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A Narrative Review of Human Clinical Trials to Improve Lactose Digestion and Tolerance by Feeding Bifidobacteria or Galacto-Oligosacharides.
Mysore Saiprasad, S, Moreno, OG, Savaiano, DA
Nutrients. 2023;(16)
Abstract
Supplementation with the probiotic Bifidobacterium and prebiotic galacto-oligosaccharides (GOS) could improve gut health and benefit lactose intolerant individuals. A narrative review was conducted to identify human clinical trials that evaluated lactose digestion and/or tolerance in response to consumption of Bifidobacterium, GOS, or both. A total of 152 studies on Bifidobacterium and GOS or both were published between 1983 and 2022. Out of the 152 studies, 20 were human clinical trials conducted in lactose intolerant subjects; 8 studies were conducted with Bifidobacterium supplementation and 3 studies involved GOS supplementation. Five studies reported favorable outcomes of Bifidobacterium supplementation in managing lactose intolerance (LI). Similarly, three studies reported favorable outcomes with GOS supplementation. The other three studies reported neutral outcomes. In conclusion, most studies reported a favorable effect of Bifidobacterium and GOS on managing the symptoms of LI. No study has examined the effects of combined supplementation with Bifidobacterium and GOS in lactose intolerant subjects. Future research could examine if co-supplementation with Bifidobacterium and GOS is a more effective strategy to reduce the dairy discomfort in LI individuals.
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Relationships of Intestinal Lactase and the Small Intestinal Microbiome with Symptoms of Lactose Intolerance and Intake in Adults.
Jansson-Knodell, CL, Krajicek, EJ, Ramakrishnan, M, Rogers, NA, Siwiec, R, Bohm, M, Nowak, T, Wo, J, Lockett, C, Xu, H, et al
Digestive diseases and sciences. 2022;(12):5617-5627
Abstract
BACKGROUND Approximately two-thirds of adults are genetically predisposed to decreased lactase activity after weaning, putting them at risk of lactose intolerance. However, symptoms are a poor marker of lactose maldigestion. AIMS We assessed association between self-reported lactose intolerance and intestinal lactase, lactose intake, and the small intestinal microbiome. METHODS Patients 18-75 years presenting for upper endoscopy were recruited prospectively. Observational study participants completed a lactose intolerance symptom questionnaire and reported lactose intake. Post-bulbar biopsies were obtained to measure lactase activity and assess the small intestinal mucosal microbiome. We compared intestinal lactase between patients with and without lactose intolerance. We assessed associations between lactose intolerance symptoms and lactase and lactose intake. We examined associations of small bowel microbial composition with self-reported lactose intolerance and symptoms. RESULTS Among 34 patients, 23 (68%) reported lactose intolerance. Those with lactose intolerance had higher total symptom scores, more frequent bowel urgency, and more bowel movements after consuming dairy. The proportion of individuals with abnormal lactase activity did not differ by lactose intolerance status. Median lactase levels were correlated with total lactose intolerance symptom scores (p = 0.038) and frequency of bowel urgency (p = 0.012). Daily lactose intake did not differ between groups. In 19 patients, we observed significant associations of small intestinal microbiome beta diversity with stool consistency after consuming dairy (p = 0.03). CONCLUSIONS Intestinal lactase is associated with lactose intolerance symptoms and bowel urgency in adults but does not distinguish the clinical phenotype entirely. Studying other contributing factors (microbiota, diet) may further clarify the pathophysiology of lactose intolerance.
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A double-blind, 377-subject randomized study identifies Ruminococcus, Coprococcus, Christensenella, and Collinsella as long-term potential key players in the modulation of the gut microbiome of lactose intolerant individuals by galacto-oligosaccharides.
Azcarate-Peril, MA, Roach, J, Marsh, A, Chey, WD, Sandborn, WJ, Ritter, AJ, Savaiano, DA, Klaenhammer, TR
Gut microbes. 2021;(1):1957536
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Abstract
Background. Our recent publication (Chey et al., Nutrients 2020) showed that a 30-day administration of pure galacto-oligosaccharides (GOS) significantly reduced symptoms and altered the fecal microbiome in patients with lactose intolerance (LI). Results. In this addendum, we performed an in-depth analysis of the fecal microbiome of the 377 LI patients randomized to one of two GOS doses (Low, 10-15 grams/day or High, 15-20 grams/day), or placebo in a multi-center, double-blinded, placebo-controlled trial. Sequencing of 16S rRNA amplicons was done on GOS or placebo groups at weeks zero (baseline), four (end of treatment), nine, 16 and 22. Taxa impacted by treatment and subsequent dairy consumption included lactose-fermenting species of Bifidobacterium, Lactobacillus, Lactococcus, and Streptococcus. Increased secondary fermentation microorganisms included Coprococcus and Ruminococcus species, Blautia producta, and Methanobrevibacterium. Finally, tertiary fermenters that use acetate to generate butyrate were also increased, including Faecalibacterium prausnitzii, Roseburia faecis, and C. eutactus. Conclusions. Results confirmed and expanded data on GOS microbiome modulation in LI individuals. Microbiome analysis at 16 and 22 weeks after treatment further suggested relatively long-term benefits when individuals continued consumption of dairy products.
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Yogurt, cultured fermented milk, and health: a systematic review.
Savaiano, DA, Hutkins, RW
Nutrition reviews. 2021;79(5):599-614
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Plain language summary
Many fermented foods are associated with health benefits, including fermented dairy products. Whereby diary itself is part of many nutritional guidelines, the guidances rarely distinguish between dairy and fermented dairy. This qualitative, systematic review sought to capture how consumption of fermented milk products influences health. The review included 108 studies, with over 70% reporting beneficial health outcomes. A small number of studies reported insignificant or neutral results and four unfavourable ones. The aspects of health that were considered included lactose digestion and tolerance, gut health and disease, diarrhoea and constipation, irritable bowel syndrome, cardiovascular health and disease, hypertension, blood lipids, cancer risk, colorectal/breast/prostate cancer, weight and body composition, diabetes risk and metabolic syndrome and bone health. The authors concluded that eating fermented dairy products aided lactose digestion and showed a consistent link with reduced risk of breast and colorectal cancer, type 2 diabetes, and improved weight maintenance, cardiovascular, bone, and gastrointestinal health. As dairy appears to increase the risk for prostate cancer, fermented dairy seems to be no different here to unfermented dairy at increasing the risk. Some potential mechanisms are proposed in the discussion section, how fermented dairy may elicit its health benefits. Given the predominant health benefits of fermented dairy, the authors encouraged to include fermented dairy into national nutrition guidelines and stress distinction between dairy and fermented dairy products. This review captures current evidence of the widespread health benefits of fermented dairy consumption worthwhile considering in clinical practice. In the absence of more clear findings in relation to prostate cancer and prevention, a cautious approach to dairy and fermented dairy consumption may be warranted.
Abstract
Consumption of yogurt and other fermented products is associated with improved health outcomes. Although dairy consumption is included in most dietary guidelines, there have been few specific recommendations for yogurt and cultured dairy products. A qualitative systematic review was conducted to determine the effect of consumption of fermented milk products on gastrointestinal and cardiovascular health, cancer risk, weight management, diabetes and metabolic health, and bone density using PRISMA guidelines. English language papers in PubMed were searched, with no date restrictions. In total, 1057 abstracts were screened, of which 602 were excluded owing to lack of appropriate controls, potential biases, and experimental design issues. The remaining 455 papers were independently reviewed by both authors and 108 studies were included in the final review. The authors met regularly to concur, through consensus, on relevance, methods, findings, quality, and conclusions. The included studies were published between 1979 and 2017. From the 108 included studies, 76 reported a favorable outcome of fermented milks on health and 67 of these were considered to be positive or neutral quality according to the Academy of Nutrition and Dietetics' Quality Criteria Checklist. Of the 32 remaining studies, the study outcomes were either not significant (28) or unfavorable (4), and most studies (18) were of neutral quality. A causal relationship exists between lactose digestion and tolerance and yogurt consumption, and consistent associations exist between fermented milk consumption and reduced risk of breast and colorectal cancer and type 2 diabetes, improved weight maintenance, and improved cardiovascular, bone, and gastrointestinal health. Further, an association exists between prostate cancer occurrence and dairy product consumption in general, with no difference between fermented and unfermented products. This article argues that yogurt and other fermented milk products provide favorable health outcomes beyond the milk from which these products are made and that consumption of these products should be encouraged as part of national dietary guidelines. Systematic review registration: PROSPERO registration no. CRD42017068953.
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Lactose Intolerance: A Concise Review to Skim the Surface.
Jansson-Knodell, CL, Krajicek, EJ, Savaiano, DA, Shin, AS
Mayo Clinic proceedings. 2020;(7):1499-1505
Abstract
Lactose intolerance is a common but poorly understood cause of gastrointestinal symptoms. Contrary to popular belief, there is much more to its diagnosis beyond symptoms with exposure and management beyond milk- and dairy-product avoidance. In this article, we review definitions, genetic basis, pathogenesis, clinical signs, as well as diagnostic and management strategies.
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Milk Containing A2 β-Casein ONLY, as a Single Meal, Causes Fewer Symptoms of Lactose Intolerance than Milk Containing A1 and A2 β-Caseins in Subjects with Lactose Maldigestion and Intolerance: A Randomized, Double-Blind, Crossover Trial.
Ramakrishnan, M, Eaton, TK, Sermet, OM, Savaiano, DA
Nutrients. 2020;12(12)
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Lactose intolerant people cannot digest a sugar molecule in milk called lactose, leading to uncomfortable symptoms like abdominal pain, bloating, flatulence, diarrhoea and faecal urgency. The symptoms may appear within a few hours of consuming the milk. Previous studies in the Chinese and Australian populations have shown that milk consumption containing only the A2 β-casein protein caused fewer lactose intolerance symptoms than milk containing both A1 and A2 β-casein protein. Casein is a protein abundant in milk. Conventional milk contains both A1 and A2 β-casein protein. The digestion of A1 β-casein protein releases a peptide called β-casomorphin-7, which may contribute to lactose intolerance symptoms. This randomised, double-blind, crossover single-meal trial aims to determine the tolerance of four different types of milk that contain A1 and A2 β-casein protein to varying concentrations among 33 people with lactose intolerance and maldigestion. The participants who consumed milk containing only A2 β-casein protein reported less abdominal pain than those who drank conventional milk or Jersey milk. The results of this study will need to be confirmed by further research in a larger population. Healthcare professionals can use this study when making dietary recommendations.
Abstract
Acute-feeding and multiple-day studies have demonstrated that milk containing A2 β-casein only causes fewer symptoms of lactose intolerance (LI) than milk containing both A1 and A2 β-caseins. We conducted a single-meal study to evaluate the gastrointestinal (GI) tolerance of milk containing different concentrations of A1 and A2 β-casein proteins. This was a randomized, double-blind, crossover trial in 25 LI subjects with maldigestion and an additional eight lactose maldigesters who did not meet the QLCSS criteria. Subjects received each of four types of milk (milk containing A2 β-casein protein only, Jersey milk, conventional milk, and lactose-free milk) after overnight fasting. Symptoms of GI intolerance and breath hydrogen concentrations were analyzed for 6 h after ingestion of each type of milk. In an analysis of the 25 LI subjects, total symptom score for abdominal pain was lower following consumption of milk containing A2 β-casein only, compared with conventional milk (p = 0.004). Post hoc analysis with lactose maldigesters revealed statistically significantly improved symptom scores (p = 0.04) and lower hydrogen production (p = 0.04) following consumption of milk containing A2 β-casein only compared with conventional milk. Consumption of milk containing A2 β-casein only is associated with fewer GI symptoms than consumption of conventional milk in lactose maldigesters.
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Galacto-Oligosaccharide RP-G28 Improves Multiple Clinical Outcomes in Lactose-Intolerant Patients.
Chey, W, Sandborn, W, Ritter, AJ, Foyt, H, Azcarate-Peril, MA, Savaiano, DA
Nutrients. 2020;(4)
Abstract
Background and Aims: Lactose intolerance (LI) is a global problem affecting more than half of the world's population. An ultra-purified, high-concentration galacto-oligosaccharide, RP-G28, is being developed as a treatment for patients with LI. The efficacy and safety of RP-G28 in reducing symptoms of lactose intolerance were assessed in a blinded, randomized, placebo-controlled trial. Methods: In this multiclinical site, double-blinded, placebo-controlled trial, 377 patients with LI were randomized to one of two doses of orally administered RP-G28 or placebo for 30 days. A LI test and symptom assessment were performed at baseline and on day 31. The primary endpoint was a ≥4-point reduction or a score of zero on LI composite score on day 31. Voluntary milk and dairy intake and global outcome measures assessed patients' overall treatment satisfaction and quality of life before therapy and 30 days after therapy. This study received Institutional Review Board (IRB) approval. Results: For the primary endpoint, 40% in the RP-G28 groups reported a ≥4-point reduction or no symptoms on LI symptom composite score compared to 26% with placebo (P = 0.016). Treatment with RP-G28 also led to significantly higher levels of milk and dairy intake and significant improvements in global assessments compared to placebo. RP-G28 but not placebo led to significant increases in five Bifidobacterium taxa. Conclusions: RP-G28 for 30 days significantly reduced symptoms and altered the fecal microbiome in patients with LI. Treatment with RP-G28 also improved milk/dairy consumption and quality of life and was safe and well tolerated.
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Gender, Age, Race and Lactose Intolerance: Is There Evidence to Support a Differential Symptom Response? A Scoping Review.
Lapides, RA, Savaiano, DA
Nutrients. 2018;(12)
Abstract
Research evaluating the relationship between lactose intolerance (LI) symptoms and age, gender and race is reviewed. An exhaustive search was conducted on the Google Scholar and PubMed databases. The evidence suggests that women, the elderly or specific racial groups are not more susceptible to LI, but rather dose, body size and genetic differences in lactase non-persistence (LNP) are the primary drivers of intolerance symptoms.
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Effect of school wellness policies and the Healthy, Hunger-Free Kids Act on food-consumption behaviors of students, 2006-2016: a systematic review.
Mansfield, JL, Savaiano, DA
Nutrition reviews. 2017;(7):533-552
Abstract
Federal regulation mandates that the US National School Lunch Program nutrition standards align with the Dietary Guidelines for Americans. As students consume a substantial proportion of their nutrition during school lunch, increasing access to healthy foods is proposed to improve student dietary outcomes. The purpose of this review is to assess whether policy changes impacted food-consumption behaviors of students during periods when (1) school wellness policies were implemented (2006-2007); (2) the Healthy, Hunger-Free Kids Act was passed (2010-2012); and (3) the Healthy, Hunger-Free Kids Act was implemented (2012-present). PubMed, Web of Science, and Science Direct were searched for primary research studies. Policy evaluations and interventions implemented from 2006 to 2016 were included. A total of 31 studies evaluating plate waste, dietary intake, food selection, and/or purchasing patterns were identified and reviewed. Fourteen of 19 intervention and longitudinal observation studies reported improved food-consumption behaviors (increased selection, intake, and sales of healthy foods, and decreased plate waste). Only 2 of 12 one-time observation studies reported food-consumption behaviors meeting target nutrition standards. The majority of studies indicated that increasing access to healthy foods during school lunch improved students' dietary intakes. Challenges related to study design, adaptation period, quality of foods, and policy implementation likely affect a school lunch program's ability to impact students' food-consumption behaviors. Ongoing evaluation of these programs is warranted.
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Lactose digestion from yogurt: mechanism and relevance.
Savaiano, DA
The American journal of clinical nutrition. 2014;(5 Suppl):1251S-5S
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Yogurt is traditionally consumed throughout the world among populations who are seemingly unable to digest lactose. This review provides a historical overview of the studies that show lactose digestion and tolerance from yogurt by lactose-intolerant people. The lactose in yogurt is digested more efficiently than other dairy sources of lactose because the bacteria inherent in yogurt assist with its digestion. The bacterial lactase survives the acidic conditions of the stomach, apparently being physically protected within the bacterial cells and facilitated by the buffering capacity of yogurt. The increasing pH as the yogurt enters the small intestine and a slower gastrointestinal transit time allow the bacterial lactase to be active, digesting lactose from yogurt sufficiently to prevent symptoms in lactose-intolerant people. There is little difference in the lactase capability of different commercial yogurts, because they apparently contain Lactobacillus bulgaricus and Streptococcus thermophilus in sufficient quantities (10(8) bacteria/mL). However, Lactobacillus acidophilus appears to require cell membrane disruption to physically release the lactase. Compared with unflavored yogurts, flavored yogurts appear to exhibit somewhat reduced lactase activity but are still well tolerated.