JACN Did you know that you can get alerts when a new issue is online?
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

This Article
Right arrow Abstract Freely available
Right arrow Figures Only
Right arrow Full Text (PDF)
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Parra, M. D.
Right arrow Articles by Martínez, J. A.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Parra, M. D.
Right arrow Articles by Martínez, J. A.
Journal of the American College of Nutrition, Vol. 26, No. 3, 288-294 (2007)
Published by the American College of Nutrition

Acute Calcium Assimilation from Fresh or Pasteurized Yoghurt Depending on the Lactose Digestibility Status

M. Dolores Parra, PhD, Blanca E. Martínez de Morentin, MD, RD, José M. Cobo, PhD, Irene Lenoir-Wijnkoop, RD and J. Alfredo Martínez, PhD, FACN

Department of Physiology and Nutrition, University of Navarra (Edif. Investigación), C/ Irunlarrea, Pamplona (M.D.P., B.E.M., J.A.M.)
Red INDE, C/ Buenos Aires, Barcelona (J.M.C., I.L.-W.), SPAIN

Address reprint requests to: Prof. J. Alfredo Martínez, Dpt. Physiology and Nutrition. University of Navarra, C/ Irunlarrea s/n. 31008 Pamplona, SPAIN. E-mail: jalfmtz{at}unav.es


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIAL AND METHODS
 RESULTS
 CONCLUSION
 ACKNOWLEDGMENTS
 REFERENCES
 
Objective: The major aim of this trial was to evaluate the potential interaction of fresh or pasteurized yoghurt intake with lactose intolerance on calcium assimilation by means of the stable isotope 43Ca as a tracer.

Methods: Forty volunteers (age: 32 ± 7 years) participated in this parallel simple blind study (20 of them with moderate lactose intolerance). The protocol included the intake of a test meal consisting on 43Ca-labelled fresh or pasteurized yoghurt. Volunteers, in whom the calcium status was assessed, collected the 24-h urine before and after the test meal to measure the stable isotope output. The intake-related 43Ca enrichment in urine was measured by isotopic rate mass spectrometry.

Results: In lactose tolerant and intolerant volunteers taken together, the fresh yoghurt consumption resulted in a statistically higher circulating calcium levels (p = 0.028) and urinary 43Ca output (p = 0.017) than after the pasteurized yoghurt intake. The lactose maldigestion status resulted in higher urinary 43Ca excretion (p = 0.013) after the fermented milk consumption, regardless of the nature of ingested product (p = 0.887).

Conclusions: This novel and non-aggressive protocol allowed the in vivo comparison of calcium utilization from two different dairy sources, revealing a higher acute calcium assimilation from fresh as compared to the pasteurized yoghurt, in both lactose digesting and maldigesting subjects.

Key words: calcium assimilation, stable isotopes, yoghurt, lactose maldigestion


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIAL AND METHODS
 RESULTS
 CONCLUSION
 ACKNOWLEDGMENTS
 REFERENCES
 
The nutritional value of calcium is mainly attributed to the key role played on bone growth and homeostasis [1]. However, calcium is additionally involved in numerous biological processes such as Ca-mediated signal transmission [2], body weight regulation [2, 3] or insulin function [4].

The metabolic involvement of this mineral makes of interest to establish daily requirements [5], and to assess calcium bioavailability from different food sources [6, 7], as well as in different biological and physiological states, like pregnancy [8], childhood [9], menopause [10] or poor lactose hydrolysis capacity (lactose maldigestion), including lactose intolerance (accompanied by clinical symptoms after lactose intake) [11].

Dairy products, specifically milk, yoghurt and cheese, provide most of calcium in the typical Western diet [12]. Indeed, a number of studies have been published using different methods to evaluate calcium bioavailability from these sources [6, 13–14]. In fact, calcium absorbability, or the availability of calcium for absorption by the intestines, is the first step towards bioavailability, which also depends on incorporation of absorbed calcium into bone, urinary excretion and faecal loss of endogenous calcium, physiological factors, particularly hormones, and certain types of food [15].

Single meal studies have been performed in humans to measure calcium absorption using tracer methods, by including a radioisotope in the test meal. In this way, radioactivity is monitored in the whole body [16] or from blood samples [17] to assess calcium assimilation, defined as the process of digestion and absorption in the gastrointestinal tract [18].

The hazards related to radioactivity led to devise methods applying stable isotopes as tracers to evaluate calcium utilization from different foods, following different approaches [19–21]. Among them, stable isotope single-tracer protocols have been developed to perform comparative analyses of in vivo calcium availability from different foods [17].

Based on these assumptions, the aim of the present study was to evaluate the impact of moderate lactose maldigestion on calcium assimilation (digestion plus absorption in the gastrointestinal tract), comparing the effect of live yoghurt or pasteurized yoghurt intake by using the stable isotope 43Ca as tracer.


   MATERIAL AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIAL AND METHODS
RESULTS
 CONCLUSION
 ACKNOWLEDGMENTS
 REFERENCES
 
Subjects
The recruitment pattern was devised to include a homogeneous group of volunteers concerning lifestyle and socio-economic characteristics. This process was carried out from the volunteer database of the Department of Physiology and Nutrition of the University of Navarra and through newspaper and radio advertisements. Volunteers were selected and monitored by a physician at the Department of Physiology and Nutrition of the University of Navarra. All were in apparent good health, as assessed by medical history, physical examination and routine blood analyses at baseline. General inclusion criteria were no history of metabolic, immune and/or gastrointestinal disease, no current medication, no severe obesity (body mass index >35 kg/m2).

Forty volunteers (50% of them with mild to moderate lactose maldigestion) were enrolled to participate in this trial after this biochemical characterisation (Table 1). Before the inclusion, a hydrogen breath test was carried out to confirm the lactose maldigestion degree of volunteers, since only lactose tolerant and volunteers with moderate lactose maldigestion were allowed to be included in the trial. The breath test was performed by ingestion of 25g lactose dissolved in 250 ml water [22] after a night fast (dinner at 20:00h–21:00h), beginning between 8:00h and 9:00h. The hydrogen content in breath was measured by an H2-specific electrochemical sensor (EC60 Gastrolyzer, Bendfont, UK), at baseline and after the lactose intake, at 15-minute intervals during four hours. The result was considered as positive when a 20ppm increment in breath hydrogen and/or symptoms were detected during the test period [23]. Volunteers with severe lactose maldigestion symptoms or discomfort were not enrolled in the trial based on ethical reasons. Dietary milk and dairy product intake was asked during the medical history in order to assure that the included volunteers were able to consume three yoghurts per day during three days without discomfort and a diary to register adverse effects was given to volunteers. The physician revised the diary during the visits at the Metabolic Unit to assure that no adverse effects were reported. Enrolled participants (n = 40) gave their written informed consent to be involved in this experimental trial, which was previously approved by the local Ethics Committee at the University of Navarra (Ref. 3/2004). Finally, the effect of lactose malabsorption on calcium assimilation from fresh and pasteurized yoghurt was analyzed by using the experimental data obtained from thirty-two volunteers, since eight participants did not complete the trial.


View this table:
[in this window]
[in a new window]

  		Table 1. Groups Description and Biochemical Parameters at Baseline

 
Trial Design and Measurements
Ten days before the nutritional intervention (adaptation period), volunteers were not allowed to consume fermented milk products. After that time, the volunteers received three cups per day of the assigned product (125g per unit). The first part of the study involved the fresh yoghurt intervention (starter ferments content: L. bulgaricus >108 CFU/g) and L. thermophilus >108 CFU/g) and the second part, the pasteurized yoghurt intervention (starter ferments content: L. bulgaricus <10 CFU/g and L. thermophilus <10 CFU/g). Both treatments were administered in a simple-blind pattern (Fig. 1), beginning with the fresh product intervention.


Figure 1
View larger version (28K):
[in this window]
[in a new window]

  		Fig. 1. Product composition and trial design.

 
At inclusion, serum levels of glucose, insulin and lipid profile were measured by automatized analyses (ABX, USA) using a COBAS MIRA equipment (Roche, Switzerland), as biochemical markers of nutritional status. In order to evaluate the general status of calcium metabolism, blood levels of calcium, magnesium and phosphorus were measured by colorimetric methods (Beckman, USA), as well as the alkaline phosphatase activity (Beckman, USA) and the 24h-urinary calcium output (Beckman, USA).

The calcium assimilation study started at 8:00 a.m. and was performed after an overnight fast. The protocol included the ingestion of the assigned test meal, fresh or pasteurized yoghurt, which contained 0.013mg/kg body weight of 43CaCO3 extrinsically incorporated by addition of the tracer to the yoghurt and homogenisation two hours before the intake as described elsewhere [24]. Blood was taken before and at 60 minutes after the ingestion of the test meal [10] to measure circulating calcium. The total calcium absorbed one hour after the ingestion was calculated by the trapezoidal area procedure: [(blood calcium (mg/dl) at fasting state + blood calcium (mg/dl) at postprandial time)/2] x sampling period (h).

Volunteers collected the 24-h urine sample before and after the labelled product ingestion to measure the 43Ca-enrichment in urine in relation to baseline excretion values (24h-urine sample recovered before the product ingestion). The 43Ca enrichment in urine was measured by isotopic rate mass spectrometry (Finnigan, Germany), and was mathematically transformed into the percentage of excreted tracer (%43Ca). Eight volunteers separately performed the whole experimental trial without 43Ca in the ingested product to take into account the natural isotope content in urine.

Statistical Analysis
The Kolmogorov-Smirnov and the Shapiro-Wilk tests were applied to explore normality of the variables. Comparison between parametric variables was evaluated using the Student t-test, while non-parametric variables were analyzed by the Mann-Whitney U test and the Wilcoxon matched pair test. In agreement with the experimental design, a factorial 2x2 analysis of the variance was performed to examine potential interactions between the product intake and the lactose maldigestion status based on its known robustness. Results were expressed as the mean ± standard deviation and considered statistically significant if two-sided P-values were <0.05. All statistical analyses were carried out using the SPSS 11.0 version for Windows 98 (SPSS Inc., Chicago, USA).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIAL AND METHODS
 RESULTS
CONCLUSION
 ACKNOWLEDGMENTS
 REFERENCES
 
Baseline Measurements
At baseline, the lactose maldigesting group and the control volunteers showed comparable nutritional status, as assessed by the biochemical analyses performed in blood (Table 1). However, the lactose maldigesters had plasma phosphorus statistically lower (p = 0.011) and magnesium levels marginally lower (p = 0.058) than the control group, but all within the normal laboratory healthy reference range. No differences were detected between groups for circulating calcium (p = 0.212) and alkaline phosphatase activity (p = 0.912). Therefore, both groups were considered as nutritionally comparable at baseline.

Serum Calcium after Product Intake
The experimental design to evaluate the in vivo calcium assimilation included the measurement of circulating calcium changes in blood at 60 minutes after the yoghurt intake. In the lactose maldigesters, plasma levels of calcium statistically increased after the fresh yoghurt ingestion (9.6 ± 0.3 mg/dL vs 9.9 ± 0.4 mg/dL; p = 0.003) with no changes after the pasteurized product intake (9.4 ± 0.5 mg/dL vs 9.4 ± 0.4 mg/dL; p = 0.854). With respect to lactose digesting volunteers, circulating calcium marginally increased (9.4 ± 0.3 mg/dL vs 9.6 ± 0.4 mg/dL; p = 0.094) after the fresh yoghurt consumption, while no statistical changes were detected after the pasteurized yoghurt intake (9.6 ± 0.3 mg/dL vs 9.7 ± 0.3 mg/dL; p = 0.559). Taken together in both groups of subjects accordingly with the 2x2 factorial design, with and without lactose maldigestion, circulating calcium markedly increased (p = 0.001) one hour after the fresh yoghurt intake, while no changes (p = 0.760) were detected after the pasteurized consumption at the same postprandial time (Fig. 2).


Figure 2
View larger version (21K):
[in this window]
[in a new window]

  		Fig. 2. Product-related effect (mean value is indicated with a thick line) for the change in blood calcium at 60-minute after the intake of fresh or pasteurized yoghurt found in subjects with (n = 16) and without (n = 16) lactose maldigestion.

 
Furthermore, according to the experimental design, the analysis of the data (Table 2) evidenced the statistically (p = 0.028) significant product-related effect, while no effect (p = 0.367) was found concerning lactose maldigestion nor product-lactose maldigestion interaction (p = 0.893).


View this table:
[in this window]
[in a new window]

  		Table 2. Data from the Calcium Assimilation Study Concerning Serum Calcium Changes and Urinary Calcium Excretion in Lactose Tolerant and Intolerant Volunteers after Fresh or Pasteurized Yoghurt Intake

 
Urinary 43Ca Urine Enrichment after Product Intake
Daily calcium excretion in urine was measured to assure the steady state for included volunteers. No differences were detected in total urinary calcium before the intake of products (before fresh yoghurt intake: 156 ± 78 mg/24h vs or before pasteurized yoghurt intake 150 ± 56 mg/24h; p = 0.715). Similarly, no changes in urinary calcium content were found after the experimental product intake (156 ± 60 mg/24h vs 169 ± 62 mg/24h; p = 0.349). Furthermore, the experiment carried out in eight volunteers with no labelled products showed that the 43Ca enrichment in urine was negligible (0.2 ± 0.9% vs 0.3 ± 0.9%; p = 0.203) after the unlabelled fresh or pasteurized yoghurts intake (fresh yoghurt: .0.17 ± 0.91% pasteurized yoghurt: 0.31 ± 0.89%; p = 0.203). This result assured that the chosen tracer dose was enough to detect changes related to 43Ca assimilation. In contrast, taken together lactose tolerant and intolerant volunteers, the fresh yoghurt consumption involved a statistically higher urinary 43Ca-enrichment (2.97 ± 1.02% vs 2.53 ± 0.82%; p = 0.017).

The analysis of the variance marginally showed significant differences (p = 0.095) in urinary 43Ca enrichment depending on product intake (Table 2). After the labelled product consumption, the lactose maldigestion status involved different (p = 0.020) urinary 43Ca enrichment, regardless (p = 0.861) of the fresh or pasteurized yoghurt intake (Table 2), so volunteers with moderate lactose maldigestion showed a high (p = 0.021) urinary 43Ca enrichment (Fig. 3).


Figure 3
View larger version (21K):
[in this window]
[in a new window]

  		Fig. 3. Effect of lactose maldigestion in 43Ca enrichment (mean and standard deviation) assessed in 24-hour urine after the ingestion of fresh or pasteurized yoghurt in 24 volunteers, twelve with lactose tolerance and twelve with moderate lactose maldigestion (n = 12).

 

   DISCUSSION
 
Lactose maldigestion is a relevant factor influencing milk and dairy product consumption, since lactase-deficiency often produces gastrointestinal symptoms after lactose intake [25]. Unless other calcium enriched foods are regularly consumed, milk and other dairy products are the commonest sources, and limiting consumption of these foods can increase the risk of inadequate intake of this mineral [26, 27]. As a result, most of lactose intolerant or maldigester people are at particular risk of calcium intake below recommended levels [25]. Moreover, reduction in calcium absorption has been described in lactose intolerant people, who improved the mineral assimilation by the intake of dairy products containing lactose [27]. Hence, the purpose of the present trial was to compare the calcium assimilation after fresh or pasteurized yoghurt intake, evaluating the potential involvement of lactose maldigestion in this process.

As previously described, lactose maldigesting subjects could benefit from improved intake of calcium-rich non-dairy foods or specific dairy products if they are well tolerated, as yoghurt [29]. However, calcium utilization depends upon individual factors, such as the lactase-deficiency degree as well as on food characteristics [30]. Thus, several studies have shown that yoghurt is better tolerated than milk [11], because some lactase activity from yoghurt bacteria could participate in lactose digestion, as well as the delayed oro-cecal transit time [23, 31]. Therefore, yoghurt could allow lactose maldigesting people to comfortably consume a dairy food naturally rich in calcium.

Under our experimental conditions, the acute calcium uptake from the fresh yoghurt was higher than from the pasteurized, as evidenced by the increase in circulating plasma levels of calcium one hour after intake [31]. The heat treatment of yoghurt to increase the shelf live of the product could diminish the effect on lactose digestibility due apparently to enzymatic inactivation [32], together with the proposed effect on oro-caecal transit time, described as shorter for the pasteurized yoghurt [23]. This finding could be partially explained because calcium assimilation seems to be enhanced by lactose absorption [11]. Moreover, changes in the structure of the yoghurt related to the pasteurization process could also modify the calcium disposal. In fact, some proteins are denaturated and aggregated during the heating process, and a non-specifically binding to calcium has been described, decreasing the availability of the mineral to be absorbed [33].

Urinary calcium output can be interpreted as an indirect marker of retention, since calcium homeostasis in adults involves that the entry of this mineral from the gut equals the urinary calcium excretion on a daily basis, since other excretion routes are considered unchanged in normal subjects [34]. Based on this statement, results obtained from circulating plasma levels after intake could be supported by urinary analyses, if a steady state of calcium turnover was reached [34]. In order to maintain a comparable dynamic equilibrium, volunteers followed a adaptation period, in which the fermented dairy product consumption was avoided before the experimental intervention [35]. With respect to bone metabolism, calcium is controlled with a slow turnover, so it could be considered under strict balance with the exception of children/childhood, pregnant or ageing people, who were not included in the study. Thus, bone turnover was considered constant during the experimental period. Moreover, the study involved intra-subject comparisons (pair tests) and the experiments were carried out within 30 days. Hence, total calcium excretion in urine was considered constant and a marker of the balanced status in calcium metabolism during the intervention period.

After the acute intake of both fresh and pasteurized products, the urinary calcium output was higher in lactose maldigesting subjects as compared to controls. This observation could reflect the habitual low intake of calcium from milk products in subjects with lactose maldigestion and a lower percent absorption demands in this people [25].

We completed the assimilation study of calcium by using the single labelling method [16]. In order to reduce time-consuming procedures, aggressiveness and economic cost, we carried out a stable isotope single-tracer protocol to perform comparative analyses in vivo of calcium availability from different foods, following the principles of single meal studies by including a isotope in the test meal [17]. The 43Ca was the selected tracer based on non hazardous and non radioactive features and the possibility to quantify the enrichment in urine with a high degree of accuracy [24]. After the calcium balance homogenization of volunteers, the acute ingestion of the single-labelled yoghurt was carried out, considering changes on 43Ca enrichment in urine after the test yoghurt intake as an indirect marker of calcium assimilation. The tracer dose was fixed based on previous works [24]. The natural isotope content of volunteers, as well as the isotope enrichment due to the tested products could affect the assay. However, no changes in 43Ca-urine content were detected after the non-labelled product intake, suggesting that the adjusted tracer dose could be able to detect changes in 43Ca enrichment in urine depending on tracer assimilation [17].

The trend of a higher calcium excretion after the fresh yoghurt intake as compared to the pasteurized fermented milk, confirmed the observed increase in blood calcium levels, suggesting a higher acute bioavailability, which may be of importance in lactose intolerance as has been found for short-term leucine assimilation [36].


   CONCLUSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIAL AND METHODS
 RESULTS
 CONCLUSION
ACKNOWLEDGMENTS
 REFERENCES
 
The comparative study concerning these two products showed that calcium assimilation was improved in the fresh as compared to the pasteurized fermented milk intake, in both lactose digesting and maldigesting subjects. Therefore, yoghurt containing live ferments can be considered as an important calcium source, since it could involve an optimised calcium assimilation, although further investigations are needed to confirm these results and their possible implications for human health.


   ACKNOWLEDGMENTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIAL AND METHODS
 RESULTS
 CONCLUSION
 ACKNOWLEDGMENTS
REFERENCES
 
The authors wish to thank Iñigo Navarro from the Department of Chemistry (University of Navarra, Spain) for the help in preparing urine samples, as well as Paul Field from the Institute of Marine and Coastal Sciences (Rudgers University, USA) for the analysis of 43Ca content in urine samples and Danone for the supplied products. We also thank our nurse Salomé Pérez, and our technicians Ana Lorente and Verónica Ciaurriz for excellent technical assistance.

Received March 3, 2005. Accepted March 9, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIAL AND METHODS
 RESULTS
 CONCLUSION
 ACKNOWLEDGMENTS
 REFERENCES
 

  1. Jackson KA, Savaiano DA: Lactose maldigestion, calcium intake and osteoporosis in Africa-, Asian., and Hispanic-Americans.J Am Coll Nutr20 :198S –207S,2001 .[Abstract/Free Full Text]
  2. Zemel MB, Thompson W, Milstead A, Morris K, Campbell P: Calcium and dairy acceleration of weight and fat loss during energy restriction in obese adults.Obes Res12 :582 –590,2004 .[Medline]
  3. Zemel MB, Shi H, Greer B, Dirienzo D, Zemel P: Regulation of adiposity by dietary calcium.FASEB J14 :1132 –1138,2000 .[Abstract/Free Full Text]
  4. Chang I, Cho N, Kim S, Kim JY, Kim E, Woo JE, Nam JH, Kim SJ, Lee MS: Role of calcium in pancreatic islet cell death by IFN-gamma/TNF-alpha.J Immunol172 :7008 –7014,2004 .[Abstract/Free Full Text]
  5. Nieves JW: Calcium, vitamin D, and nutrition in elderly adults.Clin Geriatr Med19 :321 –335,2003 .[Medline]
  6. Recker RR, Bammi A, Barger-Lux MJ, Heaney RP: Calcium absorbability from milk products, an imitation milk, and calcium carbonate.Am J Clin Nutr47 :93 –95,1988 .[Abstract/Free Full Text]
  7. Bacciottini L, Tanini A, Falchetti A, Masi L, Franceschelli F, Pampaloni B, Giorgi G, Brandi ML: Calcium bioavailability from a calcium-rich mineral water, with some observations on method.J Clin Gastroenterol38 :761 –766,2004 .[Medline]
  8. O'Brien KO, Nathanson MS, Mancini J, Witter FR: Calcium absorption is significantly higher in adolescents during pregnancy than in the early postpartum period.Am J Clin Nutr78 :1188 –1193,2003 .[Abstract/Free Full Text]
  9. Abrams SA, Griffin IJ, Davila PM: Calcium and zinc absorption from lactose-containing and lactose-free infant formulas.Am J Clin Nutr76 :442 –446,2002 .[Abstract/Free Full Text]
  10. Nordin BE, Morris HA, Wishart JM, Scopacasa F, Horowitz M, Need AG, Clifton PM: Modification and validation of a single-isotope radiocalcium absorption test.J Nucl Med39 :108 –113,1998 .[Abstract/Free Full Text]
  11. Wynckel A, Jaisser F, Wong T, Drueke T, Chanard J: Intestinal absorption of calcium from yogurt in lactase-deficient subjects.Reprod Nutr Dev31 :411 –418,1991 .[Medline]
  12. Adolfsson O, Meydani SN, Russell RM: Yogurt and gut function.Am J Clin Nutr80 :245 –256,2004 .[Abstract/Free Full Text]
  13. Smith TM, Kolars JC, Savaiano DA, Levitt MD: Absorption of calcium from milk and yogurt.Am J Clin Nutr42 :1197 –1200,1985 .[Abstract/Free Full Text]
  14. Van Dokkum W, De La Gueronniere V, Schaafsma G, Bouley C, Luten J, Latge C: Bioavailability of calcium of fresh cheeses, enteral food and mineral water. A study with stable calcium isotopes in young adult women.Br J Nutr75 :893 –903,1996 .[Medline]
  15. Gueguen L, Pointillart A: The bioavailability of dietary calcium.J Am Coll Nutr.19 :119S –136S,2000 .[Abstract/Free Full Text]
  16. Hansen M, Sandstrom B, Jensen M, Sorensen SS: Effect of casein phosphopeptides on zinc and calcium absorption from bread meals.J Trace Elem Med Biol11 :143 –149,1997 .[Medline]
  17. Heaney RP, Sowell MS, Wolf RL: Estimation of true calcium absorption in men.Clin Chem48 :786 –788,2002 .[Free Full Text]
  18. Evenepoel P, Hiele M, Luypaerts A, Geypens B, Buyse J, Decuypere E, Rutgeerts P, Ghoos Y: Production of egg proteins, enriched with L-leucine-13C1, for the study of protein assimilation in humans using the breath test technique.J Nutr127 :327 –331,1997 .[Abstract/Free Full Text]
  19. Moser-Veillon PB, Mangels AR, Vieira NE, Yergey AL, Patterson KY, Hill AD, Veillon C: Calcium fractional absorption and metabolism assessed using stable isotopes differ between postpartum and never pregnant women.J Nutr131 :2295 –2299,2001 .[Abstract/Free Full Text]
  20. Tahiri M, Tressol JC, Arnaud J, Bornet FR, Bouteloup-Demange C, Feillet-Coudray C, Brandolini M, Ducros V, Pepin D, Brouns F, Roussel AM, Rayssiguier Y, Coudray C: Effect of short-chain fructooligosaccharides on intestinal calcium absorption and calcium status in postmenopausal women: a stable-isotope study.Am J Clin Nutr77 :449 –457,2003 .[Abstract/Free Full Text]
  21. Beck AB, Bugel S, Sturup S, Jensen M, Molgaard C, Hansen M, Krogsgaard OW, Sandstrom B: A novel dual radio- and stable-isotope method for measuring calcium absorption in humans: comparison with the whole-body radioisotope retention method.Am J Clin Nutr77 :399 –405,2003 .[Abstract/Free Full Text]
  22. Pochart P, Dewit O, Desjeux JF, Bourlioux P: Viable Starterculture, beta-galactosidase activity and lactose in duodenum after yoghurt ingestion in lactase-deficient humans.Am J Clin Nutr49 :828 –831,1989 .[Abstract/Free Full Text]
  23. Labayen I, Forga L, Gonzalez A, Lenoir-Wijnkoop I, Martinez JA: Relationship between lactose digestion, gastrointestinal transit time and symptoms in lactose malabsorbers after daily consumption.Aliment Pharmacol Ther15 :543 –549,2001 .[Medline]
  24. Field P, Shapses S, Cifuentes M, Sherrell RM: Precise and accurate determinationof calcium isotopes ratios in urine using HR-ICP-SFMS.J Anal At Spectrom18 :727 –733,2003 .
  25. Nicklas TA: Calcium intake trends and health consequences from childhood through adulthood.J Am Coll Nutr22 :340 –356,2003 .[Abstract/Free Full Text]
  26. McBean LD, Miller GD: Allaying fears and fallacies about lactose maldigestion.J Am Diet Assoc98 :671 –676,1998 .[Medline]
  27. Griessen M, Cochet B, Infante F, Jung A, Bartholdi P, Donath A, Loizeau E, Courvoisier B: Calcium absorption from milk in lactose-deficient subjects.Am J Clin Nutr49 :377 –384,1989 .[Abstract/Free Full Text]
  28. Obermayer-Pietsch BM, Bonelli CM, Walter DE, Kuhn RJ, Fahrleitner-Pammer A, Berghold A, Goessler W, Stepan V, Dobnig H, Leb G, Renner W: Genetic predisposition for adult lactose maldigestion and relation to diet, bone density, and bone fractures.J Bone Miner Res19 :42 –47,2004 .[Medline]
  29. Jarvis JK, Miller GD: Overcoming the barrier of lactose maldigestion to reduce health disparities.J Natl Med Assoc94 :55 –66,2002 .[Medline]
  30. Caroccio A, Montalto G, Cavera G, Notarbatolo A: Lactose maldigestion and self-reported milk maldigestion: relationship with lactose maldigestion and nutrient intake. Lactase Deficiency Study Group.J Am Coll Nutr17 :631 –636,1998 .[Abstract/Free Full Text]
  31. Nordin BE, Need AG, Morris HA, O'Loughlin PD, Horowitz M: Effect of age on calcium absorption in postmenopausal women.Am J Clin Nutr80 :998 –1002,2004 .[Abstract/Free Full Text]
  32. Paia M, Antoine JM, Mateos-Guardia JA, Leplingard A, Lenoir-Wijnkoop I: Assessment of the benefits of live yoghurt: methods and markers for in vivo studies of the physiological effects of yoghurt cultures.Microbial Ecol Health Dis15 :79 –87,2003 .
  33. Halpern GM: Benefits of yoghurt.Int J Immunother9 :65 –68,1993 .
  34. Davies KM, Rafferty K, Heaney RP: Determinants of endogenous calcium entry into the gut.Am J Clin Nutr80 :919 –923,2004 .[Abstract/Free Full Text]
  35. Nickel KP, Martin BR, Smith DL, Smith JB, Miller GD, Weaver CM: Calcium bioavailability from bovine milk and dairy products in premenopausal women using intrinsic and extrinsic labelling techniques:J Nutr126 :1406 –1411,1996 .[Abstract/Free Full Text]
  36. Parra D, Martinez JA: Amino acid uptake in lactose intolerance from a probiotic milk.Br J Nutr , in press,2007 .



This article has been cited by other articles:


Home page
 AMERICAN JOURNAL OF LIFESTYLE MEDICINEHome page
D. J. Gaskin and J. Z. Ilich
Lactose Maldigestion Revisited: Diagnosis, Prevalence in Ethnic Minorities, and Dietary Recommendations to Overcome It
American Journal of Lifestyle Medicine, May 1, 2009; 3(3): 212 - 218.
[Abstract] [PDF]

Home page
 Nutr Clin PractHome page
A. Minocha
Probiotics for Preventive Health
Nutr Clin Pract, April 1, 2009; 24(2): 227 - 241.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Figures Only
Right arrow Full Text (PDF)
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Parra, M. D.
Right arrow Articles by Martínez, J. A.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Parra, M. D.
Right arrow Articles by Martínez, J. A.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS