The Effects of Probiotics in Lactose Intolerance a Systematic Review
Nutrients. 2020 May; 12(5): 1487.
Furnishings of Prebiotic and Probiotic Supplementation on Lactase Deficiency and Lactose Intolerance: A Systematic Review of Controlled Trials
Rosaura Leis
iDepartment of Pediatrics, University Clinical Hospital of Santiago de Compostela, 15704 Santiago de Compostela, Spain; moc.liamg@lortsaced.jm (M.-J.d.C.); moc.liamg@sielsnaciparuasor (R.P.); se.sagres@ocip.ecuoc.zul.airam (Thou.L.C.)
2IDIS-Health Inquiry Institute of Santiago de Compostela, 15704 Santiago de Compostela, Spain
threeCIBEROBN, Instituto Salud Carlos III, 28029 Madrid, Spain
4Facultad de Medicina, Departamento de Pediatría, Universidad de Santiago de Compostela, 15704 Santiago de Compostela, Spain; moc.liamg@samaledalemrac
María-José de Castro
1Department of Pediatrics, University Clinical Hospital of Santiago de Compostela, 15704 Santiago de Compostela, Kingdom of spain; moc.liamg@lortsaced.jm (M.-J.d.C.); moc.liamg@sielsnaciparuasor (R.P.); se.sagres@ocip.ecuoc.zul.airam (Grand.L.C.)
iiIDIS-Health Research Institute of Santiago de Compostela, 15704 Santiago de Compostela, Kingdom of spain
5CIBERER, Instituto Salud Carlos III, 28029 Madrid, Spain
Carmela de Lamas
4Facultad de Medicina, Departamento de Pediatría, Universidad de Santiago de Compostela, 15704 Santiago de Compostela, Spain; moc.liamg@samaledalemrac
María L. Couce
aneDepartment of Pediatrics, Academy Clinical Hospital of Santiago de Compostela, 15704 Santiago de Compostela, Spain; moc.liamg@lortsaced.jm (M.-J.d.C.); moc.liamg@sielsnaciparuasor (R.P.); se.sagres@ocip.ecuoc.zul.airam (Grand.L.C.)
2IDIS-Health Research Institute of Santiago de Compostela, 15704 Santiago de Compostela, Spain
4Facultad de Medicina, Departamento de Pediatría, Universidad de Santiago de Compostela, 15704 Santiago de Compostela, Spain; moc.liamg@samaledalemrac
vCIBERER, Instituto Salud Carlos Three, 28029 Madrid, Spain
Received 2020 Mar 31; Accepted 2020 May eleven.
Abstract
Lactose intolerance (LI) is characterized past the presence of primarily gastrointestinal clinical signs resulting from colonic fermentation of lactose, the absorption of which is impaired due to a deficiency in the lactase enzyme. These clinical signs can be modified by several factors, including lactose dose, residual lactase expression, concurrent ingestion of other dietary components, gut-transit fourth dimension, and enteric microbiome composition. In many of individuals with lactose malabsorption, clinical signs may be absent later consumption of normal amounts of milk or, in particular, dairy products (yogurt and cheese), which comprise lactose partially digested past live bacteria. The abdominal microbiota can be modulated past biotic supplementation, which may alleviate the signs and symptoms of LI. This systematic review summarizes the available evidence on the influence of prebiotics and probiotics on lactase deficiency and LI. The literature search was conducted using the MEDLINE (via PUBMED) and SCOPUS databases following Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines, and included randomized controlled trials. For each study selected, the risk of bias was assessed following the Cochrane Collaboration methodology. Our findings showed varying degrees of efficacy but an overall positive relationship betwixt probiotics and LI in relation to specific strains and concentrations. Limitations regarding the wide heterogeneity between the studies included in this review should be taken into account. Simply one report examined the benefits of prebiotic supplementation and LI. So further clinical trials are needed in order to gather more prove.
Keywords: prebiotics, probiotics, lactose intolerance, hydrogen breath test, vomiting, diarrhea, flatulence, intestinal pain
one. Introduction
Lactose intolerance (LI) is one of the most common forms of food intolerance and occurs when lactase action is reduced in the brush border of the small bowel mucosa [1,2]. It is characterized past the presence of gastrointestinal symptoms including vomiting, diarrhea, flatulence, and abdominal hurting, which are acquired past colonic fermentation of unabsorbed lactose [3,iv]. The severity of LI, and of the same symptoms, tin can vary considerably between individuals.
Lactase deficiency can be chief, secondary, or built. The most frequent form is master lactase deficiency, a consequence of lactase non-persistence characterized by a progressive decline in lactase activity [5]. The prevalence of developed-type lactase deficiency varies among different ethnic groups and geographic locations (following a due north–south gradient), ranging from 5%–fifteen% in Northern Cardinal Europe and North American countries to xl% in Mediterranean countries and 65%–90% in African, Asian, and South American countries [6,seven,8]. In Europe, it is related to the presence of two single nucleotide polymorphisms (SNPs), C/T-13910 and Chiliad/A-22018, which mediate lactase downregulation after infancy [ix]. Secondary lactase deficiency is acquired by pathologies (e.g., celiac disease, Crohn's illness, or infection) and procedures (due east.g., surgery) that affect the pocket-sized intestine and induce a loss of enzyme activity [10,11,12]. Congenital lactase deficiency is characterized by the total absence of lactase activeness [thirteen]. This form is extremely rare and manifests at nativity, soon later on the introduction of milk. Lactase levels are minimal or absent in affected infants, which have an otherwise normal abdominal mucosa. Gastrointestinal mucosal biopsy is the gold standard for the diagnosis of lactase deficiency, although the hydrogen breath exam (HBT) is as well commonly used [14,15]. Bacterial fermentation of undigested and unabsorbed lactose leads to an increase in exhaled hydrogen. A deficit in the lactase enzyme leads to lactose malabsorption, since the disaccharide cannot exist absorbed and is instead fermented by gut microbiota, leading to the development of clinical signs feature of LI. Management of LI typically consists of reducing, or even avoiding, the consumption of dairy products [16,17]. All the same, because dairy products plant a loftier-quality source of calcium, potassium, poly peptide, and vitamin B and D, abstention of these foods tin can increment the risk of morbidity, including bone fracture, osteoporosis, and nutrient deficiencies [xviii,19,20]. The most preferred and reliable handling option involves the consumption of lactose-free dairy products. Furthermore, lactase enzyme supplementation in tablet grade [21] can be employed in a timely manner when ingesting products with lactose. Yet, the effects of exogenous lactase assistants in reducing LI symptoms vary considerably [22].
Clinical symptomatology in LI is modified by several factors, including the load of the lactose substrate, lactase activity, the speed of abdominal transit, the rate of gastric elimination, and colonic compensation [1,ii,23]. Probiotics and prebiotics have attracted considerable interest in recent years as potential symptomatic treatments for lactase insufficiency, owing to their ability to modulate the gastrointestinal flora, promoting lactase digestion and increasing colonic compensation [24,25]. Indeed, consumption of yoghurt containing live bacterial cultures has been shown to better maldigestion and symptoms in lactase-deficient individuals. Moreover, consumption of fresh rather than pasteurized yoghurt is associated with improved lactose assimilation [26]. All the same, information technology should be borne in mind that unabsorbed lactose may constitute a good prebiotic, helping to maintain a healthier intestinal flora [27]. Information technology should be noted that probiotics and prebiotics supplementation would non be a substitute for the lactose-free products.
Despite the same findings, data on the human relationship between prebiotic and/or probiotic supplementation and to clinical outcomes in LI individuals remain inconclusive. This systematic review presents an updated evaluation of the bachelor prove from clinical trials (CT) assessing the impact of this blazon of intervention on the clinical signs of LI and on HBT results in lactase-scarce individuals.
2. Materials and Methods
This review was carried out following Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines [28], and was registered in the International Prospective Annals of Systematic Reviews (PROSPERO). The review question, "Practise biotics influence lactose intolerance?" was formulated co-ordinate to Population, Intervention, Comparison, Outcome, Settings (PICOS) [29] criteria (Table 1).
Table one
Population, Intervention, Comparison, Outcome, Settings (PICOS) criteria [29] for the inclusion of studies of the effects of prebiotics and probiotics on lactose intolerance.
| Parameter 1 | Inclusion Criteria |
|---|---|
| Population | Lactose-intolerant subjects |
| Intervention | Controlled intake of biotics |
| Comparison | Non-exposed control grouping |
| Outcomes | Symptoms of lactose intolerance and signs of lactose malabsorption |
| Settings | Controlled trials |
2.1. Literature Search
The manufactures included in this review were selected from SCOPUS and PUBMED databases. Moreover, a manual search of the reference list of included ones was washed in order to ensure that all eligible studies were selected. ("Lactobacillus" [Mesh] OR "Bifidobacterium" [Mesh] OR "Saccharomyces boulardii" [Mesh] OR "Streptococcus thermophilus" [Mesh] OR "Prebiotics" [Mesh] OR "Probiotics" [Mesh]) AND "Lactose Intolerance" [Mesh] was the PUBMED search formula used. The Scopus database was searched using the following formula: "Lactose Intolerance" AND ("Lactobacillus" OR "Bifidobacterium" OR "Saccharomyces boulardii" OR "Streptococcus thermophilus" OR Prebiotics OR Probiotics).
2.2. Inclusion and Exclusion Criteria
Manufactures considered for inclusion were any controlled trial, randomized or not, published in English or Spanish between 1 January 1900 and 31 December 2019. All studies of LI patients of whatsoever age and ethnicity who underwent an intervention with prebiotics and/or probiotics were considered. The following exclusion criteria were applied: Patients with chronic diseases and/or studies that combine the consumption of biotics with other non-biotic elements, not controlled in some way by an independent arm, that could interfere with the results.
2.iii. Intervention Types
Studies considered for inclusion were those involving interventions with prebiotics and/or probiotics in populations with altered lactose absorption. Whatever report that met these characteristics, regardless of elapsing, intensity, or type of biotic used, was considered for inclusion.
2.4. Chief Outcome Measures
The primary outcome measures of lactose metabolism were the concentration of exhaled hydrogen after lactose intake and the percentage of patients with normalized HBT results. For the cess of gastrointestinal symptomatology, nosotros considered all studies that provided data on symptom comeback, either using standardized scales for symptom measurements or past measuring symptom disappearance.
two.v. Written report Selection
Two authors (G.-J.d.C. and C.d.50.) independently selected the nine articles [xxx,31,32,33,34,35,36,37,38], ultimately, included in the review from a total of 633 studies obtained by database searches. In cases in which no consensus was reached, R.L., R.P., and M.L.C. acted equally arbitrators.
two.vi. Data Extraction
The 2 authors independently extracted the following data from the selected articles: Publication year; number of participants by sex, age, intervention characteristics, and treatment duration; trial type; issue measures; results; and conclusions. Whatsoever discrepancies were arbitrated past the remaining authors.
2.7. Assessment of Risk of Bias
Post-obit the methodology of The Cochrane Collaboration, London, UK [39], ii evaluators independently assessed the hazard of bias in each written report. For each study, each of the following risks of bias were assessed: Pick bias (random sequence generation, allocation concealment); performance bias (blinding of participants and personnel); detection bias (blinding of issue assessment); compunction bias (incomplete outcome data); reporting bias (selective reporting); and any other forms of bias. For each study, the chance of each type of bias was classified as low, high or, in cases in which insufficient information were reported, unclear. In cases of a lack of consensus, R.Fifty. and M.L.C. acted as arbitrators.
3. Results
Figure i summarizes the process by which articles were selected for this systematic review. The SCOPUS search generated 528 articles, while de PUBMED search allowed united states of america to obtain 45 more than studies. Two more than articles, from the manual review of the bibliography of the participating articles, were included. Of the 633 manufactures identified in database searches, 61 duplicate articles were excluded, and 555 were excluded due to a lack of relevance of the abstract (205 did not include a LI population, 124 lacked a biotic intervention, 122 were preclinical studies, 101 were systematic or narrative reviews, and 3 were published in languages other than English or Spanish). Of the 17 total-text articles reviewed, four were excluded due to the lack of a control group; two due to unsuitable intervention characteristics; one due to the absence of data on gastrointestinal symptoms or lactose metabolism; and one due to the publication language. Ultimately, ix [30,31,32,33,34,35,36,37,38] articles were selected for inclusion in this systematic review.
Menstruation chart depicting literature search procedure.
3.1. Study Characteristics
Table two and Table iii summarize the main characteristics of the nine [30,31,32,33,34,35,36,37,38] selected randomized clinical trials (RCTs), which are ordered co-ordinate to the age of the study population. Five crossover trials were included [thirty,31,35,36,38]. All studies [30,31,32,33,34,35,36,37,38] were published after 1983, and 5 [31,32,33,34,35] in the last 10 years. In total, the ix studies included 304 LI patients, of whom 111 participated in crossover clinical trials. The age of the written report populations ranged from 5 to 75 years, and but one study [thirty] involved a pediatric population. One of the included studies [34] involved an intervention with prebiotics (xv 1000 RP-G28 (95% GOS)/day in capsules). Of the viii studies [30,31,32,33,35,36,37,38] involving probiotic interventions, iii [31,33,37] consisted of an intervention with a single strain and five [30,32,35,36,38] with two or iii strains. All of the probiotic interventions [30,31,32,33,35,36,37,38] involved some species of Lactobacillus: L. acidophilus (five) [30,31,36,37,38]; L. bulgaricus (2) [36,38]; 50. plantarum (1) [32]; L. reuteri (ane) [33]; or Fifty. rhamnosus (i) [35]. Other strains studied included Bifidobacterium animalis [32], Bifidobacterium longum [35], and Streptococcus thermophilus [30,38]. The dose of probiotic used ranged from x7 [38] CFU (colony-forming units) to 1010 CFU [xxx,32]. 3 [30,36,38] of the studies included in the review, all of which were crossover studies, were based on a punctual intervention, while in the remaining six [31,32,33,34,35,37] the duration of the intervention ranged from six days to 6 weeks (hateful, 24.83 ± 12.86 days).
Tabular array 2
Effects of prebiotics and probiotics on symptoms of lactose intolerance in 170 individuals with lactose malabsorption in controlled trials.
| Reference | n | Age, y 1 | Intervention | Trial Type (Intervention Duration) | Outcome Measure | Results 2 | Conclusions |
|---|---|---|---|---|---|---|---|
| Montes et al. (1995) [30] | 20 (11F) | v–16 | IG1: 10ten CFU L. acidophilus IG2: 108 CFU L. acidophilus + 1010 CFU S. thermophilus (250 mL milk) | Crossover RCT (-) | Mean 8-h symptom score for abdominal pain, bloating, borborygmi and flatus (0 = absent-minded, iv = astringent symptoms) afterward ingestion of 2 yard/kg of lactose | Symptom score: IG1 0.nine ± 0.43; IG2 1.62 ± 0.71; CG iv.6 ± 0.73 | Significantly lower symptom score |
| Pakdaman et al. (2016) [31] | 38 | 18–75 | 109 CFU DDS-1 strain of L. acidophilus/mean solar day (capsules) | Crossover RCT (4 weeks) | Hateful vi-h symptom scores (0 = no symptoms, x = most astringent symptoms) after ingestion of 25 1000 of lactose | Abdominal cramping: IG 1.94 ± 2.341; CG 2.39 ± 2.188 Bowel sounds: IG two.76 ± ii.536; CG 2.86 ± 2.497 Diarrhea: IG 1.34 ± two.462; CG 1.69 ± 2.558 Flatulence: IG 3.xvi ± 2.873; CG 3.21 ± ii.699 Vomiting: IG 0.08 ± 0.379; CG 0.36 ± 0.936 Overall symptoms: IG ix.28 ± ix.202; CG 10.51 ± 9.327 | Significantly less abdominal cramping, diarrhea, vomiting and lower overall symptom score |
| Roškar et al. (2017) [32] | 44 (36F) IG 22 | IG 28 (nineteen–54) CG 31 (18–55) | 10ten CFU L. plantarum + 1010 CFU B. animalis/day (capsules) | RCT (six weeks) | Mean LI symptom cess score (0 = absent, ten = worst) | Intestinal pain: IG 2.4 (i.3–3.four); CG 2.three (0.nine–3.7) Diarrhea: IG 0.iii (−0.1;0.eight); CG 0.6 (−0.three;i.5) Flatulence: IG iv.2 (2.9–5.5); CG 4.two (2.8–5.v) Rumble: IG iii.9 (2.8–5.i); CG 3.6 (ii.i–5.1) Vomiting: IG 0.2 (−0.ii;0.7); CG 0.2 (−0.one;0.iv) Full (Ʃ): IG 11.i (7.9–fourteen.3); CG: 10.eight (6.four–five.three) | No significant differences |
| Ojetti et al. (2010) [33] | 40 (33F) IG xx | IG 33 ± 11 CG 32 ± 12 | 8 × xviii CFU L. reuteri/day (capsules) | RCT (10 days) | Mean 8-h symptom scores values (0 = absent, 10 = severe symptoms) after ingestion of 25 g of lactose | Abdominal pain: IG 6.9 ± 1.07; CG seven.1 ± 0.72 Bloating: IG ix.95±0.88; CG vii.1 ± 0.72 Diarrhea: IG 2.95±2.07; CG 5.9 ± 0.85 Flatulence: IG 3.95 ± 1.35; CG: 5.15 ± 0.93 | Meaning improvement in abdominal pain, bloating, diarrhea, and flatulence |
| Savaiano et al. (2013) [34] | 85 (49F) IG 57 | 41 | 15 g RP-G28 (95% GOS)/day (capsules) | RCT (35 days) | Rate of disappearance of abdominal pain (%) | Abdominal hurting: IG 72%; CG 28% | Significantly higher rate of disappearance of intestinal hurting |
| Vitellio et al. (2019) [35] | 23 (19F) | 48 ± iii.1 | 4 × ten9 CFU B. longum BB536 + ten9 CFU L. rhamnosus/solar day (packets) | Crossover RCT (4 weeks) | Hateful VAS perceived symptom score (0 = absent, 100 = worst) [intestinal hurting and bloating] and mean BSFS (1 = constipation, 7 = diarrhea) | Abdominal pain: IG 39 ± 6; CG 53 ± 7 Bloating: IG 60 ± 5; CG 77 ± 4 Bowel movements: IG 3 ± 0; CG 3 ± 0 | Significantly less bloating |
| Lin et al. (1998) [36] | twenty | - | IG1: iv × xviii CFU Fifty. acidophilus/24-hour interval IG2: four × xix CFU L. acidophilus/twenty-four hours IG3: four × xeight CFU Fifty. bulgaricus/twenty-four hour period IG4: 4 × 109 CFU Fifty. bulgaricus/twenty-four hours (400 mL milk) | Crossover RCT (-) | Hateful 8-h symptom score for stomach pain, gas, and diarrhea (0 = absent-minded, v = astringent) after ingestion of 25 chiliad of lactose | Symptom score: IG1 nine.8; IG2 half dozen.five; IG3 3.9; IG4 2.8; CG 12.5 | Significantly lower symptom score in IG2, IG3, and IG4 |
Tabular array 3
Effects of prebiotics and probiotics on lactose digestion in 179 individuals with lactose malabsorption in controlled trials.
| Reference | n | Age, y 1 | Intervention | Trial Type (Intervention Duration) | Effect Measure | Results 2 | Conclusions |
|---|---|---|---|---|---|---|---|
| Kim et al. (1983) [37] | 24 IG 6 × 3 | twenty–31 | IG1: ane.25 × 107 CFU L. acidophilus/kg/24-hour interval IG2: 1.25 × xviii CFU 50. acidophilus/kg/solar day IG3: one.25 × x9 CFU L. acidophilus/kg/day (milk ten mL/kg/day) | RCT (6 days) | Change in mean breath H concentration (ppm) three h after ingestion of 5 mL/kg milk | Change in mean breath H concentration: IG1-xv.2; IG2-1.one; IG3-19.2; CG-0.3 | Significant change in mean breath H concentration in IG1 and IG3. |
| Lin et al. (1991) [38] | ten (4F) | 24–40 | IG1: 10seven CFU L. acidophilus NCFM/day IG2: x8 CFU L. acidophilus NCFM/day IG3: 10seven CFU L. acidophilus LA1/day IG4: 108 CFU L. acidophilus LA1/day IG5: ten7 CFU L. acidophilus LA2/day IG6: ten8 CFU 50. acidophilus LA2/twenty-four hour period IG7: ten7 CFU Southward. thermophilus/L. bulgaricus/day IG8: x8 CFU Due south. thermophilus/L. bulgaricus/day (400 mL milk) | Crossover RCT (-) | Mean individual breath H concentration viii h after ingestion of 25 g lactose | Breath H concentration: IG1 36.33; IG2 35.08; IG3 27.64; IG4 22.43; IG5 31.03; IG6 25.32; IG7 24.1; IG8 9.81; CG 30.78 | Significantly lower breath H concentration in IG4 and IG8 |
| Ojetti et al. (2010) [33] | 40 (33F) IG 20 | IG 33 ± 11 CG 32 ± 12 | viii × 10eight CFU L. reuteri/twenty-four hour period (capsules) | RCT (x days) | HBT normalization rate (%) Hateful tiptop H2 excretion (ppm) | HBT normalization rate: IG 35%; CG 0% Superlative H2: IG 23.1 ± 7.85; CG 31.7 ± viii.3 | Significantly higher HBT normalization rate and reduced mean peak Htwo excretion |
| Savaiano et al. (2013) [34] | 85 (49F) IG 57 | 41 | xv g RP-G28 (95% GOS)/twenty-four hours (capsules) | RCT (35 days) | Mean alter in HBT values ii h after ingestion of 25 g lactose | HBT change: IG-10.12; CG 13.95 | No pregnant differences |
| Lin et al. (1998) [36] | 20 | - | IG1: 4 × xeight CFU L. acidophilus/day IG2: 4 × 10nine CFU L. acidophilus/24-hour interval IG3: 4 × 10eight CFU L. bulgaricus/solar day IG4: 4 × 109 CFU L. bulgaricus/day (400 mL milk) | Crossover RCT (-) | Mean hourly breath H concentration 8 h after ingestion of 25 g lactose | Breath H: IG1 262; IG2 231; IG3 188; IG4 135; CG 280 | Significantly lower jiff H concentration in IG3 and IG4 (L. bulgaricus) |
3.2. Prebiotics, Probiotics, and LI Symptoms
Seven [30,31,32,33,34,35,36] of the manufactures included in this systematic review assessed the furnishings of prebiotics or probiotics on symptoms of LI in 170 subjects with lactose malabsorption afterward ingestion of two–l g/kg of lactose. Four of the studies were crossover RCTs [30,31,35,36]. The study involving prebiotic supplementation [34] evaluated rate of disappearance of abdominal pain. The remaining half dozen studies [thirty,31,32,33,35,36] evaluated gastrointestinal symptoms using different standardized scales (of 0–4 or 0–100) to rate symptom intensity. Simply one [32] of these seven studies [thirty,31,32,33,34,35,36] reported no significant result of the intervention. The study in question conducted the longest intervention (vi weeks), using a high daily dose of probiotics (10ten CFU L. plantarum + 1010 CFU B. animalis). However, in this same written report an evaluation performed 2 weeks later completion of the intervention revealed that probiotic supplementation was associated with a significant decrease in diarrhea and flatulence.
3.3. Prebiotics, Probiotics, and Lactose Digestion
Of the nine [30,31,32,33,34,35,36,37,38] studies included in this review, simply five [33,34,36,37,38], bookkeeping for 179 individuals with lactose malabsorption, included data on lactose maldigestion subsequently ingestion of 20–50 k of lactose. In social club to reduce external factors in HBT and symptom results, the included studies followed a standardized method, consisting of dietary restrictions for the previous days, low intake of sugar, carbohydrates, and cobweb, and fasting for eight–10 h earlier the lactose challenge. In these five studies, lactose metabolism was evaluated by HBT. Two of the five studies [36,38] were crossover RCTs consisting of a punctual probiotic intervention earlier the ingestion of 25 g of lactose. The but study [34] that reported no significant effect of the intervention was the 1 in which participants underwent a prebiotic intervention. Studies comparison different doses of probiotics [36,37,38] observed significant differences between the effects of high doses and the furnishings of lower doses.
3.four. Run a risk-of-Bias Cess
Risk-of-bias cess revealed that none of the studies included [30,31,32,33,34,35,36,37,38] had a high risk of selection bias, and that the gamble of random sequence generation was depression in all cases. The adventure of reporting bias was uncertain for all 9 studies [xxx,31,32,33,34,35,36,37,38]. A high hazard of compunction bias was observed for only one study [30], and a high risk of performance bias for two (22%) [xxx,33]. A loftier risk of detection bias was observed for two (22%) [30,38] studies. The take chances of other biases was high in the five crossover studies [30,31,35,36,38], due to the high risk of deport-over, and in one multicenter report [34], which lacked standardized protocols.
The study with the highest risk of biased results was that of Montes et al. [30], for which the level of hazard was deemed low for only one of the 7 forms of bias assessed. Our analyses revealed that there was no loftier risk of any of the forms of bias assessed in 2 studies [32,37]. In the 6 [31,33,34,35,36,38] remaining articles, the risk of bias was deemed high for only ane [31,33,34,35,36] or two [38] of the forms of bias assessed. Farther information on the risk-of-bias assessment can be found in the Supplementary Materials.
4. Discussion
This systematic review of RCTs assesses the effects of probiotic or prebiotic supplementation on HBT results and on the clinical signs of LI. Probiotic supplementation improved both outcomes in patients with LI. Prebiotic supplementation, which was assessed in only one study [34], had a beneficial effect on clinical signs of LI but not on HBT results.
Evaluation of the RCTs included in this review revealed that probiotic supplementation in individuals with LI significantly reduced intestinal cramping, diarrhea, airsickness, bloating, and/or flatulence. This upshot, together with the reduction in exhaled H2, may exist explained by several mechanisms. First, upon reaching the digestive system probiotics act as a source of lactase in the intestinal tract [40], increasing the overall hydrolytic chapters and colonic fermentation [41]. 2d, probiotics exert antagonistic furnishings on heterofermentative bacteria (which produce gas), enhancing colonic compensation [42] by secreting antibiotic-like substances [43], adhering competitively to the mucosa, and modulating the permeability of the intestinal barrier [44,45]. Other mechanisms, like decreasing lactose load [46] and delaying gastric emptying and orocecal transit time, which are dependent on the accompanying matrix, should be irrelevant [47].
Common criteria used to select the genus, species, and strains of probiotic microorganisms include tolerance to the intestinal environment, capacity to adhere to the intestinal mucosa, and competitive exclusion of pathogens [48]. In the nine studies evaluated here, well-nigh of the species of probiotics administered (including 50. acidophilus, L. reuteri, Fifty. rhamnosus, and L. bulgaricus, S. thermophilus, and B. longum) were effective in attenuating clinical signs. Only ane written report [32], in which L. plantarum and B. animalis were administered, observed no pregnant event of the probiotic on clinical signs. However, beneficial furnishings of both microorganisms have been demonstrated both in vitro and in vivo. Specifically, B. animalis is one of the most mutual leaner plant in gut microbiota and one of the best studied probiotic bifidobacteria; this bacterium has stiff mucus adherence properties, inhibits pathogens, and improves barrier part [49], besides as enhancing lactose digestion and increasing transit fourth dimension in patients with LI [50]. The lack of upshot of this probiotic may be explained past the fact that different types and different concentrations of probiotics may exert different effects, and just specific combinations of probiotics may exist constructive in alleviating symptoms, in line with the global guidelines of the Earth Gastroenterology Organisation [https://www.worldgastroenterology.org/UserFiles/file/guidelines/probiotics-and-prebiotics-english-2017.pdf].
Prebiotics are functional foods that stimulate the growth of beneficial native gut bacteria and increase colon permeability [51], potentially mitigating the symptoms of LI. Specifically, galacto-oligosaccharides (GOS) have been shown to increase the abundance of lactose-fermenting Bifidobacterium, Faecalibacterium, Lactobacillus, and Roseburia species in the gut [52]. It should be noted that mechanisms of GOS utilization by intestinal leaner are not fully understood, and efficacy and response vary between strains [53].
Lactase deficiency and lactose malabsorption in humans is ordinarily assessed using the HBT [1], which measures the concentration of exhaled H2 afterward ingestion of lactose. The increment in exhaled Hii results from the release of gases by heterofermentative bacteria that assimilate lactose [53]. However, the correlation between lactose malabsorption (or the load of undigested lactose) and LI (presence of symptoms) is not always clear: The HBT is thought to produce five%–15% fake negatives, mainly due to not-hydrogen production and methyl hydride production [54,55,56].
While one study included in this systematic review found no significant subtract in exhaled H2 concentration following a probiotic intervention, the authors did notice a significant subtract in abdominal hurting [34]. This may be explained by the fact that gases are partially responsible for the symptoms of LI. In a study of thirty self-described "severely lactose intolerant individuals", Suarez et al. [57] found that HBT values were normal in 30% of the participants. This pct exceeds the estimated charge per unit of imitation negatives due to marsh gas product and suggests a role of other pathophysiological mechanisms in LI (e.g., an osmotic consequence caused by the presence of lactose molecules in the gastrointestinal tract) [58]. Furthermore, patient-related factors not direct related to lactose digestion are too implicated in LI. These include feet, loftier levels of psychosocial stress, and functional gastrointestinal disorders such equally irritable bowel syndrome [59].
It should be noted that dose is a disquisitional parameter when administering probiotics, every bit the changes that occur in the composition of the microflora depend on the minimum number of microorganisms required for colonization [60]. The importance of dose option has also been emphasized by the joint working group of the FAO/WHO (2002), which recommended defining probiotics as "live microorganisms which when administered in adequate amounts confer a health benefit on the host". Nigh of the studies included in this review tested but a unmarried dose of probiotics, ranging from 108 –1011 CFU/mean solar day. Only 1 study (Lin et al. 1998) compared two different doses (4 × 10eight and 4 × 109 CFU/24-hour interval) for ii different Lactobacillus species (L. acidophilus and Fifty. bulgaricus), and reported a dose-dependent effect on clinical signs of LI. In measuring the effects on HBT, one study (Lin et al. 1991) compared different doses (10seven–10viii CFU/solar day) for three different L. acidophilus strains (NCFM, LA1, and LA2) and the combination of S. thermophilus and L. bulgaricus, and reported amend results with higher doses.
Another factor that should be taken into account is the duration of the intervention and its impact later discontinuation. This consequence was addressed in a study of individuals with IL who underwent a iv-week probiotic intervention consisting of a combination of Lactobacillus casei Shirota and Bifidobacterium breve Yakult [61]. The intervention improved symptoms and decreased the concentration of exhaled hydrogen, and the furnishings persisted for at least iii months subsequently discontinuation. However, data from patients with other gastrointestinal diseases, such as irritable bowel syndrome, advise that the effects of probiotics may wane several weeks after discontinuation [62]. Because LI is a chronic condition and changes in gut microbiota may not persist, long-term efficacy trials, especially those that examine effects afterwards cessation of handling, are needed.
The limitations of this review are related to the high heterogeneity of the selected studies, including the historic period of the participants (ane study was conducted in children, one study did not mention the age of the participants and the remaining ones were conducted in adults). Abdominal microbiota varies with historic period [63], which implies that results may non be comparable between children and adults. Another limitation is the wide variation of the duration of the intervention, ranging from a timely intervention to vi weeks probiotics administration. Given that duration of the intervention is a cardinal gene to see changes in gut flora following probiotics and prebiotics consumption, longer interventions are desirable in order to ensure that a potential consequence can be observed.
v. Conclusions
The findings of this systematic review support the beneficial effects of probiotic supplementation on HBT results and on LI symptoms, every bit evidenced past decreases in the concentration of exhaled hydrogen and reductions in abdominal cramping, diarrhea, airsickness, bloating, and/or flatulence. Further long-term trials should exist conducted in order to determine the persistence of the benign furnishings of probiotic administration and whether symptoms worsen later discontinuing supplementation. Based on our findings, prove supporting the beneficial furnishings of prebiotic supplementation remains inconclusive.
Supplementary Materials
The post-obit material is available online at https://www.mdpi.com/2072-6643/12/5/1487/s1. Figure S1, Risk-of-bias summary: Summary of the authors' rating on each hazard-of-bias item for each study. Figure S2, Risk-of-bias graph: Review of the authors' judgments on each risk-of-bias item, expressed as percentages across studies.
Writer Contributions
R.L. and Thou.L.C. contributed to the design, methodology and supervision of the study. R.P. contributed to presentation of results and drafting of the manuscript. C.d.L. and M.-J.d.C. contributed to data selection, extraction, and analysis, presentation of the results and drafting of the manuscript All authors have read and agreed to the published version of the manuscript.
Funding
This research received no external funding.
Conflicts of Involvement
The authors declare no conflict of interest.
References
i. Misselwitz B., Butter M., Verbeke K., Trick M.R. Update on lactose malabsorption and intolerance: Pathogenesis, diagnosis and clinical management. Gut. 2019;68:2080–2091. doi: 10.1136/gutjnl-2019-318404. [PMC costless article] [PubMed] [CrossRef] [Google Scholar]
ii. Fassio F., Facioni Thousand.South., Guagnini F. Lactose Maldigestion, Malabsorption, and Intolerance: A Comprehensive Review with a Focus on Current Management and Future Perspectives. Nutrients. 2018;10:1599. doi: 10.3390/nu10111599. [PMC free article] [PubMed] [CrossRef] [Google Scholar]
3. Deng Y., Misselwitz B., Dai N., Fox M. Lactose Intolerance in Adults: Biological Mechanism and Dietary Direction. Nutrients. 2015;seven:8020–8035. doi: 10.3390/nu7095380. [PMC free article] [PubMed] [CrossRef] [Google Scholar]
iv. Di Costanzo M., Berni Canani R. Lactose Intolerance: Common Misunderstandings. Ann. Nutr. Metab. 2018;73:thirty–37. doi: 10.1159/000493669. [PubMed] [CrossRef] [Google Scholar]
5. Silberman Due east.South., Jin J. Lactose Intolerance. JAMA. 2019;322:1620. doi: 10.1001/jama.2019.9608. [PubMed] [CrossRef] [Google Scholar]
six. Liebert A., López Southward., Jones B.Fifty., Montalva Northward., Gerbault P., Lau W. World-wide distributions of lactase persistence alleles and the complex furnishings of recombination and selection. Hum. Genet. 2017;136:1445–1453. doi: 10.1007/s00439-017-1847-y. [PMC gratis article] [PubMed] [CrossRef] [Google Scholar]
7. Storhaug C.50., Fosse S.K., Fadnes L.T. Country, regional, and global estimates for lactose malabsorption in adults: A systematic review and meta-assay. Lancet Gastroenterol. Hepatol. 2017;2:738–746. doi: 10.1016/S2468-1253(17)30154-ane. [PubMed] [CrossRef] [Google Scholar]
8. Leis R., Tojo R., Pavón P., Douwes A. Prevalence of lactose malabsorption in Galicia. J. Pediatr. Gastroenterol. Nutr. 1997;25:296–300. doi: x.1097/00005176-199709000-00009. [PubMed] [CrossRef] [Google Scholar]
9. Ingram C.J., Mulcare C.A., Itan Y., Thomas M.Thousand., Swallow D.M. Lactose digestion and the evolutionary genetics of lactase persistence. Hum. Genet. 2009;124:579–591. doi: 10.1007/s00439-008-0593-6. [PubMed] [CrossRef] [Google Scholar]
ten. Hu Y., Gui Fifty., Chang J., Liu J., Xu S., Deng C., Yu F., Ma Z., Wang G., Zhang C. The incidence of infants with rotavirus enteritis combined with lactose intolerance. Pak. J. Pharm. Sci. 2016;29:321–323. [PubMed] [Google Scholar]
xi. Szilagyi A., Galiatsatos P., Xue X.A. Systematic review and meta-analysis of lactose digestion, its touch on on intolerance and nutritional effects of dairy food restriction in inflammatory bowel diseases. Nutr. J. 2016;xv:67. doi: 10.1186/s12937-016-0183-8. [PMC free article] [PubMed] [CrossRef] [Google Scholar]
12. Ojetti 5., Gabrielli M., Migneco A., Lauritano C., Zocco M.A., Scarpellini E., Nista E.C., Gasbarrini G., Gasbarrini A. Regression of lactose malabsorption in coeliac patients after receiving a gluten-free diet. Scand. J. Gastroenterol. 2008;43:174–177. doi: 10.1080/00365520701676138. [PubMed] [CrossRef] [Google Scholar]
13. Heyman One thousand.B. Committee on Nutrition. Lactose intolerance in infants, children, and adolescents. Pediatrics. 2006;118:1279–1286. doi: ten.1542/peds.2006-1721. [PubMed] [CrossRef] [Google Scholar]
14. Rezaie A., Buresi Thousand., Lembo A., Lin H., McCallum R., Rao S., Schmulson M., Valdovinos Chiliad., Zakko S., Pimentel One thousand. Hydrogen and Methane-Based Breath Testing in Gastrointestinal Disorders: The North American Consensus. Am. J. Gastroenterol. 2017;112:775–784. doi: 10.1038/ajg.2017.46. [PMC gratuitous commodity] [PubMed] [CrossRef] [Google Scholar]
15. Rojo C., Jaime F., Azócar L., Hernández C., Villagrán A., Miquel J.F., Arancibia G. Concordance between Lactose Quick Test, hydrogen-methane jiff test and genotyping for the diagnosis of lactose malabsorption in children. Neurogastroenterol. Motil. 2018;30:e13271. doi: 10.1111/nmo.13271. [PubMed] [CrossRef] [Google Scholar]
16. Shaukat A., Levitt M.D., Taylor B.C., MacDonald R., Shamliyan T.A., Kane R.Fifty., Wilt T.J. Systematic review: Effective management strategies for lactose intolerance. Ann. Intern. Med. 2010;152:797–803. doi: ten.7326/0003-4819-152-12-201006150-00241. [PubMed] [CrossRef] [Google Scholar]
17. Szilagyi A., Ishayek N. Lactose Intolerance, Dairy Avoidance, and Treatment Options. Nutrients. 2018;x:1994. doi: 10.3390/nu10121994. [PMC costless article] [PubMed] [CrossRef] [Google Scholar]
18. Hodges J.K., Cao S., Cladis D.P., Weaver C.Thousand. Lactose Intolerance and Bone Health: The Challenge of Ensuring Adequate Calcium Intake. Nutrients. 2019;11:718. doi: 10.3390/nu11040718. [PMC gratuitous commodity] [PubMed] [CrossRef] [Google Scholar]
19. Savaiano D. Lactose intolerance: An unnecessary risk for low bone density. Nestle Nutr. Workshop Ser. Pediatr. Program. 2011;67:161–171. doi: 10.1159/000325582. [PubMed] [CrossRef] [Google Scholar]
20. Grenov B., Briend A., Sangild P.T., Thymann T., Rytter M.H., Hother A.L., Mølgaard C., Michaelsen K.F. Undernourished Children and Milk Lactose. Nutrient Nutr. Bull. 2016;37:85–99. doi: 10.1177/0379572116629024. [PubMed] [CrossRef] [Google Scholar]
21. Ianiro G., Pecere S., Giorgio 5., Gasbarrini A., Cammarota G. Digestive Enzyme Supplementation in Gastrointestinal Diseases. Curr. Drug Metab. 2016;17:187–193. doi: 10.2174/138920021702160114150137. [PMC costless article] [PubMed] [CrossRef] [Google Scholar]
22. Ibba I., Gilli A., Boi M.F., Usai P. Furnishings of exogenous lactase administration on hydrogen breath excretion and intestinal symptoms in patients presenting lactose malabsorption and intolerance. BioMed Res. Int. 2014;2014:680196. doi: ten.1155/2014/680196. [PMC free article] [PubMed] [CrossRef] [Google Scholar]
23. de Vrese Thousand., Stegelmann A., Richter B., Fenselau S., Laue C., Schrezenmeir J. Probiotics—Compensation for lactase insufficiency. Am. J. Clin. Nutr. 2001;73:421S–429S. doi: x.1093/ajcn/73.ii.421s. [PubMed] [CrossRef] [Google Scholar]
24. Morelli L. Yogurt, living cultures, and gut health. Am J Clin Nutr. 2014;99:1248S–1250S. doi: 10.3945/ajcn.113.073072. [PubMed] [CrossRef] [Google Scholar]
25. Singh R.K., Chang H.W., Yan D., Lee K.M., Ucmak D., Wong K., Abrouk Grand., Farahnik B., Nakamura M., Zhu T.H., et al. Influence of diet on the gut microbiome and implications for human health. J. Transl. Med. 2017;xv:73. doi: 10.1186/s12967-017-1175-y. [PMC free commodity] [PubMed] [CrossRef] [Google Scholar]
26. Saborido R., Leis R. Yogurt and dietary recommendations for lactose intolerance. Nutr. Hosp. 2018;35:45–48. doi: 10.20960/nh.2287. [PubMed] [CrossRef] [Google Scholar]
27. Szilagyi A. Lactose—A potential prebiotic. Aliment. Pharmacol. Ther. 2002;16:1591–1602. doi: 10.1046/j.1365-2036.2002.01321.ten. [PubMed] [CrossRef] [Google Scholar]
28. Moher D., Shamseer L., Clarke M., Ghersi D., Liberati A., Petticrew M., PRISMA-P Grouping Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 argument. Syst. Rev. 2015;4:1. doi: 10.1186/2046-4053-4-1. [PMC free article] [PubMed] [CrossRef] [Google Scholar]
29. Sackett D.L., Strauss S.E., Richardson W.S. Show-Based Medicine: How to Practice and Teach EBM. Churchill-Livingstone; London, United kingdom of great britain and northern ireland: 2000. [Google Scholar]
30. Montes R.M., Bayless T.M., Saavedra J.M., Perman J.A. Effect of milks inoculated with Lactobacillus acidophilus or a yogurt starter culture in lactose-maldigesting children. J. Dairy Sci. 1995;78:1657–1664. doi: 10.3168/jds.S0022-0302(95)76790-X. [PubMed] [CrossRef] [Google Scholar]
31. Pakdaman Thou.N., Udani J.K., Molina J.P., Shahani Chiliad. The effects of the DDS-1 strain of lactobacillus on symptomatic relief for lactose intolerance—A randomized, double-blind, placebo-controlled, crossover clinical trial. Nutr. J. 2016;15:56–67. doi: 10.1186/s12937-016-0172-y. [PMC free article] [PubMed] [CrossRef] [Google Scholar]
32. Roškar I., Švigelj Thou., Štempelj M., Volfand J., Štabuc B., Malovrh Š., Rogelj I. Effects of a probiotic product containing Bifidobacterium animalis subsp. animalis IM386 and Lactobacillus plantarum MP2026 in lactose intolerant individuals: Randomized, placebo-controlled clinical trial. J. Funct. Foods. 2017;35:1–8. doi: x.1016/j.jff.2017.05.020. [CrossRef] [Google Scholar]
33. Ojetti V., Gigante One thousand., Gabrielli M., Ainora M.E., Mannocci A., Lauritano E.C., Gasbarrini G., Gasbarrini A. The upshot of oral supplementation with Lactobacillus reuteri or tilactase in lactose intolerant patients: Randomized trial. Eur. Rev. Med. Pharmacol. Sci. 2010;fourteen:163–170. [PubMed] [Google Scholar]
34. Savaiano D.A., Ritter A.J., Klaenhammer T.R., James One thousand.M., Longcore A.T., Chandler J.R., Walker W.A., Foyt H.L. Improving lactose digestion and symptoms of lactose intolerance with a novel galacto-oligosaccharide (RP-G28): A randomized, double-blind clinical trial. Nutr. J. 2013;12:160. doi: 10.1186/1475-2891-12-160. [PMC free article] [PubMed] [CrossRef] [Google Scholar]
35. Vitellio P., Celano G., Bonfrate L., Gobbetti M., Portincasa P., De Angelis K. Effects of bifidobacterium longum and lactobacillus rhamnosuson gut microbiota in patients with lactose intolerance and persisting functional gastrointestinal symptoms: A randomised, double-blind, Crossover study. Nutrients. 2019;xi:886. doi: 10.3390/nu11040886. [PMC complimentary article] [PubMed] [CrossRef] [Google Scholar]
36. Lin One thousand.Y., Yen C.L., Chen S.H. Management of lactose maldigestion by consuming milk containing lactobacilli. Dig. Dis. Sci. 1998;43:133–137. doi: 10.1023/A:1018840507952. [PubMed] [CrossRef] [Google Scholar]
37. Kim H.S., Gilliland S.E. Lactobacillus acidophilus equally a dietary adjunct for milk to aid lactose digestion in humans. J. Dairy Sci. 1983;66:959–966. doi: 10.3168/jds.S0022-0302(83)81887-6. [PubMed] [CrossRef] [Google Scholar]
38. Lin M.Y., Savaiano D., Harlander S. Influence of nonfermented dairy products containing bacterial starter cultures on lactose maldigestion in humans. J. Dairy Sci. 1991;74:87–95. doi: x.3168/jds.S0022-0302(91)78147-2. [PubMed] [CrossRef] [Google Scholar]
39. Higgins J.P.T., Altman D.K., Sterne J.A.C. In: Cochrane Handbook for Systematic Reviews of Interventions. Higgins J.P.T., Green S., editors. The Cochrane Collaboration; London, United kingdom of great britain and northern ireland: 2006. [(accessed on 9 March 2020)]. Version 5.1.0. Bachelor online: www.cochrane-handbook.org. [Google Scholar]
40. He T., Priebe Thousand.One thousand., Zhong Y., Huang C., Harmsen H.J., Raangs Thou.C., Antoine J.M., Welling M.W., Vonk R.J. Effects of yogurt and bifidobacteria supplementation on the colonic microbiota in lactose-intolerant subjects. J. Appl. Microbiol. 2008;104:595–604. doi: 10.1111/j.1365-2672.2007.03579.x. [PubMed] [CrossRef] [Google Scholar]
41. Dhama K., Latheef Southward.Grand., Munjal A.Thou., Khandia R., Samad H.A., Iqbal H.M.North., Joshi Southward.Chiliad. Probiotics in Curing Allergic and Inflammatory Weather—Inquiry Progress and Futuristic Vision. Recent Pat. Inflamm. Allergy Drug Discov. 2017;10:105–118. doi: ten.2174/1872213X10666161226162229. [PubMed] [CrossRef] [Google Scholar]
42. Solomons N.West. Fermentation, fermented foods and lactose intolerance. Eur. J. Clin. Nutr. 2002;56:S50–S55. doi: x.1038/sj.ejcn.1601663. [PubMed] [CrossRef] [Google Scholar]
43. Corr S., Hill C., Gahan C.G. Understanding the mechanisms by which probiotics inhibit gastrointestinal pathogens. Adv. Nutrient Nutr. Res. 2009;56:i–15. doi: 10.1016/S1043-4526(08)00601-iii. [PubMed] [CrossRef] [Google Scholar]
44. Bischoff S.C., Barbara G., Buurman W., Ockhuizen T., Schulzke J.D., Serino M., Tilg H., Watson A., Wells J.K. Intestinal permeability—A new target for disease prevention and therapy. BMC Gastroenterol. 2014;14:189. doi: 10.1186/s12876-014-0189-vii. [PMC gratuitous article] [PubMed] [CrossRef] [Google Scholar]
45. Belkaid Y., Hand T.W. Role of the microbiota in immunity and inflammation. Prison cell. 2014;157:121–141. doi: 10.1016/j.jail cell.2014.03.011. [PMC costless commodity] [PubMed] [CrossRef] [Google Scholar]
46. Savaiano D.A. Lactose digestion from yogurt: Machinery and relevance. Am. J. Clin. Nutr. 2014;99:1251S–1255S. doi: x.3945/ajcn.113.073023. [PubMed] [CrossRef] [Google Scholar]
47. Born P., Sekatcheva M., Rösch T., Classen M. Carbohydrate malabsorption in clinical routine: A prospective observational study. Hepatogastroenterology. 2006;53:673–677. [PubMed] [Google Scholar]
48. Shokryazdan P., Faseleh Jahromi M., Liang J.B., Ho Y.W. Probiotics: From Isolation to Application. J. Am. Coll. Nutr. 2017;36:666–676. doi: 10.1080/07315724.2017.1337529. [PubMed] [CrossRef] [Google Scholar]
49. Zhu D., Dominicus Y., Huo Chiliad.C., Yang L., Liu F., Li A., Meng X.C. Complete genome sequence of Bifidobacterium animalis subsp. lactis KLDS 2.0603, a probiotic strain with digestive tract resistance and adhesion to the abdominal epithelial cells. J. Biotechnol. 2016;220:49–fifty. doi: 10.1016/j.jbiotec.2016.01.013. [PubMed] [CrossRef] [Google Scholar]
fifty. Zhong Y., Huang C.Y., He T., Harmsen H.M. Result of probiotics and yogurt on colonic microflora in subjects with lactose intolerance. Wei Sheng Yan Jiu. 2006;35:587–591. [PubMed] [Google Scholar]
51. Davis L.Thousand., Martínez I., Walter J., Goin C., Hutkins R.W. Barcoded pyrosequencing reveals that consumption of galactooligosaccharides results in a highly specific bifidogenic response in humans. PLoS Ane. 2011;6:e25200. doi: 10.1371/journal.pone.0025200. [PMC costless article] [PubMed] [CrossRef] [Google Scholar]
52. Azcarate-Peril M.A., Ritter A.J., Savaiano D., Monteagudo-Mera A., Anderson C., Magness S.T., Klaenhammer T.R. Impact of brusk-chain galactooligosaccharides on the gut microbiome of lactose-intolerant individuals. Proc. Natl. Acad. Sci. USA. 2017;114:E367–E375. doi: 10.1073/pnas.1606722113. [PMC free article] [PubMed] [CrossRef] [Google Scholar]
53. Arnold J.Westward., Simpson J.B., Roach J., Bruno-Barcena J.K., Azcarate-Peril 1000.A. Prebiotics for Lactose Intolerance: Variability in Galacto-Oligosaccharide Utilization past Abdominal Lactobacillus rhamnosus. Nutrients. 2018;10:1517. doi: 10.3390/nu10101517. [PMC free article] [PubMed] [CrossRef] [Google Scholar]
54. Knudsen C.D., Di Palma J.A. Carbohydrate challenge tests: Do yous need to mensurate methane? S. Med. J. 2012;105:251–253. doi: 10.1097/SMJ.0b013e318252d428. [PubMed] [CrossRef] [Google Scholar]
55. Harvie R.M., Constrict C.J., Schultz M. Evaluation of lactulose, lactose, and fructose breath testing in clinical do: A focus on methane. JGH Open. 2019;four:198–205. doi: x.1002/jgh3.12240. [PMC costless article] [PubMed] [CrossRef] [Google Scholar]
56. de Lacy Costello B.P., Ledochowski M., Ratcliffe N.G. The importance of methane breath testing: A review. J. Breath Res. 2013;vii:024001. doi: 10.1088/1752-7155/seven/ii/024001. [PubMed] [CrossRef] [Google Scholar]
57. Suarez F.L., Savaiano D.A., Levitt Yard.D. A comparison of symptoms afterwards the consumption of milk or lactose-hydrolyzed milk by people with self-reported severe lactose intolerance. N. Engl. J. Med. 1995;333:one–4. doi: 10.1056/NEJM199507063330101. [PubMed] [CrossRef] [Google Scholar]
58. Camilleri G., Sellin J.H., Barrett M.E. Pathophysiology, Evaluation, and Management of Chronic Watery Diarrhea. Gastroenterology. 2017;152:515–532. doi: 10.1053/j.gastro.2016.10.014. [PMC free commodity] [PubMed] [CrossRef] [Google Scholar]
59. Dainese R., Casellas F., Mariné-Barjoan E., Vivinus-Nébot M., Schneider South.K., Hébuterne X., Piche T. Perception of lactose intolerance in irritable bowel syndrome patients. Eur. J. Gastroenterol. Hepatol. 2014;26:1167–1175. doi: 10.1097/1000000.0000000000000089. [PubMed] [CrossRef] [Google Scholar]
threescore. Larsen C.Due north., Nielsen S., Kaestel P., Brockmann E., Bennedsen Grand., Christensen H.R., Eskesen D.C., Jacobsen B.L., Michaelsen K.F. Dose-response study of probiotic leaner Bifidobacterium animalis subsp lactis BB-12 and Lactobacillus paracasei subsp paracasei CRL-341 in healthy young adults. Dose-response study of probiotic leaner Bifidobacterium animalis subsp lactis BB-12 and Lactobacillus paracasei subsp paracasei CRL-341 in healthy immature adults. Eur. J. Clin. Nutr. 2006;60:1284–1293. [PubMed] [Google Scholar]
61. Almeida C.C., Lorena South.L., Pavan C.R., Akasaka H.M., Mesquita K.A. Beneficial effects of long-term consumption of a probiotic combination of lactobacillus casei shirota and bifidobacterium breve yakult may persist later suspension of therapy in lactose-intolerant patients. Nutr. Clin. Pract. 2012;27:247–251. doi: 10.1177/0884533612440289. [PubMed] [CrossRef] [Google Scholar]
62. Begtrup L.Thou., de Muckadell O.B., Kjeldsen J., Christensen R.D., Jarbøl D.E. Long-term treatment with probiotics in master intendance patients with irritable bowel syndrome—A randomised, double-bullheaded, placebo controlled trial. Scand. J. Gastroenterol. 2013;48:1127–1135. doi: 10.3109/00365521.2013.825314. [PubMed] [CrossRef] [Google Scholar]
63. Maynard C., Weinkove D. The gut microbiota and ageing. Subcell. Biochem. 2018;90:351–371. doi: x.1007/978-981-13-2835-0_12. [PubMed] [CrossRef] [Google Scholar]
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