Hydrogen excretion upon ingestion of dairy products in lactose-intolerant male subjects: importance of the live flora
European Journal of Clinical Nutrition (2001) 55, 509±512
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Original Communication
Hydrogen excretion upon ingestion of dairy products in lactoseintolerant male subjects: importance of the live ¯ora
X Pelletier1*, S Laure-Boussuge1 and Y Donazzolo1
1
OPTIMED, GieÁres, France
Objective: To assess the effects of the ingestion of milk, yoghurt (108 bacteria=ml), heat-treated yoghurt (< 15
bacteria=ml) and two products obtained by dilution of yoghurt with heat-treated product (106 and 105 bacteria=ml)
on hydrogen production and symptoms of lactose intolerance in lactose malabsorbers.
Design: Double-blind, randomised cross-over design.
Setting: The study was performed in the phase 1 clinical unit of OPTIMED, Nancy, France.
Subjects: Twenty-four male lactose malabsorbers were selected for the study.
Interventions: Hydrogen production and adverse events were followed during 8 h after ingestion of the products.
Results: The results clearly demonstrate that ingestion of yoghurt with 108 bacteria=ml leads to lower H2 excretion
and complaints than the other products. Results observed with the products containing a reduced population of live
¯ora remain better than those observed with milk.
Conclusions: The importance of a high population of the live ¯ora is underlined.
Sponsorship: This work was supported by the `Mission Scienti®que de SYNDIFRAIS'.
Descriptors: dairy product; yoghurt; live ¯ora; lactose malabsorbtion; human
European Journal of Clinical Nutrition (2001) 55, 509±512
Introduction
Milk is an important source of calcium and of animal
proteins. In subjects who lack the ability to digest lactose
(lactose malabsorbers), milk consumption may result in
development of digestive discomfort symptoms (Bayless &
Rosenweig, 1966; Littman & Hammond, 1965). This may
lead them to spontaneously reduce their consumption of
milk and dairy products (Gilliland & Kim, 1984), thus
diminishing their calcium and protein intake. It is known
that the presence of a living ¯ora improves milk tolerance
in lactose poor digesters (Kolars et al, 1984; Savaiano et al,
1984; Dewitt et al, 1988). When yoghurt is heated before
consumption, the concentration of living bacteria
diminishes, depending on the conditions of heating. The
consequences of this treatment are unclear: the production
of hydrogen, which re¯ects the lactose maldigestion, is
either enhanced after thermisation (Gilliland & Kim, 1984;
Lerebours et al, 1989; McDonough et al, 1987) or
*Correspondence: X Pelletier, OPTIMED, 2 avenue de Vignate,
38610 GieÁres, France.
E-mail:
Guarantor: X Pelletier.
Contributors: S Laure-Boussuge and Y Donazzolo.
Received 22 February 2000; revised 7 December 2000;
accepted 11 December 2000
unchanged (Martini et al, 1987; Shermak et al, 1995;
Varela-Moreiras et al, 1992). This study was undertaken
to determine whether the extent of the thermisation might
explain those discrepancies and, more generally, to compare the responses to the ingestion of dairy products with
different living ¯ora contents in lactose malabsorbers.
Methods
This study was performed after submitting the protocol to
the Ethics Committee (Comite Consultatif pour la Protection des Personnes dans la Recherche MeÂdicale). Volunteers received written information and an oral presentation
of the study. They all gave their written informed consent
before the beginning of the study.
Subjects
Twenty-four male lactose malabsorbers were selected.
Subjects were 28.4 4.1 y old (range 21 ± 35), weighed
69.3 9.5 kg (56 ± 88), were 173.6 8.1 cm tall (159 ±
191) (means s.d.). Lactose malabsorption was con®rmed
after consuming 25 g lactose in 250 ml tap water. Hydrogen
concentration was determined in breath during 3 h following lactose ingestion. Subjects with a breath H2 increase of
more then 30 ppm over the basal value were considered
lactose malabsorbers.
Yoghurt and lactose malabsorption
X Pelletier et al
510
Products
Subjects then ingested ®ve dairy products according to
a double-blind randomised scheme. Products were: standard yoghurt (108 bacteria=ml); heat-treated yoghurt
(70 C30 s; 15 bacteria=ml); a geli®ed and acidi®ed milk
(no live ¯ora); and two fermented dairy products (106
bacteria=ml and 105 bacteria=ml), obtained by dilution
1=100 and 1=1000, respectively, of yoghurt (108 bacteria=ml) with the heat-treated yoghurt (15 bacteria=ml). All
products were processed from the same batch of milk by
CIRDC (Le Plessis-Robinson, France). Fermented products
were obtained after inoculation of Streptococcus thermophilus Lactobacillus bulgaricus starter culture (S85).
Both products obtained by dilution and heat-treated product
contained 0.54% gums to obtain the same texture as
yoghurt. Acidi®ed milk was obtained by addition of lactic
acid and Glucono-delta-lactone to a milk with 2.5% starch
to thicken it. The ®nal pH was 4.60. The lactose concentration and the number of living bacteria were checked
using standard procedures throughout the conservation of
the products and remained constant. The characteristics of
the products are listed in Table 1.
At each test, subjects received 25 g lactose in one of the
products. Hydrogen excretion was monitored before (T0)
and every 30 min during 8 h after administration of the
product, using an H2 monitor with electrochemical cell
Table 1
(GMI, UK). Adverse events, either spontaneously reported
or reported after interview, were thoroughly documented. A
3-day-or-more wash-out period was observed between two
administrations. Subjects excreting more than 25 ppm
hydrogen in breath under fasting conditions (T0) were
asked to undergo another test.
Statistical analysis
The analysis was performed on the following data, calculated for hydrogen concentration (ppm) in breath:
(1) AUCi, incremental area under the curve, calculated
in reference to the T0 value, expressed as ppm H2min;
(2) Cmax, maximal hydrogen concentration in ppm;
(3) Tmax, time of the maximal value, in min; (4) variation,
(Cmax 7 C0)100=C0. Results were analysed with a
two-way ANOVA. If ANOVA produced a statistically
signi®cant difference, products were compared with the
Bonferonni test. The frequency of the observed adverse
events has been compared using the w2 test.
Results
The evolution of hydrogen excretion upon ingestion of the
different products is described in Figure 1. The calculated
parameters are detailed in Table 2.
Characteristics of the products
Yoghurt: 108 bacteria=ml
Diluted product: 106 bacteria=ml
Diluted product: 105 bacteria=ml
Heat treated yoghurt: 15 bacteria=ml
Geli®ed milk: no live ¯ora
L. bulgaricus
(cell=ml)
S. thermophilus
(cell=ml)
Lactose
(%)
Dry matter
(%)
Fat
(%)
Total beta-galactosidase
(U=ml)
2.2108
2.7106
2.6105
< 15
Ð
6.6108
7.7106
7.2105
< 15
Ð
5.7
5.6
5.6
5.6
5.1
15.2
15.1
15.2
14.5
17.0
3.8
3.8
3.8
3.7
4.3
5.200 0.500
0.030 0.009
0.007 0.008
< 0.001
0
Figure 1 Evolution of H2 concentra (...truncated)