Short-term effect of ligature-induced periodontitis on cardiovascular variability and inflammatory response in spontaneously hypertensive rats

Abstract

Background: We previously reported that periodontal disease (PD) induces high arterial pressure variability (APV) consistent with sympathetic overactivity and elicits myocardial inflammation in Balb/c mice. However, it is unknown whether PD can change APV and heart rate variability (HRV) in spontaneously hypertensive (SHR) and normotensive Wistar-Kyoto (WKY) rats. This study aimed to evaluate the hemodynamic level, HRV, and APV associating with myocardial inflammation and plasma concentrations of oxide nitric (NO) in SHR and WKY rats with PD.

Methods: Three weeks after bilateral ligation of the first mandibular molar, or Sham operation, the rats received catheters into the femoral artery and had their arterial pressure (AP) recorded the following day. Subsequently, plasma, heart, and jaw were collected. The NO was quantified by the chemiluminescence method in plasma, and the myocardial IL-1β concentrations were evaluated by ELISA. In the jaw was evaluated linear alveolar bone loss induced by PD.

Results: The linear alveolar bone loss in jaws of SHR with PD was higher than in all other groups. AP and heart rate were higher in SHR than in their WKY counterparts. SHR with PD showed lower AP than control SHR. HRV and APV were different between SHR and WKY rats; however, no differences in these parameters were found between the animals with PD and their control counterparts. Plasma NO and myocardial IL-1β concentrations were higher in SHR with PD as compared to control WKY. A significant correlation was found between linear alveolar bone loss and plasma NO and myocardial IL-1β concentrations.

Conclusion: Our results demonstrated that short-term PD lowered the AP in SHR, which might be due to the higher levels of plasma NO. Even though PD did not affect either HRV or APV, it did induce myocardial inflammation, which can determine cardiovascular dysfunction in long-term PD.

Keywords: Arterial pressure variability; Heart rate variability; Myocardial inflammation; Nitric oxide; Periodontitis.

Fig. 1

Effect of periodontitis in alveolar bone loss. (A) Representative images of right and left jaws of buccal and lingual surfaces of WKY rats and SHR, with and without PD. (B) Linear and area of the alveolar bone loss was measured macroscopically by mean of the lingual and buccal surfaces of the right and left jaws. The yellow dashed lines indicate the three distances measured in the teeth and yellow solid lines indicate alveolar bone loss area. Quantifications were performed using ImageJ 1.50i software, a version of Wayne Rasband, National Institutes of Health, USA (https://imagej.nih.gov/ij/). Data are mean ± SEM. * P < 0.05 compared to sham operated WKY. ^#P < 0.05 compared to sham operated SHR. Wistar Kyoto rats without periodontal disease (WKY + Sham, n = 7); Wistar Kyoto rats with periodontal disease (WKY + PD, n = 10); Spontaneously hypertensive rats without periodontitis (SHR + Sham, n = 7); Spontaneously hypertensive rats with periodontitis (SHR + PD, n = 6). M1: lower first molar; M2: second lower molar; and M3: third molar

Fig. 2

Symbolic dynamics analysis. Percentage of occurrence of families from symbolic dynamics analysis of systolic arterial pressure (A; 0 V and 1 V) and pulse interval (B; 0 V and 2UV). * P < 0.05 compared to WKY + Sham and ^#P < 0.05 compared to WKY + PD. WKY rats without periodontal disease (WKY + Sham, n = 7); Wistar Kyoto rats with periodontal disease (WKY + PD, n = 10); Spontaneously hypertensive rats without periodontitis (SHR + Sham, n = 7); Spontaneously hypertensive rats with periodontitis (SHR + PD, n = 6)

Fig. 3

Plasma nitrate and inflammatory cytokine in the myocardial tissue. Bar Graphs show: Panel A, plasma nitrate level (indirect measurement of nitric oxide); Panel B, interleukin-1 beta (IL-1β) myocardial tissue concentration; Panel C, correlation between linear alveolar bone boss and plasma nitrate concentration; and Panel D, correlation between linear alveolar bone boss and IL-1β myocardial tissue concentration. *P < 0.05 compared to WKY + Sham and ^#P < 0.05 compared to WKY + PD. Wistar Kyoto rats without periodontal disease (WKY + Sham, n = 6); Wistar Kyoto rats with periodontal disease (WKY + PD, n = 6–8); Spontaneously hypertensive rats without periodontitis (SHR + Sham, n = 5–6); Spontaneously hypertensive rats with periodontitis (SHR + PD, n = 5–7)