios. These children ranged in age from 4 to 17 years and were thus likely demonstrating the normal down-regulation of lactase as a result of nonpersistent or adult-type hypolactasia (3). Four of these five were from ancestries in which lactase nonpersistence is the prevalent phenotype (1 Hispanic, 2 Asian, and 1 black). When analyzed for relations between dyspeptic symptoms and disaccharidases activities by t test, we found that emesis was related to low lactase activity (P ≤ 0.038), but no other relation between symptoms and low disaccharidases was detected.

Table 1
Table 1
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Maltase-glucoamylase Isoforms

Figure 1 shows typical autoradiograms of immunoprecipitated MGA glycoproteins labeled in organ culture experiments of human intestine with [35S]methionine. These MGA isoforms are similar to those previously reported by Naim et al. (14). Type 1 phenotype was classified according to the Naim glycosylation pattern with unglycosylated, high mannose, and mature isoforms (14). This phenotype was found in 13 of 20 intestinal organ cultures. A novel finding of additional bands, named the type 2 phenotype, was discovered in seven subjects (Fig. 1). The type 2 phenotype may represent a variation of MGA dimerization resulting from altered processing of the pro-MGA enzyme, but could also represent increased turnover with degradative fragments. The isoform phenotypes were reproducible between duplicate biopsy specimens. Endoglycosidase F/GF was used to identify N-linked glycans from high-mannose glycoproteins (14). Mature glycoproteins are resistant to this enzyme activity. Our experiments demonstrated digestion of high-mannose chains of the glycoproteins, which confirms the identification of each form of glycoproteins. Surprisingly, there was no relation between isoform phenotypes and glucoamylase activity (P ≥ 0.4).

Fig. 1
Fig. 1
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Maltase-glucoamylase Coding Sequences

Controls with normal glucoamylase or maltase activities may have single nucleotide polymorphisms (SNP) in the MGA coding region (16). In an Asian subject (subject no. 2, Table 1) with isolated low activity of glucoamylase (25 EU) and borderline sucrase (22 EU), a novel MGA SNP at A2393G was detected by sequencing that codes a tyrosine to cysteine change in a beta-sheet in exon 20 following the barrel structure with the N-terminal catalytic site. This heterozygous SNP was confirmed by digestion with Eco 57I restriction enzyme. The same heterozygous A2393G SNP polymorphism was identified by sequence and confirmed by Eco 57I digestion in two white control subjects with normal glucoamylase activities (Fig. 2). No other mutations were detected in the intestinal MGA cDNA of this subject, suggesting that low glucoamylase activity was not a reflection of a cDNA mutation.

Fig. 2
Fig. 2
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The subjects with normal glucoamylase activities had differing glycoprotein isoforms phenotypes (I and II). These two subjects had the previously described MGA SNP when sequenced and the novel A2393G, but did not have additional polymorphisms or mutations in cDNA (16).

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Is glucoamylase deficiency clinically significant?

Lebenthal et al. (6) reported that 9 of 511 infants with chronic diarrhea had primary glucoamylase deficiency and normal intestinal histology. Seven were challenged with 2 g/kg of glucose polymers and rice starch oral loads, and three developed diarrhea. The diarrhea was relieved after elimination of starch from the diet and relapsed after 4 g/kg starch was fed. These infants were younger than the subjects in our study.

We found 12 dyspeptic subjects (mean age, 8 years) with low activity of glucoamylase. All had episodic or persistent symptoms localized to the epigastrium or upper abdomen associated with pain, discomfort, bloating, early satiety, nausea, or vomiting. None had chronic diarrhea (19,20). Many older dyspeptic children and adults with sucrase or lactase deficiencies do not experience chronic diarrhea (5,21,22). Colonic fermentation plays a compensatory role in salvage of calories in adults with pharmacologic starch malabsorption (23). Although diarrhea can result from the osmotic effect of proximally unabsorbed carbohydrates (24), the effect of glucoamylase deficiency may not be clinically observed because of the lower osmotic load of proximally malabsorbed starch oligomers.

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How Common Is Low Glucoamylase Activity in Dyspeptic Children?

We found 12 individuals (28%) with low activity of glucoamylase from a sample of 44 dyspeptic patients. This incidence cannot be extrapolated to the general population; however, deficiency of low glucoamylase and other disaccharidases in half of this study population correlated with dyspeptic symptoms.

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Do Defects of Maltase-glucoamylase Processing Parallel Those Reported in SI Deficiencies?

Our hypothesis was that, because of molecular similarities to SI, the defects reported in SI processing might also be found in subjects with low glucoamylase activity and that the abnormal activity might be secondary to mutations of MGA cDNA. Approximately half of our subjects with low glucoamylase activity had small intestinal organ cultures. These revealed the high-mannose immature and complex glycosylated mature isoforms that have been described as stages in normal MGA proenzyme synthesis and processing (14). Although two peptide-distinct phenotypes were identified, there was no difference in glucoamylase activities between subjects with the different isoform patterns. Conversely, there was no detectable decrease in total protein labeling or autoradiodensity of the isoforms on the blots of subjects with low glucoamylase activities. In addition, there were no mutations in MGA cDNA associated with selective glucoamylase deficiency or altered MGA isoforms on organ culture. The failure to find defective MGA processing and cDNA mutations in subjects with glucoamylase deficiency is inconsistent with our hypothesis that deficiencies of glucoamylase and congenital sucrase-isomaltase deficiency would share the same pathogenetic mechanism (7–13,16).

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Have Multiple Disaccharidase Deficiencies Been Reported?

Although rare, deficiency of multiple disaccharidases has been described. Eggermont and Hers (25) noted that the glucoamylase activity of eight sucrose-intolerant patients was 35% of the normal level. Skovbjerg and Krasilnikoff (26) demonstrated a subset of sucrase-isomaltase–deficient patients with MGA deficiency. Savilahti et al. (2) reported a sucrase-deficient patient with congenital lactase deficiency. Lebenthal et al. (6) reported two of nine infants with primary glucoamylase deficiency with either sucrase or lactase deficiencies. Two clinical phenotypes have been described in sucrose intolerance, one of these also has starch intolerance (5,27). A 2.5-month-old infant with history of chronic diarrhea and failure to thrive was found to have normal small intestinal histology with decreased activity of sucrase, lactase, maltase, and glucoamylase. The diagnosis of multiple deficiencies of sucrase, lactase, maltase, and glucoamylase, or multiple disaccharidase deficiency, was made (16). This infant had normal pro-MGA enzyme synthesis and no mutations in MGA coding region. This appears to be similar to the eight older dyspeptic children in our study with combined low activities of glucoamylase, sucrase, and lactase.

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How Can the Multiple Disaccharidase Deficiencies Be Explained?

The genes of glucoamylase, sucrase, and lactase are located on chromosome 7, 3, and 2, respectively. It is unlikely that mutations on different chromosomes would occur simultaneously in the coding regions of all three genes. To date, no coding mutations have been found in reported cases of glucoamylase or lactase deficiency (1,16). Pleiotropic regulation of the three genes could be responsible for the multiple low disaccharidase concentrations (16). Shared regulation of turnover of the messages or enterocyte synthesis and processing of these peptides is also plausible.

In summary, 28% of a population of dyspeptic children had low glucoamylase activities. Of these children, all had low activity of one or more additional disaccharidases. A multiple disaccharidase deficiency involving glucoamylase, sucrase, and lactase activities was found in 18% of our dyspeptic children, and half of all the dyspeptic children had low activity of one or more disaccharidases. Biochemical and molecular investigations of biopsy specimens from children with low glucoamylase activities found no alterations in coding sequence of MGA or of posttranslational processing to account for the enzyme deficiency.

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The authors thank the Pediatric Gastroenterologists of the Section of Gastroenterology and Nutrition, Department of Pediatrics, Baylor College of Medicine and Pediatric Digestive Disease Group at Texas Children's Hospital, for providing access to the study subjects and the research biopsy results; Dr. William J. Klish for his leadership of the Section of Gastroenterology and Nutrition and for making the Gastroenterology and Nutrition Fellowship to WK possible; and the contribution of Polycose from Ross Laboratories, Columbus, OH. The new MGA coding region SNP has been registered with GenBank.

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1. Enattah NS, Sahi T, Savilahti E, et al. Identification of a variant associated with adult type hypolactasia. Nat Genet 2002; 30:233–7.

2. Savilahti E, Launiala K, Kuitunen P. Congenital lactase deficiency. Arch Dis Childhood 1983; 58:246–52.

3. Wang, YX, Harvey, CB, Hollux EJ, et al. The genetically programmed downregulation of lactase in children. Gastroenterology 1998; 114:1230–6.

4. Gundmand-Hφyer E, Krasilnikoff PA, Skovbjerg H. Sucrose-isomaltose malabsorption. Adv Nutr Res 1984; 6:233–69.

5. Treem WR. Congenital sucrase-isomaltase deficiency. J Pediatr Gastroenterol Nutr 1995; 21:1–14.

6. Lebenthal E, Khin-Muang-U, Zheng B, et al. Small intestinal glucoamylase deficiency and starch malabsorption: A newly recognized alpha-glucosidase deficiency in children. J Pediatr 1994; 124:541–6.

7. Naim, HY, Roth, J, Sterchi, E, et al. Sucrase-isomaltase deficiency in humans: Different mutations disrupt intracellular transport, processing, and function of an intestinal brush border enzyme. J Clin Invest 1988; 82:667–79.

8. Hauri HP, Roth J, Sterchi EE, et al. Transport to cell surface of intestinal sucrase-isomaltase is blocked in the Golgi apparatus in a patient with congenital sucrase-isomaltase deficiency. Proc Natl Acad Sci U S A 1985; 82:4423–7.

9. Lloyd ML, Olsen WA. A study of the molecular pathology of sucrase-isomaltase deficiency: A defect in the intracellular processing of the enzyme. N Eng J Med 1987; 316:438–42.

10. Ouwendijk J, Moolenaar CEC, Peters WJ, et al. Congenital sucrase-isomaltase deficiency: Identification of a glutamine to proline substitution that leads to a transport block of sucrase-isomaltase in a pre-Golgi compartment. J Clin Invest 1996; 97:633–41.

11. Jacob, R, Zimmer JR, Schmitz J, et al. Congenital sucrase-isomaltase deficiency arising from cleavage and secretion of a mutant form of the enzyme. J Clin Invest 2000; 106:281–7.

12. Spodsberg, N, Jacob, R, Alfalah, M, et al. Molecular basis of aberrant protein transport in an intestinal enzyme disorder. J Biol Chem 2001; 276:23506–10.

13. Moolenaar CEC, Ouwendijk J, Wittpoth M, et al. A mutation in a highly conserved region in brush-border sucrase-isomaltase and lysosomal alpha-glucosidase results in Golgi retention. J Cell Sci 1997; 110:557–67.

14. Naim HY, Sterchi EE, Lentze MJ. Structure, biosynthesis, and glycosylation of human small intestinal maltase-glucoamylase. J Biol Chem 1988; 263:19709–17.

15. Nichols B, Eldering J, Avery S, Hahn D, Quaroni A, Sterchi E. Human small intestinal maltase-glucoamylase cDNA cloning. J Biol Chem 1988; 273:3076–81.

16. Nichols B, Avery SE, Karnsakul W, et al. Congenital maltase-glucoamylase deficiency associated with lactase and sucrase deficiencies: Pleiotropic gene regulation? J Pediatr Gastroenterol Nutr 2002 (in press).

17. Lebenthal E, Lee PC. Glucoamylase and disaccharidase activities in normal subjects and in patients with mucosal injury of the small intestine. J Pediatr 1980; 97:389–93.

18. Dahlqvist A. Method for assay of intestinal disaccharidases. Analy Biochem 1964; 7:18–25.

19. Hyams JS, Davis P, Sylvester FA, et al. Dyspepsia in children and adolescents: A prospective study. J Pediatr Gastroenterol Nutr 2000; 30:413–8.

20. Thompson WG, Longstreth G, Drossman DA, et al. C. Functional bowel disorders and D. functional abdominal pain. In: Drossman DA, Corazziari E, Talley NJ, Thompson WG, Whitehead WE, eds. Rome II. The functional gastrointestinal disorders. Diagnosis, pathophysiology and treatment: A multinational consensus. McLean, VA: Degnon Associates, 2000:351–432.

21. Cooper BT, Scott, Hopkins J. Adult onset sucrase-isomaltase deficiency with secondary disaccharidase deficiency resulting from severe dietary carbohydrate restriction. Dig Dis Sci 1983; 28:473–7.

22. Ringrose RE, Preiser H, Welsh JD. Sucrase-isomaltase (palatinase) deficiency diagnosed during adulthood. Dig Dis Sci 1980; 25:384–7

23. Mortensen PB, Clausen MR. Short-chain fatty acids in the human colon: relation to gastrointestinal health and disease. Scand J Gastroenter Suppl 1996; 216:132–48.

24. Mainguet P, Vanderhoeden R, Loeb H, Eggermont E. Congenital maltase-sucrase and maltase-isomaltase deficiency in an adult. Digestion 1973; 8:353–9.

25. Eggermont E, Hers HG. The sedimentation properties of the intestinal α-glucosidases of normal human subjects and of patients with sucrose intolerance. Eur J Biochem 1969; 9:488–96.

26. Skovbjerg H, Krasilnikoff PA. Maltase-glucoamylase and residual isomaltase in sucrose intolerant patients. J Pediatr Gastroenterol Nutr 1986; 5:365–71.

27. Treem WR. Clinical heterogeneity in congenital sucrase-isomaltase deficiency. J Pediatr 1996; 128:727–9.

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Maltase-glucoamylase; Sucrase-isomaltase; Lactase-phlorizin hydrolase; Multiple disaccharidase deficiency

© 2002 Lippincott Williams & Wilkins, Inc.


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