The Postural Autonomic Regulation of Pulpal Blood Flow

Abstract

Evidence suggests that postural changes in systemic blood pressure may significantly affect blood flow in the dental pulp. This in vivo study examined the responses of pulpal perfusion, systemic blood pressure, and heart rate to postural changes in humans. The experiments were done on 21 premolars in 16 participants aged 20-31 yrs. Pulpal blood flow recordings were measured by means of a laser Doppler Flowmeter. A blood pressure monitor was used to record blood pressure and heart rate. All measurements were simultaneously recorded for 1 min, 5 min after participants made postural changes. Changing from supine to standing caused a significant reduction in pulpal perfusion, while heart rate and diastolic blood pressure increased significantly. A significant non-linear relationship was found between percentage changes in pulpal perfusion and heart rate resulting from standing up. We speculate that when patients arise from the supine position, the shift in venous blood to the legs transiently (2-10 sec) lowers venous return and cardiac output, causing less inhibition of the vasomotor center, which, in turn, results in increased heart rate and blood pressure, but a decrease in pulpal blood flow. These results suggest that pulpal blood flow is affected by postural change, presumably via the autonomic nervous system.

Keywords

dental pulp supine position circulation blood pressure heart rate autonomic nervous system

Introduction

Several regulatory mechanisms of pulpal blood flow have been investigated in animals. These studies indicate that blood flow in dental pulp is regulated by neuronal, local, and humoral mechanisms (Luukko et al., 2011). Such mechanisms are mainly focused on the intrapulpal nerve functions mediating a spread of vascular reactions (Olgart et al., 1991; Matthews and Vongsavan, 1994; Andrew and Matthews, 2002), and vasoactive substances affecting changes in blood flow (Heyeraas et al., 1994; Kerezoudis et al., 1994; Berggreen and Heyeraas, 1999). The observations that pulpal vasodilatation or vasoconstriction could be produced by an electrical stimulation of single pulpal nerve fibers, or an application of pain-producing stimuli to the cat dentin, with no associated change in arterial blood pressure, suggested that the local control of pulpal blood flow would not induce change in systemic blood pressure (Andrew and Matthews, 2002).

However, it has been found that the dental pulp is not auto-regulated (Tønder, 1975) and that the effect of systemic blood pressure on pulpal blood flow in dogs is more prominent than that of local mechanisms (Tønder, 1980; Sasano et al., 1989). Since the homeostatsis of blood pressure is under short-term control by baroreceptors that depend mainly on the innervation of the heart and blood vessels by the autonomic nervous system (Smith et al., 1994), it can be assumed that these mechanisms could have some effects on autonomic neuronal control of pulpal perfusion. Tønder (1975) demonstrated that pulpal sympathetic fibers in dog canines were activated through the carotid baroreceptor reflex. Consistent with this, an alteration in human body position has been shown to cause a significant change in pulpal blood flow (Firestone et al., 1997). These measurements were performed in upper canine teeth of 10 human participants (aged 18-47 yrs), in supine, sitting, and standing positions. Since changing the body’s position requires numerous cardiovascular and autonomic adaptations to prevent postural hypotension, the significantly higher pulpal perfusion, obtained following the supine position in this study, indicates the possibility that there may be an involvement of cardiovascular autonomic modulation in pulpal blood flow. However, this study was limited by a small sample size, and a lack of evidence for an involvement of simultaneous cardiovascular change affecting pulpal vascularity. Thus, the present experiments were carried out to further investigate the relationship between pulpal blood flow and reflex autonomic activity due to postural changes in humans.

Materials & Methods

The experiments were done on 21 healthy premolars in 16 participants (mean age, 22 yrs; range, 20-31 yrs), 4 men and 12 women. All participants were in good health, with no chronic medical diseases. Those with a systolic blood pressure or a diastolic blood pressure greater than 140 and 90 mm Hg, respectively, were excluded. Radiographic and clinical examinations confirmed that all teeth were fully erupted, vital, and free from caries and periodontal disease.

The study was approved by the Ethics Committee on the Use of Human Rights Related to Human Experimentation of the Faculty of Dentistry, Srinakharinwirot University, and complied with the principles of the Declaration of Helsinki. An informed consent was obtained from each participant. The experiments were carried out in the faculty’s clinic.

All participants were asked to avoid consuming alcohol and caffeine, and refrained from smoking for 12 hrs prior to the experimental day. Also, they were required to be well-rested and to eat a light breakfast about 45 min before the experiment. The participants were allowed to rest for 5 min, after which the measurements of pulpal blood flow, blood pressure, and pulse were obtained for 1 min following each supine, sitting, and standing position. All supine and sitting measurements were performed with the participant sitting in a dental chair. An automatic blood pressure monitor (Omron^® model T6, Novi, MI, USA) was used to record blood pressure and heart rate. Since the experimental conditions of participants were at rest, the mean arterial pressure (MAP) was approximated from the equation, MAP = the diastolic blood pressure plus one-third of the pulse pressure.

Either 1 or 2 upper or lower premolars were used randomly in each participant for recording the pulpal blood flow with a Moor Type MBF3D/42 blood flow monitor (Moor Instruments, Axminster, England). During recording, an opaque black rubber dam (Four D Rubber Co. Ltd., Heanor, England) was applied to the tooth to minimize the contribution of blood flow in tissues outside the tooth (Soo-Ampon et al., 2003; Kijsamanmith et al., 2011). The probe of the instrument (o.d. 1.5 mm) contains two 0.2-mm-diameter optical fibers with their centers separated by 0.5 mm. A clip-on splint made from self-curing acrylic resin on a plaster model of the tooth was used to fix the probe to the tooth. The probe tip was supported on the tooth surface by a short length of stainless-steel tube (i.d. 1.5 mm) that was incorporated into the splint. The tube was positioned so that it was perpendicular to the enamel surface, with its center 2 mm from the gingival margin and over the central long axis of the crown of the tooth. The rotation of the probe around its long axis within the tube was kept constant between trials by the alignment of marks on the probe and tube. This precaution was necessary to ensure that reproducible results were obtained under each of the experimental conditions.

The flux signal from the blood flow monitor was transferred to a computer and analyzed with the Moorsoft program (Moor Instruments, Axminster, England). The sensitivity of blood flow signal was standardized as described previously, and recordings were made with an upper bandwidth setting of 14.9 kHz and a time constant of 0.1 sec. Blood flow was measured in arbitrary perfusion units (Vongsavan and Matthews, 1993). The mean blood flow signal was determined over a period of 1 min, during the recordings at each position.

Statistical Analysis

The raw data on pulpal blood flow and heart rate are summarized as box-plots in Figs. 1A and 1B. Each box represents the median (a line through its center) and the 25th and 75th percentiles. Whiskers above and below the box indicate the 90th and 10th percentiles. Differences in pulpal blood flow and heart rate values obtained from the supine, sitting, and standing positions were performed by Kruskal-Wallis one-way analysis of variance (ANOVA) on ranks, followed by the Tukey test. This test was used because the data for pulpal blood flow and heart rate were not drawn from a continuous distribution. Since all the corresponding blood pressure values were normally distributed, the significance of changes was determined by one-way ANOVA. Where this showed significant effects, we used the Holm-Sidak method for multiple pairwise comparisons of mean values, to determine whether there were any significant differences between subgroups.

Figure 1.

Pulpal blood flow, blood pressure, and heart rate responses to changes in body position. (A,B) Pulpal blood flow and heart rate recorded during supine, sitting, and standing positions (n = 21). The line through the center of each box indicates the median and the lower and upper limits of the box, the 25th and 75th percentiles, respectively. The bars below and above each box indicate the 10th and 90th percentiles. (C) Mean arterial pressure obtained from supine, sitting, and standing positions (n = 21). The error bars represent ± 1 SD.

We normalized data for pulpal blood flow and heart rate by expressing the values recorded when participants were standing as percentages of the corresponding values obtained when they were supine. Non-linear regression analyses were used to assess the relationship between them. The p values < 0.05 are considered significant.

Results

All data obtained from supine, sitting, and standing positions are summarized in the Table. Overall, changes in pulpal blood flow, heart rate, and blood pressure in response to the body positions are shown in Fig. 1. Postural changes caused a significant effect on the median pulpal blood flow (p = 0.007, Kruskal-Wallis one-way ANOVA on ranks). Multiple comparisons between the individual median values obtained when participants were in different positions showed that the supine position produced an increase in the median blood flow, 2.5 (range, 1.65-3.60) perfusion units, when compared with that in the standing position, 1.65 (range, 0-2.4) perfusion units (Fig. 1A). This change was significant (p < 0.05, Tukey test, n = 21). However, the differences in the corresponding values did not differ significantly between the supine/sitting positions and the standing/sitting positions.

Table.

Postural Effect on Pulpal Blood Flow, Blood Pressure, and Heart Rate

					p Value
Type	n	Supine (A)	Sitting (B)	Standing (C)	(A)-(B)	(B)-(C)	(A)-(C)	% Standing/Supine
PBF (PU)	21	2.5 (0.2-5.5)	2.2 (0.6-5.3)	1.7 (0.1-3.6)	NS	NS	0.007	65.9 (1.8-350)
HR (bpm)	21	71 (62-84)	70 (60-92)	79 (64-113)	NS	NS	0.026	110.4 (92.9-166.2)
SBP (mm Hg)	21	104.3 (8.1)	108.8 (7)	108.6 (6.0)	NS	NS	NS	105.1 (8)
DBP (mm Hg)	21	65.1 (7.4)	71.2 (5.4)	76.4 (7.3)	0.003	< 0.001change/	< 0.001	119.0 (13.5)
MAP (mm Hg)	21	78.2 (7)	83.7 (5.4)	87.1(6.1)	0.025	NS	0.017	89.5 (8.5)

PBF = pulpal blood flow; SBP = systolic blood pressure; DBP = diastolic blood pressure; MAP = mean arterial pressure; HR = heart rate; NS = non-significant. The PBF and HR values are median (range); the SBP, DBP, and MAP values are mean (SD).

The effects of body posture on the median heart rate values revealed a significant change (p = 0.026, Kruskal-Wallis one-way ANOVA on ranks). The median heart rate increased significantly, from 71 (range, 66.5-76) beats per min in the supine position to 79 (range, 73-84.8) beats per min in the standing position (p < 0.05, Tukey test, n = 21) (Fig. 1B). However, comparisons between the median heart rates during supine/sitting and sitting/standing positions were not significant.

The simultaneous recordings of blood pressure following postural changes were also determined (Table). We found highly significant changes of the mean diastolic pressure (p = < 0.001, one-way ANOVA, n = 21) and the mean MAP (p = < 0.001, one-way ANOVA, n = 21) recorded during different postures. The differences among the mean diastolic pressures obtained from all positions were significant (p < 0.05, Holm-Sidak method). Furthermore, the mean MAP decreased significantly, from 87.11 mm Hg (SD 6.08) in the standing position to 78.19 mm Hg (SD 6.94) in the supine position (Fig. 1C). This was also found when the mean of sitting MAP, 83.73 mm Hg (SD 5.41), and that of supine MAP were compared (p < 0.05, Holm-Sidak method). However, there was no statistical difference between the mean of standing MAP and that of sitting MAP. Over the same measurement, the differences among the mean systolic blood pressures recorded during all positions were not significant (p = 0.071, one-way ANOVA, n = 21).

The non-linear regression analysis between pulpal blood flow and heart rate changes in response to posture is shown in Fig. 2 (R² = 0.50, p = 0.0045), in which we normalized data for pulpal blood flow and heart rate by expressing the results recorded when participants were standing as percentages of the corresponding values obtained when they were supine.

Figure 2.

Non-linear regression analysis showed the curve relationship between changes of pulpal blood flow and heart rate from supine to standing. We normalized data by expressing the values recorded when participants were standing as percentages of the corresponding values obtained when they were supine (n = 14).

Discussion

These experiments demonstrated that pulpal perfusion decreases in response to movement to the standing position in healthy young adults. Since this decrease is significantly associated with an increase in heart rate, it appears that the modulation in autonomic system that occurs during postural change is capable of affecting blood flow in the dental pulp.

The results we observed for changes in pulpal blood flow were also consistent with those of the study by Firestone et al. (1997). However, in those experiments, the laser Doppler recording system was used without the black rubber dam, allowing for signal contamination outside the tooth (Soo-Ampon et al., 2003; Kijsamanmith et al., 2011). This could account for the significantly higher blood flow signal recorded compared with that obtained in the present experiments.

The cardiovascular changes associated with the gravitational stress of standing are well-known. When an individual stands, about 500 to 1,000 mL of venous blood move from the upper to the lower part of the body. This transient decrease in venous return causes a transient drop in cardiac output and blood pressure. In healthy individuals, a drop in blood pressure results in decreased parasympathetic and increased sympathetic activations through baroreflex-mediated autonomic regulation. Decreased parasympathetic and increased sympathetic activity induces rapid increased activity to the heart. Sympathetic activation causes increased vasoconstriction to all arterials, including those in the dental pulp. This increases systemic blood pressure but decreases pulpal perfusion. Although our findings indicated that an increase in heart rate was significantly correlated to a drop in pulpal blood flow in individuals moving from supine to standing positions, such correlation between blood pressure and blood flow could not be found. This was probably due to the fact that the expected transient drop in systemic blood pressure occurred and was replaced by a compensatory increase in blood pressure during the 5 min that elapsed after postural changes were made. That is the observation we missed in the present experiments.

Soo-Ampon et al. (2002) demonstrated a significant reduction of pulpal blood flow recorded in upper central incisors, along with a marked increase in heart rate, after limited exercise in healthy young participants. However, this appears to contradict the results of several reports (Watson et al., 1992; Lobo et al., 2012) showing that pulpal blood flow in response to exercise was unpredictable and that there was no relationship between increased pulse rate and pulpal blood flow. This can be attributed to a contaminated signal from non-pulpal tissues, probably up to 80% when recorded without the use of the black rubber dam (Soo-Ampon et al., 2003).

Apparently, factors controlling heartbeat could possibly influence pulpal blood flow. When people move from lying to standing positions, there is a decrease in cardiac output of approximately 20 to 30%. Since exercise, anxiety, and excitement are physiologic conditions capable of increasing cardiac rate up to 700% (Barrett et al., 2010), it appears, in the present experiments, that minimal pulpal blood flow in a healthy middle-aged man would exist during the daytime. Furthermore, in individuals in a resting supine position during sleep, pulpal blood flow is maximized, mainly due to minimal sympathetic vasoconstrictor activity in the pulp. These mechanisms will be exaggerated when the pulp is inflamed, resulting in an increase of already-raised pulp tissue pressure (Van Hassel, 1971; Stenvik et al., 1972; Tønder and Kvinnsland, 1983; Heyeraas and Kvinnsland, 1992; Heyeraas and Berggreen, 1999). This increase, then, would be sufficient to stimulate the intradental nerve, giving rise to the clinical condition of insomnia due to a severely throbbing toothache. The results of the current study support the speculations of Pashley and Liewehr (2006), that patients with pulpitis often call dentists at night, when they cannot sleep because of pulpal pain that slowly disappears when they assume the upright position to drive to the dentist’s office. In a standing individual, the sympathetic innervation of the pulp would lower perfusion pressure, allowing tissue pressures to fall somewhat, thereby relieving pulpal pain.

Also, these experiments suggest that there is a partial vasoconstriction of sympathetic nerves in the dental pulp during standing, compared with more vasodilator tone when reclining. The possible explanation may involve evidence in experimental animals indicating the presence of specific autonomic receptors and agonist effects in dental pulp (Yu et al., 2002; Bowles et al., 2003; Hargreaves et al., 2003; Souza et al., 2007).

Studies have shown that there is a lesser increase in heart rate upon standing in older compared with younger individuals (Smith and Porth, 1991). This may be attributed to a decrease in baroreceptor reflexes in the elderly. Such changes possibly become more evident in diseased conditions, particularly orthostatic hypotension and autonomic neuropathy. The findings from this study provide an important basis for further study on the systemic factors modulating vascular changes in the periodontium. Also, the effects of certain systemic diseases or anti-hypertensive agents on degenerative changes in pulpal or periodontal conditions should be investigated.

Footnotes

Acknowledgements

The authors thank Professor Bruce Matthews, Associate Professor Sittichai Wanachantararak, and Associate Professor Nopakun Vongsavan for their valuable comments and equipment support.

This study was supported by The Thailand Research Fund (RSA5580049).

The authors declare no potential conflicts of interest with respect to the authorship and/or publication of this article.

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