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Biomedical subjects

J D Rudney

Publications and source records attributed to J D Rudney.

At least 19 recordsLinked to original sources
PubMed2005

The vital status of human buccal epithelial cells and the bacteria associated with them.

OBJECTIVE: We have shown that buccal epithelial cells (BEC) from humans can contain a polymicrobial intracellular flora. Members of that flora can induce proinflammatory responses. However, our subjects all had healthy oral mucosa. This might reflect tolerance of bacterial invasion by live BEC. Alternatively, inflammation might not occur if invaded cells were mostly dead, and thus unable to mount a response. This study addressed that issue, by determining the vital status of BEC and the bacteria associated with them. DESIGN: Initial experiments indicated that BEC were anomalously permeable to the DNA stain propidium iodide. We used that property to develop a protocol that combined the DNA stains SYTO 9 and propidium iodide (indicators of bacterial viability) with the esterase substrate calcein blue AM (an indicator of BEC viability), and Annexin V Alexa Fluor 647 conjugate (an apoptosis marker). That protocol was applied to BEC collected from 36 human subjects. RESULTS: On average, 70% of BEC displayed calcein blue staining, with no binding of Annexin V, 25% showed signs of apoptosis, and 5% did not stain with calcein blue. The mean percent of BEC with live cell-associated bacteria was 29%. Collectively, 25% of total BEC displayed calcein blue staining and live (SYTO 9 stained) bacteria. Only 1% of total BEC were negative for calcein blue and associated with live bacteria. CONCLUSIONS: Our findings suggest that live BEC are tolerant of bacterial invasion. This may be due to complex interactions between members of the polymicrobial flora and their host BEC.

Adult↗
PubMed2005

Actinobacillus actinomycetemcomitans, Porphyromonas gingivalis, and Tannerella forsythensis are components of a polymicrobial intracellular flora within human buccal cells.

Previously, we used in situ hybridization and confocal microscopy to detect the periodontal pathogens Actinobacillus actinomycetemcomitans, Porphyromonas gingivalis, and Tannerella forsythensis within buccal epithelial cells taken directly from the mouth. This study tested the hypothesis that the intracellular flora of buccal cells is polymicrobial. Mixtures containing a red fluorescent universal probe paired with green fluorescent versions of either A. actinomycetemcomitans-, P. gingivalis-, or T. forsythensis-specific probes were hybridized with buccal cells collected from each of 38 healthy humans. We verified co-localization of probe pairs within cells by generating three-dimensional reconstructions. Intracellular bacteria were detected in every subject. Each cell that was labeled with a species-specific probe also contained bacteria recognized only by the universal probe. Bacteria labeled with specific probes often occupied smaller regions within larger masses of bacteria. Those findings suggest that future studies of invasion by oral bacteria may need to include microbial consortia.

Adult↗
PubMed2005

Streptococci dominate the diverse flora within buccal cells.

Previously, we reported that intracellular Actinobacillus actinomycetemcomitans, Porphyromonas gingivalis, and Tannerella forsythensis were present within buccal epithelial cells from human subjects, as lesser components of a polymicrobial flora. In this study, we further characterized that intracellular flora by using the same double-labeling techniques to identify Fusobacterium nucleatum, Prevotella intermedia, oral Campylobacter species, Eikenella corrodens, Treponema denticola, Gemella haemolysans, Granulicatella adiacens, and total streptococci within buccal epithelial cells. All those species were found within buccal cells. In every case, species recognized by green-labeled species-specific probes were accompanied by other bacteria recognized only by a red-labeled universal probe. Streptococci appeared to be a major component of the polymicrobial intracellular flora, being present at a level from one to two logs greater than the next most common species (G. adiacens). This is similar to what is observed in oral biofilms, where diverse species interact in complex communities that often are dominated by streptococci.

Campylobacter rectus↗
PubMed2004

Human salivary function in relation to the prevalence of Tannerella forsythensis and other periodontal pathogens in early supragingival biofilm.

OBJECTIVE: Previously, we screened 149 subjects and established four groups high or low for salivary killing of oral bacteria, and for aggregation and live and dead adherence of oral bacteria (as a combined factor). Caries scores were significantly lower in both High Aggregation-Adherence groups. Subsequently, we found that supragingival total biofilm DNA, total streptococci and two major streptococcal rRNA variants also were significantly lower in the High Aggregation-Adherence groups. In this study, we looked at the effects of those differences in salivary function on three periodontal pathogens. DESIGN: Quantitative PCR was used to determine levels of Actinobacillus actinomycetemcomitans, Porphyromonas gingivalis and Tannerella forsythensis (formerly Bacteroides forsythus) in stored DNA extracts of overnight supragingival biofilm collected from buccal upper central incisors (UC), lingual lower central incisors (LC) and buccal upper and lower first molars (BM) and lingual upper and lower first molars (LM) of subjects in the four groups. RESULTS: A. actinomycetemcomitans and P. gingivalis were almost completely absent from these samples. T. forsythensis was found in 11 of 35 persons at the buccal molar site. Only two of those subjects were in the High Aggregation-Adherence groups, and that difference was statistically significant. The mean quantity of T. forsythensis also was significantly lower in the High Aggregation-Adherence groups. CONCLUSIONS: The difference between the Low and High Aggregation-Adherence groups might reflect direct interactions of salivary proteins with T. forsythensis. Alternatively, the higher levels of total biofilm and total streptococci seen in the Low Aggregation-Adherence groups might create a favourable environment for early secondary colonization of T. forsythensis.

Aggregatibacter actinomycetemcomitans↗
PubMed2003

Streptococcal diversity in oral biofilms with respect to salivary function.

OBJECTIVE: In a previous study, we screened 149 subjects and established four groups high or low for salivary killing of oral bacteria, and for aggregation and live and dead adherence of oral bacteria (as a combined factor). Caries scores were significantly lower in both High Aggregation-Adherence groups. In this study we looked at the effects of those differences in salivary function on the quantity and diversity of oral biofilm streptococci. DESIGN: Subjects from those four groups were recalled for collection of overnight oral biofilm from buccal upper central incisors, lingual lower central incisors, buccal upper and lower first molars, and lingual upper and lower first molars. At each site, groups were compared for total biofilm (by DNA concentration), total streptococci (by quantitative PCR), and streptococcal diversity (by Streptococcus-specific denaturing gradient gel electrophoresis). RESULTS: Total biofilm DNA and total streptococci were correlated. Both were highest on buccal molar surfaces and lowest on lingual lower central incisors, and both were significantly lower in the High Aggregation-Adherence groups (particularly at the buccal molar site). Fifty distinct bands were observed in denaturing gradient gels. There was great diversity within and between sites. Three major bands were present in almost every person at every site. Densities for two of those bands were significantly lower in both High Aggregation-Adherence groups. Other less-prevalent bands also showed the same pattern. CONCLUSION: These findings are consistent with our caries results in suggesting that differences in salivary function can influence the quantity and composition of streptococci in oral biofilms.

Bacterial Adhesion↗
PubMed2003

Endpoint quantitative PCR assays for Bacteroides forsythus, Porphyromonas gingivalis, and Actinobacillus actinomycetemcomitans.

BACKGROUND: Conventional polymerase chain reaction (PCR) assays for periodontal pathogens are so sensitive that they detect infections of no clinical significance. Quantitative PCR (qPCR) may provide a solution to this problem. However, most qPCR systems require expensive real-time thermal cyclers. OBJECTIVE: Our goal was to develop qPCR assays which would allow endpoint quantification. MATERIALS AND METHODS: 16S rRNA primers for Bacteroides forsythus, Porphyromonas gingivalis, and Actinobacillus actinomycetemcomitans were adapted to the Amplifluor qPCR system, which incorporates fluorescein into the PCR product so that endpoint fluorescence is proportional to the original amount of template. DNA dilutions representing known numbers of cells were used as standard curves. Pooled subgingival plaques from the four deepest pockets of 21 severe adult periodontitis patients were assayed. Buccal molar supragingival plaque from 35 dental students provided healthy controls. Endpoint fluorescence was measured with a microplate reader. RESULTS: Optimized standard curves were linear in log-log or semilog fits over a range of 100-10(6) cells. Countable B. forsythus was present in all patients, with counts (as logs) from 2.4 to 7.3 (mean = 5.0), and 11 controls with counts from 2.1 to 4.5 (mean = 3.0). P. gingivalis was present in 11 patients and no controls, with counts from 2.2 to 4.7 (mean = 3.2). A. actinomycetemcomitans was present in two patients, with counts of 1.5 and 3.5. CONCLUSIONS: Amplifluor qPCR assays discriminated between plaque samples differing by one log or more, allowing major infections to be distinguished from minor ones. This approach allows high-throughput qPCR of plaque samples, using equipment available to many laboratories.

Adult↗
PubMed2002

Simultaneous measurement of the viability, aggregation, and live and dead adherence of Streptococcus crista, Streptococcus mutans and Actinobacillus actinomycetemcomitans in human saliva in relation to indices of caries, dental plaque and periodontal disease.

Salivary proteins have multiple functions and many share similar functions, which may be why it has been difficult to relate variations in their concentrations to oral health and ecology. An alternative is to focus on variations in the major functions of saliva. An hydroxyapatite-coated microplate model has been developed that simultaneously measures saliva-promoted bacterial viability, bacterial aggregation, and live and dead bacterial adherence, while simulating oral temperature and shearing forces from swallowing. That model was applied to resting whole and stimulated parotid saliva from 149 individuals, using representative strains of Streptococcus crista, S. mutans, and Actinobacillus actinomycetemcomitans. Two major factors were defined by multivariate analysis (this was successful only for whole-saliva). One factor was correlated with aggregation, live adherence and dead adherence for all three strains; the other was correlated with total viability of all three strains. Participants were grouped <25th percentile and >75th percentile for each factor. Those groups were compared for clinical indices of oral health. Caries scores were significantly lower in those with high scores for aggregation-adherence, regardless of whether total viability scores were low or high. Live bacteria always predominated on surfaces when live and dead adherence scores were expressed as ratios. However, participants with high scores for aggregation-adherence showed significantly more dead adherent bacteria than those with low scores (these ratios were uncorrelated with total viability). This finding may indicate that extreme differences in the ability to kill bacteria on surfaces can influence caries risk.

Adult↗
PubMed2001

Intracellular Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis in buccal epithelial cells collected from human subjects.

The mouth may provide an accessible model for studying bacterial interactions with human cells in vivo. Using fluorescent in situ hybridization and laser scanning confocal microscopy, we found that human buccal epithelial cells from 23 of 24 subjects were infected with intracellular bacteria, including the periodontal pathogens Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis, as well as other species which have yet to be identified. Buccal cell invasion may allow fastidious anaerobes to establish themselves in aerobic sites that otherwise present an unfavorable environment. Exfoliated buccal epithelial cells might provide a protected route for bacterial transmission between different oral sites within and between hosts.

Aggregatibacter actinomycetemcomitans↗
PubMed2001

Persistent presence of Bacteroides forsythus as a risk factor for attachment loss in a population with low prevalence and severity of adult periodontitis.

BACKGROUND: Previous longitudinal studies investigating the role of microorganisms in periodontitis have focused on subjects with a high prevalence and severity of disease. The complex profile of microbial species in severe cases of periodontitis might not allow us to differentiate which bacterial species initiate disease or which species simply proliferate after disease progression. This prospective longitudinal study followed a group of 205 subjects who showed a low prevalence and severity of adult periodontitis, and thus allowed us to monitor early microbiological changes in the development of periodontitis. METHODS: Subgingival plaque was collected from proximal surfaces of a posterior sextant at 6-month intervals for 2 years. During the monitoring period, 44 subjects had either attachment loss or attachment gain. Using multiplex polymerase chain reaction (PCR), all plaque samples from those 44 subjects were analyzed for the presence of Actinobacillus actinomycetemcomitans, Bacteroides forsythus, and Porphyromonas gingivalis. RESULTS: Both subjects with attachment loss and those with attachment gain had a high prevalence of these 3 periodontal pathogens. The mere presence of any of the 3 species at a site could not predict future attachment loss at that specific site. However, subjects with a persistent presence of B. forsythus at any site across all visits had 5.3 times higher odds of having at least one site in their mouth losing attachment compared to subjects with occasional or no presence of B. forsythus. CONCLUSIONS: The persistence of B. forsythus identified subjects at higher risk, but not which specific sites in those subjects would lose attachment.

Actinobacillus Infections↗
PubMed2000

Effects of Streptococcus crista and human saliva on the viability of Fusobacterium nucleatum ATCC 10953.

Associations with facultative species might help planktonic oral anaerobes survive when they traverse saliva. This study investigated whether co-aggregation with Streptococcus crista ATCC 51110 enhanced the viability of Fusobacterium nucleatum ATCC 10953. Two tubes each of co-aggregates and Fus. nucleatum ATCC 10953 alone were prepared. One of each set was resuspended in buffer, and the other in clarified saliva from each of 20 donors. After 1 h, cells were stained for viability. The median percentage of viable Fus. nucleatum ATCC 10953 in buffer with Strep. crista (86%) was significantly higher (p=0.04) than in buffer alone (77%). A similar trend was observed for saliva with Strep. crista (81%) and saliva alone (74%), although that difference was not significant (p=0.41). The median percentage of Fus. nucleatum co-aggregated in buffer (44%) was significantly reduced after incubation in saliva (16%) (p<0.0002). No such change was seen when saliva was replaced with purified salivary proline-rich glycoprotein, which can bind both species. For co-aggregate suspensions, there was no difference in the viability of fusobacteria that were or were not in direct contact with Strep. crista. In both cases, viability was significantly reduced in saliva relative to buffer. Strep. crista may enhance the viability of planktonic Fus. nucleatum ATCC 10953, but it is not yet clear whether that requires co-aggregation. Transmission of fusobacteria through saliva could depend on the interplay between protective factors, such as the presence of streptococci, and antimicrobial factors, which kill cells or disassociate co-aggregates.

Anti-Bacterial Agents↗
PubMed2000

Saliva and dental plaque.

Dental plaque is being redefined as oral biofilm. Diverse overlapping microbial consortia are present on all oral tissues. Biofilms are structured, displaying features like channels and projections. Constituent species switch back and forth between sessile and planktonic phases. Saliva is the medium for planktonic suspension. Several major functions can be defined for saliva in relation to oral biofilm. It serves as a medium for transporting planktonic bacteria within and between mouths. Bacteria in transit may be vulnerable to negative selection. Salivary agglutinins may prevent reattachment to surfaces. Killing by antimicrobial proteins may lead to attachment of dead cells. Salivary proteins form conditioning films on all oral surfaces. This contributes to positive selection for microbial adherence. Saliva carries chemical messengers which allow live adherent cells to sense a critical density of conspecifics. Growth begins, and thick biofilms may become resistant to antimicrobial substances. Salivary macromolecules may be catabolized, but salivary flow also may clear dietary substrates. Salivary proteins act in ways that benefit both host and microbe. All have multiple functions, and many do the same job. They form heterotypic complexes, which may exist in large micelle-like structures. These issues make it useful to compare subjects whose saliva functions differently. We have developed a simultaneous assay for aggregation, killing, live adherence, and dead adherence of oral species. Screening of 149 subjects has defined high killing/low adherence, low killing/high adherence, high killing/high adherence, and low killing/low adherence groups. These will be evaluated for differences in their flora.

Anti-Bacterial Agents↗
PubMed1999

Identification of oral mitis group streptococci by arbitrarily primed polymerase chain reaction.

"Mitis group" streptococci are commensal but may play some role in dental caries, septicemia or endocarditis. Rapid genotypic identification would aid studies of dental plaque ecology, or diagnostic use. AP-PCR with 58 unpaired arbitrary primers was used to characterize 7 Streptococcus gordonii, 11 Streptococcus sanguis, 2 Streptococcus crista, 5 Streptococcus parasanguis, 18 Streptococcus oralis, and 36 Streptococcus mitis (22 biovar 1 and 14 biovar 2). S. parasanguis 16S rRNA variable region primer RR2 produced species-specific bands with all S. gordonii and S. sanguis. Human V beta 1 T-cell receptor primer 434 yielded concordant genotypic identification of all phenotypically defined S. crista and S. parasanguis, 83% of S. oralis, and 74% of S. mitis biovar 1. Amplicon patterns for S. mitis biovar 2 were heterogeneous. Findings suggest that primers RR2 and 434 in succession will allow rapid identification of genotypic groups corresponding closely to mitis group species established by phenotype.

Bacterial Typing Techniques↗
PubMed1999

Improved multiplex PCR using conserved and species-specific 16S rRNA gene primers for simultaneous detection of Actinobacillus actinomycetemcomitans, Bacteroides forsythus, and Porphyromonas gingivalis.

Among putative periodontal pathogens, Actinobacillus actinomycetemcomitans, Bacteroides forsythus, and Porphyromonas gingivalis are most convincingly implicated as etiological agents in periodontitis. Therefore, techniques for detection of those three species would be of value. We previously published a description of a multiplex PCR that detects A. actinomycetemcomitans and P. gingivalis. The present paper presents an improvement on that technique, which now allows more sensitive detection of all three periodontal pathogens. Sensitivity was determined by testing serial dilutions of A. actinomycetemcomitans, B. forsythus, and P. gingivalis cells. Primer specificity was tested against (i) all gene sequences from the GenBank-EMBL database, (ii) six A. actinomycetemcomitans, one B. forsythus, and four P. gingivalis strains, (iii) eight different species of oral bacteria, and (iv) supra- and subgingival plaque samples from 20 healthy subjects and subgingival plaque samples from 10 patients with periodontitis. The multiplex PCR had a detection limit of 10 A. actinomycetemcomitans, 10 P. gingivalis, and 100 B. forsythus cells. Specificity was confirmed by the fact that (i) none of our forward primers were homologous to the 16S rRNA genes of other oral species, (ii) amplicons of predicted size were detected for all A. actinomycetemcomitans, B. forsythus, and P. gingivalis strains tested, and (iii) no amplicons were detected for the eight other bacterial species. A. actinomycetemcomitans, B. forsythus, and P. gingivalis were detected in 6 of 20, 1 of 20, and 11 of 20 of supragingival plaque samples, respectively, and 4 of 20, 7 of 20, and 13 of 20 of subgingival plaque samples, respectively, from periodontally healthy subjects. Among patients with periodontitis, the organisms were detected in 7 of 10, 10 of 10, and 7 of 10 samples, respectively. The simultaneous detection of three periodontal pathogens is an advantage of this technique over conventional PCR assays.

Aggregatibacter actinomycetemcomitans↗
PubMed1999

Cumulative correlations of lysozyme, lactoferrin, peroxidase, S-IgA, amylase, and total protein concentrations with adherence of oral viridans streptococci to microplates coated with human saliva.

Redundancy refers to the observation that many salivary proteins exhibit similar properties in vitro. It is possible that bacterial adherence to salivary pellicle occurs as a cumulative effect of multiple proteins. This study determined the joint and individual contributions of salivary amylase, S-IgA, lysozyme, salivary peroxidase, lactoferrin, and total protein concentrations to adherence by oral viridans streptococci in microplates coated with whole saliva from 123 persons. Strains used were: Streptococcus gordonii Blackburn, 10558, Streptococcus mitis 10712, 903, Streptococcus oralis 10557, 9811, and Streptococcus sanguis 10556, 13379. Rabbit antibody against 13379 was used for the detection of adherence. This antibody cross-reacted with all strains. Absorbance was standardized against saliva pooled from five donors. All saliva samples had been previously assayed for amylase, lactoferrin, lysozyme, secretory IgA, peroxidase, and total protein. Adherence scores for all strains except 13379 were significantly and positively correlated. Salivas binding high or low levels of one strain tended to bind others correspondingly. Multiple regression indicated significant contributions to 10558 adherence from total protein and lactoferrin (positive), and peroxidase and lysozyme (negative). Similar results were obtained for Blackburn and 903. Significant individual correlations were seen for 9811 and total protein (positive), 10557 and peroxidase (negative), and 13379 and lactoferrin (negative). Salivas with high adherence scores contained significantly more protein and lactoferrin, and significantly less peroxidase, than salivas with low adherence scores. These findings support the hypothesis that multiple proteins contribute to the adherence of streptococcal strains in vivo.

Amylases↗
PubMed1996

Multiplex PCR using conserved and species-specific 16S rRNA gene primers for simultaneous detection of Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis.

Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis are strongly associated with periodontitis. However, little is known about their distribution in periodontally healthy individuals, because culturing techniques are not sufficiently sensitive. A modified multiplex PCR was developed to address that question. Our method uses two species-specific forward primers in combination with a single reverse primer. These primers target variable and conserved regions of the 16S rRNA gene. Sensitivity was determined by testing serial dilutions of A. actinomycetemcomitans and P. gingivalis cells. Primer specificity was tested against (i) six A. actinomycetemcomitans strains and four P. gingivalis strains, (ii) seven different species of oral bacteria, and (iii) supra- and subgingival plaque from 20 subjects. The multiplex PCR had a lower limit of detection of 2 A. actinomycetemcomitans and 30 P. gingivalis cells. Species-specific amplicons were obtained for all A. actinomycetemcomitans and P. gingivalis strains tested and did not occur with seven other bacterial species unless A. actinomycetemcomitans and P. gingivalis were added. Neither target species was detected in supragingival plaque; A. actinomycetemcomitans was detected in one subgingival specimen, and P. gingivalis was detected in another. When plaque samples were spiked with 10 A. actinomycetemcomitans cells and 100 P. gingivalis cells, species-specific amplicons were detected. These findings show our multiplex PCR to be highly sensitive and specific while allowing simultaneous detection of A. actinomycetemcomitans and P. gingivalis. This assay has potential applications in epidemiological studies, diagnosis, treatment planning, and monitoring of periodontal pathogens.

Aggregatibacter actinomycetemcomitans↗
PubMed1996

Saliva protein binding to streptococcal layers placed at different oral sites in 48 persons.

Preliminary studies of 10 subjects suggested that saliva protein binding to oral bacteria might vary among oral sites. This study investigated saliva protein binding to layers of oral streptococci in an expanded sample of 48 subjects. Those persons were at opposite extremes for unstimulated whole saliva amylase, sIgA, lactoferrin, and lysozyme in an initial screening of 128 individuals. Layers of Streptococcus gordonii Blackburn or Streptococcus oralis 10557 on enamel chips were placed on buccal left and right upper premolars and molars (UL, UR), labial upper central incisors (UC), and lingual lower central incisors (LL). After a 10-minute exposure to saliva, bacterial extracts were assayed for bound amylase, sIgA, lactoferrin, and lysozyme. Those proteins also were quantified in unstimulated whole saliva collected after chip exposure. Both strains bound significantly more amylase at UL and UR, and significantly less at UC. Blackburn bound more amylase than 10557 at all sites. Significantly less sIgA was bound at UC; strain differences for sIgA were inconsistent across sites. Significantly more lactoferrin and lysozyme were bound at LL. There were no strain differences for lactoferrin; 10557 bound significantly more lysozyme at UL and UR. Subjects at opposite extremes for saliva protein concentrations differed for bound amylase and lactoferrin; those differences were smaller than site and strain differences. Bound protein levels were correlated across sites and strains. Correlations between whole saliva and bound proteins were moderate and were most consistent at LL. These findings suggest that saliva protein effects on oral ecology may vary among oral sites.

Analysis of Variance↗
PubMed1995

The prediction of saliva swallowing frequency in humans from estimates of salivary flow rate and the volume of saliva swallowed.

Saliva swallowing frequency is an important factor in models of oral clearance. It varies widely among individuals, and the basis for that variation has not been established. This study evaluated the use of unstimulated flow rate and the volume of saliva swallowed as predictors of swallowing frequency in 128 first-year dental students. A microphone was placed over the larynx, and swallowing activity was recorded for 30 min between 3-6:00 p.m. The average interval between swallows was determined, and individuals retained saliva in the mouth for a period equal to that time. Retained saliva was spat out, and volume was determined gravimetrically. Four replicate tubes were collected. Flow rate was determined as sample volume over average swallow time. A subset of 10 individuals was measured on two further occasions 2-3 months apart. An independent estimate of flow rate was taken on the second occasion. Repeat-measures analysis of variance and intraclass correlations were used to estimate the reproducibility of replicate volumes, and of measurements taken on different occasions. Associations between swallowing interval, saliva volume, and flow rate were evaluated by multiple regression. Replicate volumes were highly reproducible, as were measurements of volumes, swallow times, and flow rates on different occasions. Saliva volume and flow rate jointly accounted for 99% of variance in swallowing intervals. Swallowing intervals were shortest for individuals who combined high flow rates with small saliva volumes; current models suggest that their oral clearance might be most efficient. Swallowing intervals were longest for individuals with low flow rates and large volumes; their oral clearance might be the least efficient.

Acoustics↗