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INTRODUCTION |
The gastrointestinal response to polyol ingestion includes a laxation effect and is accompanied by an increase in colonic fermentation and breath hydrogen excretion. However, most studies have involved ingestion of pure polyol or polyol solutions and few have dealt with the ingestion of polyol used as a bulk sweetener in confectionery items. This study was conducted to investigate the gastrointestinal events that occur when the polyol maltitol is ingested after its incorporation at different levels into milk chocolate.
Ingested sucrose contributes to the glycemic index and it is also generally considered to be cariogenic. The development of non-sugar confectionery (i.e., with no added sugar) provides an alternative product of similar texture and taste that addresses both of these phenomena and thus is suitable for diabetics and/or persons anxious about dental caries. Replacement of sucrose by polyols such as maltitol is well documented (Zumbe et al. 1994
). On the basis of its technological and organoleptic qualities, high purity, crystalline D-maltitol (such as maltisorb; Roquette Freres, Lestrem, France) is an excellent substitute for sucrose in products such as non-sugar chocolate (Le Bot 1993, Oliger 1994, Rapaille et al. 1994, Sicard and Le Bot 1994). In fact, non-sugar milk chocolate contains 40-45% maltitol (Zumbe et al. 1994).
D-Maltitol (4-O-
-D-glucopyranosyl-D-sorbitol) is a widely used sweetening agent because of its physicochemical properties, natural sweetening power (80% that of glucose; Sicard and Le Bot 1994) and low cariogenicity. It is the alcohol of the disaccharide maltose and is prepared in a pure state by hydrogenation of 
-D-maltose over Raney nickel; upon hydrolysis, maltitol yields equimolar amounts of sorbitol and glucose. In humans, maltitol causes a lower rise in blood glucose and insulin levels than a corresponding dose of glucose or sucrose (Felber et al. 1987) and is thus suitable for use as a sweetening agent in diabetic food.
In healthy humans, partial hydrolysis of most polyols (sugar alcohols) occurs in the small intestine, but absorption is incomplete and a mixture of hydrolysates and undigested polyol contribute to a carbohydrate pool that is available for bacterial fermentation in the colon (Billaux et al. 1991, Livesey 1992). The ingestion of polyols is associated with increased levels of colonic fermentation and with a dose-dependent increase in gastrointestinal symptomatology including colic, flatus and borborygmi (Koutsou et al. 1996). If the fermentative capacity of the colon is exceeded, osmotic diarrhea occurs (Hammer et al. 1989, Rambaud and Flourie 1994, Saunders and Wiggins 1981).
Disaccharide alcohols require hydrolysis before absorption, and maltitol is cleaved slowly by enzymes of the small intestine brush border (Lian-Loh et al. 1982, Rosiers et al. 1985, Wursch and Del Vedovo 1981, Wursch et al. 1990, Ziesenitz and Siebert 1987), in particular by -glycosidases (Zunft et al. 1983). In vitro enzymatic hydrolysis of maltitol is 10% that of maltose (Dahlqvist and Telenius 1965, Nilsson and Jagerstad 1987) and results in unhydrolyzed polyol, together with unabsorbed hydrolysates such as sorbitol, reaching the large intestine. These, along with other undigested material, are available for metabolism by the colonic bacteria (Beaugerie et al. 1990, Wursch et al. 1989). The products of this fermentation are H2, CO2, CH4 (in methanogenic individuals) and short-chain fatty acids. Studies on the metabolic fate of ingested [U14C]-maltitol (Oku et al. 1991) demonstrated detectable breath hydrogen responses 1 h after consumption, with a peak at 3.5 h. On the basis of their observations, Oku et al. (1991) concluded that a major portion of ingested maltitol escapes ileal digestion and absorption, leading to subsequent colonic fermentation. However, it is worthy of note that maltitol may also competitively inhibit the hydrolysis of maltose (Nilsson and Jagerstad 1987, Yoshizawa et al. 1975).
Few data exist in the public domain concerning the gastrointestinal consequences of ingesting maltitol incorporated into confectionery products. This study investigated gastrointestinal tolerance and breath hydrogen excretion after ingestion of two doses of crystalline maltitol incorporated into milk chocolate with the aim of determining whether adverse symptomatology occurs and whether it is dose related.
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SUBJECTS AND METHODS |
Subjects.
Subjects were volunteers to whom the purpose and nature of the studies had been explained and who gave written consent and were remunerated for their participation in the study. Ethical approval was provided by the University of Salford Occupational Health and Hygiene Service.
Twenty subjects were recruited at random from members of the student population of The University of Salford who responded to publicity notices posted on campus. There were 9 men and 11 women between the ages of 18 and 24 y with body mass indices (mean ± SD) of 25.1 ± 3.9 kg/m2 (men) and 22.0 ± 1.2 kg/m2 (women). To minimize transfer of information among participants, potential subjects who were close friends, who lived in the same accommodation or who were in class together were excluded.
Individual prescreening of potential volunteers ensured that none had been previously adapted to maltitol, that they had no history of either gastrointestinal or metabolic disease and were not subject to any dietary restrictions, prescribed diets or supplementary fiber intake. It also ensured that they had not received antibiotics, steroids, laxatives or any other drugs for 1 mo before the study. These exclusions were applied to the 6-wk study period, but the taking of oral contraceptives was not prohibited. Any medication prescribed during the study was to be reported to enable assessment of subjects' suitability for continued participation; no reports of this nature were made by the subjects.
Subjects were told that they were free to leave the study at any time but that if they did so, they would be questioned to determine the reason for their leaving. No such withdrawals occurred.
Test materials.
Test products were identical except for their added carbohydrate ingredient and were supplied by Roquette Freres AG as 100-g bars of milk chocolate with identical appearance and packaging. Each 100-g bar contained 40 g bulk sweetener as either sucrose (S), maltitol (M) (4-O--D-glucopyranosyl-D-sorbitol) or sucrose and maltitol (SM, 10:30 wt/wt). Sweetness levels were not adjusted by addition of intense sweetener. Bars had identical wrappers, which were distinguished by codes that were not revealed to the investigators until after the completion of the study.
Study design and restrictions.
In this double-blind, controlled, crossover study, subjects were tested twice with each product in randomized order determined by a Latin square design applied to each leg of the crossover study. The crossover related to consumption in fasting and nonfasting conditions. After an introductory interview, 10 subjects were randomly assigned to one group in which S, SM and M were consumed during wk 1-3 while fasting and again during wk 4-6 while not fasting. The other crossover group of 10 subjects first consumed the products while not fasting and later while fasting. Consumption days were separated by periods of 1 wk.
For 12 h before the test day, the 24 h of the test day and for 12 h thereafter, all subjects agreed to restrict their intake of milk and fruit juice to 300 mL each per 24 h and to refrain totally from drinking alcohol. Fasting subjects were instructed not to consume any food or liquid after 2200 h on the night before the chocolate consumption day and to consume the test product as breakfast. Subjects were allowed to drink up to 200 mL of liquid to facilitate consumption; a normal meal pattern was resumed at noon on the day of consumption. Nonfasting subjects consumed products within 30 min of the completion of their normal breakfast. Both groups were instructed to eat the entire 100 g of chocolate within 30 min.
Interview protocol.
Only after successful prescreening were subjects given additional information concerning the study. This consisted of a formal invitation on a printed sheet, which also explained briefly the perceived advantages of polyols incorporated into confectionery items, but did not mention potential gastrointestinal symptomatologies including laxation. Maltitol was not specifically named as a polyol. All trial restrictions and conditions were then explained verbally as was the need for confidentiality to prevent transfer of information among participants.
The time of product consumption was recorded on printed sheets by both fasting and nonfasting subjects. They also kept and returned dietary diaries listing all foods and beverages consumed in the evening before the test day, at breakfast in nonfasting subjects and in all subsequent meals on the test day. These diaries were not analyzed in detail but were checked for adherence to dietary restrictions.
On the day after consumption of each product, participants were individually debriefed according to a set protocol to determine if they had adhered to the dietary restrictions and consumption regimen. They were then questioned about their recorded gastrointestinal symptomatology as well as sensorial and textural data, the latter being included so that subjects' attention was not focused on gastrointestinal symptoms.
Gastrointestinal symptoms.
Gastrointestinal symptoms and laxation were recorded for the 24-h period after consumption of each product. At the postconsumption interviews, participants were questioned about information that they had recorded on the printed sheets concerning the separate sensations of borborygmi, colic and flatus. These symptoms were described to the subjects as follows: borborygmi were rumbling noises from the abdominal area, colic was pain experienced in the abdominal area and flatus was the expulsion of gases through the anus. Subjects were asked to describe the degree of symptoms they had experienced. From these answers, each symptom was ranked on a hedonic scale in which 0 indicated normal function, 1 indicated mild symptoms, 2 indicated moderate symptoms and 3 indicated severe symptoms. The number of toilet visits made during the 24-h period after consumption was recorded and the consistency of feces passed on each occasion classified as either watery, normal or hard. Because subjects were not monitored during toilet visits, information relating to fecal volume was not determined.
Breath hydrogen measurement.
In a separate experiment, 10 non-adapted (did not regularly consume polyol), fasting subjects were tested with each chocolate product in a random order with tests separated by 1 wk. None of these subjects had taken part in the previous study. There were five men and five women between the ages of 18 and 24 y, with body mass indices (mean ± SD) of 22.8 ± 2.0 kg/m2 (men) and 22.3 ± 1.3 kg/m2 (women). Test products were consumed within 30 min immediately before breath testing; the positive control was a 20-mL dose of lactulose syrup (0.67 kg/L; Duphar Laboratories, Southampton, Hampshire, UK) given in 250 g of mushroom soup, i.e., a total dose of 13.4 g lactulose. The negative control was a test period during which no product was consumed. The method of hydrogen breath testing was as described by Lee et al. (1994). Comparisons were not made between means at each sampling point for each consumption regimen, but the total breath H2 excretion, (0-6 h) was derived by integration of the total area under each breath H2 curve.
Statistics.
Subjects' responses relating to symptomatology were categorical (yes/no), and intolerance data were considered to be nonparametric. Products S, SM and M were compared by contingency table analysis using 2 × 2 and 4 × 4 transition tables and analyzed by chi-square tests. The first method used the formula of McNemar (1947) to test for any difference between products without taking into account product order; the binomial test was used when four subjects reported symptoms or when the expected frequency in each cell of the contingency table was <5. The order of product presentation and thus the efficacy of the crossover design itself was tested using the method of Gart (1969). In each case a probability (P) of <0.05 indicated a significant difference in symptomatology between products, i.e., 1) symptomatology is different between products; 2) symptomatology depends on product presentation order. The 4 × 4 transition table analysis was used to test differences in the severity of symptoms reported.
Differences between subjects in the frequency of passing feces were assumed to be parametric and were analyzed after one-way ANOVA by paired t tests. Breath hydrogen measurements were also considered to be parametric and, an ANOVA was conducted after transformation using log10 to test for significant differences between product and subject groups; breath H2 excretion between 0 and 6 hours was compared using paired Student's t tests.
Apart from the body mass indices given above, all means are given with the SEM.
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RESULTS |
The McNemar and Gart tests demonstrated that there was no significant difference (n = 20, P > 0.05) in reported symptomatology between fasting and nonfasting periods (Table 1). Furthermore, there was no significant difference (P > 0.05) between fasting and nonfasting periods according to whether the polyol-containing chocolate products were eaten first or second. Because each subject ingested each product twice (once fasting and once nonfasting), further statistical evaluations considered product differences in terms of data sets in which n = 40 (Table 2). The ranking of positive symptoms as either mild, moderate or severe was considered by using 4 × 4 transition tables, which revealed that there was no significant increase in severe or moderate symptomatology of any description in relation to an increased intake of maltitol (P > 0.05).
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Table 1.
Intolerance symptoms in 20 human subjects after ingestion of 100 g chocolate containing 40 g sucrose, 10 g sucrose + 30 g maltitol or 40 g maltitol while fasting and not fasting1-4
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Table 2.
Intolerance symptoms in 20 human subjects after ingestion of 100 g chocolate containing 40 g sucrose, 10 g sucrose + 30 g maltitol or 40 g maltitol1
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Although ingestion of 40 g maltitol in chocolate resulted in significantly more borborygmi (P < 0.05) and flatus (P < 0.01) compared with those after consumption of chocolate containing sucrose only, in both cases these symptoms were ranked by subjects as only mild. No other significant differences in symptomatology were revealed (Table 2). Most subjects visited the toilet to pass feces on only one occasion during the postconsumption period, and the number of toilet visits made was not significantly different after ingestion of either 30 g maltitol (P = 0.07) or 40 g maltitol (P = 0.07) compared with 40 g sucrose. Similarly, most subjects passed normal feces; no one passed loose feces on more than one occasion after consumption of any of the products tested.
There was evidence that when mild symptomatology did occur, subjects tended to experience a grouping of symptoms that was significant at the 1% level; 18 subjects reported multiple symptomatology after consumption of 40 g maltitol compared with 7 subjects after 30 g maltitol and 3 subjects after sucrose (P < 0.01). A mean symptom score was derived by assigning a value of 0, 1, 2 or 3 to each symptom recorded, according to the hedonic scale outlined earlier; in relation to frequency of loose feces passed, loose feces passed on one occasion scored 1, on two occasions scored 2 and on 3 or more occasions scored 3. The mean symptom score for all individuals was positively correlated (r = 0.667, P < 0.01) with the dose of maltitol ingested. There was a significant increase in symptomatology with 40 g maltitol compared with 30 g maltitol (P < 0.05) and sucrose (P < 0.01), but there was no significant difference in symptomatology between sucrose and 30 g maltitol (P = 0.20) (Fig. 1).
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| Fig 1.
Symptom scores for 20 human subjects after ingestion of 100 g chocolate containing 0, 30 or 40 g maltitol. Values are arithmetic means ± SEM. (The maximum possible score was 12; a score of 1 would mean that on average subjects suffered 1 mild symptom on 1 occasion). Bars without common letters were different (P < 0.05).
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Some time after polyol consumption there was a sharp rise in breath H2 concentrations (defined as an increase > 5 µmol/L). This marked the beginning of colonic fermentation, effectively the orocecal transit time. This was calculated as 115.5 ± 18.7 min after consumption of 30 g maltitol and 87.0 ± 14.3 min after consumption of 40 g maltitol. From the shape of the curves in Figure 2, it is clear that consumption of 40 g maltitol provoked the greatest H2 response followed by, in descending order, 13.4 g lactulose, 30 g maltitol, sucrose and no product. The total breath H2 excretion was significantly greater after the ingestion of 30 g maltitol (P < 0.05) and 40 g maltitol (P < 0.01) compared with sucrose and no product (Fig. 3). Ingestion of 40 g maltitol in chocolate led to a greater total breath H2 excretion compared with that after eating chocolate containing either 30 g maltitol (P < 0.05) or sucrose (P < 0.01).
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| Fig 2.
Breath hydrogen concentration in humans after ingestion of no product or 100 g chocolate containing 40 g sucrose, 10 g sucrose + 30 g maltitol, 40 g maltitol or a control meal containing 13.4 g lactulose. Values are arithmetic means ± SEM, n = 10.
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| Fig 3.
Area under breath hydrogen curve [cumulative breath hydrogen, mmol/(L·6 h)] of humans after ingestion of no product or 100 g chocolate containing 40 g sucrose, 10 g sucrose + 30 g maltitol, 40 g maltitol or a control meal containing 13.4 g lactulose. Values are arithmetic means ± SEM, n = 10. Bars without common letters were different (P < 0.05).
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The total breath H2 excretion after lactulose was 183 ± 40 µmol/L. Assuming breath hydrogen after ingestion of 13.4 g lactulose to be 100%, on average, 34.7% (10.4 ± 1.4 µmol/L) of a 30-g ingested dose of maltitol was fermented in the colon. Similarly, an average of 49.2% (19.7 ± 4.0 µmol/L) of a 40-g ingested dose of maltitol was fermented in the colon.
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DISCUSSION |
This study demonstrated that an acute oral intake of 30 g crystalline maltitol in milk chocolate resulted in no marked increase in adverse symptoms, an observation that has major implications for manufacturers of confectionery products. Our results are consistent with those of Abraham et al. (1981) and Beaugerie et al. (1991) who demonstrated that a 20- to 30-g dose of maltitol syrup could be well tolerated without undesirable symptoms.
Although ingestion of 40 g maltitol in chocolate resulted in significantly more borborygmi (P < 0.05) and flatus (P < 0.01) compared with that after consumption of chocolate containing sucrose, these symptoms were ranked as mild in both cases. Colic and loose feces, potentially more distressing symptoms, were uncommon even at the higher dose of 40 g maltitol, and the incidence was not significantly higher than after consumption of the 30 g maltitol or sucrose-containing chocolate. Ingestion of 30 g (P = 0.55) or 40 g (P = 0.24) maltitol did not cause any significant increase in laxation; nine subjects passed loose feces on one occasion after eating 40 g maltitol but this was not significantly greater than after consumption of 30 g maltitol (four subjects) or 40 g sucrose (six subjects). These results indicate that the colonic fermentative capacity had not been exceeded in these subjects. Therefore, we can report from this study of 20 healthy individuals that crystalline maltitol consumed in milk chocolate did not have a significant laxative effect when ingested at either 30 or 40 g/d. The relatively small total breath H2 excretion after consumption of 30 g maltitol is suggestive of a low level of intestinal fermentation, which is consistent with the low level of symptomatology reported after consumption of chocolate containing this amount of polyol.
Despite this overall low level of symptomatology in relation to individual side effects, significantly more subjects experienced multiple symptomatology after consumption of maltitol compared with sucrose (P < 0.01). This may be due in part to intersubject variations in symptom perception and description, but there is little doubt that some individuals appear to be more susceptible than others to the consequences of incompletely hydrolyzed maltitol and unabsorbed sorbitol in the small intestine and its eventual entry into and fermentation in the large intestine (Dahlqvist and Telenius 1965, Nilsson and Jagerstad 1987). McBurney (1991) showed that starch malabsorption is lower during the luteal phase of the menstrual cycle compared with the follicular phase. The menstrual cycle of the 11 women taking part in this study was not controlled; thus a type II statistical error might exist in our comparisons between sweeteners. However, the women in the study were examined over 6-wk time scales, which would have included more than one luteal phase. The nine men would not, of course, have been subject to any such malabsorption of starch.
No significant differences in symptomatology occurred between fasting and non-fasting periods (P > 0.05), although 14 subjects reported flatus after consumption of chocolate containing 40 g maltitol after fasting versus 9 subjects when they were not fasting. These results suggest that symptomatology arising from maltitol consumption is very low and is comparable in subjects when fasting and nonfasting, indicating that consumption of other foodstuffs together with maltitol had little effect on the gastrointestinal tolerance of this polyol. It seems that a partitioning of unhydrolyzed maltitol and unabsorbed sorbitol may have occurred during both fasting and nonfasting, leading to a similar, gradual delivery of such molecules to the large intestine, a consideration of some importance in relation to the propensity of consumers to eat confectionery items as intermeal snacks.
Notwithstanding these data relating to symptomatology, it is apparent that, compared with 40 g sucrose, the ingestion of 30 g maltitol (P < 0.05) or 40 g maltitol (P < 0.01) led to a significant, dose-related increase in total breath H2 excretion. No direct information was obtained in this study concerning either the extent of upper intestinal hydrolysis of maltitol or the stoichiometry of H2 production in vivo (Livesey et al. 1993). Despite this lack of comparative stoichiometric data, the use of lactulose fermentation as a reference point has allowed maltitol hydrolysis and constituent sugar absorption to be estimated as 65.3% of the 30 g dose and 50.8% of the 40 g dose, results that are in broad agreement with the 50% malabsorption of maltitol reported by Beaugerie et al. (1991) and Wursch et al. (1989).
Therefore, this study has confirmed that the ingestion of milk chocolate containing maltitol leads to an elevated breath H2 response compared with that after the consumption of milk chocolate containing only sucrose, a difference that is significant at the 1% level and is indicative of a greater degree of intestinal gaseousness due to bacterial fermentation of maltitol and sorbitol. The breath H2 response was also dose related, which is consistent with the lower reported symptomatology after ingestion of 30 g maltitol compared with 40 g maltitol.
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ACKNOWLEDGMENT |
The authors gratefully acknowledge Philip Scarf, Department of Mathematics and Computer Science, University of Salford for expert assistance in the statistical analysis of data.
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Abstract
Introduction
Abstract
Towards the Year 2000 (Rugg-Gunn, A. J., ed.), pp. 112-135. The Royal Society of Chemistry, Cambridge, UK.
