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Review |
Department of Foods and Nutrition, Purdue University, West Lafayette, Indiana
Address reprint requests to: Dennis A. Savaiano, Ph.D., Department of Foods and Nutrition, Purdue University, 1260 Stone Hall, Rm 110, West Lafayette, IN 47907-1260. savaiano{at}cfs.purdue.edu.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONI. OSTEOPOROSISII. CALCIUM AND ETHNIC...III. LACTOSE MALDIGESTIONCONCLUSIONREFERENCES |
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Key words: lactose intolerance, lactose maldigestion, Asian-Americans, Hispanic-Americans, calcium, osteoporosis
Key teaching points:
• The risk of minorities developing osteoporosis may be more elevated than previously recognized.
• Most minority groups do not consume adequate amounts of calcium.
• Lactose intolerance is a barrier that may limit dairy calcium intake.
• Lactose intolerance can be managed by following simple dietary management strategies.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONI. OSTEOPOROSISII. CALCIUM AND ETHNIC...III. LACTOSE MALDIGESTIONCONCLUSIONREFERENCES |
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I. OSTEOPOROSIS |
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TOPABSTRACTINTRODUCTIONI. OSTEOPOROSISII. CALCIUM AND ETHNIC...III. LACTOSE MALDIGESTIONCONCLUSIONREFERENCES |
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Nationally, over 25 million people are afflicted with osteoporosis [3], resulting in approximately 1.5 million fractures [4] and more than 60,000 nursing home admissions annually [5]. The health care costs associated with osteoporotic fractures represented 1.5% of the National Personal Health Care Expenditures and 2.4% of the National Hospital Care Expenditures in 1995 [1]. The total monetary consequence of osteoporosis and osteoporotic fracture in 1995 was estimated to be $13.8 billion [1]. As life expectancy grows, there will be an increasing number of older Americans who reach the age of highest risk. A larger elderly population may have a profound effect on fracture incidence, possibly tripling the occurrence of hip fractures by 2040 [2,4].
Osteoporosis Characterized
Typically in humans, bone loss occurs at a rate of 6% to 8% per decade [6] and begins around the age of 40 for both men and women [6,7]. A bone mineral density greater than 2.5 standard deviations below the mean for young adult women is the criteria set by the World Health Organization (WHO) used to diagnose osteoporotic bones in women [8,9]. White females have a two- to threefold greater risk of enduring a hip fracture than white males [10,11]. It has been estimated that one of every six Caucasian women will experience a hip fracture related to osteoporosis in her lifetime [12]. Since males have a significantly lower risk of fracture, additional research on male and younger populations must be completed before diagnostic categories can be established for these groups [8].
The skeletal sites commonly associated with osteoporotic fractures are the vertebrae, hip and distal radius; however, fractures also occur at other sites [1,5,13]. Osteoporotic bones fracture easily because they cannot sustain light trauma from routine activities [13,14]. The primary characteristic of osteoporosis is low bone mass; however, other factors in the elderly, such as an increased tendency to fall due to poor muscle tone [4,15] and differences in bone geometry [12], apparently also contribute to the risk of osteoporotic fracture. Decreased bone mass is due to a combination of factors, some of which are genetic, while others are environmental or lifestyle choices [14]. Factors cited include cessation of gonadal hormone production, excessive alcohol consumption and cigarette smoking, nutritional deficiencies and physical inactivity [14].
Ethnic Differences in the Occurrence of Osteoporosis
From a lifestyle perspective, minority populations in the U.S. should be at a greater risk for developing osteoporosis. However, most evidence indicates that African-Americans and Hispanic-Americans have a lower risk of developing osteoporosis and osteoporotic fracture than Caucasians [10,11,16,17]. This contradiction illustrates the importance of biological and/or genetic factors in the etiology of this disease. One important illustration of the difference in osteoporosis among ethnic populations comes from state of California hospital discharge data for 1983 and 1984. Silverman et al. [11] determined the age-specific incidence of hip fracture among non-Hispanic whites, African-Americans, Asians and Hispanics. Caucasian and Asian women were found to have the highest risk for osteoporosis, with fracture rates of 140.7/100,000 and 85.4/100,000, respectively. Hispanic- and African-American females had lower age-adjusted rates, at 49.7/100,00 and 57.3/100,000, respectively.
African-Americans.
Several investigators have found that when comparing Caucasians, Hispanic-Americans and Asian-Americans with the African-American population, African- Americans have the lowest risk of osteoporotic fractures [10,11,18,19]. Most of the data on osteoporotic fractures and the African-American population concentrates on the incidence of fracture at a single site, the hip. The consistently observed lower incidence of hip fracture in this population is apparently in part attributed to the attainment of higher bone mass achieved during growth and development [18,20]. Baron and colleagues [21] measured fracture incidence in African-Americans and whites older than 65 years at various skeletal sites to ascertain whether or not the fracture risks for the chosen sites follow the same trend as hip fracture incidence. Medicare claims were used to evaluate the fracture risks of the hip, distal radius and ulna, proximal humerous and ankle. Overall, fractures occurred more frequently in women than in men, and white women were at a higher risk than African-American women for fractures at all sites studied. Risk was positively correlated with increasing age for all fractures, except for those which occurred at the ankle.
Even though African-Americans have a higher bone density [20,22] and seem to be protected from osteoporotic fractures to some extent, the risk of fracture is still present. Nearly 300,000 African-Americans have osteoporosis [16]. As African-American women grow older, their risk for osteoporotic fractures increases to a level resembling that of Caucasian women [23]. Specifically, for the femoral neck, the ratio of African-American women to white women with osteoporosis at age 50 is 1:7; however, at age 80 the ratio is 1:2 [23]. Therefore, osteoporosis should not be ignored as an important health issue in this population.
Hispanic-Americans.
Apparently, the Hispanic-American population may have an intermediate risk for development of osteoporosis, with an incidence of osteoporotic fracture of approximately one-half that of Caucasians [17]. According to results from NHANES III [16], approximately 100,000 Mexican-American women have osteoporosis (as defined by WHO diagnostic criteria). However, it is not clear whether or not this definition is applicable to this population and other minority populations due to differences in ethnicity [8], since little controlled experimental evidence has been reported on bone health in Hispanic populations. In a four-year longitudinal study investigating bone mass, nutrition, muscle strength and other factors contributing to fracture risk in postmenopausal Mexican-American women, Villa et al. [24] found no significant differences in average bone mineral density at the spine, hip and forearm sites when comparing non-Hispanic-Caucasian and Hispanic-American subjects. However, the difference between hip fracture rates was quite significant. The incidence of hip fractures in the Hispanic-American population was similar to the incidence of hip fractures found in the African-American population [24].
Asian-Americans.
Asian-American and Caucasian women possess some of the same risk factors associated with increased fracture rates. Early studies demonstrated that Asian subjects had lower bone densities than their Caucasian counterparts [25,26], while recent studies have concluded that these two populations have comparable bone densities after controlling for height and weight [19,27]. Even though Asian women may have comparable to lower bone masses than Caucasians, their incidence of hip fracture has been consistently estimated to be lower [11,19,28]. Ross et al. [29] estimates this difference to be one half. However, it appears that the incidence of vertebral fractures in Asian-American women may be higher than the incidence in Caucasians [30]. Thus, low bone mass may lead to elevated fracture rates at different sites among different ethnic populations.
National Osteoporosis Risk Assessment
Preliminary results from the National Osteoporosis Risk Assessment (NORA) indicate that osteoporosis may be more prevalent in minority populations than previously recognized. These results question current views that osteoporosis is predominately a "white woman’s" disease by suggesting that low bone mass and postmenopausal osteoporosis may be more widespread in some minority populations than previously thought. Hip fracture rates in the non-Caucasian population were nearly identical to that observed in Caucasians (2.97 vs. 3.06 fractures per 100 person years) [31]. This ongoing large-scale survey is being conducted on up to 210,000 postmenopausal women who have no previous history of osteoporosis [31].
The predominant public health perspective is that African- Americans have a substantially lower risk of osteoporosis and other minority populations have an intermediate risk of osteoporosis. Additional data from NORA may alter this perspective. However, even though the incidence of osteoporosis may be lower in some populations, it may still be unacceptably high and should be addressed as an important health concern.
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II. CALCIUM AND ETHNIC POPULATIONS |
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TOPABSTRACTINTRODUCTIONI. OSTEOPOROSISII. CALCIUM AND ETHNIC...III. LACTOSE MALDIGESTIONCONCLUSIONREFERENCES |
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Sources of Calcium
Dairy Sources.
Calcium is present in many foods, but is most concentrated in those foods originating from milks. Human milk contains approximately 32 mg of calcium per 100 mL, providing the infant with 463 mg of calcium per 1,000 kcal [39], thus insuring adequate bone development and metabolic function. One serving of milk, yogurt or cheese supplies approximately 300 mg of calcium [39]. The calcium content of numerous foods has been measured and reviewed [40–42]. Dairy products provide approximately 75% of the calcium consumed in the United States [43].
Non-Dairy Sources.
Some non-dairy foods contain an appreciable amount of calcium. Foods such as tortillas, beans, fish with bones, Chinese cabbage and kale contain moderate amounts of calcium and may be preferred by some populations. The calcium levels in various non-dairy foods have been reviewed [44] and are listed in Table 1. Calcium bioavailability can be an issue if the primary calcium source is of plant origin [44]. Typically, calcium absorption is low from plant foods containing high concentrations of oxalate and phytate [44]. For example, approximately sixteen one-half cup servings of spinach would need to be consumed to equal the amount of calcium in one cup of milk [44]. Calcium-fortified foods, including orange juice, fruit punches and cereals, and calcium supplements are other calcium-rich alternatives. Calcium-fortified foods may provide 10% to 20% of the RDA for calcium per serving [41].
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The National Health and Nutrition Examination Surveys have evaluated the level of calcium intake in Caucasian, Hispanic-American and African-American populations. Results from a recent survey, NHANES II [50], indicated that mean calcium intakes of white and Hispanic-American women were similar, within 60 mg for each age group presented (11–17, 18–39, 40–54 and 55–74 years). Non-Hispanic whites and Mexican-American women 40 to 54 years of age consumed approximately 617 and 561 mg of calcium per day, respectively. Black women in the 40-to-54- and 55-to-74-year-old age groups ingested 423 and 460 mg of calcium per day, respectively. Mean calcium intakes for non-Hispanic African-American men 40 to 54 years of age were 563 mg of calcium per day, while men aged 55 to 74 consumed 628 mg per day. Non-Hispanic white males and Mexican-American males in the 55-to-74-year-old age group had similar calcium intakes at 785 and 743 mg of calcium per day, respectively.
Evaluation of calcium intake in the Asian-American population has not been included in NHANES. Calcium consumption in this population has been less well studied. However, Asian-Americans have been found, with some consistency, to consume less dietary calcium when compared to the Caucasian population [47,51,52]. Kim and colleagues [51] evaluated the nutritional status of an elderly Asian-American population. Chinese, Japanese and Korean elderly men had mean calcium intakes of 734 ±43 mg/day, 609 ±69 mg/day and 613 ±65 mg/day, respectively. Mean calcium intakes for Chinese, Japanese and Korean women were lower, 567 ±28 mg/day, 531 ±46 mg/day and 441 ±39 mg/day, respectively. Wu-Tso and co-workers [52] also evaluated dietary intakes of young adult and elderly Asian-Americans. The sample population included 142 Asians of Chinese, Vietnamese and Japanese origin. Young adult Asian subjects between the ages of 19 and 42 had a mean calcium intake of 651 ±234 mg/day, while the elderly Asian participants aged 50 to 84 consumed 582 ±319 mg of calcium per day. Thus, from these two relatively small samples, it appears that Asian-American women mirror the calcium consumption of the other minority groups, having intakes well below the recommended dietary intake.
Calcium Intake and Acculturation
Asian-American and Hispanic-American dietary practices limit calcium intake, probably due to the interaction of traditional cultural food practices and food availability. However, there is some evidence to suggest that acculturation can lead to increased calcium consumption in these populations [53,54]. Acculturation is a "multi-dimensional process of overall adaptation of groups and individuals to a new society; cultural, psychological, social and political changes are involved" [55]. Acculturation appears to influence dietary patterns of milk consumption among Hispanic- and Asian-Americans in a positive way [53,55]. Moderate increases in milk consumption (6% to 8%) have been reported in acculturated Hispanic-Americans [53]. Further, in one study, the majority of the calcium consumed by Hispanic-American women was provided by dairy foods rather than traditional foods such as tortillas and refried beans (which supplied 10% and 3% of calcium, respectively) [56].
Migrant populations may continue to include certain traditional foods and exclude others, while adopting non-traditional "American" foods after immigration [55]. With immigration to the United States, some traditional Asian foods may be replaced by more "American" foods (such as cereal, bread, sandwiches, soft drinks and milk) [54]. Milk consumption in college-aged Asians significantly increased after living in the U.S. [54].
Despite acculturation, calcium consumption among Hispanic- and Asian-American populations is not adequate. Therefore, health professionals have encouraged these populations to further incorporate dairy and/or non-dairy calcium-rich foods into their diets. Lactose intolerance may be one barrier to increased dairy calcium intake for some individuals. However, lactose maldigestion should not be a limiting factor to dairy calcium intake since maldigesters can tolerate moderate amounts of lactose daily.
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III. LACTOSE MALDIGESTION |
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TOPABSTRACTINTRODUCTIONI. OSTEOPOROSISII. CALCIUM AND ETHNIC...III. LACTOSE MALDIGESTIONCONCLUSIONREFERENCES |
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Approximately 50 million people in the United States are lactose maldigesters [41,61]; however, the prevalence of lactose maldigestion varies widely among ethnic groups within the U.S. Generally, the highest prevalence of lactose maldigestion is observed in Asians, African-Americans and Native Americans, at approximately 100%, 75% and 100%, respectively. In the Hispanic population, lactose maldigestion is not as prevalent as in other subgroups, but is present in approximately half of the population (
53%) [62,63]. Northern Europeans and Caucasians in the United States have the lowest prevalence of lactose maldigestion [61,62]. Estimates of Caucasian maldigesters in the U.S. range from 6% to 22% [61,62]. As the minority populations in the U.S. are expected to multiply in coming years, the number of lactose maldigesters is also expected to increase. Based on U.S. Department of Commerce 1990 census data, 29% of the population was estimated to be lactose maldigesters. Projections for 2000 indicate that 31%, or 82 million people, will be lactose maldigesters; this number could possibly increase to 98 million by the year 2025 (Tables 3 and 4).
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Lactase non-persistence is the norm rather than the exception, as approximately 70% of the world’s population loses the ability to digest large amounts of lactose after weaning [66]. This lactase non-persistence is inherited as an autosomal recessive trait [67]. The remaining 30% of the population, mostly of Northern European decent, are lactase-persistent and retain the infant level of lactase [66]. Lactase persistence most likely originated as a mutation in populations who used milks as important foods for adult nutrition [43,62].
Maldigestion of lactose is a result of the low lactase activity at the brush border, relative to the concentration of lactose passing through the small intestine. Unhydrolyzed lactose passes to the large intestine where it is fermented by colonic bacteria. The gases created by fermentation are responsible for the development of intolerance symptoms such as abdominal pain, bloating, flatulence and very acute diarrhea.
Dietary Management of Lactose Maldigestion
Lactose maldigesters and their symptomatic response to lactose consumption have been extensively studied. The occurrence of intolerance symptoms from lactose is dependent upon several factors, including the dose consumed [61,65,68,69], the degree of colonic adaptation [70,71], the rate of gastric emptying [61,72] and the physical form of the food that carries the lactose (solid versus liquid) [73]. Although the prevalence of lactose maldigestion varies widely among ethnic populations (from 20% to 100%), no physiological or symptomatic differences have been observed among maldigesters from these populations. Lactose maldigestion can be managed by consuming small amounts of milk at each meal (a cup or less containing 12 grams of lactose) [74]. This amount of lactose is well tolerated. In addition to the various dietary management strategies (Table 5), commercial over-the-counter aids are available.
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Coingestion of lactose with a meal apparently decreases and delays peak hydrogen production and significantly reduces symptoms of intolerance [76]. The reduced symptoms can most likely be attributed to delayed gastric emptying, which allows more time for the residual intestinal lactase to digest the lactose, thereby decreasing the amount of lactose available for fermentation, therefore improving lactose tolerance [76].
Lactose tolerance can also be improved by modifying the amount and form of the lactose-containing foods consumed. It has been reported that some types of milk and cheeses are more tolerable than others [41]. For example, whole milk is better tolerated than an aqueous lactose solution or low-fat milk [77]. Chocolate milk may also improve tolerance to lactose [78]. Fat content and the presence of additional sugars in the milk, as well as osmolality, may affect the tolerance level in maldigesters [79].
Live culture yogurt is another alternative to milk, even though the lactose content per gram of yogurt may be greater than that of whole milk [6,61,80]. Importantly, lactose in yogurt is digested better than lactose in milk, and yogurt is well tolerated by symptomatic lactose maldigesters [81]. The increased tolerance to yogurt is thought to be due to the microbial beta-galactosidase activity that digests the lactose in these products in vivo as well as the delay in transit of the gelled foodstuff [82].
Over-the-counter digestive aids are additional alternatives which allow maldigesters to incorporate dairy foods into their diet. The digestive aids commercially available include lactase tablets, lactase preparations, lactose-free milk and prehydrolyzed milk. Since lactose maldigesters can tolerate up to one cup of milk, these products should be used when more than one cup of milk will be ingested in one sitting [41].
In addition to biologically tolerating lactose, maldigesters must also psychologically adapt by changing their behavior in order to consume adequate calcium from dairy foods over an extended period. Adequate dairy calcium intake is possible for symptomatic maldigesters, if the dietary management strategies are incorporated into daily living.
Lactose Maldigestion and Osteoporosis
It is likely that the intolerance symptoms experienced after dairy consumption are the cause of milk avoidance and decreased calcium intake [58] through a classical behavioral learned aversion mechanism. Several investigators have found a correlation between lactose maldigestion, low calcium intakes and the incidence of osteoporosis [57,58,60], although the findings have not been uniform [83].
Birge and co-workers (1967) [60] were the first to attempt to assess the relationship between osteoporosis and lactose maldigestion. Nineteen osteoporotic Caucasians over the age of 50 who were patients at the National Institute of Arthritis and Metabolic Diseases participated in the study. Non-osteoporotic patients served as a control group, matched for age and ethnicity. Nine of the 19 osteoporotic patients (47%) and none of the controls were classified as lactose maldigesters. Calcium intakes over the previous ten years were estimated for both groups, yielding significant differences. Estimated calcium intake for the osteoporotic lactose maldigesters were 200 mg/day of calcium, whereas the control and lactose digesting osteoporotic groups consumed approximately 650 mg of calcium per day. This study provides initial evidence that long-term avoidance of calcium because of symptomatic lactose maldigestion may be associated with the etiology of osteoporosis.
Newcomer et al. [59] in 1978 reported on the prevalence of lactose maldigestion in 30 Caucasian postmenopausal women with osteoporosis and 31 female controls matched for age and ethnicity. Of the 30 women with osteoporosis, eight were classified as lactose maldigesters, while only one of the 31 controls was a maldigester. Maldigesters consumed only 530 mg of calcium per day; significantly less than the 811 mg of calcium per day consumed by digesters. The increased prevalence of lactose maldigestion in osteoporotic females is in agreement with the study by Birge et al. [60].
Horowitz et al. (1987) [84] determined the prevalence of lactose maldigestion in 46 Caucasian women with postmenopausal osteoporosis. Twenty-five of the 46 osteoporotic subjects (54%) were classified as lactose maldigesters. Milk intake of the maldigesters was significantly lower than that of the digesters. Of those subjects who were determined to be maldigesters, 76% reported having gastrointestinal symptoms following lactose consumption.
Callegari and colleagues (1990) [57] studied lactose maldigestion and milk consumption in postmenopausal northern Italian women. Bone mineral content and digestion of lactose were evaluated in 155 women. The authors reported a significant relationship between osteoporosis and low calcium intake. Osteoporosis was observed in 25.9% of the women who consumed 
250 mg of calcium per day. However, in women with calcium intakes below 250 mg per day, the percentage diagnosed with osteoporosis increased to 46.6%. One hundred and seven of the 155 women in this study were classified as lactose maldigesters (69%), 57% reported prior knowledge of their maldigestion and attempted to restrict their intake of dairy foods.
Wheadon and co-workers (1991) [85] evaluated the prevalence of lactose maldigestion in a small sample of osteoporotic women from New Zealand and a group of age-matched controls. The two elderly groups had similar prevalences of lactose maldigestion (9 of the 15 osteoporotic subjects and 10 of the 16 controls). Interestingly, only six out of 50 women in a young control group were maldigesters. In this study, elderly lactose maldigesters did not consume less calcium or dairy than either the elderly or the young controls. It is possible that dairy food consumption in New Zealand is so well established in the culture that the avoidance behavior observed in other studies is not present.
In 1995, Corazza et al. [58] studied fifty-eight postmenopausal Caucasian Italian women who were suspected to be osteoporotic (due to back pain) to evaluate the degree to which lactose maldigestion might affect the development of osteoporosis. Thirty-three of the 58 women (57%) who participated in this study had bone densities low enough to classify them as osteoporotic. There were no significant differences in the prevalence of lactose maldigestion between the osteoporotic and non-osteoporotic groups. A positive relationship between calcium intake and bone mineral density was observed. Further, symptom scores for lactose maldigestion negatively correlated with dietary calcium consumption from dairy products. This study, like that of Wheadon et al. [85], demonstrates that lactose maldigestion alone did not cause decreased calcium intake. However, lactose maldigestion with the occurrence of gastrointestinal symptoms did cause avoidance of dairy foods and compromised dietary calcium intake.
Historically, different hypotheses have linked lactose maldigestion to the pathogenesis of osteoporosis. Decreased calcium intake [59,60,85,86] and/or impaired calcium absorption [59,86] are postulated mechanisms by which the two conditions have been associated. Recent studies have confirmed that calcium absorption is not impaired or altered due to lactose maldigestion [9,84,87].
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CONCLUSION |
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TOPABSTRACTINTRODUCTIONI. OSTEOPOROSISII. CALCIUM AND ETHNIC...III. LACTOSE MALDIGESTIONCONCLUSIONREFERENCES |
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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TOPABSTRACTINTRODUCTIONI. OSTEOPOROSISII. CALCIUM AND ETHNIC...III. LACTOSE MALDIGESTIONCONCLUSIONREFERENCES |
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