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Review Lactic Acid Bacteria and the Human Gastrointestinal Tract

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Review Lactic Acid Bacteria and the Human Gastrointestinal Tract European Journal of Clinical Nutrition (1999) 53, 339±350 ß 1999 Stockton Press. All rights reserved 0954±3007/99 $12.00 http://www.stockton-press.co.uk/ejcn Review Lactic acid bacteria and the human gastrointestinal tract H Hove1*, H Nùrgaard1 and P Brùbech Mortensen1 1Medical Department CA, Division of Gastroenterology, Rigshospitalet and Paediatric Department L, Gentofte University Hospital, Denmark. Objective: This review summarises the effects of lactic acid bacteria on lactose malabsorption, bacterial=viral or antibiotic associated diarrhoea, and describes the impact of lactic acid bacteria on cancer and the fermentative products in the colon. Results: Eight studies (including 78 patients) demonstrated that lactase de®cient subjects absorbed lactose in yogurt better than lactose in milk, while two studies (25 patients) did not support this. Two studies (22 patients) showed that unfermented acidophilus milk was absorbed better than milk, while six studies (68 patients) found no signi®cant differences. Addition of lactose hydrolysing enzyme, lactase, to milk improved lactose malabsorption in seven studies (131 lactose malabsorbers), while one study (10 malabsorbers) demonstrated no improvement. Lactic acid bacteria alleviated travellers' diarrhoea in one study (94 individuals) while a study including 756 individuals was borderline statistically signi®cant. One study (50 individuals) did not ®nd an effect of lactic acid bacteria on travellers' diarrhoea. Six studies (404 infants) demonstrated a signi®cant effect of lactic acid bacteria on infant diarrhoea, while one study (40 infants) did not. Lactic acid bacteria moderated antibiotic associated diarrhoea in three studies (66 individuals), while two studies (117 individuals) were insigni®cant. Conclusions: Lactase de®cient subjects bene®t from a better lactose absorption after ingestion of yoghurt compared with milk and from milk added lactase, whereas ingestion of unfermented acidophilus milk does not seem to improve lactose absorption. The majority of studies support that lactic acid bacteria alleviate bacterial=viral induced diarrhoea, especially in infants, while the effect on antibiotic associated diarrhoea is less clear. Experimental studies indicate an effect of lactic bacteria on human cell cancer lines, but clinical evidence is lacking. A `stabilising' effect of lactic acid bacteria on the colonic ¯ora has not been documented. Descriptors: lactic acid bacteria; lactobacilli; bi®dobacteria; lactate; lactic acid; lactose malabsorption; antibiotic associated diarrhoea; diarrhoea; rotavirus; colonic cancer Introduction (homofermentative) or at least 50% (heterofer-mentative) lactate producers (Kandler, 1983, Table 1). Interest in the bene®cial effects of lactic acid bacteria dates to Studies on the ¯ora of the gastrointestinal tract report the Russian scientist, E. Metchnikoff (1845 ± 1919), who that numbers of bi®dobacteria may exceed 1011 per gram of proposed that the extended longevity of the Balkan people faeces (Finegold et al, 1983) accounting for 6 ± 25% of all could be attributable to their practice of ingesting fermented cultivable bacteria in faeces (Kitsuoka, 1984; Scardovi, milk products (Metchnikoff, 1908). He believed that gastro- 1986) whereas lactobacilli only constitute 0 ± 1% of the intestinal disturbances occur by intestinal growth of putre- bacteria in the faeces of healthy humans (Hill & Drasar, factive microbes, and that lactic acid bacteria could minimise 1975; Gorbach, 1971; 1986, Brown, 1977). The exception or prevent the harmful effects of these microbes. The role of of this condition is the dominant presence of bi®dobacteria lactic acid bacteria within the gastrointestinal tract has been in breast-fed infants (Stark & Lee, 1982). Lactic acid one of the most controversial subjects of the area of intestinal bacteria are described to be of nutritional and therapeutic microbial ecology. No other group of bacteria has been bene®t to the host in several clinical conditions. The proposed to be responsible for so many different bene®cial proposed effects of lactic acid bacteria on the intestinal actions, but non-conclusive or insigni®cant results are often tract are mentioned in Table 2. Discussion of these speci®c reported when attempts are made to con®rm that lactic acid health targets follow. bacteria improve the health of the host. Lactic acid bacteria supposedly exert an impact on the Lactic acid bacteria consists of heterogeneous group of small as well as the large intestine. First, bacterial derived gram-positive bacteria, whose main fermentation product lactase from ingested lactic acid bacteria might enhance the from carbohydrate is lactate. The group comprises cocci hydrolysis of lactose to glucose and galactose in the small (streptococcus, pediococcus, leuconostoc) and rods (lacto- intestine, which are rapidly absorbed or fermented. Sec- bacillus and bi®dobacterium), which are either exclusively ondly, lactic acid bacteria may have an impact on the colonic ¯ora in situations in which some sort of imbalance *Correspondence: Hanne Hove, Ph.D., Hovmarksvej 77, 2920 exists. The exact nature of this microbial imbalance and Charlottenlund. Received 14 August 1998; revised 7 December 1998; accepted how it is corrected by the ingestion of lactic acid bacteria is 20 December 1998 not known. Lactic acid bacteria H Hove et al 340 Table 1 The genera of lactic acid bacteria, their fermentation type and main products (Kandler, 1983) Genus Fermentation type Main product Con®guration of lactate Streptococcus homofermentative lactate L-lactate Pediococcus homofermentative lactate DL-lactate Lactobacillus homofermentative lactate DL-lactate Leuconostoc heterofermentative lactate : acetate D-lactate Bi®dobacterium heterofermentative lactate : acetate L-lactate Table 2 Studies evaluating the clinical effect of lactic acid bacteria Positive studies Negative studies Yogurt improves lactose absorption compared with milk? (Table 3 a) 8 2 Unfermented acidophilus milk improves lactose absorption compared with milk? (Table 3 b) 2 6 Lactase relieves lactose malabsorption among lactose malabsorbers? (Table 5) 7 1 Lactic acid bacteria reduce incidence of travellers diarrhoea? (Table 6 a) 1 2 Lactic acid bacteria reduce incidence of diarrhoea among infants? (Table 6 b) 6 1 Lactic acid bacteria alleviate antibiotic associated diarrhoea? (Table 7 a) 3 2 Over the past decade there has been increased interest in where intake of marked bi®dobacteria resulted in a rise in bacterial food supplements, called probiotics. The de®ni- faecal levels to approximately 108 bi®dobacteria=g faeces tion of a probiotic being: `A live microbial feed supplement followed by a gradual decrease after ingestion ceased. which bene®cially affects the host animal by improving its Thus, attempts to increase the number of lactic acid intestinal microbial balance' (Fuller, 1989). There are bacteria in the gastrointestinal tract by ingestion generally several characteristics that are of importance for organisms results in a temporary colonisation of the gut, which used as probiotics (Kim, 1988). These include: the organ- persists as long as the lactic acid bacteria are ingested ism should maintain viability and activity in the carrier (Goldin et al, 1992; Deneke et al, 1988; Saxelin et al, food before consumption, should survive the upper gastro- 1991). After consumption of a bacterium, recovery from intestinal tract, be capable of surviving and growing in the the faeces is not evidence of implantation, even if recovery intestine, be a normal inhabitants of the intestinal tract, and persists for a period after consumption has stopped. Con- eventually produce bene®cial effects when in the intestinal tinued faecal recovery of ingested lactic acid bacteria may tract. Further, the organism must be non-pathogenic and be because of residence time in the large intestine that non-toxic. exceeds microbial generation time. Survival through the gastrointestinal tract Impact on the small intestine The effect of lactic acid bacteria in the intestine requires that the bacteria or at least their enzymes survive the acid Relieving lactose intolerance in lactose malabsorbers gastric content and are active after the passage of the Lactose is the predominate carbohydrate in milk, and it stomach. Studies of orally administered lactic acid bacteria requires enzymatic hydrolysis to the monosaccharides glu- have demonstrated that the lactic acid bacterial counts in cose and galactose before intestinal absorption. Small the small intestine increase signi®cantly after ingestion intestinal epithelial cells (enterocytes) produce b-galacto- (Robins-Browne et al, 1981). The ability of Bi®dobacter- sidase in childhood, and some people continue to produce ium bi®dum to survive the passage through the upper b-galactosidase throughout life, but globally most adults gastrointestinal tract when ingested in fermented milk are lactose malabsorbers and are as non-milk consumers was investigated by Pochart et al (1992) using in vivo deprived of an important source of protein and calcium. ileal perfusion, and he found that the average number of Although lactose malabsorption is common worldwide, the bi®dobacteria recovered from the terminal ileum consti- symptomatic expression of lactose intolerance is less so. tuted approximately 25% of the number ingested (ingested Lactose intolerance has a substantial psychological compo- dose 1010 bacteria). This is in consistency with a study of nent: among individuals who believed they
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