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, 54 (2), 134-142

Periodontal Disease Susceptible Matrilines in the Cayo Santiago Macaca Mulatta Macaques

Affiliations

Periodontal Disease Susceptible Matrilines in the Cayo Santiago Macaca Mulatta Macaques

Jeffrey L Ebersole et al. J Periodontal Res.

Abstract

Objective and background: The expression of periodontitis, including age of onset, extent, and severity is considered to represent an interaction of the individual's oral microbiome and host response to the microbial challenge that is modified by both genetics and environmental factors. The aim of this study was to determine the distribution of periodontitis in a population of nonhuman primates, to document features of familial distribution that could reflect heritability and transmission of microbes with enhanced virulence.

Material and methods: This report presents our findings from evaluation of periodontal disease bone defects in skulls from 569 animals (5-31 years of age) derived from the skeletons of the rhesus monkeys (Macaca mulatta) of Cayo Santiago derived from eight matrilines over 6-9 generations. The distance from the base of alveolar bone to the cemento-enamel junction on 1st /2nd premolars and 1st /2nd molars from all four quadrants was evaluated as a measure of periodontal disease. Additionally, we documented the presence of periodontitis in 79 living descendants within these matrilines.

Results: The results demonstrated an increased extent and severity of periodontitis with aging across all matrilines. Extensive heterogeneity in disease expression was observed among the animals and this was linked to specific periodontitis susceptible matrilines. Moreover, we identified some matrilines in which the members appeared to show some resistance to more severe disease, even with aging.

Conclusion: Linking these disease variations to multigenerational matriarchal family units supported familial susceptibility of periodontitis. This familial disease relationship was reinforced by the distribution of naturally-occurring periodontitis in the living descendants.

Keywords: familial risk; nonhuman primates; periodontitis.

Figures

Figure 1:
Figure 1:
(A) Age of the members of each matriline whose skulls were evaluated. Bars denote mean age ± SD (vertical brackets) (B) Distribution of animals from different age groups in each of the matrilines.
Figure 1:
Figure 1:
(A) Age of the members of each matriline whose skulls were evaluated. Bars denote mean age ± SD (vertical brackets) (B) Distribution of animals from different age groups in each of the matrilines.
Figure 2:
Figure 2:
Correlation analysis of bone defects (BD) with age for all matrilines. (A-D) demonstrate the correlation of mean bone defect measures on maxillary and mandibular premolars and molars for each skull in the various matrilines, with linear regression noted. (E) The mean rate of bone defect formation for each matriline over the entire age of the members is shown. Asterisk (*) denotes significantly different than other groups at least a p<0.05 and the hashtag (#) denotes the group that as significantly different from 22, 022, 004 and DM at least at p<0.05.
Figure 2:
Figure 2:
Correlation analysis of bone defects (BD) with age for all matrilines. (A-D) demonstrate the correlation of mean bone defect measures on maxillary and mandibular premolars and molars for each skull in the various matrilines, with linear regression noted. (E) The mean rate of bone defect formation for each matriline over the entire age of the members is shown. Asterisk (*) denotes significantly different than other groups at least a p<0.05 and the hashtag (#) denotes the group that as significantly different from 22, 022, 004 and DM at least at p<0.05.
Figure 2:
Figure 2:
Correlation analysis of bone defects (BD) with age for all matrilines. (A-D) demonstrate the correlation of mean bone defect measures on maxillary and mandibular premolars and molars for each skull in the various matrilines, with linear regression noted. (E) The mean rate of bone defect formation for each matriline over the entire age of the members is shown. Asterisk (*) denotes significantly different than other groups at least a p<0.05 and the hashtag (#) denotes the group that as significantly different from 22, 022, 004 and DM at least at p<0.05.
Figure 2:
Figure 2:
Correlation analysis of bone defects (BD) with age for all matrilines. (A-D) demonstrate the correlation of mean bone defect measures on maxillary and mandibular premolars and molars for each skull in the various matrilines, with linear regression noted. (E) The mean rate of bone defect formation for each matriline over the entire age of the members is shown. Asterisk (*) denotes significantly different than other groups at least a p<0.05 and the hashtag (#) denotes the group that as significantly different from 22, 022, 004 and DM at least at p<0.05.
Figure 2:
Figure 2:
Correlation analysis of bone defects (BD) with age for all matrilines. (A-D) demonstrate the correlation of mean bone defect measures on maxillary and mandibular premolars and molars for each skull in the various matrilines, with linear regression noted. (E) The mean rate of bone defect formation for each matriline over the entire age of the members is shown. Asterisk (*) denotes significantly different than other groups at least a p<0.05 and the hashtag (#) denotes the group that as significantly different from 22, 022, 004 and DM at least at p<0.05.
Figure 3:
Figure 3:
(A) Bars denote the mean bone defect for the matrilines for total mouth (BD Tol), maxillary (BD Max) and mandibular (BD Mand) quadrants. Vertical brackets enclose 1 SD. (B) Bars denote the mean % of sites with bone measures of < 3, >4, and >5 mm in each skull stratified by matriline. Asterisk (*) denotes significantly different than other groups at least a p<0.05. (C) Bars signify the frequency of skulls (animals) in each matriline that demonstrated bone defects of >5 mm. Asterisk (*) denotes significantly different than other groups at least a p<0.05.
Figure 3:
Figure 3:
(A) Bars denote the mean bone defect for the matrilines for total mouth (BD Tol), maxillary (BD Max) and mandibular (BD Mand) quadrants. Vertical brackets enclose 1 SD. (B) Bars denote the mean % of sites with bone measures of < 3, >4, and >5 mm in each skull stratified by matriline. Asterisk (*) denotes significantly different than other groups at least a p<0.05. (C) Bars signify the frequency of skulls (animals) in each matriline that demonstrated bone defects of >5 mm. Asterisk (*) denotes significantly different than other groups at least a p<0.05.
Figure 3:
Figure 3:
(A) Bars denote the mean bone defect for the matrilines for total mouth (BD Tol), maxillary (BD Max) and mandibular (BD Mand) quadrants. Vertical brackets enclose 1 SD. (B) Bars denote the mean % of sites with bone measures of < 3, >4, and >5 mm in each skull stratified by matriline. Asterisk (*) denotes significantly different than other groups at least a p<0.05. (C) Bars signify the frequency of skulls (animals) in each matriline that demonstrated bone defects of >5 mm. Asterisk (*) denotes significantly different than other groups at least a p<0.05.
Figure 4:
Figure 4:
(A) demonstrates the mean bone defect for the skulls in each matriline stratified according to age of the animal at the time of death. (B) description of frequency of sites in skulls of each matriline stratified on age. (C) description of frequency of sites in skulls of each matriline stratified on age. Bars denote group mean and vertical brackets enclose 1 SD. Asterisk (*) denotes significantly different than other groups at least a p<0.05. Hashtag (#) denotes the groups with significantly less disease compared to all other matrilines at least at p<0.05.
Figure 4:
Figure 4:
(A) demonstrates the mean bone defect for the skulls in each matriline stratified according to age of the animal at the time of death. (B) description of frequency of sites in skulls of each matriline stratified on age. (C) description of frequency of sites in skulls of each matriline stratified on age. Bars denote group mean and vertical brackets enclose 1 SD. Asterisk (*) denotes significantly different than other groups at least a p<0.05. Hashtag (#) denotes the groups with significantly less disease compared to all other matrilines at least at p<0.05.
Figure 4:
Figure 4:
(A) demonstrates the mean bone defect for the skulls in each matriline stratified according to age of the animal at the time of death. (B) description of frequency of sites in skulls of each matriline stratified on age. (C) description of frequency of sites in skulls of each matriline stratified on age. Bars denote group mean and vertical brackets enclose 1 SD. Asterisk (*) denotes significantly different than other groups at least a p<0.05. Hashtag (#) denotes the groups with significantly less disease compared to all other matrilines at least at p<0.05.

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