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Diagnosis, Symptoms, and Calcium Intakes of Individuals with Self-Reported Lactose Intolerance

University of British Columbia, Vancouver, British Columbia, CANADA

Address reprint requests to: Susan I. Barr, PhD, RDN, Professor of Nutrition, University of British Columbia, 2205 East Mall, Vancouver, B.C., CANADA V6T 1Z4. E-mail: sibarr{at}interchange.ubc.ca

	ABSTRACT

TOP FOOTNOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION ACKNOWLEDGMENTS REFERENCES

 
Objective: To determine methods of diagnosis, symptoms, and calcium intake from food and supplements for individuals with self-reported lactose intolerance.

Methods/Design: Cross-sectional survey using a mailed questionnaire.

Subjects/Setting: A convenience sample of 189 adults with self-reported lactose intolerance living in the metropolitan area of Vancouver Canada responded to posters or advertisements, and 159 returned completed questionnaires.

Measures of Outcome: Methods of diagnosis, symptoms experienced and their severity were self-reported. Estimated calcium intake from food and supplements was assessed using a food frequency questionnaire. Data were analyzed using descriptive statistics, chi-square, Pearson correlation analysis, t-tests and Analysis of Variance.

Results: Participants were 47 ± 15 years of age; 72% female and 28% male; 67% Caucasian; and 54% had self-diagnosed their lactose intolerance. Of the 42% diagnosed by a physician, only 10% had been diagnosed by valid tests. Mean estimated food calcium intake was 591 ± 382 mg/d and did not differ between those who were self- or physician-diagnosed. Only 11.5% of participants met their age-appropriate Adequate Intake (AI) from food calcium sources alone. Calcium supplements were used by 65% and provided an average of 746 ± 703 mg calcium/day to those who used them; mean intakes of this group met the AI.

Conclusions: Calcium intake from food sources alone is inadequate to meet the AI in individuals with self-reported lactose intolerance. Physicians managing lactose intolerance need current information on how the AI can be met through appropriate food choices and possible supplementation.

Key words: dietary supplements, lactose intolerance, dietary calcium, survey

Abbreviations: AI = adequate intake • ANOVA = analysis of variance • BCNS = British Columbia Nutrition Survey • DRI = dietary reference intake • FFQ = food frequency questionnaire • UL = tolerable upper intake level

	INTRODUCTION

TOP FOOTNOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION ACKNOWLEDGMENTS REFERENCES

 
Despite a wealth of research conducted since the 1970s [1–17], misperceptions about lactose intolerance are prevalent [18]. There is little understanding that lactose maldigestion (incomplete lactose digestion due to low levels of ß-galactosidase) is not synonymous with lactose intolerance (symptoms such as bloating, cramps and diarrhea that may or may not occur in association with undigested lactose in the intestinal tract). Many studies have identified that the majority of those with lactose maldigestion do not experience the symptoms of lactose intolerance after consuming moderate quantities of lactose [4,6,8,10,15,16,19–23]. For example, in a randomized double-blind trial among individuals who believed they were severely lactose intolerant, participants consumed 8oz of trial milk (lactose-free and lactose containing milk) daily at breakfast for one week. No significant difference in response between lactose-free and lactose containing milk (12g) was observed for symptoms including bloating, flatus and abdominal pain [23].

In addition to the findings that many lactose maldigesters do not experience symptoms of lactose intolerance following mod-erate lactose loads, substantial proportions (up to 62%) of those who believe they are lactose intolerant actually digest lactose normally [1,4,6,21,24,25]. While symptoms such as diarrhea, bloating and flatulence can occur as a result of lactose maldigestion, they are not specific to lactose maldigestion and may also be experienced after ingestion of other foods.

Less research has assessed how individuals with self-reported lactose intolerance decide that they are lactose intolerant: Specifically, few data exist on diagnostic procedures used in a community setting, and the prevalence of self-diagnosis. In addition, few data are available on how the perception of having lactose intolerance alters intake of milk and dairy products. Irrespective of whether those who believe they are lactose intolerant actually experience symptoms when tested under blinded conditions, perceived lactose intolerance may be just as important as true lactose intolerance since ensuing dietary changes may compromise calcium intake.

Accordingly, the purpose of this study was to obtain descriptive data on adults with self-reported lactose intolerance. The specific aims were to assess how the diagnosis had been made, the symptoms experienced and their severity, and calcium intake from foods and supplements.

	MATERIALS AND METHODS

TOP FOOTNOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION ACKNOWLEDGMENTS REFERENCES

 
The study used an exploratory survey design administered to a convenience sample of self-selected study participants. Participants were recruited from the metropolitan Vancouver area using recruitment posters and advertisements in community newspapers. Inclusion criteria were self-reported lactose intolerance, being 19 years of age, and ability to read English. Upon seeing an advertisement, potential participants contacted one of the investigators by telephone. Eligibility was confirmed (those with secondary lactose intolerance due to Crohn’s or celiac disease were excluded) and eligible interested participants were sent a questionnaire package and a stamped addressed envelope for return. A follow-up mailing was sent to those who did not return their questionnaire after three weeks, and a second follow-up (including another questionnaire) was sent three weeks later. The University’s Behavioral Research Ethics Board approved the study protocol.

Questionnaire
A questionnaire was developed to collect data for this study. Questions to elicit method of diagnosis, symptom severity, and foods that induce symptoms were included. To determine diagnosis, participants were asked whether they had diagnosed themselves, or whether a physician or other health-care practitioner made the diagnosis. Those who were diagnosed by a physician were asked to specify any diagnostic tests used. Symptom severity was queried by asking participants to indicate whether their global symptoms following consumption of one cup of milk (any fat content) with a meal were severe, somewhat severe, moderate, somewhat mild or mild. An open-ended question asked participants to list the symptoms of lactose intolerance they experienced. Participants were asked to indicate whether or not they experienced symptoms when consuming a variety of lactose-containing foods; however, severity of symptoms and type of symptom experienced in relation to specific food consumption were not assessed.

A food frequency questionnaire (FFQ) was used to assess food calcium intake over the past month, and included questions regarding calcium supplement use. The FFQ was modified from an educational tool designed to estimate the previous day’s calcium intake [26]. It included commonly-consumed plant and dairy source of calcium, as well as calcium-fortified beverages. The instrument was validated by comparing intakes assessed using the FFQ and a three day food record in a sample of 42 adults. Calcium intakes assessed by the two methods were correlated (Spearman’s correlation coefficient = 0.74, p < 0.01), although mean intakes from the three day food record were approximately 100 mg/d higher than those estimated with the FFQ (926 ± 353 mg/d vs. 825 ± 397 mg/d, p < 0.05) [S.E. Hogan and J. Pilgrim, personal communication].

The entire data collection instrument was pre-tested for clarity by 12 individuals with self-reported lactose intolerance, who also completed it two weeks later to assess test-retest reliability. Pearson product-moment correlations were used to assess reliability. Severity of symptoms assessed by the questionnaire were reliable (r = 0.98, p < 0.01). Similarly, open-ended responses listing participant symptoms of lactose intolerance, and involvement of a physician in diagnosis of lactose intolerance were reliable (r = 1.0, p < 0.01 and r = 0.90, p < 0.01, respectively). Calcium intake assessed by the FFQ was reliable (r = 0.97, p < 0.01). Furthermore, total intake of calcium from supplements was reliable (r = 0.93, p < 0.01).

Statistical Analyses Performed
Data were entered into a database and verified for accuracy. Descriptive statistics were calculated to provide information on participants’ mean calcium intake. Analysis of Variance (ANOVA) was used to assess whether differences in calcium intake existed between gender or age groups, and t-tests were used for comparisons between two groups. Chi-square was used to assess differences in proportions, and Pearson correlation analysis was used to assess relationships between continuous variables. All analyses were two-tailed and conducted at a significance level of p < 0.05.

	RESULTS

TOP FOOTNOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION ACKNOWLEDGMENTS REFERENCES

 
Participants
The survey was distributed to 189 participants who responded to advertisements. Twenty-four did not return the survey, and six participants returned it too late to be included in the analysis. Thus, data are based on responses of 159 individuals (completion rate = 84.1%). The sample included 44 (27.7%) men and 115 (72.3%) women, who were 47 ± 15 years of age (range = 19–87). Mean age did not differ by gender, averaging 47 ± 16 years and 46 ± 13 years for women and men, respectively. Most (67%) were Caucasian; other major ethnic groups were Asian and South Asian. Participants were grouped into age categories using the Dietary Reference Intake (DRI) age groupings [27]; the distribution of participants in each age group did not differ by gender.

Diagnosis
Over half the participants (n = 85, 53.8%) self-diagnosed their lactose intolerance, and a physician diagnosed 42% (n = 67). Only 4% were diagnosed by a dietitian, homeopath or naturopath. There were no differences between self- and physician-diagnosed individuals in terms of gender (71% vs. 72% female, respectively; ² = 0.12, p = 0.73), age (45.5 vs. 48.0 years; t = –1.0, p = 0.32), or ethnicity (59 vs. 71% Caucasian; ² = 2.1; p = 0.15). For the participants who were diagnosed by a physician, 76.1% (n = 51/67) of their physicians used a description of symptoms as a diagnostic tool. Other tests (in some cases, in addition to symptom description) were used by 29.9% (n = 20/67) of physicians and included food and symptom diaries, elimination diets, and elimination and challenge trials. Only 10.4% (n = 7) of physician-diagnosed participants had confirmable diagnoses with blood glucose measurements following a lactose load (lactose tolerance test). The hydrogen breath test was not used.

Symptoms
When consuming one cup of milk with a meal, 69% reported severe or somewhat severe symptoms, 21% reported moderate symptoms and 10% reported somewhat mild or mild symptoms. These proportions did not differ significantly between self- and physician-diagnosed participants. More than half the participants reported abdominal distension, diarrhea and gas/flatulence as symptoms of lactose intolerance, as shown in Table 1. Gastrointestinal noise was the least frequently mentioned symptom. Non-associated symptoms are symptoms reported by participants that are not established as diagnostic criteria. Non-associated symptoms were reported by more than a quarter of respondents, and included migraines, thickened mucous and insomnia. Other symptoms included vomiting and nausea. Similar proportions of self- and physician-diagnosed individuals reported all symptoms, with the exception of gas/flatulence, which was reported by more self- than physician-diagnosed individuals (72% vs. 54%, ² = 5.3, p = <0.05).

Estimated Total Calcium Intake.
Total calcium intake from combined food and supplementary calcium sources was estimated for the 52 participants who provided complete information on supplement use and complete data for the FFQ. Among this group, mean total calcium intake was 1313 ± 711 mg/d, and was significantly higher than calcium intake from food sources alone (p < 0.001). Mean calcium intakes met the AI, and 32 participants (61.5%) met the AI appropriate to their age. However, five (10%) had total calcium intakes in excess of the tolerable upper intake level (UL) of 2500 mg/d [27].

Intake of Self- versus Physician-Diagnosed Participants.
Table 4 presents patterns of calcium intake from food alone, supplements alone, and combined food and supplements among self- versus physician-diagnosed participants. Among this group with complete data on supplemental calcium intake, similar proportions of self- and physician-diagnosed participants consumed calcium supplements (50% and 47%, respectively). This was also the case when supplement use among the entire group was compared. Calcium intakes from food, supplements, or the combination of food plus supplements did not differ between physician-diagnosed and self-diagnosed participants.

	DISCUSSION

In our sample, over half the participants had self-diagnosed their lactose intolerance, and of those who were diagnosed by a physician, only 10% had a diagnosis based on an objective testing method such as a lactose tolerance test. In most cases the physician’s diagnosis was based on a description of symptoms. This reliance on subjective assessments by both individuals and physicians means that it is probable that some of our participants were neither lactose maldigesters nor lactose intolerant. For these individuals who digest lactose normally, use of objective diagnostic methods could therefore reduce the prevalence of misdiagnosis. However, whether these methods should be advocated as a routine component of diagnosis can be debated. In this regard, it is important to consider whether a confirmable diagnosis would alter how the condition was managed. This could occur for those who digest lactose; presumably they would not be counseled to avoid use of lactose-containing foods. However, this advice also appears inappropriate for those who maldigest lactose: current research indicates that elimination of lactose-containing foods is not required, and that most lactose maldigesters tolerate useful quantities without noticeable symptoms [4,6,8,10,20]. For example, in a double blind study, symptom experience following consumption of one glass of milk with a meal did not differ when lactose-containing or lactose-hydrolyzed milk was consumed [6], and in both cases, mean symptom scores were classified as "trivial".

In contrast to findings of blinded studies, most of our participants (69%) indicated that they experienced severe or somewhat severe symptoms if they ingested one cup of fluid milk with a meal. Many also experienced discomfort when consuming a variety of lactose-containing foods, although there was no association between the amount of lactose contained per serving of food and the proportion who reported discomfort. The reasons for the difference between findings of blinded trials and self-reports of those with lactose intolerance are difficult to ascertain, but several explanations are possible. Although well-controlled works reveal no relationship between dose and symptoms at relatively small doses, [6,8,10], other studies with large doses indicate a dose-dependent relationship [28,29]. Thus it is possible that some individuals may have experienced severe symptoms on one or more occasions following a large lactose load, resulting in a diagnosis of lactose intolerance. Following such a diagnosis, they may have come to anticipate symptoms with smaller amounts of lactose. Alternatively, other research has suggested that individuals who experience symptoms may have "sensitive" gastrointestinal tracts, and that this sensitivity is mistakenly attributed to lactose [30]. Thus, advice to individuals who believe they are lactose intolerant could focus on how to include lactose-containing foods without discomfort, and need not differ between those found to digest or to maldigest lactose based on a lactose tolerance test.

The perception that consuming dairy products would lead to discomfort might be anticipated to lead to reduced use of those foods, with potential impacts for calcium intake, and this appeared to have occurred in our study. Estimated calcium intake from food sources in these individuals with self-reported lactose intolerance averaged 591 ± 382 mg/d, so was considerably below the AIs of 1000 mg and 1200 mg for those aged 19–50 and 51 and above, respectively [27]. Comparisons to population-based studies must be made with caution because our study used a FFQ that may have underestimated calcium intake by approximately 100 mg, and population studies generally use 24-hr recalls. However, the available data suggest that our participants’ calcium intake from food was lower than that of healthy Canadian and American adults. For example, calcium intakes estimated in the British Columbia Nutrition Survey (BCNS), the Food Habits of Canadians Study and the Third National Health and Nutrition Examination Survey ranged from 729–875 mg/d among women, and 958–1375 mg/d in men [31–33].

When assessing calcium intake, however, it is also important to consider the contribution of supplements. The proportion of our participants who consumed a supplement containing calcium (65%) was considerably higher than is typically seen in population studies. For example, in 1998–1999, 8.7% of ambulatory US adults had used a calcium supplement during the previous week [34], and a recent Canadian study classified 5.8% of men and 16.1% of women as calcium supplement users [35]. It is possible that the geographic location of our study contributed to the high prevalence of supplement use, as the BCNS, conducted in 1999, found that 29% of adult British Columbians had used a supplement containing calcium on the day prior to the survey [31]. Nevertheless, the prevalence of calcium supplement use among our participants was still more than double that observed in other studies.

The impact of supplementation on the adequacy of our participants’ total calcium intake is limited by the fact that only 58% of those who took supplements provided complete information. However, the data suggest that in this group, supplementation increased mean intakes so that they met the AI of 1000 mg for those aged 19–50, and 1200 mg for those aged 50 and over. Data from the present study corroborate recent Canadian evidence [35] indicating that use of calcium supplements significantly increased mean calcium intake.

The other consideration regarding supplement use relates to the risk of exceeding the UL. Five of the 52 participants (10%) who provided complete information on food and supplement use exceeded the UL for calcium, while no one had an intake above the UL from food alone. Few comparative data are available; nevertheless, this appears to be somewhat higher than the 5.3% of supplement users exceeding the UL in the study of Troppmann and colleagues [35].

It was interesting to observe that calcium intake from food, prevalence of calcium supplementation, and calcium intake from supplements did not differ between those who had self-diagnosed their lactose intolerance and those who were diagnosed by a physician. This may be due to the fact that many physicians do not discuss nutrition interventions with their patients, due in part to a lack of nutrition education during medical training [36,37]. Lack of time for dietary counseling, and what may be perceived as an apparent lack of patients’ compliance with dietary intervention may also limit physician initiated nutrition discussions.

Limitations of this study include those inherent to the use of a convenience sample to select participants, and the fact that all data were self-reported. Furthermore, the relatively small proportion of men who responded to advertisements meant that power to detect potential differences by gender and age was limited. Finally, the inaccuracy inherent in using a food frequency questionnaire to assess calcium intakes must be recognized. However, even if our participants’ calcium intakes were underestimated to some degree, they were still well below current recommendations. Thus, these limitations do not invalidate our finding that many individuals with self-reported lactose intolerance are likely to have inadequate calcium intakes, which in turn have potential implications for their bone health [38–40]. And although not assessed in our study, the low calcium intakes of our study participants were likely accompanied by low intakes of vitamin D, since in Canada fluid milk is one of the few foods fortified with this vitamin. Concerns exist regarding the potential for calcium and vitamin D insufficiency and associated repercussions among individuals who are lactose intolerant [22,39,40]. Our study suggests that these concerns are valid whether lactose intolerance has been self-diagnosed or diagnosed by a physician, and emphasize the need for attention to ensuring nutrient adequacy in this group.

	CONCLUSION

TOP FOOTNOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION ACKNOWLEDGMENTS REFERENCES

 
Individuals with self-reported lactose intolerance are unlikely to meet the AI for calcium from food sources alone. Health professionals can play an important role in informing these individuals about how to include lactose-containing foods without experiencing symptoms, as well as providing information on other food sources of calcium, and if needed, advice on appropriate supplementation. However, because calcium intakes and use of calcium supplements did not differ between self-diagnosed and physician-diagnosed individuals, there appears to be a need for physician education regarding lactose maldigestion/intolerance. For those individuals who are unwilling or unable to meet the AI from food sources alone, supplements may be needed to optimize calcium intakes. Guidance on supplement use is required to ensure that intakes are adequate without being excessive.

	ACKNOWLEDGMENTS

TOP FOOTNOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION ACKNOWLEDGMENTS REFERENCES

 
We would like to thank the people who participated in this study for their time and support, and also, the British Columbia Dairy Foundation for their financial support of this project.

	FOOTNOTES

TOP FOOTNOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION ACKNOWLEDGMENTS REFERENCES

 
Present affiliation of Heather Y. Lovelace, MSc, RDN: Vancouver General Hospital and Health Sciences Centre, Vancouver, British Columbia, CANADA.

Supported in part by a grant from the British Columbia Dairy Foundation.

Dr. Barr is a member of the Medical Advisory Board of the International Dairy Foods Association.

Received November 5, 2003. Accepted June 27, 2004.

	REFERENCES

TOP FOOTNOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSION ACKNOWLEDGMENTS REFERENCES

 

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