Clinical implications of lactose malabsorption versus lactose intolerance

Journal of Clinical Gastroenterology

Volumn 47, Issue 6, 2013, Pages 471-480

  Levitt, Michael ^a   Wilt, Timothy ^a   Shaukat, Aasma ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Diarrhea; Hypolactasia; Lactase deficiency; Lactose intolerance; Lactose malabsorption

Indexed keywords

BETA GALACTOSIDASE; EXCIPIENT; GLUCOSE; LACTASE; LACTOSE; PROBIOTIC AGENT; RIFAXIMIN; YOGHURT;

ABSORPTION; ADAPTATION; AFRICAN AMERICAN; AMERICAN INDIAN; ASIAN; BUTTER; CELIAC DISEASE; CHEESE; CHROMOSOME 2; CLINICAL FEATURE; CONTROLLED CLINICAL TRIAL (TOPIC); ENTERITIS; ENZYME ACTIVITY; FERMENTATION; FOOD INTAKE; GLUCOSE BLOOD LEVEL; HISPANIC; HUMAN; ICE CREAM; INTESTINE BIOPSY; INTESTINE INFECTION; LACTASE DEFICIENCY; LACTOSE INTOLERANCE; LACTOSE TOLERANCE; MALABSORPTION; MEAL; MILK; NOMENCLATURE; NUTRIENT; PATHOPHYSIOLOGY; PHYSICIAN; PRIORITY JOURNAL; PROMOTER REGION; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM; SMALL INTESTINE MUCOSA; SPIROMETRY; STOMACH EMPTYING; SURVIVAL; TABLET;

HUMANS; LACTASE; LACTOSE; LACTOSE INTOLERANCE;

EID: 84879883386     PISSN: 01920790     EISSN: 15392031     Source Type: Journal    
DOI: 10.1097/MCG.0b013e3182889f0f     Document Type: Review

References (73)

1. Pilson ME, Kelly AL. Composition of the milk from Zalophus californianus, the California sea lion. Science. 1962;135: 104-105.
2. Wojcik KY, Rechtman DJ, Lee ML, et al. Macronutrient analysis of a nationwide sample of donor breast milk. J Am Diet Assoc. 2009;109: 137-140.
3. Eadala P, Waud JP, Matthews SB, et al. Quantifying the "hidden" lactose in drugs used for the treatment of gastrointestinal conditions. Aliment Pharmacol Ther. 2009;29: 677-687.
4. Sunshine P, Kretchmer N. Intestinal disaccharidases: absence in two species of sea lions. Science. 1964;144: 850-851.
5. Welsh JD, Poley JR, Bhatia M, et al. Intestinal disaccharidase activities in relation to age, race, and mucosal damage. Gastroenterology. 1978;75: 847-855.
6. Swallow DM, Hollox EJ. The genetic polymorphism of intestinal lactase activity in adult humans. In: Scriver CR, Beaudet AL, Sly WS, et al, eds. The Metabolic and Molecular Basis of Inherited Disease. 8th ed. New York, NY: McGraw- Hill; 2000: 1664-1665.
7. Shatin R. Evolution and lactase deficiency. Gastroenterology. 1968;54: 992-993.
8. Swallow DM. Genetics of lactase persistence and lactose intolerance. Annu Rev Genet. 2003;37: 197-219.
9. Wang Y, Harvey CB, Pratt WS, et al. The lactase persistence/ non-persistence polymorphism is controlled by a cis-acting element. Hum Mol Genet. 1995;4: 657-662.
10. Enattah NS, Jensen TG, Nielsen M, et al. Independent introduction of two lactase-persistence alleles into human populations reflects different history of adaptation to milk culture. Am J Hum Genet. 2008;82: 57-72.
11. Simoons FJ. Primary adult lactose intolerance and the milking habit: a problem in biologic and cultural interrelations. II. A culture historical hypothesis. Am J Dig Dis. 1970;15: 695-710.
12. Hertzler SR, Savaiano DA. Colonic adaptation to daily lactose feeding in lactose maldigesters reduces lactose intolerance. Am J Clin Nutr. 1996;64: 232-236.
13. Bond JH, Levitt MD. Quantitative measurement of lactose absorption. Gastroenterology. 1976;70: 1058-1062.
14. Levitt MD. Production and excretion of hydrogen gas in man. N Engl J Med. 1969;281: 122-127.
15. Pimentel M, Kong Y, Park S. Breath testing to evaluate lactose intolerance in irritable bowel syndrome correlates with lactulose testing and may not reflect true lactose malabsorption. Am J Gastroenterol. 2003;98: 2700-2704.
16. Nucera G, Gabrielli M, Lupascu A, et al. Abnormal breath tests to lactose, fructose and sorbitol in irritable bowel syndrome may be explained by small intestinal bacterial overgrowth. Aliment Pharmacol Ther. 2005;21: 1391-1395.
17. Caride VJ, Prokop EK, Troncale FJ, et al. Scintigraphic determination of small intestinal transit time: comparison with the hydrogen breath technique. Gastroenterology. 1984;86: 714-720.
18. Posserud I, Stotzer PO, Bjornsson ES, et al. Small intestinal bacterial overgrowth in patients with irritable bowel syndrome. Gut. 2007;56: 802-808.
19. Corazza GR, Menozzi MG, Strocchi A, et al. The diagnosis of small bowel bacterial overgrowth. Reliability of jejunal culture and inadequacy of breath hydrogen testing. Gastroenterology. 1990;98: 302-309.
20. Cloarec D, Bornet F, Gouilloud S, et al. Breath hydrogen response to lactulose in healthy subjects: relationship to methane producing status. Gut. 1990;31: 300-304.
21. Newcomer AD, McGill DB, Thomas PJ, et al. Prospective comparison of indirect methods for detecting lactase deficiency. N Engl J Med. 1975;293: 1232-1236.
22. Hammer HF, Santa Ana CA, Schiller LR, et al. Studies of osmotic diarrhea induced in normal subjects by ingestion of polyethylene glycol and lactulose. J Clin Invest. 1989;84: 1056-1062.
23. Wolin MJ. Fermentation in the rumen and human large intestine. Science. 1981;213: 1463-1468.
24. Tomlin J, Lowis C, Read NW. Investigation of normal flatus production in healthy volunteers. Gut. 1991;32: 665-669.
25. Strocchi A, Levitt MD. Factors affecting hydrogen production and consumption by human fecal flora. The critical roles of hydrogen tension and methanogenesis. J Clin Invest. 1992;89: 1304-1311.
26. Christl SU, Murgatroyd PR, Gibson GR, et al. Production, metabolism, and excretion of hydrogen in the large intestine. Gastroenterology. 1992;102: 1269-1277.
27. Bond JH Jr, Levitt MD, Prentiss R. Investigation of small bowel transit time in man utilizing pulmonary hydrogen (H2) measurements. J Lab Clin Med. 1975;85: 546-555.
28. Leichter J. Comparison of whole milk and skim milk with aqueous lactose solution in lactose tolerance testing. Am J Clin Nutr. 1973;26: 393-396.
29. Jones DV, Latham MC, Kosikowski FV, et al. Symptom response to lactose-reduced milk in lactose-intolerant adults. Am J Clin Nutr. 1976;29: 633-638.
30. Cheng AH, Brunser O, Espinoza J, et al. Long-term acceptance of low-lactose milk. Am J Clin Nutr. 1979;32: 1989-1993.
31. Rorick MH, Scrimshaw NS. Comparative tolerance of elderly from differing ethnic backgrounds to lactose-containing and lactose-free dairy drinks: a double-blind study. J Gerontol. 1979;34: 191-196.
32. Newcomer AD, McGill DB, Thomas PJ. Tolerance to lactose among lactase-deficient American Indians. Gastroenterology. 1978;74: 44-46.
33. Suarez FL, Savaiano DA, Levitt MD. A comparison of symptoms after the consumption of milk or lactose-hydrolyzed milk by people with self-reported severe lactose intolerance. N Engl J Med. 1995;333: 1-4.
34. Vesa TH, Marteau P, Zidi S, et al. Digestion and tolerance of lactose from yoghurt and different semi-solid fermented dairy products containing Lactobacillus acidophilus and bifidobacteria in lactose maldigesters - is bacterial lactase important? Eur J Clin Nutr. 1996;50: 730-733.
35. Suarez FL, Savaiano D, Arbisi P, et al. Tolerance to the daily ingestion of two cups of milk by individuals claiming lactose intolerance. Am J Clin Nutr. 1997;65: 1502-1506.
36. Suarez FL, Adshead J, Furne JK, et al. Lactose maldigestion is not an impediment to the intake of 1500mg calcium daily as dairy products. Am J Clin Nutr. 1998;68: 1118-1122.
37. Stephenson LS, Latham MC. Lactose intolerance and milk consumption: the relation of tolerance to symptoms. Am J Clin Nutr. 1974;27: 296-303.
38. Kwon PH Jr, Rorick MH, Scrimshaw NS. Comparative tolerance of adolescents of differing ethnic backgrounds to lactose-containing and lactose-free drinks. II. Improvement of a double-blind test. Am J Clin Nutr. 1980;33: 22-26.
39. Reasoner J, Maculan TP, Rand AG, et al. Clinical studies with low-lactose milk. Am J Clin Nutr. 1981;34: 54-60.
40. Rask Pedersen E, Jensen BH, Jensen HJ, et al. Lactose malabsorption and tolerance of lactose-hydrolyzed milk. A double-blind controlled crossover study. Scand J Gastroenterol. 1982;17: 861-864.
41. Lybeck Sørensen K, Vergara Meersohn M, Sonne J, et al. A new type of low-lactose milk. Tolerance by lactose malabsorbers and evaluation of protein nutritional value. Scand J Gastroenterol. 1983;18: 1063-1068.
42. Rosado JL, Solomons NW, Lisker R, et al. Enzyme replacement therapy for primary adult lactase deficiency. Effective reduction of lactose malabsorption and milk intolerance by direct addition of beta-galactosidase to milk at mealtime. Gastroenterology. 1984;87: 1072-1082.
43. Cavalli-Sforza LT, Strata A. Double-blind study on the tolerance of four types of milk in lactose malabsorbers and absorbers. Hum Nutr Clin Nutr. 1987;41: 19-30.
44. Brand JC, Holt S. Relative effectiveness of milks with reduced amounts of lactose in alleviating milk intolerance. Am J Clin Nutr. 1991;54: 148-151.
45. Johnson AO, Semenya JG, Buchowski MS, et al. Correlation of lactose maldigestion, lactose intolerance, and milk intolerance. Am J Clin Nutr. 1993;57: 399-401.
46. Hertzler SR, Huynh BC, Savaiano DA. How much lactose is low lactose? J Am Diet Assoc. 1996;96: 243-246.
47. Montalto M, Nucera G, Santoro L, et al. Effect of exogenous beta-galactosidase in patients with lactose malabsorption and intolerance: a crossover double-blind placebo-controlled study. Eur J Clin Nutr. 2005;59: 489-493.
48. Casellas F, Aparici A, Casaus M, et al. Subjective perception of lactose intolerance does not always indicate lactose malabsorption. Clin Gastroenterol Hepatol. 2010;8: 581-586.
49. Spiller RC. Problems and challenges in the design of irritable bowel syndrome clinical trials: from published trials. Am J Med. 1999;107:91S-97S.
50. Wilt TJ, Shaukat A, Shamliyan T, et al. Lactose Intolerance and Health. No. 192 (Prepared by the Minnesota Evidencebased Practice Center Under Contract No. HHSA 290-2007- 10064-I.) AHRQ Publication No. 10-E004. Rockville, MD: Agency for Healthcare Research and Quality; 2010.
51. Shaukat A, Levitt MD, Taylor BC, et al. Systematic review: effective management strategies for lactose intolerance. Ann Intern Med. 2010;152: 797-803.
52. Savaiano DA, Boushey CJ, McCabe GP. Lactose intolerance symptoms assessed by meta-analysis: a grain of truth that leads to exaggeration. J Nutr. 2006;136: 1107-1113.
53. Gould B. Dairy markets data and graphs. Available at: http:// future.aae.wisc.edu/tab/sales.html#23. Accessed June 26, 2012.
54. Farup PG, Monsbakken KW, Vandvik PO. Lactose malabsorption in a population with irritable bowel syndrome: prevalence and symptoms. A case-control study. Scand J Gastroenterol. 2004;39: 645-649.
55. Vernia P, Marinaro V, Argnani F, et al. Self-reported milk intolerance in irritable bowel syndrome: what should we believe? Clin Nutr. 2004;23: 996-1000.
56. Ferguson A, Macdonald DM, Brydon WG. Prevalence of lactase deficiency in British adults. Gut. 1984;25: 163-167.
57. Gupta D, Ghoshal UC, Mizri A, et al. Lactose intolerance in patients with irritable bowel syndrome from northern India: a case-control study. J Gastroenterol Hepatol. 2007;22: 2261-2265.
58. Eastwood MA, Walton BA, Brydon WG, et al. Fecal weight, constituents, colonic motility, and lactose tolerance in the irritable bowel syndrome. Digestion. 1984;30: 7-12.
59. Newcomer AD, McGill DB. Irritable bowel syndrome. Role of lactase deficiency. Mayo Clin Proc. 1983;58: 339-341.
60. Lisker R, Solomons NW, Briceno RP, et al. Lactase and placebo in the management of the irritable bowel syndrome: a double-blind, cross-over study. Am J Gastroenterol. 1989;84: 756-762.
61. Parker TJ, Woolner JT, Prevost AT, et al. Irritable bowel syndrome: is the search for lactose intolerance justified? Eur J Gastroenterol Hepatol. 2001;13: 219-225.
62. Tolliver BA, Jackson MS, Jackson KL, et al. Does lactose maldigestion really play a role in the irritable bowel? J Clin Gastroenterol. 1996;23: 15-17.
63. Bohmer CJM, Tuynman HARE. The clinical relevance of lactose malabsorption in irritable bowel syndrome. Eur J Gastroenterol Hepatol. 1996;8: 1013-1016.
64. Gremse DA, Greer AS, Vacik J, et al. Abdominal pain associated with lactose ingestion in children with lactose intolerance. Clin Pediatr (Phila). 2003;42: 341-345.
65. Järvinen RM, Loukaskorpi M, Uusitupa MI. Tolerance of symptomatic lactose malabsorbers to lactose in milk chocolate. Eur J Clin Nutr. 2003;57: 701-705.
66. Unger M, Scrimshaw NS. Comparative tolerance of adolescents of differing ethnic backgrounds to lactose-containing and lactose-free dairy drinks. Initial experience with a double-blind procedure. Nutr Res. 1981;1: 227-233.
67. Vesa TH, Lember M, Korpela R. Milk fat does not affect the symptoms of lactose intolerance. Eur J Clin Nutr. 1997;51: 633-636.
68. Nielsen OH, Schiotz PO, Rasmussen SN, et al. Calcium absorption and acceptance of low-lactose milk among children with primary lactase deficiency. J Pediatr Gastroenterol Nutr. 1984;3: 219-223.
69. Lin MY, Dipalma JA, Martini MC, et al. Comparative effects of exogenous lactase (beta-galactosidase) preparations on in vivo lactose digestion. Dig Dis Sci. 1993;38: 2022-2027.
70. Xenos K, Kyroudis S, Anagnostidis A, et al. Treatment of lactose intolerance with exogenous beta-D-galactosidase in pellet form. Eur J Drug Metab Pharmacokinet. 1998;23: 350-355.
71. Newcomer AD, Park HS, O'Brien PC, et al. Response of patients with irritable bowel syndrome and lactase deficiency using unfermented acidophilus milk. Am J Clin Nutr. 1983;38: 257-263.
72. Briet F, Pochart P, Marteau P, et al. Improved clinical tolerance to chronic lactose ingestion in subjects with lactose intolerance: a placebo effect? Gut. 1997;41: 632-635.
73. Cappello G, Marzio L. Rifaximin in patients with lactose intolerance. Dig Liver Dis. 2005;37: 316-319.