September 1992, Volume 42, Issue 9

Review Articles

YOGHURT (DM1!): A PROBIOTIC AND THERAPEUTIC VIEW

Zaigham Abbas  ( Department of Medicine, The Aga Khan University Hospital, Stadium Road, Karachi. )
Wasim Jafri  ( Department of Medicine, The Aga Khan University Hospital, Stadium Road, Karachi. )

Yoghurt is one of the staple dairy products of Indo-Pakistan subcontinent. This is the name given to the traditional yoghurt which is prepared and sold commer­cially in the earthenware pans. The simmering milk is cooled down in these pans and is inoculated with the starter substance from the previous day’s dahi. Lassi, prepared from dahi is a popular beverage. Yoghurt is taken with meals as bland or with added salt or sugar and with salads. It is also recommended as a source of nutrition and household remedy for ill health, pOor appetite and digestive disturbances. Dahi oryoghurt is produced by the fermentation of milk. The bacteria involved are the lactobacillus bul­garicus and streptococcus thermophilous. In a study by Naeem and Rizvi1, organisms cultured from dahi were streptococcus lactic, streptococcus thermophilous, lac­tobacillus acidophilus, lactobacillus casei, lactobacillus bulgaricus and leuconostoc citrovorum. The pH varied between 3.4 to 6.0. Many claims have been made concerning prophylactic and therapeutic effects of yoghurt. Yoghurt is rich in nutrients and probiotics. Probiotics are live microbial feed supplements which beneficially affect the host animal by improving microbial balance2. Our intes­tinal microflora provide protection against various dis­eases. Yoghurt starter bacteria, lactobacillus bulgaricus and streptococcus thermophilous are the part of probiotic preparations currently on the market. They may be operating by production of antimicrobial substances, competition for adhesion to receptors and stimulation of immunity3. Although there are many claims of yoghurt and its probiotic effects, the amelioration of symptoms of lactose intolerance has been worked in details.
Lactose intolerance
Kolars et al4 showed that lactose was better ab­sorbed in lactase deficient subjects after ingestion of yoghurt than after consumption of milk or powdered lactose in water despite nearly equal lactose loads. Ingestion of 18 grams of lactose in yoghurt resulted only about one third as much hydrogen excretion in breath as a similar load of lactose in milk or water. This enhanced absorption is believed to be due to B galactosidase (B gal) activity of its endogenous bacteria. Lactobacillus bul­garicus and streptococcus thermophilous produce higher amount of lactase or B gal than other microor­ganisms with lactase potentials5,6 . 40-50% of the lactose is hydrolyzed during fermentation5, the residual level of lactose and high lactase activity make yoghurt very suitable product for lactase deficient persons who can absorb roughly 50% of a lactose load; a finding supported by direct measurement of lactose absorption through aspiration of the terminal ileum7. The buffering capacity of yoghurt protects the bacteria and their enzymes from gastric degradation by slowing the decrease of gastric pH8. It has been shown that three times more acid is required to acidify yoghurt than to acidify milk8. Yoghurt B gal was stable at pH 4.0 but inactivated at lower pH. However, this buffering capacity also prevents microbial B gal from hydrolysing lactose in the duodenum9. Moreover, as pH is still low in duodenum, so B gal is not active and process of hydrolysis and absorption occurs lower down in the small intestine where the pH is progressively increased. Intracellular location of the enzyme and integrity of the bacterial cell membrane is an additional protective factor from acidic pH8. When yoghurt was sonicated to disrupt microbial cell structure, only 20% of the activity remained after incubation at pFI 4.0 for 60 minutes. Acidified milk alone or with disrupted yoghurt micro­organisms caused twice as much lactose malabsorption as did the acidified milk containing intact organisms8. Some experimental studies suggest that yoghurt may increase the lactase activity in mucosal cells either by adherence of lactase of bacterial origin10 or by stimula­tion of brush border of the enterocytes11. A recent study did not demonstrate any increase in the lactase or B gal activity in the intestinal mucosa after a long term (8 day) ingestion of yoghurt12. Biopsies in this study were taken from the 3rd part of duodenum, 10-12 hours after the last yoghurt ingestion, so this study does not show what happens to the enzyme activity lower down in intestine. The results are contrary to a previous experimental study in rats which showed increase in enzyme activity after prolonged yoghurt intake13. The orofaecal transit time for yoghurt is significant­ly longer than the milk. This allows greater time for any residual intestinal lactase activity to act. This also explains the better absorption even from heated yoghurt as compared to milk in some studies14, while other workers have shown that the beneficial effect of yoghurt is destroyed by pasteurization12. It has been shown that microbial endogenous lactase is superior to exogenous commercial lactase in alleviating lactose maldigestion15. Though the commercially available preparations do their job16, they are expensive. Moreover, to get the best results one has to incubate the milk with them before consumption to achieve lactose hydrolysis17. All yoghurts are not created equal. Lactose malabsorbing subject may absorb lactose better from different brands of yoghurt. This variation could be due to whether products were pasteurized which had destroyed the B gal activity, way of storage and transport and intrinsic differences in the B gal activity of cultures18. This would not be a great problem in case of yoghurt which is produced by the shopkeepers on daily basis and no heat treatment is given to the formed product. Lactose malabsorption frequently occurs in patients with symptomatic giardiasis19 because of the non-specific damage to the mucosa of the infection site by various mechanisms20-22. Such children may benefit from the administration of yoghurt whose lactose ap­pears to be well absorbed23. Yogliurt may be an ap­propriate food for the renutrition of malnourished children with chronic diarrhoea and lactase deficiency24.
Cancer
Antitumour activity of yoghurt has been studied in experimental animals. Feeding of fermented milk products decreased the DNA synthesis of in­traperitoneally transplanted ehrlich ascitic tumours25. Lactobacilli used in the fermentation of milk products, may survive in the digestive tract26 and interfere with other gut bacteria. Alternation in the intestinal bacterial enzyme activity was observed during feeding milk supple­ments with lactobacillus acidophilus27,28. Oral ad­ministration of such strains decreased the concentration of three faecal enzymes (B glucuronidase, azoreductase, nitroreductase) 28 that had the capacity to convert procar­cinogens to carcinogens in the colon. Another study confirmed decrease in nitroreductase activity but B glucuronidase and azoreductase activity remained un­changed29. Difference in the strains of lactobacilli are likely to be responsible for these differences but this study confirmed that the lactobacillus acidophilus and bilIdobacterium bifidum in the daily products lead to metabolic changes in the colonic flora. Such changes may influence estrogen, steroid and bile acid metabolism and interfere enterohepatic circulation30-33. Moreover, glycopeptides from the cell wall of lactobacillus bul­garicus have shown to have antitumour action34. Further­more, micro-organisms provided by yoghurt may stimu­late immunological activity in the host and increase interferon production by the lymphocytes35. Lactobacil­lus casei given per os to the mice has shown to increase the phagocytic activity of macrophages36. The immune stimulation could be relevant to the dietary yoghurt’s effect on inhibition of tumour cell proliferation. In a case control study from Netherlands a significantly lower consumption of fermented milk products was observed among breast cancer cases as compared to the popula­tion controls37.
Intestinal infections
Oral antibiotics often alter the intestinal flora and this may end up in pseudo-membranous colitis38. This disease caused by clostridium difficile can be cured by administration of faecal enema from healthy adults39. A particular strains of lactobacillus is effective in prevent­ing relapses of pseudo membranous colitis40. Bifidobac­terium longum is a part of normal intestinal microflora. Yoghurt containing this species may decrease the fre­quency of gastrointestinal disorders by reducing an­tibiotic induced alternations in the intestinal microflora41. In addition to the restoration of intestinal microflora, yoghurt also has some antimicrobial effect. Antibiotic production have been shown by lactic strep­tococci and lactic bacilli42. Low pH due to lactic acid has also shown to kill pathogens but acidity may not always be enough to be bacteriocidal. Various pathogens may survive in yoghurt or dahi. Contamination may occur during handling of milk, inoculation and storage. Staphylococcus aureus, streptococcus faecalis, es­cherichia coli, enterobacter aerogenosa, bacillus cereus, yeasts and mould have been recovered from some of the specimens of dahi from Lahore1. It is important to observe all hygienic measures while dealing with dahi. Fermented milk consumption decreases the in­cidence of salmonella carrier state43 and reduces the risk of travellers diarrhoea caused by enterotoxigenic es­cherichia coli44. Volatile fatty acids produced by lactic acid bacteria may be responsible for controlling the colonization of the gut by shigella sonnei and E. coli45.
Osteoporosis
Calcium supplementation in the form of dairy products decreases the rate of vertebral bone loss in premenopausal women46. In another study women with postmenopausal idiopathic osteoporosis were found to have significantly greater chance of lactase deficiency47 which could predispose to osteoporosis either through reduced intake of milk secondary to intolerance or impaired calcium absorption. Though the presence of lactose enhances absorption of calcium from the milk; in lactase deficiency it might inhibit its absorption48-50. The yoghurt would certainly be a better choice in terms of tolerance to overcome the problem of decrease dietary intake of calcium. The relation of lactase, lactose and calcium appears to be a complex one as one of the studies showed that calcium was absorbed equally well from milk and yoghurt in hypolactasic subjects51. Further work is needed to resolve the issue.
Miscellaneous
Yoghurt, like milk is a good source of protein, riboflavin, folic acid and calcium. Its folic acid content is higher than the milk52. Digestibility of the milk protein is increased due to its partial predigestion during the fermentation process53. Yoghurt may be used by the geriatric population as a mild laxative54 because of its lactose and lactic acid content. It also has hypocholesterolemic effect55 but such activity is also present in the milk. It is hoped that in the years to come much more detailed and important scientific knowledge would be available for this ancient natural food.

REFERENCES

1. Naeem, K. and Rizvi, A.R. Studies on the physical and bacterial quality of dahi with special reference to public health. 3. Pat Mcd. Aaaoc., 1986;36:87-89.
2. Fuller, R. Probiotica in man and animals. 3. AppL Bacteriol., 1989;66:365-78.
3. Fuller, R. Probiotics in human medicine. Gut, 1991;32:439-42.
4. Kolars, J.C, Levitt, M.D., Aouji, M. and Savaino, D.A. Yogburt - an autodigeating source of lactose. N. Engl.J.Med., 1984;310:1-3.
5. Kilara, A. and Shabani, K.M. Lactase activity of cultured and acidified dairy products.). Dairy Sci., 1976;59:2031-35.
6. Wierzbicki, LB. and Koiskowski, F.V. Lsctaae potentials ofvsrioua organisms grown in whey.). Dairy Sci., 1973;56:26-29.
7. Wierzbiclti, LB. and Koiskowski, F.V. Quantitative messurementof lactose absorption. Gastroenterology, 1976;70: 1058-62.
8. Martini, MC., Bollwcg, G.L., Levitt, M.D. and Savaiano, D.A. Lactose digestion by yoghurt B-galactosidase: influence of pH and microbial cell integrity. Am.), Clin. Nutr., 1987;45:432-36.
9. Pocbart, P., Dewit, 0., Desjeux, J.F. and Bourlioux, P. Viable starter culture, B-galactosidase activity and lactose in duodenum afteryoghurtingestion in lactase-defi­cient humans. Am.J.Clin.Nutr., 1989;49:828-31.
10. Garvie, Ed., Cole, C.B., Fuller, R and Hewitt, D. The effect of yoghurt on some components of the gut microflora and on the metabolism of lactose in the rat.). Appl. Bacteriol., 1984;56:237-45.
11. Besnier, MO., Bourlioux, P., Fourniat, 3., Ducluzeau, Rand Aumaitre, A Influence of yoghurt feeding on intestinal lactose activity in germ free or conventional mice. Ann. Microbiol. (Paris), 1983;134A:219-30.
12. Lereboura, B., Ndam, C.N.D., Lavoine, A, Hellot, M.F., Antoine, J.M. and Cohn, Q Yoghurt and fermented-then-pasteurized milk: effects of short-term ingestion on lactose absorption and mucosal lactase activity in lactose deficient subjects. Am.). Clin. Nutr., 1989;49:823-27.
13. Goodenough, E.R. and Kleyn, D.H. Influence ofviable yoghurt microflora on digestion of lactose by the rat.). Dairy Sci., 1976;59:601-6.
14. Marteau, P., Flourie, B., Pochart, P., Chastang, C., Deajeux, ).F. and Rambausi, ).C Effect of microbial lactose activity in yoghurt on the intestinal absorption of lactose: an in vivo study in lactose-deficient humans. Br.). Nutr., 1990;64:71-79.
15. Onwulate, CL, Rao, D.R. and Vankineni, P. Relative efficiency of yogburt, sweet acidophilus milk, hydrolyzed-lactose milk and a commercial lsctase tablet in alleviating lactose maldisgestion. Am.J.Clin.Nutr., 1989;49:1233-37.
16. Rosado, ).L, Solomons, N.W., Liskey, R and Bourges, H. Enzymes replacement therapy for primary adult lactase deficiency. Effective reduction of lactose ealabsorp­don and milk intolerance by direct addition of B-galactosidase to milk at meal time. Gastroenterology, 1986;87:1072-81
17. Schneider, RE., Corona, E., Rosales, F., Schneider, F.E., Rodriguez, 0. and Pinedo, 0. Effect of temperature on the lactose hydrolytic capacity of a lactase derived from kluyseromyees lsctis. Am.J.Clin.Nutr., 1990;51:197-201.
18. Sytock, D.H. and Dipalma, ).A. All yoghurta are not created equaL Am.J.Clin.Nutr., 1988;47:454-57.
19. Vega-Franco, L, Meza, C, Romero, ).L., Alania, SE. and Meijerink, 1 Breath hydrogen test in children with giardissis. 3. Pediatr. Gsstroenterol. Nutr., 1987;6:365-68.
20. Poley, ).R and Rosenfield, S. Malabsorption in giardiasis: presence of a luminal barrier (mucoid pseudomembrane). Ascanningand transmission electron microscope study.J. Pediatr. GastroenteroL Nutr., 1982;1:63-80.
21. Saha, TIC and Ghosh, T.K. Invasion of small intestinal mucosa by gierdia lamblia in man. Gastroenterology, 1977;372:402-5.
22. Brandborg, L.L, Tankersley, CB., Gotleib, 5., Barancik, M. and Ssrtor, V.E. Histological demonstration of mucosal invasion by giardie lambia in man. Gastroenterology, 1977;52:143-50.
23. Mantovani, M.P., Guandalini, S., Eeuba, P., Corvino, C. and diMsatino, L Lactose malabsorption in children with symptomatic giardia lamblis intection: feasibility of yoghurt supplementation. ).Pediatr. Gastroenterot Nutr., 1989;9:295-300.
24. Dewit, 0., Boudraa, G., Touhami, M. and Deajeux, ).F. Breath hydrogen teatand stools characteristics after ingestion ofmilk andyoghyrt in malnourished childrenwith chronic diarrhoea and lactase deficiency.). Tropical Pediatr., 1987;33:177-180.
25. Reddy, G.V., Friend, BA., Shahani, K.M., Farmer, RE. ct si. Antitumour activity of yoghurteomponents.). Food Prot., 1983;46:8-11.
26. Shahani, 1CM. and Ayebo, AD. Role of dietary lactobscillus in gastrointestinal microecology. Am.J.Clin.Nutr., 1980;33:2448-57.
27. Goldin, B.R. and Gorback, S.L Alternations in focal microflora enzymes related to diet, age, lactobacillus supplements and dimethylhydrazine. Cancer, 1977;40:2421-26.
28. Marteau, P., Pochart, P., Flourie, B., Pellier, P., Santos, L., Desjeux, ).F. and Rambaud, ).C Effect chronic ingestion of a fermented daily product containing lactobacillus acidophilus and bifidobacterium bifidum on metabolic activities of the coloniemictoflora in humans. Am.J.Clin.Nutr., 1990;52:685-88.
29. Goldin, BR. and Gorbach, S.L. The effect of milk and lactobacillua feeding on human intestinal bacterial enzyme activity.). Clin. Nutr., 1984; 39:756-61.
30. Hill, M.)., Goddard, P-and Williams, RE. Gut bacteria and aetiology of cancer of the breast. Lancet, 1971;2:472-73.
31. Gorbach, S.L Estrogens, breast cancer and intestinal flora. Rev. Infect. Dia., 1984;6 (suppl.1):585-90.
32. Papatestas, AE., Panvelliwalla, D., Tartter, P.I., Miller, S., Pertsemlidis, D. and Aufaes, AH. )r., Fecal steroid metabolites and breasteaneer. Cancer, 1982;49:1201-S.
33. Miller, S.R, Pspatestaa, A.E., Panvelliwalla, D., Pertsemlidia, D. and Aufses, AH. Feeah steroid excretion and degradation and breastcancer stage.). Surg. Res., 1983;34:555-59.
34. Bogdanov, 1G., Velichkov, V.T., Gurevich, Al. et sh. Antitumour action of glycopep­tides from the cell wall of lactobacilluabulgaricus. Bull. Exp. Biot Med., 1978;84:1750-53.
35. DeSimone, C, Salvadore, B.B., Negri, R., Ferrazzi, M., Baldinelli, Land Vesely, R. The adjuvant effect of yoghurt on production of gamma interferon by Con A-stimulated human peripheral blood lymphocytes. Nutr. Rep. Int., 1986;33:419-33.
36. Perdigon, G., DeMsciaa, M.E.N., Alvarez, S., Oliver, G. and DeRuix Holgada, A.A.P. Effect of perorally administered lactobacilli on macrophage activatio in mice. Infect. Immun., 198453:404-10.
37. Veer, P.v., Detker, 3M., Lamers, J.W.J., Kok, F.)., Schouten, E.G. et at Consumption of fermented milk products and breast cancer. a case control study in Netherlands. Cancer Res., 1989;49:4020-23.
38. Nord, CE., Heimdahh, A. and Kager, L Antimicrobial induced alternations of the human oropharyngeah and intestinal microflora. Seand. ). Infect. Dis., 1986; SuppL 49:64-72.
39. Schwan, A, Sjolin, 5., Trottestam, U. and Aronsson, B. Relapsing clostridium difficile enterocolitis cured byrectal infusion of normal feces. Scand.). Infect. Dis., 1984;16:211­15.
40. Gorbach, S.L, Chang, T.W. and Goldin, B. Successful treatment of relapsing cloatridium difficile colitis with lactobacillus GG. Lancet, 1987;2:1519.
41. Colombel, J.F., Cortot, A, Neut, C and Romond, C. Yoghurt with bifidobacterium longum reduces erythromycin-induced gastrointestinal effect (letter). Lancet, 1987;2:43.
42. Reddy, G.V., Shahani, K.M., Friend, B.A and Chandan, R.C. Natural antibiotic activity of lactobacillus acidophilus and bulgaricus III. Production and partial purification of bulgarian from lactobacillus bulgaricus. Cull Dairy Prod.J., 1983;18:15- 19.
43. Aim, L. The effect of lactobacillus acidophilus administration upon tbe survival of aalmonells in randomly selected human carriers. Frog. Food Nutr. Sci., 1983;7:13-17.
44. Clementa, ML, Levine, M.M., Ristaino, P.A., Days, yE. and Hughes, T.P. Exogenous lactobacilli fed to man - their fate and ability to prevent diarrhoeai disease. Frog. Food Nutr. Sci., 1983;7:29-37.
45. Pongpech, P. and Hentges, D.J. Inhibition of shigelia sonnei and enterotoxigenic eacherichia coli by volatile fatty acids in mice. Microbial Ecology Health Disc., 1989;2:153-61.
46. Baran, D., Sorensen, A., Grimes, J., Lew, R., Karellas. A. et al Dietary modification with dairy products forpreventingvertebral bone loss in premenopausal women: a threeyear progressive study. I.Clin. Gaatroenterol. Metab., 1989;70:264-70.
47. Newcomer, A.D., Hodgson, S.F., McGill, D.B. and Thomas, P3. Lactaae deficiency: prevalence in osteoporosis. Ann. Intern. Med., 1987;89:218-21.
48. Condon, JR., Nassim, J.R., Millard, F.J.C. and Stainthorpe, EM. Calcium and phosphorus metabolism in relation to lactose intolerance. Lancet, 1970;1:1027-29.
49, ECocian, J., Skala, Land Bakos, K. Calcium absorption from milk and lactose free milkin healthy subjects and patientawith lactose intolerance. Digestion, 1973;9:317-24.
50. Cochet, B., Jung, M., Griessen, M., Bartholdi, P., Schaller, P. and Donath, A. Effects of lactose on intestinal calcium absorption in normal and lactase-deficient subjects. Gastroenterology, 1983;84:935-40.
51. Smith, T.M., Kolars, J.C., Savaiano, D.A. and Levitt, M.D. Absorption of calcium from milk andyoghurt. Am.J.Clin.Nutr., 1985;42:1197-200.
52. AIm. L Effect of fermentation of B-vitamin content of milk in Sweden. 3. Daisy Sci., 1980;65:353-59.
53, Death, H.C. and Tamine,A.Y. Yoghurt: nutritive and therapeuticaspecta.J.Food Pros., 1981;44:78-86.
54. Seneca, H. and Gaymont, S. Clinical uses ofyoghurt. J.Am.Geriatr. Soc., 1957;5:932-35.
55. Hepner, G., Fried, R., StJeor, S., Fusetti, L. and Morin, R. Hypocholesterolemic effect ofyoghurtand milk. Am.J.Clin. Nutr., 1979;32:19-24.
56. Thompson, LU., Jenkins, D.J., Amer, M.A., Reichert, It, Jenkins, A. and Kamulaky, 1. The effectoffermented and unfermented milks onserum cholesterol. Am.J. Clin. Nutr., 1982;36:1106-11
57. Koyosswa, H., Sugawara, C., Sugawara, N. and Miyake, H. Effect of skim milk and yogburt on serum lipids and development of sudanophilic lesiona in cholesterol-fed rabbits. Am.J.Clin.Nutr., 1984;40:479-84.

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