Cited by 160Seaweed-derived Bioactive CompoundsBacterial biofilms and quorum sensingOral microbiology and periodontitis research

Antimicrobial and Antibiofilm Activities of Sulfated Polysaccharides from Marine Algae against Dental Plaque Bacteria

Open access
Jun, Joon-Young, Jung, Min-Jeong, Jeong, In-Hak, Yamazaki, Koji, Kawai, Yuji, Kim, Byoung-Mok·2018·Marine Drugs

Abstract

Dental plaque biofilms cause various dental diseases; therefore, inhibiting the growths of the dental plaque bacteria which produce biofilms can be a strategy for preventing dental disease. Certain sulfated polysaccharides from marine algae exert antimicrobial activities against human bacterial pathogens in addition to their physiological benefits. On the basis of these observations, the antimicrobial and antibiofilm activities of sulfated polysaccharides from different marine algae were evaluated against dental plaque bacteria. Among the sulfated polysaccharides, a fucoidan from Fucus vesiculosus showed notable antimicrobial activities against the selected dental plaque bacteria, including some foodborne pathogenic bacteria. The minimum inhibitory concentrations were of 125 to 1000 µg mL−1. Regarding the antibiofilm activity, the fucoidan at the concentrations of above 250 µg mL−1 completely suppressed the biofilm formations and planktonic cell growths of Streptococcus mutans and S. sobrinus. However, no eliminative effect on the completed biofilm was observed. The fucoidan consisted of almost fucose base polysaccharide containing approximately 14.0% sulfate content. The average molecular weight of the fucoidan was changed by heat treatment (121 °C for 15 min) and it affected the antimicrobial activity.

AI snapshot

Written from the paper’s full text.

TL;DR

Sulfated polysaccharides from marine algae were screened against dental plaque bacteria, and a crude fucoidan from *Fucus vesiculosus* (F85) showed antimicrobial and antibiofilm activity. F85 inhibited dental plaque bacteria at MICs of 125–1000 µg mL⁻¹ and, above 250 µg mL⁻¹, completely suppressed biofilm formation and planktonic growth of *Streptococcus mutans* and *S. sobrinus*, but did not eliminate completed biofilm.

Key findings

  • Among the tested sulfated polysaccharides, only fucoidan F85 from *F. vesiculosus* inhibited all dental plaque bacteria tested, with MICs of 125–1000 µg mL⁻¹; *S. mutans* KCTC 5458 was the most sensitive.
  • F85 also inhibited *Listeria monocytogenes* KCTC 13064 (250 µg mL⁻¹), *Staphylococcus aureus* KCTC 3881 (500 µg mL⁻¹), and two lactic acid bacteria (500 µg mL⁻¹ each), but not Gram-negative bacteria; ampicillin MICs for dental plaque bacteria were 0.8–12.5 µg mL⁻¹.
  • F85 at ≥250 µg mL⁻¹ completely suppressed biofilm formation and planktonic cell growth of *S. mutans* and *S. sobrinus*; however, no eliminative effect was observed on completed biofilm, and treatment at stage 3 (24 h) had no effect.
  • F85 contained approximately 14.0% sulfate and was mostly fucose-based (>87.4% fucose); its weight-average molar mass was ca. 74,214 g mol⁻¹ without heat treatment and decreased to ca. 13,875 g mol⁻¹ after heat treatment (121 °C, 15 min), which affected antimicrobial activity. F95 from the same species showed no antimicrobial activity despite ca. 7.5% sulfate.

Methods

  • Eight sulfated polysaccharides were isolated from five brown, two green, and one red edible marine algae, and four commercial fucoidans (F85, F95, M85, U95) plus γ-carrageenan were also tested.
  • Antimicrobial activity was screened by broth microdilution MIC against six foodborne pathogenic bacteria, eight dental plaque bacteria, and two lactic acid bacteria; antibiofilm activity was measured by crystal violet staining and planktonic cell counts in 96-well plates.
  • Chemical analyses included total sugar, sulfate, pH, composite monosaccharides by HPAEC-PAD, and molecular weight by gel permeation chromatography; statistical comparisons used one-way ANOVA, LSD/Tukey tests, and independent two-sample t-tests (p < 0.05).

Limitations

  • Stated: reproducing an artificial dental plaque microbiota in vitro is not easy because many oral bacteria are unculturable, so only a single or small number of combined strains can be tested.
  • Stated: F85 did not eliminate completed biofilm, and the time-course data suggested it might not possess a direct killing effect.
  • Evident from the text: the study is in vitro only, the antimicrobial mechanism of sulfated polysaccharides was not clearly revealed, and only one screened fucoidan (F85) showed broad activity against the dental plaque bacteria tested.

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

Integrity signals

Registry

Crossref · 10.3390/md16090301

Cites

28 of 28 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 9 cited sources checked · 0 supported · 0 flagged

  • Findingown data

    The MICs of ampicillin were 0.8 to 12.5 μg mL−1 for the dental plaque bacteria.

    “The MICs of ampicillin (as a standard antimicrobial agent) were in the ranges of 0.8 to 12.5 µg mL−1 for the dental plaque bacteria.”
    Quote in the paperNot a substantial claim
  • Findingown data

    Fucoidan F85 inhibited the growth of Listeria monocytogenes KCTC 13064 at 250 μg mL−1.

    “In addition, the fucoidan F85 inhibited the growths of Listeria monocytogenes KCTC 13,064 (250 µg mL−1), Staphylococcus aureus KCTC 3881 (500 µg mL−1), and the two lactic acid bacteria (500 µg mL−1 in both), but not of the Gram-negative bacteria.”
    Quote in the paperNot a substantial claim
  • Findingown data

    Two sulfated polysaccharides from Undaria pinnatifida and Kjellmaniella crassifolia had growth inhibitory effects against Salmonella typhimurium at 1000 μg mL−1.

    “Beside the fucoidan F85, the two sulfated polysaccharides from brown algae Undaria pinnatifida and Kjellmaniella crassifolia had growth inhibitory effects against Salmonella typhimurium at a concentration of 1000 µg mL−1 (in both).”
    Quote in the paperNot a substantial claim
  • Findingown data

    Fucoidan F85 inhibited the growth of Staphylococcus aureus KCTC 3881 at 500 μg mL−1.

    “In addition, the fucoidan F85 inhibited the growths of Listeria monocytogenes KCTC 13,064 (250 µg mL−1), Staphylococcus aureus KCTC 3881 (500 µg mL−1), and the two lactic acid bacteria (500 µg mL−1 in both), but not of the Gram-negative bacteria.”
    Quote in the paperNot a substantial claim
  • Findingown data

    Fucoidan F85 did not inhibit the growth of Gram-negative bacteria tested.

    “In addition, the fucoidan F85 inhibited the growths of Listeria monocytogenes KCTC 13,064 (250 µg mL−1), Staphylococcus aureus KCTC 3881 (500 µg mL−1), and the two lactic acid bacteria (500 µg mL−1 in both), but not of the Gram-negative bacteria.”
    Quote in the paperNot a substantial claim
  • May combine two claims. 18
  • The quote only partly states this claim. 1
  • Classified as probably not a substantial claim. 13
  • May combine two claims.

    Findingown data

    Fucoidan F95 did not inhibit the growth of any bacterial strains tested, though it is also from F. vesiculosus.

    “In contrast, the fucoidan F95 did not inhibit growths of any bacterial strains, though it is also originated from the F. vesiculosus.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    Planktonic cells of S. mutans proliferated immediately after inoculation, while biofilm formation had a lag phase for 6 h.

    “The planktonic cells proliferated after the inoculation immediately, while the biofilm formation seemed to have a lag phase for 6 h.”
    Quote in the paperSubstantial claim
  • The quote only partly states this claim.

    Findingown data

    In BHI broth, S. mutans treated with fucoidan F85 at 125 μg mL−1 showed no increase in cell count.

    “In contrast, there was no increase in the S. mutans treated with fucoidan at 125 µg mL−1, and the S. mutans treated with fucoidan F85 at 250 µg mL−1 showed a constant decrease to ca 3.3 log CFU mL−1 for 48 h.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    The total sugar contents of the four commercial fucoidans ranged from 83.5 to 90.5%, while those of the sulfated polysaccharides isolated in this study, except for that from C. fragile, ranged from 63.0 to 75.1%.

    “The total sugar contents of the four commercial fucoidans ranged from 83.5 to 90.5%, while those of the sulfated polysaccharides isolated in this study, except for that from C. fragile, ranged from 63.0 to 75.1%.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    For S. mutans KCTC 5458, antibiofilm activity of fucoidan F85 was observed at all tested concentrations (62.5-1000 μg mL−1) and tended to be concentration-dependent.

    “For S. mutans KCTC 5458 (Figure 1C), the antibiofilm activity was observed in all the tested concentrations (62.5–1000 µg mL−1), which tended to be concentration-dependent.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Findingown data

    At a concentration of 2.5 mg mL−1, the pH values of fucoidans F85 and M85 were acidic (pH 5.31 and 4.93, respectively), while those of all the isolated sulfated polysaccharides and a commercial fucoidan U95 were in the ranges of 6.05 to 7.81.

    “At a concentration of 2.5 mg mL−1, the pH values of fucoidans F85 and M85 were acidic (pH 5.31 and 4.93, respectively), while those of all the isolated sulfated polysaccharides and a commercial fucoidan U95 were in the ranges of 6.05 to 7.81.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Findingcitation

    The polysaccharide from Codium fragile prepared with the water extraction method did not contain sulfate.

    “However, the polysaccharide from Codium fragile prepared with the water extraction method [22] did not contain sulfate.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [22] Cho, 2010, Molecular characterization and biological activities of water soluble sulfated polysaccharides from Enteromorpha prolifera, Food Sci. Biotechnol. source

      Not checked in the free run.

  • May combine two claims.

    Findingown data

    For S. sobrinus KCTC 5809, fucoidan F85 had similar activity as for S. mutans in 24 h, but activities at 62.5 and 125 μg mL−1 were lost in 48 h.

    “For S. sobrinus KCTC 5809 (Figure 1D), fucoidan F85 had a similar activity as that exhibited for S. mutans in 24 h, whereas the activities of the fucoidan F85 at the concentrations of 62.5 and 125 µg mL−1 were lost in 48 h.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    In a preliminary experiment, the antimicrobial activity of fucoidan F85 decreased without heat treatment (121 °C for 15 min); the MIC for S. mutans was 1000 μg mL−1.

    “Furthermore, in a preliminary experiment, the antimicrobial activity of fucoidan F85 decreased without heat treatment (121 °C for 15 min); the MIC for S. mutans was determined to be 1000 µg mL−1 (data not shown).”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Findingnone given

    The sulfate content was higher in the brown algae (6.4-14.0%, including commercial fucoidans) than in those from the green and red algae (0-3.0%).

    “According to the algal classification based on pigments, the sulfate content was higher in the brown algae (6.4–14.0%, including commercial fucoidans) than in those from the green and red algae (0–3.0%).”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    After heat treatment (121 °C for 15 min), the Mw of fucoidan F95 was almost unchanged, whereas that of fucoidan F85 notably decreased to ca. 13,875 g mol−1.

    “After the heat treatment, the Mw of fucoidan F95 was almost unchanged, whereas that of fucoidan F85 notably decreased to ca. 13,875 g mol−1.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Findingown data

    Fucoidan F95 exhibited a basic pH (9.46), though it contained 7.5 ± 2.1% sulfate.

    “In contrast, fucoidan F95 exhibited a basic pH (9.46), though it contained 7.5 ± 2.1% sulfate.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    Biofilm formation of S. mutans was clearly distinguished from 12 h of incubation and reached nearly a maximal level at 24 h.

    “The biofilm formation was clearly distinguished from 12 h of incubation and reached nearly a maximal level at 24 h.”
    Quote in the paperSubstantial claim
  • Classified as probably not a substantial claim. May combine two claims.

    Premisecitation

    Dental caries is often associated with increases of acidogenic mutans streptococci and lactobacilli, which can metabolize sugars to acid and lead to demineralization of enamel.

    “Dental caries is often associated with increases of acidogenic mutans streptococci and lactobacilli, which can metabolize sugars to acid and consequentially lead to the demineralization of enamel [13].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [13] Marsh, 2006, Dental plaque as a biofilm and a microbial community—Implications for health and disease, BMC Oral Health source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    The elimination of microbial biofilms is not easy, and its presence displays antimicrobial resistance.

    “Therefore, the elimination of microbial biofilms is not easy, and its presence displays antimicrobial resistance [14,15].”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [14] Kaplan, 2000, Biofilm formation as microbial development, Annu. Rev. Microbiol. source

      Not checked in the free run.

    • cites [15] Karunakaran, 2011, Mechanisms of bacillus cereus biofilm formation: An investigation of the physicochemical characteristics of cell surfaces and extracellular proteins, Appl. Microbiol. Biotechnol. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Dental plaque biofilms cause dental caries, periodontitis and gingivitis.

    “In dental disease, dental plaque biofilms are known to cause dental caries, periodontitis and gingivitis, though the biofilms are also present on healthy teeth [10].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [10] Lee, 2013, Synergistic effect of fucoidan with antibiotics against oral pathogenic bacteria, Arch. Oral Biol. source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Study design and conductcitation

    The antibiofilm activities were measured according to the method recommended by O'Toole [30], with slight modifications.

    “The biofilm formations of seven dental plaque bacteria (E. faecalis KCTC 5289, S. mutans KCTC 5458, S. mutans KCCM 40105, S. oralis KCCM 41567, S. sanguinis KCTC 5643, S. sobrinus KCTC 5809, and S. sobrinus KCCM 11898) and the antibiofilm activities of fucoidan F85 against selected bacteria (E. faecalis KCTC 5289, S. mutans KCTC 5458, and S. sobrinus KCTC 5809) were measured according to the”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [30] 2011, Microtiter dish biofilm formation assay, J. Vis. Exp.

      Not checked in the free run.

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

    Study design and conductown data

    The values for the biofilm formation of several dental plaque bacteria were statistically assessed with a one-way ANOVA test; a significant difference (p < 0.05) between the means was identified by the least significant difference and Tukey's test using SPSS.

    “The values for the biofilm formation of several dental plaque bacteria were statistically assessed with a one-way ANOVA test; a significant difference (p < 0.05) between the means was identified by the least significant difference and Tukey’s test using SPSS (IBM, Armonk, NY, USA).”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    All data, except for the pHs, MICs, and Mws of the sulfated polysaccharides, were expressed as the mean ± standard deviation (SD) in triplicate.

    “All data, except for the pHs, MICs, and Mws of the sulfated polysaccharides, were expressed as the mean ± standard deviation (SD) in triplicate.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based). May combine two claims.

    Interpretationcitation

    The electrical properties of the fucoidan could be associated with the sulfate groups and it might affect the antimicrobial activity.

    “The electrical properties of the fucoidan could be associated with the sulfate groups and it might affect the antimicrobial activity.”
    Quote in the paperNot a substantial claim
  • Classified as probably not a substantial claim. May combine two claims.

    Study design and conductown data

    The values for the antibiofilm activities of fucoidan F85 against selected dental plaque bacteria were assessed by independent two-sample t-tests; the significance level between the fucoidan F85 dose-levels and the control was set at p < 0.05.

    “The values for the antibiofilm activities of fucoidan F85 against selected dental plaque bacteria were assessed by independent two-sample t-tests; the significance level between the fucoidan F85 dose-levels and the control was set at p < 0.05.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Two theories explaining antimicrobial action of sulfated polysaccharides (carrageenans) proposed by Yamashita et al. [6]: binding to bacterial surface; trapping nutrients/cationic minerals.

    “There are two theories explaining the antimicrobial action of sulfated polysaccharides (carrageenans) proposed by Yamashita et al. [6]: one suggests the binding of the sulfated polysaccharides on the bacterial surface, although in an experiment using 3H-carrageenan, no binding for S. enteritidis was observed; the other suggests the trapping of nutrients or cationic minerals induced by the sulfated”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [6] Yamashita, 2001, In vitro bacteriostatic effects of dietary polysaccharides, Food Sci. Technol. Res. source

      Not checked in the free run.

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

    Premisecitation

    Li et al. [26] described the structure of the fucoidan from F. vesiculosus, which is composed of α-(1,3)-linked fucose with sulfate groups substituted at the C-4 position on some of the fucose residues.

    “Li et al. [26] described the structure of the fucoidan from F. vesiculosus, which is composed of α-(1,3)-linked fucose with sulfate groups substituted at the C-4 position on some of the fucose residues.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [26] Li, 2008, Fucoidan: Structure and bioactivity, Molecules source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Study design and conductcitation

    The MICs of the sulfated polysaccharides for foodborne pathogenic and dental plaque bacteria were determined according to the broth micro-dilution method guided by CLSI [29], with slight modification.

    “The MICs of the sulfated polysaccharides for the foodborne pathogenic and dental plaque bacteria were determined according to the broth micro-dilution method guided by the Clinical and Laboratory Standards Institute (CLSI) [29], with slight modification.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [29] Clinical and Laboratory Standards Institute (CLSI) (2006). Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria that Grow Aerobically: Approved Standard, CLSI. [7th ed.]. Document M7-A7.

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    Not only sulfate groups, but also the Mws of sulfate polysaccharides, might play crucial roles in their antimicrobial activities.

    “As we found, not only sulfate groups, but also the Mws of sulfate polysaccharides, might play crucial roles in their antimicrobial activities.”
    Quote in the paperSubstantial claim
25 of 25
  • The paper relies on this without support.

    The antimicrobial action of sulfated polysaccharides has not been clearly revealed.

    “In contrast, the antimicrobial action of sulfated polysaccharides has not been clearly revealed.”
  • The paper relies on this without support.

    The industrial utilization of marine algal antimicrobial candidates as antimicrobial agents or food preservatives is not common.

    “However, the industrial utilization of these candidates as antimicrobial agents or food preservatives is not common.”
2 of 2

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

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.

  • Plate counts use conflicting denominators

    Minor

    The time-course method says colony counts were expressed per gram of sample, but the corresponding results report them per milliliter.

  • Eight dental plaque bacteria claimed, but seven are listed

    Minor

    The screening results say eight dental plaque bacteria were tested, while the methods identify seven dental plaque bacterial strains.

  • Eleven algal species claimed, but ten are identified

    Minor

    The paper identifies eight species used for isolation. The four commercial fucoidans add only two distinct species: two are from Fucus vesiculosus, and one is from Undaria pinnatifida, which is already among the eight. That makes ten distinct species, not eleven.

3 of 3

Cites

Flagged first, then by citations

Research works printed but not linked: 1

  1. Koo, 1995, Isolation and purification of fucoidans from Laminaria religiose and Undaria pinnatifida in Korea, J. Korean Fish. Soc., 28, 227

Cited by

Sorted by citations

Authors
Jun, J.-Y., Jung, M.-J., Jeong, I.-H., Yamazaki, K., Kawai, Y., & Kim, B.-M.
Affiliations
  • Korea Food Research Institute (KR)
  • Gangneung–Wonju National University (KR)
  • Hokkaido University (JP)
Corresponding author
Kim, Byoung-Mok
Venue
Marine Drugs
Publisher
MDPI AG
Published
2018-08-27
Volume
16
Issue
9
Pages
301
ISSN
1660-3397 (ISSN-L)
OpenAlex
W2888717357
Cited by
160
References
28
Citations by year
2026: 13 · 2025: 35 · 2024: 20 · 2023: 23 · 2022: 19 · 2021: 22 · 2020: 16 · 2019: 12
FWCI
12.53
Type
journal article
Language
en
Open access
Locations
  • Marine Drugs (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Ministry of Science and ICT, South Korea
  • Korea Food Research Institute
Topics
  • Life Sciences › Agricultural and Biological Sciences › Aquatic Science › Seaweed-derived Bioactive Compounds
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
  • Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
Keywords
sulfated polysaccharides, marine algae, fucoidan, Fucus vesiculosus, dental plaque, antibiofilm activity, antimicrobial activity, Streptococcus mutans, Streptococcus sobrinus, foodborne pathogens, minimum inhibitory concentration, molecular weight, heat treatment (food and biological processing), dental disease prevention
MeSH terms
Anti-Bacterial Agents, Dental Plaque, Drug Evaluation, Preclinical, Humans, Microbial Sensitivity Tests, Polysaccharides, Streptococcus mutans, Sulfuric Acid Esters, Streptococcus sobrinus, Biofilms, Fucus, Aquatic Organisms

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