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Blackwell Publishing, Ltd.

REVI EW
The nutrition and health benefits of yoghurt
MIC HELLE C MC KIN L E Y*
The Dairy Council, 164 Shaftesbury Avenue, London WC2H 8HL, UK

Yoghurt is one of the most popular fermented milk products worldwide and has gained widespread
consumer acceptance as a healthy food. It provides an array of nutrients in significant amounts, in
relation to its energy and fat content, making it a nutrient-dense food. In particular, yoghurt can provide
the body with significant amounts of calcium in a bioavailable form. Furthermore, yoghurt has many
health benefits beyond the basic nutrition it provides, such as improved lactose tolerance, a possible role
in body weight and fat loss, and a variety of health attributes associated with probiotic bacteria.
Keywords Body weight, Calcium, Gastrointestinal health, Lactose intolerance, Probiotics, Yoghurt.

acceptance as a healthy and nutritious food, has led


*Author for correspondence. E-mail: m.mckinley@dairycouncil.org.uk

I N T RO D U C T I O N
to their widespread popularity across all population
The introduction of fermented milk products into subgroups.
the diet of man is thought to date back to the dawn Table 1 shows the consumption of yoghurt and
of civilization, as reference is made to them in both fermented milk products in 10 European countries
the Bible and the sacred books of Hinduism according to data collected recently from nearly
(Nakazawa & Hosono 1992). Research from Britain 36 000 participants in the European Prospective
(Copley et al. 2003) has recently demonstrated the Investigation into Cancer and Nutrition (EPIC)
presence of dairy fat residues in pottery fragments study (Hjartåker et al. 2002). The largest con-
from Neolithic, Bronze Age and Iron Age settle- sumers are Sweden, France and the Netherlands,
ments, thus indicating that the practice of dairying who consume more than twice that of the UK and,
existed in Britain as far back as 6500 years ago. in general, women throughout Europe tend to con-
Although it is not certain, it is likely that consump- sume more yoghurt than men. Although the UK
tion of fermented or cultured milk products, such is by no means the biggest yoghurt consumer in
as yoghurt, butter and cheese, also occurred around Europe, it still makes a very valuable contribution
this time as they were an effective means of pro- to our diet.
longing the shelf-life of milk.
Yoghurt is a product of the lactic acid fermenta-
N U T R I T I O NA L P RO F I L E
tion of milk by addition of a starter culture contain-
ing Streptococcus thermophilus and Lactobacillus In terms of its nutritional profile, yoghurt has a
delbrueckii ssp. bulgaricus. In some countries less similar composition to the milk from which it is
traditional microorganisms, such as Lactobacillus made but will vary somewhat if fruit, cereal or
helveticus and Lactobacillus delbrueckii ssp. other components are added (Table 2). Its nutri-
lactis, are sometimes mixed with the starter culture tional similarity with milk means that yoghurt is an
(Tamime 2002). Although fermented milk products excellent source of protein, calcium, phosphorus,
such as yoghurt were originally developed simply riboflavin (vitamin B2), thiamin (vitamin B1) and
as a means of preserving the nutrients in milk, vitamin B12, and a valuable source of folate, niacin,
it was soon discovered that, by fermenting with magnesium and zinc. The protein it provides is of
different microorganisms, an opportunity existed high biological value (i.e. it contains all the amino
to develop a wide range of products with different acids essential to heath), and the vitamins and min-
flavours, textures, consistencies and, more recently, erals found in milk and dairy foods are bioavailable
health attributes. The market now offers a vast (i.e. available for absorption and use by the body).
array of yoghurts to suit all palates and meal occa- Milk and dairy products such as yoghurt, par-
*Author for sions. Yoghurts come in a variety of textures (e.g. ticularly the low-fat varieties, provide an array of
correspondence. liquid, set, smooth), fat contents (e.g. luxury, low- important nutrients in significant amounts in rela-
E-mail: info@
fat, virtually fat-free) and flavours (e.g. natural, tion to their energy and fat content, therefore mak-
dairycouncil.org.uk
fruit, cereal), can be consumed as a snack or part of ing them a nutrient-dense food. Table 3 shows the
© 2005 Society of a meal, as a sweet or savoury food, and are available contribution that one small pot of yoghurt makes to
Dairy Technology all year-round. This versatility, together with their the nutrient requirements of various age groups.

Vol 58, No 1 February 2005 International Journal of Dairy Technology 1


Vol 58, No 1 February 2005

Table 1 Reported daily consumption of yoghurt and other fermented milk products in 10 European countries obtained
using 24-h dietary recalls (n = 35 955)

Contribution Contribution Contribution


of yoghurt Total dairy of yoghurt and Total dairy of yoghurt and
and fermented intake fermented milk intake fermented milk
Total milk products (g/day) products to total (g/day) products to total
dairy intake to total dairy —men dairy intake —women dairy intake
Country (g/day) intake (%) (n = 13 031) (%)—men (n = 22 924) (%)—women

Greece 189.3 14.8 189.8 13.5 188.7 16.1


Italy 203.6 9.0 206.5 7.4 200.6 10.6
Germany 248.3 17.5 245.2 15.3 251.4 19.7
Norway 288.7 12.6 — — 288.7 12.6
France 290.9 26.1 — — 290.9 26.1
UK 301.5 8.5 301.2 7.5 301.8 9.5
Denmark 325.8 16.4 352.5 13.7 299.1 19.0
Spain 364.9 10.6 332.3 8.9 397.5 12.3
Sweden 370.1 24.0 404.2 21.6 335.9 26.4
the Netherlands 375.3 17.3 369.7 13.9 380.8 20.7

Source: Hjartåker et al. (2002)

Table 2 Nutritional compositiona of common varieties of yoghurt (per serving)

Whole milk, Whole milk, Low-fat, Low-fat, Virtually fat Greek style, Drinking
plain fruit plain fruit free, fruit plain Twinpot yoghurt
Nutrient (150 g) (150 g) (150 g) (150 g) (150 g) (150 g) (175 g) (200 g)

Protein (g) 8.6 6.0 7.2 6.3 7.2 8.6 7.2 6.2
Folate (µg) 27 15 27 24 12 9 23 24
Niacin (mg) 2.3 1.3 1.7 1.7 1.7 2.5 2.0 1.6
Riboflavin (mg) 0.40 0.24 0.33 0.32 0.44 0.20 0.33 0.32
Thiamin (mg) 0.09 0.18 0.18 0.18 0.06 0.18 0.11 0.06
Vitamin B12 (µg) 0.3 0.5 0.5 0.5 0.3 0.3 0 0.4
Calcium (mg) 300 183 243 210 195 189 228 200
Magnesium (mg) 29 20 24 23 20 20 23 22
Phosphorus (mg) 255 144 215 180 165 207 186 162
Zinc (mg) 1.1 0.6 0.9 0.8 0.6 0.8 0.7 0.6

a
Food Standards Agency (2002)

Eating dairy products, such as yoghurt, helps to diets that exclude milk and dairy products tend to
improve the overall quality of the diet and increases have poor nutrient intakes, which can affect growth
the chances of achieving nutritional recommenda- and bone health. Henriksen et al. (2000) conducted
tions. Research has shown that milk consumption a study to assess the nutrient intake of children on
is positively associated with the likelihood of cow’s milk-restricted diets. In this study, parents
children and teenagers achieving the recommended of 34 children aged 2.5–3 years completed a 4-day
intakes for vitamin A, folate, vitamin B12, calcium weighed record of their child’s food intake. They
and magnesium (Ballew et al. 2000). Consuming found that children on milk-free diets had signific-
extra milk has also been shown to improve the diet antly lower intakes of energy, fat, protein, niacin,
quality of older adults. Researchers assessed the calcium and riboflavin. Although the use of milk
effects of advising a group of adults to add three substitutes improved the nutritional quality of the
230 mL glasses of milk to their daily food intake. milk-free diets to some extent, the recommenda-
They reported that, compared to the control group, tions for riboflavin and calcium were still not met.
the milk group increased their intake of vitamin A, The authors of the study concluded that children on
riboflavin, vitamin B12, vitamin D, calcium, phos- cow’s milk-free diets could be at risk for malnutri-
phorus, potassium, magnesium and zinc (Barr tion unless precautions were taken to replace the
et al. 2000). Conversely, individuals who consume valuable nutrients from milk in the diet. Further

2 © 2005 Society of Dairy Technology


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2001; Buchowski et al. 2002; Di Stefano et al.


Table 3 Contribution of one pot (150 g) of fruit yoghurt to the daily nutritional needs
2002).
of population subgroups
One of the nutrients that yoghurt and other dairy
Percentage of daily reference products supplies in abundance is calcium, which
nutrient intake (RNI)b is vital for the development and maintenance of
Nutrient content bone health. As illustrated in Table 4, one pot of
per 50 g pot 5-year-old 14-year-old Adult Adult
yoghurt would provide a 5-year-old with 41%
Nutrient yoghurt a girl girl man woman
of their daily calcium requirements and an adult
Protein 6.0 g 31 14 11 13 or teenage girl with about a quarter of their daily
Folate 15.0 µg 15 8 8 8 calcium needs.
Niacin 1.3 mg 12 11 8 10 Milk and dairy foods are rich sources of calcium
Riboflavin 0.24 mg 30 22 14 22 because they contain significant amounts of cal-
Thiamin 0.18 mg 26 26 18 23
cium in a bioavailable form. Although other foods
Vitamin B12 0.5 µg 63 42 33 33
also contain calcium, they may not necessarily be
Calcium 183 mg 41 23 26 26
good sources because their calcium content per
Magnesium 20 mg 17 7 7 7
Phosphorus 144 mg 41 23 26 26
serving is low, or the calcium they provide is not
Zinc 0.6 mg 9 7 6 9 available for absorption and use by the body (i.e.
bioavailable), or as a result of both these factors.
a
Food Standards Agency (2002) Table 4 illustrates this concept; for example, while
b
Department of Health (1991) spinach has a high calcium content on a per serv-
ing basis, its bioavailability is poor, and hence it
would be necessary to eat 11 servings, or 963 g, of
spinach to absorb the same amount of calcium that
studies have also found that dairy avoidance in is available from one small pot of yoghurt.
children is associated with poor nutrient intake,
small stature, impaired growth and poor bone
E F F E C T O N H E A LT H
health (Isolauri et al. 1998; Black et al. 2002;
Christie et al. 2002). Furthermore, lactose intoler- Lactose intolerance
ance is associated with a low calcium intake and Lactose, the main carbohydrate found in milk and
bone mineral density in a variety of age and ethnic dairy products, is a disaccharide sugar composed
groups due to unnecessary avoidance of milk and of two monosaccharides, glucose and galactose,
dairy products (Stallings et al. 1994; Corazza et al. joined together by a condensation reaction. It can
1995; Honkanen et al. 1996; Jackson & Savaiano be hydrolysed in the body by the enzyme lactase

Table 4 Number of servings of selected calcium-containing foods that it would be necessary to consume in order to absorb
the same amount of calcium as that available from one pot of low-fat yoghurt

Number of
Calcium Estimated servings Total quantity
content Fractional absorbable needed to (g) needed
Serving per serving absorption calcium/ equal 150 g to equal 150 g
size (g)a (mg)b (%)c serving (mg) yoghurt yoghurt
Low-fat plain yoghurt 150 243 32.1 78.0 1.0 —
Kidney beans 70 (2 heaped 25.9 17.0 4.4 17.7 1239
(dried, boiled) tablespoons)
Kidney beans (canned) 70 (2 heaped 49.7 17.0 8.5 9.2 644
tablespoons)
Broccoli (boiled) 85 34.0 52.6 17.9 4.4 374
Sprouts (frozen and boiled) 90 26.1 63.8 16.7 4.7 423
Cabbage (boiled) 95 31.4 64.9 20.4 3.8 361
Spinach (boiled) 90 144 5.1 7.3 10.7 963
Watercress (raw) 20 (1/4 bunch) 34 67.0 22.8 3.4 68
Almonds 26 (12 whole) 62.4 21.2 13.2 5.9 153

Source: Adapted from Weaver and Plawecki (1994)


a
Ministry of Agriculture, Fisheries & Food (1993). Serving size shown equates to a medium portion unless otherwise
indicated
b
Food Standards Agency (2002)
c
Weaver and Plawecki (1994)

© 2005 Society of Dairy Technology 3


Vol 58, No 1 February 2005

(β-galactosidase) and the resultant simple sugars and dairy from the diet (Stallings et al. 1994;
can then be absorbed in the small intestine and Corazza et al. 1995; Honkanen et al. 1996; Jackson
used as fuel by the body. Lactose maldigestion is & Savaiano 2001; Buchowski et al. 2002; Di
difficulty in digesting the disaccharide lactose due Stefano et al. 2002), there is a clear need to better
to insufficient amounts of the enzyme lactase. If educate and inform individuals with this condition
lactose passes into the large intestine undigested, that the complete avoidance of dairy products is
it can be fermented by the colonic microflora, not usually necessary. Research shows that milk
causing adverse gastrointestinal symptoms in with meals, hard cheese and yoghurt are well toler-
some individuals, such as flatulence, diarrhoea ated (Johnson et al. 1993; Suarez et al. 1995, 1997,
and abdominal pain. This is known as lactose 1998; Pribila et al. 2000), and so calcium intake
intolerance, that is the occurrence of symptoms need not be compromised.
after persons with clinically diagnosed lactose
maldigestion consume a trigger amount of lactose Weight control
(British Nutrition Foundation 2002). Obesity is an increasing public health problem
Research has shown that lactose in yoghurt is in the UK, with one in five adults now classed as
tolerated better by individuals with hypolactasia obese (National Audit Office 2001). Fears about
than an equivalent quantity in milk (Gallagher et al. weight gain are often cited as a reason to cut down
1974; Kolars et al. 1984; McDonagh et al. 1987; on the consumption of milk and dairy products.
Dewit et al. 1988; Marteau et al. 1990a; Rosado However, there is little evidence to suggest that the
et al. 1992). Various explanations have been put consumption of milk and dairy products leads to
forward in an attempt to explain this phenomenon. excess weight gain and an emerging body of evid-
The presence of live bacteria in the yoghurt was ence suggests that this may even be counterpro-
thought to be important (Gilliland & Kim 1984; ductive. Preliminary research from in vitro animal
Savaiano et al. 1984; Lerebours et al. 1989). Some and human studies suggests that consumption of
studies, however, have failed to find any difference milk and dairy products may help to encourage
in the tolerance of heat-treated vs. fresh yoghurt weight, and fat, loss as part of a calorie-controlled
containing live bacteria (Marteau et al. 1990a; diet.
Savaiano et al. 1984; Hove et al. 1999). Similarly, Numerous observational studies in adults (Davies
it has been proposed that the bacterial enzyme et al. 2000; Lin et al. 2000; Zemel et al. 2000;
β-galactosidase, which partly resists luminal Periera et al. 2002; Jacqmain et al. 2003; Teegarden
hydrolysis and can be detected in the duodenum 2003; Zemel 2003a), children and adolescents
and terminal ileum after yoghurt consumption, is (Carruth & Skinner 2001; Novotny et al. 2003;
available to hydrolyse lactose and therefore results in Skinner et al. 2003) have demonstrated a signific-
improved tolerance (Kolars et al. 1984; McDonagh ant inverse relationship between calcium, or dairy
et al. 1987; Pochart et al. 1989; Marteau et al. consumption, and both body weight and body fat.
1990b; Martini et al. 1991). β-Galactosidase is an For example, a longitudinal study of infants who
intracellular enzyme and so will remain active as were followed until they were 8 years old (Skinner
long as the cell wall of the bacteria (whether viable et al. 2003) found that a higher dietary calcium
or nonviable) remains intact. This theory is, intake from calcium-rich foods like milk, cheese
however, confounded by the results of a study that and yoghurt was associated with a lower percent-
found no difference in digestion and tolerance to age of body fat.
lactose following ingestion of three fermented To date, two randomized controlled trials have
dairy products that had a fourfold difference in been published in this area, one in abstract form
their β-galactosidase activity (Vesa et al. 1996). (Zemel et al. 2003, 2004). In one of the studies
These results suggest that factors in addition to (Zemel et al. 2004), 32 healthy but obese subjects
lactase (β-galactosidase) activity may be contribut- were maintained for 24 weeks on low-energy diets
ing to the improved lactose tolerance associated (500 kcal /day deficit) and randomized to either the
with yoghurt. For example, the different viscosity control group (0–1 serving dairy/day + 400–500 mg
of yoghurt compared to milk may result in slower supplemental calcium /day), the high calcium group
gastric emptying and thus a longer transit through (control diet + 800 mg supplemental calcium/day)
the gastrointestinal tract, which, in turn, may or the high dairy group (3–4 servings low-fat dairy
improve the absorption and reduce the lactose load foods/day, providing a total calcium intake of
in the colon (Vesa et al. 1996). 1200–1300 mg/day). The weight loss was 6.4%,
Whatever the explanation, the science consist- 8.6% and 10.9% for the control, high calcium and
ently shows that yoghurt is well tolerated by indi- high dairy regimens, respectively; corresponding
viduals who have lactose intolerance. As lactose figures for fat loss in the trunk region were 19%,
maldigestion or intolerance is associated with a 50.1% and 66.2%, respectively. In the other study,
low calcium intake and bone mineral density, prob- Zemel et al. (2003) randomly assigned 34 healthy
ably because of the unnecessary exclusion of milk but obese women to receive 1100 mg calcium/day

4 © 2005 Society of Dairy Technology


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(in the form of three servings of fat-free yoghurt) and the demand for products that have benefits
or 500 mg calcium/day, both groups following beyond the basic nutrition they provide has driven
a calorie-controlled diet. After 12 weeks, the an explosion in the market for functional foods.
researchers found that the yoghurt group lost 22% Fermented dairy products account for the majority
more weight (average loss 13 lb), 61% more body of the European functional food market (Stanton
fat and 81% more trunkal fat than the group of et al. 2001). They have the ability to support the
dieters who simply reduced calories. viability of probiotic cultures and thus provide a
The results of both these studies indicate that suitable vehicle for their delivery into the body
calcium appears to help weight and fat loss, in addi- (Stanton et al. 2002) and are easily incorporated
tion to calorie restriction, and increase percentage into the diet.
fat loss from the trunk region. They also indicate Numerous definitions exist for ‘probiotics’
that dairy products, such as yoghurt, appear to exert (Sanders 2003). For example, they are commonly
a substantially greater effect on both fat loss and fat defined as ‘living microorganisms, which upon
distribution compared to an equivalent amount of ingestion in certain numbers, exert health benefits
supplemental calcium. beyond inherent basic nutrition’ (Guarner &
Various mechanisms to explain this effect have Schaafsma 1998); and, more recently, as ‘viable
been proposed and are discussed in detail in several nonpathogenic microorganisms which, when
review papers (Parikh & Yanovski 2003; Zemel ingested, exert a positive influence on host health
2003a,b). In vitro and animal studies have shown or physiology’ (Schrezenmeir & de Vrese 2001).
that intracellular calcium levels play a pivotal Whatever the exact definition, there is general
role in fat metabolism. High blood parathyroid agreement regarding the key selection criteria for
hormone (PTH) and 1,25-dihydroxyvitamin D levels, use of probiotic cultures in human food, that is
such as those that result from a low-calcium intake, they are generally of human origin, considered
have been shown to stimulate the influx of calcium nonpathogenic, acid and bile tolerant, have the
into human adipocytes in cell culture experiments. ability to withstand technological processes (e.g.
This, in turn, switches the cell metabolism from food production), remain viable during their shelf-
lipolysis to lipogenesis, so that fat is stored rather life period and exert beneficial health effects
than burnt (Zemel 2003a,b). Keeping concentra- (Shortt 1999). In order to be effective, therefore,
tions of calcitrophic hormones low, by increasing probiotic bacteria must not only be present in a
calcium intake, should therefore lower intradipocyte viable form and in sufficient numbers at the time
calcium concentration and switch cell metabolism of consumption but also be able to survive passage
in the opposite direction, that is decreased lipogen- through the harsh conditions of the gastrointestinal
esis and increased lipolysis. tract so that they reach their target site in live form.
Obesity is recognized as a multifactorial disease Furthermore, on arrival at their target site they
and, consequently, various strategies are needed need to be able to colonize the target area. Probiotic
to address the problem. While it is unlikely that bacteria will be at a distinct advantage if they can
ensuring an adequate intake of dairy foods will compete for substrates effectively, be versatile in
prove to be the magic bullet that solves the prob- terms of the substrates they use, use substrates
lem, this emerging research indicates that such a efficiently, have the ability of adhere to the gut
strategy may make an important contribution to epithelium and possibly also the ability to produce
an individual’s ability to control their body weight bacteriocins (such as short-chain fatty acids,
when undertaken in combination with other dietary hydrogen peroxide and antimicrobial peptides)
measures and adequate physical activity. Further that adversely affect the growth of certain bacteria
research is urgently required in this area. already in the gut (Fooks & Gibson 2002). The bac-
teria already inhabiting the gut are highly adapted
Probiotics to their environment and so represent tough com-
Professor Elie Metchnikoff, Director of the Pasteur petition for the incoming bacteria.
Institute, was one of the first to propose that The key concept underlying the proposed health
yoghurt had beneficial health effects because of the benefits of probiotics is that the gut microflora
bacteria it contained. In 1907 he postulated that plays an important role in resistance to disease and
the bacteria involved in yoghurt fermentation, promotes normal intestinal function (Salminen et al.
Lactobacillus delbrueckii ssp. bulgaricus and Stre- 1998). It is thought that factors such as changing
ptococcus thermophilus, suppressed putrefactive- lifestyles, changing dietary patterns, increasing
type fermentations by the intestinal flora, and stress and antibiotic consumption all have a harm-
that the consumption of these yoghurts played a ful effect on the balance of the gut microflora,
role in maintaining health and prolonging life causing a shift away from potentially beneficial
(Metchnikoff 1907). or health-promoting microorganisms, such as the
Since then, nutritional approaches to disease lactobacilli and bifidobacteria, towards an increase
prevention have become a priority for consumers, in harmful or pathogenic microorganisms (Fooks

© 2005 Society of Dairy Technology 5


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et al. 2001, 2002; Isolauri et al. 2002; Shanahan


Table 5 Potential health benefits of probiotics
2002; Feagan 2003; Floch 2003; Goossens et al. 2003;
Shortened duration of rotavirus diarrhoea
Ouwehand et al. 2003; Sanders 2003), and this
Reduced incidence and severity of traveller’s diarrhoea article simply gives a brief overview of some selected
Reduced incidence of antibiotic-associated diarrhoea health effects.
Reduced incidence of radiation-induced diarrhoea
Relief of symptoms of lactose intolerance Diarrhoea
Immune modulation From time to time, the balance of the intestinal flora
Fewer relapses, reduced use of steroids and improved quality of life in association with can be disturbed by pathogenic bacteria, viruses
inflammatory bowel disease and antibiotics, often resulting in diarrhoea. The
Fewer relapses in association with chronic pouchitis treatment of diarrhoea has traditionally been one
Reduced incidence and mortality from necrotizing enterocolitis of the main application areas for probiotics. Best
Reduction of symptoms associated with irritable bowel syndrome documented evidence exists for the shortening of
Alleviation of constipation
rotavirus diarrhoea in children by selected probiotic
Reduced Helicobacter pylori colonization and inflammation
strains such as L. rhamnosus GG (Guandalini et al.
Reduced faecal enzyme activity (which may reduce levels of carcinogens in the
2000), L. reuteri (Shornikova et al. 1997), L. casei
faeces)
Reduced recurrence of superficial bladder cancer
Shirota (Sugita & Togawa 1994), L. acidophilus
Enhancement of effect of radiotherapy on cervical cancer LB (Simakachorn et al. 2000), B. bifidum and
Reduced incidence nasal allergy S. thermophilus (Saavedra et al. 1994), L. delbrueckii
Reduced severity atopic dermatitis ssp. bulgaricus and S. thermophilus (Boudraa et al.
Reduced prevalence atopic disease 2001), and Bacillus coagulans (Chandra 2002).
Reduction in total and low density lipoprotein (LDL) cholesterol In addition, prevention and treatment of antibiotic-
Reduction in systolic and diastolic blood pressure associated diarrhoea appears to be feasible for
Reduced incidence urinary infections selected probiotic strains including L. acidophilus,
Reduced episodes of bacterial vaginosis L. delbrueckii ssp. bulgaricus and B. longum, with
Reduced vaginal Candida infection rate good evidence for Enterococcus faecium SF68,
Reduced symptoms and recurrence vaginitis and cystitis L. rhamnosus GG and Saccharomyces boulardii
Reduced recurrence of otitis media (Marteau et al. 2001, 2002). Many of the trials in
Alteration of gut flora influencing oxalate degradation and thus kidney
this area to date have, however, been poorly con-
stone formation
trolled and used low numbers of subjects. Further
Prevention of small bowel bacterial overgrowth
Reduced recurrence of chronic recurrent hypertrophic sinusitis
well-designed studies are therefore needed. In the
Inhibition of endotoxin-producing intestinal microflora associated with alcoholic
interim, it may be prudent to attempt prophylaxis
liver disease via probiotics in vulnerable groups such as elderly
Reduced cariogenicity people.
For traveller’s diarrhoea it is less clear whether
Source: Ouwehand et al. (2003); Sanders (2003) probiotics can reduce the incidence. A few trials
using L. rhamnosus GG (Oksanen et al. 1990;
Hilton et al. 1997) and S. boulardii (von Kollaritsch
& Gibson 2002). This, in turn, is thought to predis- et al. 1993) have suggested a potential for prevent-
pose to a number of clinical diseases such as bowel ive efficacy, but more are required before such an
cancer and inflammatory bowel disease and also approach can be medically recommended.
to make the host more susceptible to infections
(Fooks & Gibson 2002). It has been suggested Immunologic effects
that under such conditions, probiotics can exert a The immune system is an important contributor to
positive effect on health by redressing the balance diseases such as cancer, infection, gastrointestinal
of health-promoting and pathogenic bacteria in the disorders, allergy and asthma. Many sections of the
gastrointestinal tract. population may be immunocompromised, such
The microorganisms most commonly used as as infants, the elderly, surgical patients, trauma
probiotics are lactic acid bacteria such as Lacto- victims, people under stress and HIV-positive indi-
bacilli (e.g. L. acidophilus, L. casei, L. rhamnosus, viduals. The intestine is the body’s largest immune
L. reuteri, L. plantarum) and Bifidobacteria (e.g. organ and probiotics therefore present an opportun-
B. longum, B. bifidum, B. breve and B. infantis) ity to influence the response of the immune system
(Fooks & Gibson 2002), which are both found to foreign antigens. The results of human studies
naturally in the gut. The array of health benefits indicate that yoghurt consumption can increase
potentially attributable to probiotics is vast (see cytokine production, phagocytic activity, antibody
Table 5) and it is beyond the scope of this paper to production, T-cell function and natural killer
discuss each of them in turn. Many excellent review cell activity, and there is some evidence that this
papers have been published in this area (de Roos yoghurt-induced immune enhancement is associ-
& Katan 2000; Meydani & Ha 2000; Marteau ated with a lowered incidence of conditions such as

6 © 2005 Society of Dairy Technology


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cancer, gastrointestinal disorders and allergic symp- Mimura et al. 2004) and for the prophylaxis of
toms (Meydani & Ha 2000; Isolauri et al. 2002). pouchitis in patients who had ileo-pouch anal
anastomosis for ulcerative colitis (Gionchetti et al.
Inflammatory bowel disease 2003). If other investigators replicate this finding,
The term inflammatory bowel disease (IBD) it will radically change current clinical practice in
encompasses disorders such as Crohn’s disease, relation to maintenance therapy for patients with
ulcerative colitis and pouchitis. These disorders ulcerative colitis (Shanahan 2002). Promising
are characterized by chronic or recurrent intestinal results have also been obtained in Crohn’s disease
inflammation and, while their exact aetiology is with a variety of probiotics including S. boulardii
unknown, the main theory is that IBD may result (Guslandi et al. 2000), VSL#3 (Campieri et al.
from abnormal host responses to some members of 2000) and E. coli Nissle 1917. All were associated
the intestinal flora or from a defective mucosal bar- with a reduced rate of relapse when used as a
rier in genetically susceptible individuals (Ruseler replacement for (Campieri et al. 2000), or dietary
van Embden et al. 1994; Sartor 1995; Marteau adjunct to (Guslandi et al. 2000), mesalazine, or
et al. 2001). Current therapy for IBD involves when compared to a placebo (Malchow 1997).
suppression or modulation of the host immuno- Further well-designed intervention trials inves-
inflammatory response with corticosteroids to tigating the therapeutic potential of probiotics in
induce remission, or surgery to remove the dis- IBD are currently under way in Europe (Abbott
eased section of the bowel. It does not, however, 2004).
address the contribution of the intestinal microflora
to the pathogenesis (Shanahan 2002), which is an Irritable bowel disease
area where a probiotic intervention may prove Irritable bowel syndrome (IBS) is a gastrointestinal
beneficial. In theory, probiotics have the potential condition characterized by abdominal pain, bloat-
to interrupt immuno-inflammatory responses ing, excessive flatus, constipation and diarrhoea.
induced by commensal bacteria that may be The type and severity of symptoms experienced
responsible for damage to the intestinal mucosa varies widely between individuals and, in general,
(Guarner et al. 2002). the condition is poorly understood. No test currently
Several well-designed trials of probiotic therapy exists for IBS; therefore it can only be diagnosed
in human subjects with various IBD-related by excluding the presence of other gastrointestinal
conditions have been published. Some experts in anomalies.
the field believe that the evidence is now strong The gut microflora is thought to contribute to
enough to prescribe VSL#3, a mixture of four strains the development of IBS because microbiological
of lactobacilli (L. casei, L. plantarum, L. acidophilus studies indicate that IBS sufferers have irregular-
and L. delbrueckii ssp. bulgaricus), three strains ities in their colonic microflora, such as lower
of bifidobacteria (B. longum, B. breve, B. infantis) numbers of coliforms, lactobacilli and bifidobacteria,
and one strain of S. thermophilus for pouchitis; compared with healthy individuals (Madden &
Esherichia coli Nissle 1917 (a nonpathogenic Hunter 2002). Irrespective of whether this change
E. coli) for ulcerative colitis; and S. boulardii (a in microflora is a cause of IBS, or simply a symp-
nonpathogenic yeast) for Crohn’s disease (Marteau tom of the condition, the quantitative changes in
et al. 2002). bacterial species suggest that a probiotic approach
Three double-blind randomized-controlled trials may be beneficial.
have found treatment with the probiotic E. coli To date, there have been few studies involving
Nissle 1917 to be as effective as the standard drug probiotics and IBS, possibly because IBS sufferers
treatment mesalazine for maintaining remission are a very diverse group and are therefore difficult
in ulcerative colitis (Kruis et al. 1997, 2001; to study. The studies that have been conducted so
Rembacken et al. 1999). A recent randomized con- far have produced conflicting results. For example,
trolled study examined the effect of supplementa- Halpern et al. (1996) demonstrated a statistically
tion with 100 mL bifidobacteria-fermented milk significant difference in clinically defined gastro-
daily for 1 year as a dietary adjunct in the treatment intestinal function of IBS patients who were given
of ulcerative colitis. Exacerbation of symptoms an antidiarrhoeal drug containing L. acidophilus
was seen in 27% of the bifidobacteria fermented compared with patients who received a placebo. A
milk group compared to 90% of controls. The symptomatic improvement was observed in 19 out
authors concluded that probiotic supplementation of 28 patients with high volume diarrhoea follow-
was successful in maintaining remission and had ing administration of Enterococcus faecium PR88
possible preventive effects on the relapse of ulcer- (Hunter et al. 1996). Likewise, some trials using
ative colitis (Ishikawa et al. 2002). The probiotic L. plantarum 299v have resulted in symptomatic
cocktail VSL#3 has been shown to be highly improvements (Niedzielin et al. 2001; Nobaek
effective in maintaining remission in patients with et al. 2000), but not all studies using this probiotic
chronic relapsing pouchitis (Gionchetti et al. 2000; organism have proved successful (Sen et al. 2001).

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The role of L. rhamnosus GG was studied in fructo-oligosaccharide with bifidobacteria. In


a randomized, double-blind, placebo-controlled, theory, the end result of administering a synbiotic
cross-over trial (O’Sullivan & O’Morain 2000) of would be improved survival and colonization of the
24 patients with IBS. Nineteen patients completed probiotic and, in turn, increasing health benefits
the study but there was no significant difference in (Fooks & Gibson 2002).
pain, urgency or bloating between the two groups. Finally, an exciting proposition is that probiotic
There was, however, a reduction in diarrhoea in the bacteria could be genetically modified and used
probiotic group. as drug-delivery vehicles, expressing vaccines,
Although the use of probiotics in the treatment enzymes, antimicrobials or therapeutic proteins
of IBS is currently not justified, more research in within specific target areas of the gastrointestinal
this area is certainly warranted because abnormal- tract. In theory, microorganisms can be genetically
ities seen in the colonic microflora of IBS suggest engineered to produce almost any protein, which,
that a probiotic approach will ultimately be justi- in turn, could be used therapeutically if it could
fied (Madden & Hunter 2002). reach the appropriate target in the body. There is
already some evidence that this type of therapy
could be feasible. Steidler et al. (2000) demon-
THE FUTURE
strated a therapeutic benefit in animal models of
There is likely to be further growth and innovation colitis using a bacterium genetically engineered
in the yoghurt sector of the dairy market on to secrete the inflammatory cytokine interleukin-
the basis of taste, for example new products in 10 (IL-10). IL-10 is a potent immune modulator,
the children, luxury and smoothie sectors and the capable of dampening down excessive immune
introduction of new and more exotic flavours to reactions. A version of this genetically modified
keep consumers interested. In terms of nutrition bacterium that includes safety features to prevent
and health, an area with massive growth potential the escape of the inserted gene into the environ-
because of its appeal to the health-conscious ment has been developed for humans (Steidler
consumer is the functional yoghurt sector. Market et al. 2003). The first human trial investigating the
growth in this sector will be driven by the science, potential of a genetically engineered bacterium as
as all health claims made in relation to these foods a therapeutic agent will take place in Amsterdam
will need to be thoroughly substantiated. It is likely (Abbott 2004). Researchers hope that the engineered
that emphasis will be placed on target-specific bacterium will deliver a steady stream of IL-10
products containing well-characterized bacteria directly to the gut wall and so suppress the abnormal
with specific health-enhancing characteristics. immune response associated with inflammatory
Another potential growth area for the functional bowel disease.
dairy sector developments is the concept of pre-
biotics and synbiotics.
The term ‘prebiotic’ was introduced in 1995 REFERENCES
(Gibson & Roberfroid 1995). Prebiotics are defined Abbott A (2004) Gut reaction. Nature 427 284–286.
as ‘nondigestible food ingredients that beneficially Ballew C, Kuesters S and Gillespie C (2000) Beverage choices
effect the host by selectively stimulating the growth affect adequacy of children’s nutrient intakes. Archives
and/or activity of one or a limited number of bac- of Pediatrics and Adolescent Medicine 154 1148–
teria in the colon’. The most likely prebiotics are 1152.
Barr S I, McCarron D A, Heaney R P, Dawson-Hughes B,
nondigestible carbohydrates, such as oligosaccha-
Berga S L, Stern J S and Oparil S (2000) Effects of
rides (MacFarlane & Cummings 1999). For example,
increased consumption of fluid milk on energy and nutri-
fructo-oligosaccharides and inulin, found prim- ent intake, body weight, and cardiovascular risk factors in
arily in onions, chicory, garlic, leeks and artichokes, healthy older adults. Journal of the American Dietetic
are frequently studied and have been shown to Association 100 810–817.
selectively stimulate the growth of bifidobacteria Black R E, Williams S M, Jones I E and Goulding A (2002)
(Hidaka et al. 1986; Gibson & Roberfroid 1995; Children who avoid drinking cow milk have low dietary
Gibson et al. 1995). calcium intakes and poor bone health. American Journal
The prebiotic concept has largely been devel- of Clinical Nutrition 76 675–680.
oped because the viability of live probiotic bac- Boudraa G, Benbouabdellah M, Hachelaf W, Boisset M,
teria, both in food products and during their transit Desjeux J-F and Touhami M (2001) Effect of feeding
yoghurt versus milk in children with acute diarrhea and
through the gastrointestinal tract, can be variable.
carbohydrate malabsorption. Journal of Pediatric Gastro-
This has given rise to the development of syn-
enterology and Nutrition 33 307–313.
biotics: ‘mixtures of pro- and prebiotics that benefi- British Nutrition Foundation (2002) Enzyme defects and food
cially affect the host by improving the survival and intolerance. In Adverse Reactions to Food, pp 104–111.
implantation of live microbial dietary supplements Buttriss J, ed. Oxford: Blackwell Science.
in the gastrointestinal tract’ (Gibson & Roberfroid Buchowski M S, Semenya J and Johnson A O (2002) Dietary
1995). A natural symbiotic partnership could be a calcium intake in lactose maldigesting intolerant and

8 © 2005 Society of Dairy Technology


Vol 58, No 1 February 2005

tolerant African-American women. Journal of the American Gibson G R and Roberfroid M B (1995) Dietary modulation
College of Nutrition 21 47–54. of the human colonic microbiota. Introducing the concept
Campieri M, Rizzello F, Venturi A, Poggioli G, Ugolini F, of prebiotics. Journal of Nutrition 125 1401–1412.
Helwig U, Amadini C, Romboli E and Gionchetti P Gibson G R, Beatty E R, Wang X and Cummings J H (1995)
(2000) Combination of antibiotic and probiotic treatment Selective stimulation of bifidobacteria in the human colon
is efficacious in prophylaxis of post-operative recurrence by oligofructose and inulin. Gastroenterology 108 975–
of Crohn’s disease: a randomized controlled study vs 982.
mesalamine. Gastroenterology 118 G4179 (abstract). Gilliland S E and Kim H (1984) Effect of viable starter culture
Carruth B R and Skinner J D (2001) The role of dietary bacteria in yoghurt on lactose utilization in humans. Jour-
calcium and other nutrients in moderating body fat in pre- nal of Dairy Science 67 1–6.
school children. International Journal of Obesity 25 559– Gionchetti P, Rizzello F, Venturi A, Brigidi P, Matteuzzi D,
566. Bazzocchi G, Poggioli G, Miglioli M and Campieri M
Chandra R K (2002) Effect of Lactobacillus on the incidence (2000) Oral bacteriotherapy as maintenance treatment in
and severity of acute rotavirus diarrhoea in infants. A pro- patients with chronic pouchitis: a double-blind, placebo
spective placebo-controlled double-blind study. Nutrition controlled trial. Gastroenterology 119 305–309.
Research 22 65–69. Gionchetti P, Rizzello F, Helwig U, Venturi A, Lammers K M,
Christie L, Hine R J, Parker J G and Burks W (2002) Food Brigidi P, Vitali B, Poggioli G, Miglioli M and Campieri M
allergies in children affect nutrient intake and growth. (2003) Prophylaxis of pouchitis onset with probiotic
Journal of the American Dietetic Association 102 1648– therapy: a double-blind, placebo controlled trial. Gastro-
1651. enterology 124 1202–1209.
Copley M S, Berstan R, Dudd S N, Docherty G, Mukherjee A J, Goossens D, Jonkers D, Stobberingh E, van der Bogaard A,
Straker V, Payne S and Evershed R P (2003) Direct Russel M and Stockbrugger R (2003) Probiotics in
chemical evidence for widespread dairying in prehistoric gastroenterology: indications and future perspectives.
Britain. Proceedings of the National Academy of Sciences Scandinavian Journal of Gastroenterology Supplement
of the United States of America 100 1524–1529. 239 15–23.
Corazza G R, Benati G, DiSario A, Tarozzi C, Strocchi A, Guandalini S, Pensabene L, Zikri M A, Dias J A, Casali L G,
Passeri M and Gasbarrini G (1995) Lactose intolerance Hoekstra H, Kolacek S, Massar K, Micetic-Turk D,
and bone mass in postmenopausal Italian women. British Papadopoulou A, de Sousa J S, Sandhu B, Szajewska H
Journal of Nutrition 73 479–487. and Weizman Z (2000) Lactobacillus GG administered in
Davies K M, Heaney R P, Recker R R, Lappe J M, Barger- oral rehydration solution to children with acute diarrhea:
Lux M J, Rafferty K and Hinders S (2000) Calcium intake a multicenter European trial. Journal of Pediatric Gastro-
and body weight. Journal of Clinical Endocrinology and enterology and Nutrition 30 54–60.
Metabolism 85 4635–4638. Guarner F and Schaafsma G J (1998) Probiotics. Inter-
Department of Health (1991) Dietary Reference Values for national Journal of Food Microbiology 39 237–238.
Food Energy and Nutrients for the United Kingdom: Guarner F, Casellas F, Borruel N, Antolin M, Videla S,
Report of the Panel on Dietary Reference Values. Report Vilaseca J and Malagelada J-R (2002) Role of microecology
on Health Social Subjects 41. Committee on Medical in chronic inflammatory bowel diseases. European Journal
Aspects of Food Policy. London: HMSO. of Clinical Nutrition 56 S34–S38.
de Roos N M and Katan M B (2000) Effects of probiotic Guslandi M, Mezzi G, Sorghi M and Testoni P A (2000)
bacteria on diarrhea, lipid metabolism, and carcinogenesis: Saccharomyces boulardii in maintenance treatment of
a review of papers published between 1988 and 1998. Crohn’s disease. Digestive Disease and Science 45 1462–
American Journal of Clinical Nutrition 71 405–411. 1464.
Dewit O, Pochart P and Desjeux J F (1988) Breath hydrogen Halpern G M, Prindiville T, Blankenburg M, Hsia T and
concentration after lactose, milk, fresh or heated yoghurt Gershwin M E (1996) Treatment of irritable bowel syn-
ingestion by healthy young adults with or without lactose drome with Lacteol Fort: a randomised, double-blind,
malabsorption. Nutrition 4 131–135. cross-over trial. American Journal of Gastroenterology 91
Di Stefano M, Veneto G, Malservisi S, Cecchetti L, Minguzzi L, 1579–1585.
Strocchi A and Croazza G R (2002) Lactose malabsorp- Henriksen C, Eggesbø M, Halvorsen R and Botten (2000)
tion and intolerance and peak bone mass. Gastroenterology Nutrient intake among two-year-old children on cows’
122 1793–1799. milk-restricted diets. Acta Paediatrica 89 272–278.
Feagan B G (2003) Maintenance therapy for inflammatory Hidaka H, Eida T and Takizawa Teta I (1986) Effects of
bowel disease. American Journal of Gastroenterology 98 fructooligosaccharides on intestinal flora and human
S6–S17. health. Bifidobacteria Microflora 5 37–50.
Floch M H (2003) Probiotics, irritable bowel syndrome, and Hilton E, Kolakowski P, Singer C and Smith M (1997)
inflammatory bowel disease. Current Treatment Options Efficacy of Lactobacillus GG as a diarrheal preventive in
in Gastroenterology 6 283–288. travellers. Journal of Travel Medicine 4 41–43.
Food Standards Agency (2002) McCance and Widdowson’s Hjartåker A, Lagiou A, Slimani N, Lund E, Chirlaque M D,
the Composition of Foods, Sixth Summary Edition. Vasilopoulou E, Zavitsanos X, Berrino F, Sacerdote C,
Cambridge: Royal Society of Chemistry. Ocké M C, Peeters P H M, Engeset D, Skeie G, Aller A,
Fooks L J and Gibson G R (2002) Probiotics as modulators of Amiano P, Berglund G, Nilsson S, McTaggart A, Spencer
the gut flora. British Journal of Nutrition 88 S39–S49. E A, Overad K, Tjønneland A, Clavel-Chapelon F,
Gallagher C R, Mollesson A L and Caldwell J H (1974) Linseisen J, Schulz M, Hemon B and Riboli E (2002)
Lactose intolerance and fermented dairy products. Journal Consumption of dairy products in the European Pro-
of the American Dietetic Association 65 418–419. spective Investigation into Cancer and Nutrition (EPIC)

© 2005 Society of Dairy Technology 9


Vol 58, No 1 February 2005

cohort: data from 35 955 24-hour dietary recalls in 10 Madden J A J and Hunter A O (2002) A review of the role of
European countries. Public Health Nutrition 5 1259– the gut microflora in irritable bowel syndrome and the effects
1271. of probiotics. British Journal of Nutrition 88 S67–S72.
Honkanen R, Pulkkinen P, Jarvinen R, Kroger H, Lindstedt Malchow H A (1997) Crohn’s disease and Esherichia coli. A
K, Tuppurainen M and Uusitupa M (1996) Does lactose new approach in therapy to maintain remission of colonic
intolerance predispose to low bone density? A population- Crohn’s disease? Journal of Clinical Gastroenterology 25
based study of perimenopausal Finnish women. Bone 19 653–658.
23–28. Marteau P, Flourié B, Pochart P, Chastang C, Desjeux J F and
Hove H, Nrgaard H and Mortensen P B (1999) Lactic acid Rambaud J C (1990a) Effect of the microbial lactase (EC
bacteria and the human gastrointestinal tract. European 3.2.1.23) activity in yoghurt on the intestinal absorption
Journal of Clinical Nutrition 53 339–350. of lactose: an in vivo study in lactase-deficient humans.
Hunter J O, Lee A J, King T S, Barratt M E J, Linggood M A British Journal of Nutrition 64 71–79.
and Blades J A (1996) Enterococcus faecium strain PR88— Marteau P, Pochart P, Flourié B, Pellier P, Santos L, Desjeux
an effective probiotic. Gut 38(Suppl 1) A62 (abstract). F and Rambaud J (1990b) Effect of chronic ingestion of a
Ishikawa H, Akedo I, Umesaki Y, Tanaka R, Imaoka A and fermented dairy product containing Lactobacillus acido-
Otani T (2002) Randomized controlled trial of the effect philus and Bifidobacterium bifidum on metabolic activ-
of bifidobacteria-fermented milk on ulcerative colitis. ities of the colonic flora in humans. American Journal of
Journal of the American College of Nutrition 22 56–63. Clinical Nutrition 52 685–688.
Isolauri E, Sutas Y, Salo M K, Isosomppi R and Kaila M Marteau P R, de Vrese M, Cellier C J and Schrezenmeir J
(1998) Elimination diet in cow’s milk allergy: risk for (2001) Protection from gastrointestinal diseases with the
impaired growth in young children. Journal of Pediatrics use of probiotics. American Journal of Clinical Nutrition
132 1004–1009. 73 430S–436S.
Isolauri E, Kirjavainen P V and Salminen (2002) Probiotics: Marteau P, Seksik P and Jian R (2002) Probiotics and intesti-
a role in the treatment of intestinal infection and inflam- nal health effects: a clinical perspective. British Journal of
mation? Gut 50(Suppl 3) iii54–iii59. Nutrition 88 S51–S57.
Jackson K A and Savaiano D A (2001) Lactose maldigestion, Martini MC, Kukielka D and Savaino D A (1991) Lactose
calcium intake and osteoporosis in African-, Asian-, and digestion from yoghurt: influence of meal and additional
Hispanic-Americans. Journal of the American College of lactose. American Journal of Clinical Nutrition 53 1253–
Nutrition 20 198S–207S. 1258.
Jacqmain M, Doucet E, Després J-P, Bouchard C and McDonagh F E, Hitchins A D, Wong N P, Well P and
Tremblay A (2003) Calcium intake, body composition, Bodwell C E (1987) Modification of sweet acidophilus
and lipoprotein-lipid concentrations in adults. American milk to improve the utilisation by lactose intolerant persons.
Journal of Clinical Nutrition 77 1448–1452. American Journal of Clinical Nutrition 45 570–574.
Johnson A O, Semenya J G, Bucjowski M S, Enwonwu C O Metchnikoff E (1907) Prolongation of Life. London: William
and Scrimshaw N S (1993) Correlation of lactose maldi- Heinemann.
gestion, lactose intolerance, and milk intolerance. American Meydani S N and Ha W-K (2000) Immunologic effects of
Journal of Clinical Nutrition 57 399–401. yoghurt. American Journal of Clinical Nutrition 71 861–
Kolars J C, Levitt M D, Aouji M and Savaiano D A (1984) 872.
Yoghurt—an autodigesting source of lactose. New Mimura T, Rizzello F, Helwig U, Poggioli G, Schreiber S,
England Journal of Medicine 310 1–3. Talbot I C, Nicholls R J, Gionchetti P, Campieri K and
Kruis W, Schultz E, Fric P, Fixa B, Judmaier G and Stolte M Kamm M A (2004) Once daily high dose probiotic ther-
(1997) Double-blind comparison of an oral Esherichia apy (VSL#3) for maintaining remission in recurrent or
coli preparation and mesalazine in maintaining remission refractory pouchitis. Gut 53 108–114.
of ulcerative colitis. Alimentary Pharmacology and Ther- Ministry of Agriculture, Fisheries and Food (1993) Food
apeutics 1 853–858. Portion Sizes, 2nd Edition. London: HMSO.
Kruis W, Fric P and Stolte M (2001) Maintenance of Nakazawa Y and Hosono A (1992) Fermented milk in the
remission in ulcerative colitis is equally effective with orient. In Functions of Fermented Milk: Challenges for
Esherichia coli Nissle 1997 and with standard mesalamine. the Health Sciences, pp 61–78. Hosono A, ed. London:
Gastroenterology 120 A139 (abstract). Elsevier Science.
Lerebours E, Ndam C N, Lavoine A, Hellot M F, Antoine J M National Audit Office (2001) Tackling Obesity in England.
and Colin R (1989) Yoghurt and fermented-then-pasteurized Report by the Controller and Auditor General. HC 220.
milk: effects of short-term and long-term ingestion on London: The Stationery Office.
lactose absorption and mucosal lactase activity in Niedzielin K, Kordecki H and Birkenfeld B (2001) A con-
lactase-deficient subjects. American Journal of Clinical trolled, double-blind, randomised study on the efficacy
Nutrition 49 823–827. of Lactobacillus plantarum 299V in patients with irritable
Lin Y C, Lyle R M, McCabe L D, McCabe G P, Weaver C M bowel syndrome. European Journal of Gastroenterology
and Teegarden D (2000) Dairy calcium is related to and Hepatology 13 1143–1147.
changes in body composition during a two-year exercise Nobaek S, Johansson M L, Molin G, Ahrne S and Jeppsson B
intervention in young women. Journal of the American (2000) Alteration of intestinal microflora is associated
College of Nutrition 19 754–760. with reduction in abdominal bloating and pain in patients
MacFarlane G T and Cummings J H (1999) Probiotics and with irritable bowel syndrome. American Journal of
prebiotics: can regulating the activities of intestinal Gastroenterology 95 1231–1238.
bacteria benefit health? British Medical Journal 318 Novotny R, Acharya S, Grove J S, Daida Y G and Vogt T M
999–1003. (2003) Higher dairy intake is associated with lower body

10 © 2005 Society of Dairy Technology


Vol 58, No 1 February 2005

fat during adolescence. Federation of American Societies Sen S, Mullan M M, Parker T J, Woolner J T, Tarry S A and
for Experimental Biology Journal 17 A453.8 (abstract). Hunter J O (2001) Effect of Lactobacillus plantarum
O’Sullivan M A and O’Morain C A (2000) Bacterial supple- 299v on colonic fermentation and symptoms of irritable
mentation in the irritable bowel syndrome. A randomised bowel syndrome. Digestive Disease Science 47 2615–
double-blind placebo-controlled crossover study. Digest- 2620.
ive and Liver Disease 32 294–301. Shanahan F (2002) Probiotics and inflammatory bowel dis-
Oksanen P J, Salminen S, Saxelin M, Hamalainen P, Ihantola- ease: from fads and fantasy to facts and future. British
Vormisto A, Muurasniemi-Isoviita L, Nikkari S, Oksanen Journal of Nutrition 88 S5–S9.
T, Porsti I, Salminen E, Siitonen S, Stuckey H, Toppila A Shornikova A V, Casas I, Mykkänen H, Salo E and Vesikari T
and Vapaatalo H (1990) Prevention of traveller’s diarrhea (1997) Bacteriotherapy with Lactobacillus reuteri in
by Lactobacillus GG. Annals of Medicine 22 53–56. rotavirus gastroenteritis. The Pediatric Infectious Disease
Ouwehand A C, Blanchi Salvadori B, Fondén R, Mogensen Journal 16 1103–1107.
G, Salminen S and Sellars R (2003) Health effects of pro- Shortt C (1999) The probiotic century: historical and current
biotics and culture-containing dairy products in humans. perspectives. Trends in Food Science and Technology 10
Bulletin of the International Dairy Federation 380 4–19. 411–417.
Parikh S J and Yanovski J A (2003) Calcium intake and adiposity. Simakachorn N, Pichaipat V, Rithpornpaisam P, Kongkaew C,
American Journal of Clinical Nutrition 77 281–287. Tongpradit P and Varavithya W (2000) Clinical evaluation
Periera M A, Jacobs D R Jr, Van Horn L, Slattery M L, of the addition of lyophilized, heat-killed Lactobacillus
Kartashov A I and Ludwig D S (2002) Dairy consump- acidophilus LB to oral rehydration therapy in the treatment
tion, obesity, and the insulin resistance syndrome in young of acute diarrhea in children. Journal of Pediatric Gastro-
adults: the CARDIA Study. Journal of the American enterology and Nutrition 30 68–72.
Medical Association 287 2081–2089. Skinner J D, Bounds W, Carruth B R and Ziegler P (2003)
Pochart P, Bissetti N, Bourlioux P and Desjeux J F (1989) Longitudinal calcium intake is negatively related to chil-
Effect of daily consumption of fresh or pasteurised yoghurt dren’s body fat indexes. Journal of the American Dietetic
in intestinal lactose utilisation in lactose malabsorbers. Association 103 1626–1631.
Microecology and Therapy 18 105–110. Stallings V A, Oddleifson N W, Negrini B Y, Zemel B S and
Pribila B A, Hertzler S R, Martin B R, Weaver C M and Wellens R (1994) Bone mineral content and dietary
Savaiano D A (2000) Improved lactose digestion and calcium intake in children prescribed a low-lactose diet.
intolerance among African-American adolescent girls fed Journal of Paediatric Gastroenterology and Nutrition 18
a dairy-rich diet. Journal of the American Dietetic Associ- 440–445.
ation 100 524–528. Stanton C, Gardiner G, Meehan H, Collins K, Fitzgerald G,
Rembacken B J, Snelling A M, Hawkey P M, Chalmers D M Lynch P B and Ross R P (2001) Market potential for
and Axon A T (1999) Non-pathogenic Esherichia coli probiotics. American Journal of Clinical Nutrition 73
versus mesalazine for the treatment of ulcerative colitis: a S476–S483.
randomised trial. Lancet 354 635–639. Stanton C, Coakley M, Murphy J J, Fitzgerald G F, Devery R
Rosado J L, Solomons N W and Allen L H (1992) Lactose and Ross R P (2002) Development of dairy-based func-
digestion from unmodified, low-fat and lactose-hydrolysed tional foods. Science des Aliments 22 439–447.
yoghurt in adult lactose maldigesters. European Journal Steidler L, Hans W, Schotte L, Neirynck S, Obermeier F,
of Clinical Nutrition 46 61–67. Falk W, Fiers W and Remaut E (2000) Treatment of
Ruseler van Embden J G H, Schouten W R and van Lieshout murine colitis by Lactococcus lactis secreting interleukin-
L M C (1994) Pouchitis: result of microbial imbalance? 10. Science 289 1352–1355.
Gut 35 658–664. Steidler L, Neirynck S, Huyghebaert N, Snoeck V, Vermiere
Saavedra J M, Bauman N A, Oung I, Perman J A and A, Goddeeris B, Cox E, Remon J P and Remaut E (2003)
Yolken R H (1994) Feeding of Bifidobacterium bifidum Biological containment of genetically modified Lactococ-
and Streptococcus thermophilus to infants in hospital for cus lactis for intestinal delivery of human interleukin 10.
prevention of diarrhoea and shedding of rotavirus. Lancet Nature Biotechnology 21 785–789.
344 1046–1049. Suarez F L, Savaiano D A and Levitt M D (1995) A comparison
Salminen S, Ouwehand A C and Isolauri E (1998) Clinical of symptoms after the consumption of milk or lactose-
application of probiotic bacteria. International Dairy hydrolyzed milk by people with self-reported severe
Journal 8 563–572. lactose intolerance. New England Journal of Medicine
Sanders M E (2003) Probiotics: considerations for human 333 1–4.
health. Nutrition Reviews 61 91–99. Suarez F L, Savaiano D, Arbisi P and Levitt M D (1997)
Sartor R B (1995) Current concepts of the etiology and Tolerance to the daily ingestion of two cups of milk by
pathogenesis of ulcerative colitis and Crohn’s disease. individuals claiming lactose intolerance. American Jour-
Gastroenterology Clinics of North America 24 475– nal of Clinical Nutrition 65 1502–1506.
507. Suarez F L, Adshead J, Furne J K and Levitt M D (1998)
Savaiano D A El Anouar A A, Smith D E and Levitt M D Lactose maldigestion is not an impediment to the intake
(1984) Lactose malabsorption from yoghurt, pasteurized of 1,500 mg calcium daily as dairy products. American
yoghurt, sweet acidophilus milk, and cultured milk in Journal of Clinical Nutrition 68 1118–1122.
lactase-deficient individuals. American Journal of Clin- Sugita T and Togawa M (1994) Efficacy of Lactobacillus
ical Nutrition 40 1219–1223. preparation biolactis powder in children with rotavirus
Schrezenmeir J and de Vrese M (2001) Probiotics, prebiotics enteritis. Japanese Journal of Pediatrics 47 2755–
and synbiotics—approaching a definition. American 2762.
Journal of Clinical Nutrition 73 361S–364S. Tamime A Y (2002) Fermented milks: a historical food with

© 2005 Society of Dairy Technology 11


Vol 58, No 1 February 2005

modern applications—a review. European Journal of Zemel M B (2003a) Role of dietary calcium and dairy prod-
Clinical Nutrition 56 S2–S15. ucts in modulating adiposity. Lipids 38 139–146.
Teegarden D (2003) Calcium intake and reduction in weight Zemel M B (2003b) Mechanisms of dairy modulation of
or fat mass. Journal of Nutrition 133 249S–251S. adiposity. Journal of Nutrition 133 252S–256S.
Vesa T H, Marteau P, Zidi S, Pochart P and Rambaud J C Zemel M B, Shi H, Greer B, DiRienzo D and Zemel P (2000)
(1996) Digestion and tolerance of lactose from yoghurt Regulation of adiposity by dietary calcium. Federation of
and different semi-solid fermented dairy products con- American Societies for Experimental Biology Journal 14
taining Lactobacillus acidophilus and bifidobacteria in 1132–1138.
lactose maldigesters. Is bacterial lactase important? Zemel M B, Richards J D, Russell S M, Milstead A M and
European Journal of Clinical Nutrition 50 730–733. Gebhardt L P (2003) Dairy (yoghurt) augments fat loss
von Kollaritsch H, Holst H and Grobara P and Wiedermann G and reduces central adiposity during energy restriction in
(1993) Prevention of traveler’s diarrhea with Saccharomyces obese subjects. Federation of American Societies for
boulardii. Results of a placebo controlled double-blind Experimental Biology Journal 17 A1088 (Abstract).
study. Forstchritte der Medizin 111 153–156. Zemel M B, Thompson W, Milstead A, Morris K and
Weaver C M and Plawecki K L (1994) Dietary calcium: Campbell P (2004) Calcium and dairy acceleration of
adequacy of a vegetarian diet. American Journal of weight and fat loss during energy restriction in obese
Clinical Nutrition 59 1238S–41S. adults. Obesity Research 12 582–590.

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