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Cited by 80Oral microbiology and periodontitis researchGut microbiota and healthDental Health and Care Utilization

Analysis of the Effects of Dietary Pattern on the Oral Microbiome of Elite Endurance Athletes

Open access
Murtaza, Nida, Burke, Louise M., Vlahovich, Nicole, Charlesson, Bronwen, O’Neill, Hayley M., Ross, Megan L., Campbell, Katrina L., Krause, Lutz +1 more·2019·Nutrients
DOI 10.3390/nu11030614PMC PMC6471070
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Abstract

Although the oral microbiota is known to play a crucial role in human health, there are few studies of diet x oral microbiota interactions, and none in elite athletes who may manipulate their intakes of macronutrients to achieve different metabolic adaptations in pursuit of optimal endurance performance. The aim of this study was to investigate the shifts in the oral microbiome of elite male endurance race walkers from Europe, Asia, the Americas and Australia, in response to one of three dietary patterns often used by athletes during a period of intensified training: a High Carbohydrate (HCHO; n = 9; with 60% energy intake from carbohydrates; ~8.5 g kg−1 day−1 carbohydrate, ~2.1 g kg−1 day−1 protein, 1.2 g kg−1 day−1 fat) diet, a Periodised Carbohydrate (PCHO; n = 10; same macronutrient composition as HCHO, but the intake of carbohydrates is different across the day and throughout the week to support training sessions with high or low carbohydrate availability) diet or a ketogenic Low Carbohydrate High Fat (LCHF; n = 10; 0.5 g kg−1 day−1 carbohydrate; 78% energy as fat; 2.1 g kg−1 day−1 protein) diet. Saliva samples were collected both before (Baseline; BL) and after the three-week period (Post treatment; PT) and the oral microbiota profiles for each athlete were produced by 16S rRNA gene amplicon sequencing. Principal coordinates analysis of the oral microbiota profiles based on the weighted UniFrac distance measure did not reveal any specific clustering with respect to diet or athlete ethnic origin, either at baseline (BL) or following the diet-training period. However, discriminant analyses of the oral microbiota profiles by Linear Discriminant Analysis (LDA) Effect Size (LEfSe) and sparse Partial Least Squares Discriminant Analysis (sPLS-DA) did reveal changes in the relative abundance of specific bacterial taxa, and, particularly, when comparing the microbiota profiles following consumption of the carbohydrate-based diets with the LCHF diet. These analyses showed that following consumption of the LCHF diet the relative abundances of Haemophilus, Neisseria and Prevotella spp. were decreased, and the relative abundance of Streptococcus spp. was increased. Such findings suggest that diet, and, in particular, the LCHF diet can induce changes in the oral microbiota of elite endurance walkers.

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Written from the paper’s full text.

TL;DR

In elite male race walkers, three weeks of intensified training with three different dietary patterns did not produce distinct global oral microbiome clustering by diet or ethnicity, but discriminant analyses found taxon-specific shifts, especially after a ketogenic low-carbohydrate high-fat (LCHF) diet. The LCHF diet was associated with decreased relative abundance of *Haemophilus*, *Neisseria*, and *Prevotella* and increased *Streptococcus*.

Key findings

  • Weighted UniFrac PCoA showed no specific clustering of oral microbiota by diet or athlete ethnic origin at baseline or post-treatment; RDA and ANOSIM also found no significant community-composition differences between baseline and any diet.
  • Shannon alpha diversity decreased after diet-training versus subject-matched baseline, but not significantly: p = 0.1 for baseline vs HCHO and baseline vs PCHO; p = 0.62 for baseline vs LCHF.
  • After LCHF, discriminant analyses showed decreased relative abundances of *Haemophilus*, *Neisseria*, and *Prevotella* spp. and increased *Streptococcus* spp.; post-intervention LEFSe showed *Streptococcus*-affiliated OTUs enriched for LCHF, whereas Gram-negative taxa such as *Haemophilus* and *Leptotrichia* were enriched for HCHO/PCHO.
  • Mixed-effect linear regression found some taxa changed within diets—e.g., HCHO: *Atopobium* increased (p = 0.015), *Capnocytophaga* (p = 0.027) and *Porphyromonas* (p = 0.03) decreased; PCHO: *Peptostreptococcus* decreased (p = 0.009); LCHF: *Fusobacterium* decreased (p = 0.02) and *Streptococcus* increased (p = 0.048)—but significance was lost after FDR correction (FDR = 0.49 for HCHO, 0.4 for PCHO, 0.4 for LCHF).

Methods

  • Non-randomized dietary intervention nested in the “Supernova 1” study: 21 elite male race walkers aged 20–35 years, BMI 16–23 kg/m², from multiple countries, yielding 29 study experiences (13 athletes in one camp, 8 in both); athletes self-selected HCHO (n = 9), PCHO (n = 10), or LCHF (n = 10) during three weeks of intensified training at the Australian Institute of Sport.
  • Saliva was collected before (baseline) and after the three-week diet-training period; DNA was extracted and the V6–V8 hypervariable regions of 16S rRNA genes were sequenced on Illumina MiSeq, then processed in QIIME with USEARCH 6.1, Greengenes 13.8, 97% OTU clustering, and rarefaction to 6861 reads.
  • Analyses included Shannon alpha diversity, weighted/unweighted UniFrac PCoA, RDA, ANOSIM, LEFSe, sparse PLS-DA, and mixed-effect linear regression, with p < 0.05 considered significant and FDR correction applied for multiple testing.

Limitations

  • Stated by the paper: small participant number; no matching non-athlete cohort; no comprehensive habitual dietary intake data for baseline samples; elite athlete group size limited power for stringent statistical tests and subgrouping by ethnicity.
  • Stated by the paper: diet assignment was non-random, with athletes freely choosing their diet, though this was intended to promote adherence and control for random effects of rigorous dietary control.
  • Evident from the text: many taxon-level differences did not remain significant after FDR correction, and the paper did not directly measure nitrate/nitrite/NO pathway function or performance outcomes in this oral microbiome analysis; links to exercise economy and NO homeostasis are discussed as plausible interpretations.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.3390/nu11030614

Cites

Statistics

Nothing to recompute.

Claims the paper makes

0 of 8 cited sources checked · 0 supported · 0 flagged

  • Findingown data

    No substantive differences between the two baseline microbiota profiles of the eight athletes recruited in both camps were apparent, as assessed by Shannon alpha-diversity and ANOSIM beta-diversity analyses.

    “No substantive differences between the two microbiota profiles were apparent, as assessed by Shannon alpha-diversity and ANOSIM beta-diversity analyses.”
    Quote in the paperSubstantial claim
  • Findingown data

    Following consumption of the LCHF diet, the relative abundances of Haemophilus, Neisseria and Prevotella spp. were decreased.

    “These analyses showed that following consumption of the LCHF diet the relative abundances of Haemophilus, Neisseria and Prevotella spp. were decreased, and the relative abundance of Streptococcus spp. was increased.”
    • Also stated in: § 5. Conclusions · plain
      “The LCHF diet resulted in the most dramatic effects on the oral microbiota, with reductions in the relative abundance (Haemophilus, Neisseria and Prevotella), and with a coincident increase in the relative abundance of Streptococcus spp.”
    Quote in the paperSubstantial claim
  • Findingown data

    Discriminant analyses of the oral microbiota profiles by LEfSe and sPLS-DA revealed changes in the relative abundance of specific bacterial taxa, particularly when comparing the microbiota profiles following consumption of the carbohydrate-based diets with the LCHF diet.

    “However, discriminant analyses of the oral microbiota profiles by Linear Discriminant Analysis (LDA) Effect Size (LEfSe) and sparse Partial Least Squares Discriminant Analysis (sPLS-DA) did reveal changes in the relative abundance of specific bacterial taxa, and, particularly, when comparing the microbiota profiles following consumption of the carbohydrate-based diets with the LCHF diet.”
    Quote in the paperSubstantial claim
  • Findingown data

    Following consumption of the LCHF diet, the relative abundance of Streptococcus spp. was increased.

    “These analyses showed that following consumption of the LCHF diet the relative abundances of Haemophilus, Neisseria and Prevotella spp. were decreased, and the relative abundance of Streptococcus spp. was increased.”
    • Also stated in: § 5. Conclusions · plain
      “The LCHF diet resulted in the most dramatic effects on the oral microbiota, with reductions in the relative abundance (Haemophilus, Neisseria and Prevotella), and with a coincident increase in the relative abundance of Streptococcus spp.”
    Quote in the paperSubstantial claim
  • Findingown data

    RDA and ANOSIM did not identify any significant differences between the microbiota community composition at baseline and following any of the three dietary interventions.

    “Similarly, the supervised analyses by RDA and ANOSIM did not identify any significant differences between the microbiota community composition at BL and following any of the three dietary interventions (data not shown).”
    Quote in the paperSubstantial claim
  • May combine two claims. 13
  • Classified as probably not a substantial claim. 4

  • May combine two claims.

    Findingown data

    Post-intervention LefSe analyses showed that Streptococcus-affiliated OTUs were discriminating and enriched for the LCHF diet, whereas Gram-negative bacteria such as Haemophilus and Leptotrichia spp. were among the enriched and discriminating taxa for the HCHO/PCHO diets.

    “LefSe analyses was also used to examine the differences in oral microbiomes post intervention and these analyses showed that the discriminating and enriched taxa (at the OTU level) were Streptococcus affiliated OTUs for the LCHF diet intervention, whereas Gram-negative bacteria (e.g., Haemophilus and Leptotrichia spp.) were among the enriched and discriminating taxa for the HCHO/PCHO diets (Figure”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    The Shannon alpha diversity was reduced following the diet-training interventions compared to subject-matched baseline measures, but these reductions were not statistically significant (p = 0.1 for BL vs. HCHO and BL vs. PCHO; p = 0.62 for BL vs. LCHF).

    “The Shannon alpha diversity was reduced following the diet-training interventions when compared to their subject-matched BL measures; however, these reductions were not statistically significant (p = 0.1 for BL vs. HCHO and BL vs PCHO; p = 0.62 for BL vs. LCHF).”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductreasoning

    The elite nature of the athletes ensured the group size was quite small, which reduces the power needed for stringent statistical tests of significance or further subgrouping of athletes according to ethnicity.

    “Furthermore, but understandably, the elite nature of the athletes ensured the group size is quite small, which also reduces the power needed for stringent statistical tests of significance, or the further subgrouping of the athletes according to ethnicity, etc.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductown data

    The study was approved by the Ethics committee of the Australian Institute of Sports and UQ-HREC, and the clinical trial was registered with the Australian New Zealand Clinical Trials Registry.

    “The study was approved by the Ethics committee of the Australian Institute of Sports (AIS, no. 20150802) and UQ-HREC 2015001965. The clinical trial is registered by the Australian New Zealand Clinical Trials Registry (ANZCTR) and has been assigned the number ACTRN12618001529235.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationown data

    The dietary interventions do not result in dramatic changes in the overall biodiversity of the oral microbiome, but rather more subtle changes in community composition.

    “Taken together, these results suggest that the dietary interventions do not result in dramatic changes in the overall biodiversity of the oral microbiome, but rather more subtle changes in community composition.”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim. May combine two claims.

    Premisecitation

    The LCHF group experienced an increase in the oxygen cost of exercise supported by high rates of fat oxidation and thereby failed to improve race performance despite a gain in aerobic capacity.

    “However, while this was associated with improved economy and real-world race performance in the two groups who trained while consuming the HCHO and PCHO diets, the LCHF group experienced an increase in the oxygen cost of exercise supported by high rates of fat oxidation, and thereby failed to improve their race performance despite the gain in aerobic capacity [6].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [6] Burke, 2017, Low carbohydrate, high fat diet impairs exercise economy and negates the performance benefit from intensified training in elite race walkers, J. Physiol. source

      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation

    A LCHF diet might alter the baseline contribution of the nitrate-nitrite-NO pathway to NO-related health and performance benefits in athletes and reduce their responsiveness to nitrate/beetroot juice supplementation as a performance aid.

    “This suggests that a LCHF diet might alter the baseline contribution of the nitrate-nitrite-NO pathway to NO-related health and performance benefits in athletes, as well as reduce their responsiveness to nitrate/beetroot juice supplementation as a performance aid [22].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [22] Jones, 2014, Influence of dietary nitrate on the physiological determinants of exercise performance: A critical review, Appl. Physiol. Nutr. Metab. Physiol. Appl. Nutr. Metab. source

      Not checked in the free run.

  • May combine two claims.

    Study design and conductreasoning

    The lack of a matching cohort of non-athletes and the lack of comprehensive data on habitual dietary intake of athletes are acknowledged limitations of the trial design.

    “The lack of a matching cohort of non-athletes (non-race walkers) and the lack of comprehensive data on the habitual dietary intake of athletes (i.e., BL samples) are acknowledged but were beyond the logistical and financial scope of the trial design.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationreasoning

    Part of the reduced exercise efficiency observed in the Supernova 1 study might be attributed to an altered oral microbiome, resulting in reduced nitrate/nitrite reducing activity and NO generation, with coordinate effects on circulation and mitochondrial function.

    “However, based on the findings reported here, it is also plausible that part of the reduced exercise efficiency observed in the Supernova 1 study might be attributed to an altered oral microbiome, resulting in a reduction in nitrate/nitrite reducing activity and NO generation, with coordinate effects on circulation and mitochondrial function.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: Haemophilus, Neisseria and Prevotella are well-known Gram-negative nitrate/nitrite reducers, and Streptococcus spp. are not recognised to be directly involved in nitrate/nitrite reduction.

  • May combine two claims.

    Interpretationown data

    The LCHF diet resulted in the most dramatic effects on the oral microbiota, with reductions in Haemophilus, Neisseria and Prevotella and a coincident increase in Streptococcus spp.

    “The LCHF diet resulted in the most dramatic effects on the oral microbiota, with reductions in the relative abundance (Haemophilus, Neisseria and Prevotella), and with a coincident increase in the relative abundance of Streptococcus spp.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationown data

    The time between the study camps was sufficiently long to ensure a washout between the two camps and no potential carryover effects from the previous diet on the subsequent results/profiles.

    “These tests indicate that the time between the study camps was sufficiently long to ensure a “washout” between the two camps, and, thereby, no potential carryover effects from the previous diet on the subsequent results/profiles.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Study design and conductreasoning

    The non-random assignment of athletes to diets promoted adherence to the intervention and controlled for random effects of rigorous dietary control, so any effects on the oral microbiome could be attributed to the diet.

    “Therefore, any effects on the oral microbiome could be attributed to the diet, including any additional intrinsic biochemical, physiological or psychological overlay that belongs to the diet itself.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    The bacterial taxa found in this study are similar to those in the Human Oral Microbiome Database and those typically reported in other studies of mainstream human subjects.

    “The bacterial taxa found in this study are similar to those represented in the Human Oral Microbiome Database (HOMD), as well as those typically reported in other studies of mainstream human subjects [17,18].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [17] Bik, 2010, Bacterial diversity in the oral cavity of 10 healthy individuals, ISME J. source

      Not checked in the free run.

    • cites [18] Aas, 2005, Defining the normal bacterial flora of the oral cavity, J. Clin. Microbiol. source

      Not checked in the free run.

13 of 13

  • The paper relies on this without support.

    This is the first study of its type with elite endurance athletes, and one of the very few studies of diet/nutrients × oral microbiota interactions affecting the physiology and/or metabolism of healthy human subjects.

    “However, and despite these limitations, this is the first study of its type with elite endurance athletes, and one of the very few studies of the diet/nutrients × oral microbiota interactions affecting the physiology and/or metabolism of healthy human subjects.”

  • The paper relies on this without support.

    Haemophilus, Neisseria and Prevotella are well-known Gram-negative nitrate/nitrite reducers, and Streptococcus spp. are not recognised to be directly involved in nitrate/nitrite reduction.

    “Taken together, the changes seen following consumption of the LCHF diet, with respect to reductions in the relative abundances of well-known Gram-negative nitrate/nitrite reducers such as Haemophilus, Prevotella and Neisseria; and an increase in Streptococcus spp., which are not recognised to be directly involved in nitrate/nitrite reduction; raises the spectre that consumption of the LCHF diet”
2 of 2

Claims other papers make about this one

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Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

  • LCHF protein intake differs between the abstract and Methods

    Minor

    The abstract gives the LCHF diet's protein intake as 2.1 g/kg/day, while the Methods give approximately 2.2 g/kg/day.

1 of 1

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References 24 · Cited by 80

Authors
Murtaza, N., Burke, L. M., Vlahovich, N., Charlesson, B., O’Neill, H. M., Ross, M. L., Campbell, K. L., Krause, L., & Morrison, M.
Affiliations
  • Translational Research Institute (AU)
  • Australian Catholic University (AU)
  • Bond University (AU)
  • Australian Institute of Sport, Canberra, ACT 2617, Australia
Corresponding author
  • Burke, Louise M.
  • Morrison, Mark
ORCID
Venue
Nutrients
Publisher
MDPI AG
Published
2019-03-13
Volume
11
Issue
3
Pages
614
ISSN
2072-6643 (ISSN-L)
DOI
10.3390/nu11030614
PMC
PMC6471070
OpenAlex
W2921869723
Semantic Scholar
06418e5cfb1103ef40b5abb05b8d4981ddeaa867
Cited by
80
References
24
Citations by year
2026: 3 · 2025: 5 · 2024: 17 · 2023: 9 · 2022: 13 · 2021: 11 · 2020: 16 · 2019: 5 · 2018: 1
FWCI
13.05
Type
journal article
Language
en
Open access
Licence
Locations
  • Nutrients (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Bond University Research Portal (Bond University) (submittedVersion, cc-by)
  • Research Bank (Australian Catholic University) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Griffith Research Online (submittedVersion, cc-by)
Funders
CRN AESS (201300800)
Topics
  • Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
  • Health Sciences › Dentistry › Periodontics › Dental Health and Care Utilization
Keywords
oral microbiota, dietary habits, endurance athletes, race walking, ketogenic diet, low-carbohydrate high-fat diet, high-carbohydrate diet, macronutrient intake, saliva microbiota, Haemophilus, Neisseria, Prevotella, Streptococcus, diet-microbiome interactions
MeSH terms
Adult, Bacteria, Dietary Carbohydrates, Dietary Fats, Humans, Male, Mouth, Nutritional Status, Physical Endurance, Sports, Walking, Young Adult, Physical Conditioning, Human

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