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INSERM U290, Hôpital St. Lazare, Paris, France and * Department of Biochemistry and Food Chemistry, University of Turku, Turku, Finland
ABSTRACT
INTRODUCTION
SUBJECTS AND METHODS
RESULTS
DISCUSSION
ACKNOWLEDGMENT
FOOTNOTES
LITERATURE CITED
ABSTRACT 
Lactose digestion improves when the energy content of a meal is raised, perhaps due to delayed gastric emptying; however, this has not been demonstrated directly. It is not known whether lactose-intolerant subjects should consume full-fat or high energy milk instead of half-skimmed milk. In this study, breath 13CO2 and hydrogen (H2) measurements were combined to assess simultaneously the effect of increasing milk energy content on gastric emptying, digestion, and tolerance of lactose. On two separate days, 11 adult lactose maldigesters ingested, in the fasting state, a single dose of 710 kJ half-skimmed milk or 1970 kJ high energy milk. Both contained 18 g lactose and were supplemented with 100 mg 13C-glycine for breath 13CO2 measurement. For 6 h after milk ingestion, samples of expired breath were collected, and subjects scored their symptoms on a four-grade questionnaire. Gastric emptying was measured from excretion of breath 13CO2. The mean gastric emptying half-time was significantly longer after ingestion of high energy milk than after half-skimmed milk (84 ± 4 vs. 64 ± 4 min, P = 0.004). The mean area under the breath H2 excretion curve measured for 6 h was 330 ± 61 µL/L after subjects consumed high energy milk vs. 470 ± 82 µL/L after they consumed half-skimmed milk (P = 0.07). Mean symptom scores did not differ after ingestion of the two milks, but only two subjects experienced disturbing symptoms after high energy milk ingestion compared with five subjects after ingestion of half-skimmed milk (P = 0.56). Although ingestion of high energy milk delayed the gastric emptying of lactose for significantly longer than the ingestion of half-skimmed milk (P < 0.01), it did not lead to significant improvement in symptoms and reflected only a trend toward improved lactose digestion (P = 0.07), as measured by the area under the breath H2 excretion curve. These results indicate that it is not beneficial for most lactose-intolerant subjects to replace consumption of half-skimmed milk by milk with a higher energy content.
KEY WORDS: lactose intolerance · gastric emptying · milk · energy content · humansINTRODUCTION
Most of the world's adult population exhibits partial lactose maldigestion as a result of the physiologic decline in intestinal lactase and may suffer from intolerance symptoms upon lactose ingestion (Suarez et al. 1995
). Theoretically, the following three mechanisms can improve this digestion: 1) stimulation of endogenous lactase, a mechanism that has not been shown to be relevant in humans, 2) the presence of exogenous lactase in the meal, and 3) slowed gastric emptying, which can be obtained by modifying the product consumed or by ingesting it with other food. An improvement in lactose digestion was demonstrated when lactose was ingested in milk instead of an aqueous solution (Solomons et al. 1979, Welsh et al. 1981), or when it was ingested with a meal, rather than with milk alone or in aqueous lactose solution (Martini and Savaiano 1988). In these situations, the improved digestion was thought to result from slowed gastric emptying due to the increased energy content of the meal, because energy content is an important factor in controlling gastric emptying (Brener et al. 1983, McHugh and Moran 1979, Moore et al. 1981). However, the results of previous studies have not demonstrated that the improvement was due to this mechanism. Nor do we know whether lactose-intolerant subjects should replace consumption of half-skimmed milk by full-fat or high energy milk. We therefore measured breath 13CO2 and hydrogen (H2) in lactose maldigesters to determine by a direct method whether raising the energy content of milk slows down its gastric emptying and enhances its tolerance.
SUBJECTS AND METHODS
).
Design.
Breath 13CO2 and breath H2 were each measured after ingestion of a high energy milk and 1-3 wk later, after ingestion of half-skimmed milk. The tests began at 0800 h after an overnight fast and lasted for 6 h. Subjects refrained from eating, smoking and physical activity during this period. They were allowed to drink a little water (<100 mL/6 h). They scored their gastrointestinal symptoms hourly, including abdominal bloating and pain, flatulence, loose stools and borborygmi with the use of a questionnaire comprising four grades: 0, no symptoms; 1, not disturbing; 2, disturbing; and 3, intolerable. For breath H2 measurement, end alveolar breath samples were collected in air-tight syringes via a modified Haldane-Priestley tube in the fasting state and every 30 min for 6 h after ingestion of the test milk. For determination of breath 13CO2, subjects blew into 250-mL aluminium-coated bags (Quintron, Milwaukee, WI) in the fasting state and every 15 min for 4 h after test milk ingestion. Test milks were consumed in <5 min, usually within 1 min. The study was approved by the Ethics Committee of the Lariboisière Saint-Louis Medical University. All subjects gave informed written consent to participate.
Test meals.
The first test meal consisted of 500 mL of high energy milk containing 1970 kJ (Nutriset, Malaunay, France); the second consisted of 375 mL of sterilized 50%-skimmed milk (Bonmanoir, Leader Price, France), which provided 710 kJ. Composition of the test meals is shown in Table 1. Each test milk provided 18 g lactose. For breath 13CO2 measurement, 100 mg of 13C-glycine (99 AP, Euriso-top, Saint Aubin, France) was carefully stirred into the milks.
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Table 1. Composition and characteristics of the test milks |
). Orocecal transit time (OCTT)4 was determined as the interval between ingestion and a sustained rise of 5 µL/L or more in breath H2. The area under the curve for breath H2 excretion (AUCH2) was calculated according to Solomons et al. (1977). A global measure of the severity of symptoms was defined by computing the sum of the symptom scores.
. CO2 production was assumed to be 300 mmol/(m body surface2··h), and the body surface area was calculated by using the formula of Haycock et al. (1978). Using least-square algorithms, the curves for the percentage of 13C recovery were fitted to the following two formulas: 1) %13C dose/h = atbe
ct and 2) %13C cumulative dose = m(1
ekt)
where %13C dose/h is the percentage of the administered dose of 13C recovered in breath per hour, %13C cumulative dose is the cumulative percentage of this dose recovered in breath over time (t), and a, b, c, m, k and 
are constants determined by nonlinear regression analysis. From the constants obtained, three parameters describing gastric emptying were calculated: gastric emptying half-time (T1/2) = (1/k)ln(1 21/), time of maximal 13CO2 excretion (Tmax) = ln()/k, which corresponds to maximal gastric emptying, and the gastric emptying coefficient (GEC) = ln a (Maes et al. 1994). T1/2 was corrected, taking into account the 70 min required for the absorption, metabolism and excretion of 13C (Maes et al. 1994).
). Differences were considered significant when P < 0.05.
RESULTS
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Table 2. Parameters describing gastric emptying and lactose digestion after ingestion of the two test milks by lactose maldigesters1,2 |
Table 3.
The individual maximum symptom scores for each gastrointestinal symptom reported during the 6 h after ingestion of two test milks by lactose maldigesters1,2
DISCUSSION 
Fig. 3.
Correlations between the area under the curve for H2 excretion (AUCH2), gastric emptying half-time (T1/2), and orocecal transit time (OCTT) in 10 lactose maldigesters after ingestion of half-skimmed milk and high energy milk. Hydrogen was measured for 6 h; T1/2 and OCTT were determined as described in Subjects and Methods.
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0.62 , P = 0.06).
, Rehrer et al. 1992). Measurement of both breath 13CO2 and H2 provided information on the relationship between the gastric emptying rate of lactose and its digestion and tolerance.
, McHugh and Moran 1979, Moore et al. 1981). Despite the difference in gastric emptying after ingestion of the two milks, no significant difference was seen in the tolerance of lactose. The excretion of breath H2 reflected a trend toward better digestion of lactose because breath H2 tended to be lower after ingestion of high energy than half-skimmed milk (P = 0.07). Demonstration of a significant difference in production was calculated to require at least 10 subjects. The 6-h collection period of breath H2 might not have been long enough with high energy milk because it was not clear whether the time of peak H2 excretion had passed. In future studies, a longer collection period is proposed when a meal that provides more than 1000 kJ is used.
, Szilagyi et al. 1996). However, this was not observed in all studies (Roggero et al. 1985). Interestingly, Szilagyi et al. (1996) recently reported that the slowing down of OCTT by loperamide was associated with less severe symptoms of lactose intolerance, which seems to argue in favor of a direct link between motility and symptoms.
, Villako and Maaroos 1995), although this has been demonstrated in only one study (Leichter 1973). This author reported an improved digestion and tolerance of full-fat milk and suggested that this might be due to delayed gastric emptying. However, the study included no comparison of symptoms by statistical analyses, and only the rise in blood glucose after a lactose challenge was used to measure lactose maldigestion (Brummer et al. 1993). Other investigators failed to confirm any improvement in symptoms after ingestion of full-fat milk compared with fat-free milk (Cavalli-Sforza and Strata 1986, Dehkordi et al. 1995, Jones et al. 1976) or to an aqueous lactose solution (Solomons et al. 1980). Even a marked difference in the fat content of milk (0 vs. 8%) did not affect the symptom response of lactose maldigesters (Vesa et al. 1997).
ACKNOWLEDGMENT
FOOTNOTES
Manuscript received 28 February 1997. Initial reviews completed 25 April 1997. Revision accepted 4 August 1997.
LITERATURE CITED
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