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Heterogeneity of blood flow in the canine tooth in the dog

Heterogeneity of blood flow in the canine tooth in the dog

Archs oral B,ol. Vol. 25, pp. X3 to 86 Pergamon Press Lfd 1980. Printed in Great Britain HETEROGENEITY OF BLOOD FLOW IN THE CANINE TOOTH IN THE DOG ...

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Archs oral B,ol. Vol. 25, pp. X3 to 86 Pergamon Press Lfd 1980. Printed in Great Britain



Department of Physiology and School of Dentistry, University of Minnesota, Minneapolis, MN 55455 and Group Health Plan, Incorporated. St. Paul, Minnesota, U.S.A.

Summary-Regional blood flow in the dental pulp was quantitated in two groups of dogs of different ages using radioactively labelled 15-pm microspheres. In Group A (N = 9; age 4-8 months), the roots were two-thirds to fully formed. Average regional blood flows in the coronal tip (CT), remaining coronal part (RCP) and root (R) were 1.03, 0.57 and 0.52 ml/min/g, respectively for the maxillary canines and 0.77, 0.42 and 0.39 ml/min/g for the mandibular canines. In group B (N = 9; age 9-11 weeks), crowns were approximately one-half formed. Regional blood flow to the maxillary teeth averaged 0.86ml/min/g to the CT and 0.39 to RCP whereas CT was 0.58 ml/min,/g and RCP averaged 0.31 ml/min/g for the mandibular ones. In both groups, blood flow to CT was significantly greater than flow to the other pulp regions. If these microspheres are distributed according to flow, then heterogeneous flow exists, which may correlate with the anatomy of the blood vessels, and may partly account for the difference in values reoorted bv other investigators using different methods,



Quantitative values for pulp blood flow have been reported but not all methods have provided the same value. Tijnder and Aukland (1975) reported blood flows of about 0.15 ml/min/g using the H, clearance technique in dogs. Edwall (1972) obtained clearance constants (k-values) by monitoring the disappearance of a diffusible isotope placed in a cavity cut in the tooth and suggested a k-value of about 0.02 min-’ for cats. Meyer and Sha (1968) in their clearance study found an average k-value of 0.32 min-’ in dogs. The fractionation method of Sapirstein (1958) for diffusible isotopes and its modification for radioactive microspheres has been used to quantitate blood flow to the pulps of the canine tooth in dogs. The average values reported in ml/min/g varied from 0.29 to 0.73 for 4ZK and *6Rb, 0.44 to 1.29 for 25-pm diam. microspheres (Meyer, 1970), 0.37 to 0.80 for 15-pm microspheres and 0.18 to 0.37 for 8-pm microspheres (Path and Meyer, 1977). The differences between these values may depend upon a number of factors, such as the methodologic assumptions, heterogeneity of pulp blood flow, stage of tooth development and the anatomical arrangement of pulp vessels. Several observations indicate that blood flow may not be homogeneous throughout the dental pulp. Cheng and Provenza (1959) and Boling (1942) observed that capillary density is not uniform within the pulp. Corpron, Avery and Lee (1974); Klingsberg, Carvellaro and Butcher (1959). and Kramer (1960) observed that heterogeneity of capillary density varies between animal species and with stage of tooth development. The endogenous oxygen consumption of the pulp depends upon the region sampled (Fisher, 1967) and stage of development (Fisher and Schwabe, 196 1). Thus, our purpose was to quantitate blood flow to various regions in the dental pulp in the dog.

Eighteen dogs of no particular breed, of which nine were 4-8 months (Group A), and nine were 9-l i weeks of age (Group B), were anaesthetized by intravenous sodium pentobarbital (30 mg/kg) maintained with small incremental doses. Animals were artificially lung ventilated at a frequency and tidal volume sufficient to obtain a normal arterial PCOZ and P02. Heart rate and blood pressure were monitored and pulp blood flow was determined by the microsphere (15 pm dia.) method (Meyer, 1970; Path and Meyer. 1977) which involves arterial sampling to obtain the reference Row (V/t). Determination of blood flow (F) in the pulp or any portion of it by dividing the radioactivity (4) found in the pulp, or part of, by the radioactivity (A) in the reference sample, and multiplying this by V/t, i.e. F = (y/A).(V/t). This flow is divided by the weight of ea:h pulp, or portion, to determine the flow per gram. In three Group A dogs, a second quantity of radioactive microspheres of the same size but differently labelled was injected to examine reproducibility. In group A, the canine teeth were erupted or erupting and two-thirds to complete root was formed. Using the cementurn-name1 junction as a guide, the pulps were divided into root (R) and coronal portions. Path and Meyer (1977) observed that the tip of the coronal pulp appeared to be hyperaemic. Therefore. the coronal portion was sectioned into a coronal tip (CT) and remainmg coronal part (RCP) of which CT was approximately one-fifth the volume of the coronal portion. To examine the uniformity of sectioning, a CT:RCP weight ratio was determined for each pulp. In Group B, the canine teeth were unerupted and the crowns were about one-half formed; the coronal portion was divided so that CT was about onefifth of the total volume. The dental sacs were

M. G. Path and M. W. Meyer

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Fig. 1. Average blood flows and standard error of the mean (SEM) to three pulp regions and total pulp of the maxillary and mandibular canine teeth for Group A dogs. CT, coronal tip; RCP, remaining coronal part; R. root; AVE. weighted mean flow to the entire dental pulp. removed to compare with the pulp as the vascular supplies of the sac and pulp are in continuity. Data from the right and left sides were pooled to obtain a flow value for each pulp portion. Mean blood flows for the maxillary and mandibular pulps and standard error of these means (SEM) were calculated for each group. Blood flow to the total pulp was also determined by pooling the data. and the means and SEM were calculated. We analysed the heterogeneity of flow within a given tooth and







between the maxillary and mandibular canines using the paired t-test. Blood flow between Groups A and B was analysed for statistical significance using Student’s t test. RESULTS

For Group A. the mean blood flows (+SEM) to the total pulp and pulp sections of the maxillary and mandibular canine teeth are presented in Fig. 1. The






Fig. 2. Average blood flows and standard error of the mean @EM) to two regions of the coronal pulp, total pulp and dental sac of the maxillary and mandibular canine teeth for Group B dogs. CT. coronal tip; RCP, remaining coronal part: AVE. weighted mean flow to the existing coronal pulp; DS. dental sac.

Heterogeneity of pulp blood flow average blood flows in ml/min/g to the coronal tip (CT), remaining coronal part (RCP) and root (R) of the maxillary canine pulp were 1.03, 0.57 and 0.52 respectively. The mean flow to the CT was significantly higher (P < 0.01) than to the RCP and R. In the mandibular canines, the mean blood flow to CT (0.77 + 0.07) was also significantly higher (P < 0.001) than flow to either RCP or R. Maxillary pulp portions and total pulp had significantly (P < 0.02) higher blood flows than mandibular tissue. The CT:RCP weight ratio averaged 0.19 k 0.02 for the maxillary canines and 0.23 f 0.02 for the mandibular ones. In the three dogs in which a second injection of microspheres was made, the corresponding blood flows were similar. The mean flows for the pulp portions, total pulp and dental sacs for Group B dogs are presented in Fig. 2. Blood flow to CT was significantly greater (P < 0.01) than flow to RCP for both the maxillary and mandibular canines. Flow to the dental sac was greater than to CT and was significantly greater (P < 0.01) than the total flow to the maxillary and mandibular dental pulps. The CT:RCP weight ratio for the maxillary canines averaged 0.21 + 0.01 and 0.20 _t 0.01 for the mandibular ones. There were no statistical differences in blood flow between Group A and B pulp portions. In Group A, the mean CT:RCP blood flow ratio was 1.94 + 0.20 for the maxillary canines and 2.01 + 0.25 for the mandibular canines. This ratio for Group B was 2.23 t_ 0.17 and 1.96 f 0.21 for the maxillary and mandibular pulps respectively. There were no significant differences between these ratios. The cardiovascular status of the two groups remained stable. For Group A, cardiac index (+SEM) averaged 141 + 12 ml/min/kg while blood pressure and heart rate averaged 117 f 6 mm Hg and I61 & 7 beats/min. Cardiac index, blood pressure and heart rate in the Group B averaged 179_fIlml/min/kg, 100_+5mm Hg and 155_f12 beats/min. respectively. DISCUSSION

Cardiovascular status and pulp blood flows as calculated for the total pulp were similar to Path and Meyer’s (1977) findings for dogs of equivalent ages. In that study, using 15-pm microspheres, average blood flow (+SEM) to the maxillary and mandibular canines was 0.52 +_ 0.05 and 0.41 + 0.04 ml/min/g in dogs 6 months old. At 2 months, pulp blood flow averaged 0.53 & 0.1 I for the maxillary canines and 0.41 f 0.08 for the mandibular ones. A higher blood flow to the maxillary canines has been reported (Meyer, 1970; Path and Meyer, 1977). In our present study, blood flow to the dental sacs was slightly higher than flow to the dental pulps. We have found (unpublished) that, in macaque monkeys and lambs, the dental sac has a higher blood flow than its corresponding dental pulp. Vascular resistance thus may be less in the dental sac. The peripheral region containing the capillary loops and odontoblasts may have a higher blood flow than the central portion of the pulp. We were not able to section the pulps into core and peripheral portions as Fisher (1967) did with young bovine pulps


to study oxygen consumption. He found that oxygen consumption was heterogeneous, the peripheral region having twice the value of the central core portion. If oxygen consumption is coupled with blood flow, then blood flow should be heterogeneous within the pulp and the peripheral regions should have twice the blood flow. The electrodes used by TBnder and Aukland (1975) to measure pulp blood flow in canine teeth of dogs by the hydrogen method had a bared tip of 0.5 mm and were impaled into the main coronal portion of the pulp to about 1 mm. Only single washout rate constants were observed. We have repeated this work with the electrode impaled so that the bared tip measured the hydrogen concentration in the peripheral and core portions of the RCP. Only single rate constants were observed instead of two, as might be expected if the hydrogen method could differentiate heterogeneous flow compartments. When an electrode with a bared tip (4-5 mm, dia. 0.125 mm) long enough to reach the core portion of RCP by impaling the electrode via the canine tip was used, two rate constants were observed. This suggests that the core portion representing the largest fraction of the CT has a higher blood flow than the peripheral portion of the CT. The presence of centrally located small arteries pursuing a straight course to the coronal pulp noted by Cheng and Provenza (1959) supports this suggestion. Branching without change in diameter was noted as these vessels continued their course into the coronal pulp. The diversity of values reported for pulp blood flow in canine teeth could be method-dependent, and influenced by regional differences in rate. By the clearance (isotope and non-isotope) methods, the rate constant k = F/Vi; where F is the flow, i is the partition coefficient, and V is some unknown volume. If this volume is a region of low flow, the measured k is representative of this region and not the entire pulp. The k-values reported by Edwall (1972) using “‘1 in deep cavities cut in the teeth were obtained from the washout curves when these became monoexponential at about 5-15 min after depositing the isotope. However, Meyer and Sha (1968) found that the clearance curves using 1311 in a deep cavity could be fitted with a bi-exponential equation. They obtained a measure of /1 and suggested that the larger k-value was related to blood flow because the calculated flow values were similar to the flows determined by the 4zK isotope-fractionation method. Stiisseck (1970) observed that shunt diffusion of H, from arteries in the pia mater contributed to the venous H2 clearance curves when an artery and vein were in close proximity (2OOpm) for 3 mm. The proximity of the pulp arterioles and venules (Cheng and Provenza, 1959) may be suficient for diffusion between these vessels for highly diffusable radioactive or nonradioactive tracers to occur. Tiinder and Aukland (1975) suggested that the H, clearance technique may under-estimate pulp blood flow if counter-current diffusion of H2 occurs. The method also measures blood flow in an unknown volume and the calculated flow value may not be representative of the entire pulp if heterogeneity of flow exists. Blood flow to the entire pulps of canine teeth of dogs with the thorax opened, determined by diffusible (86Rb, 42K) and non-diffusible (15- or 25-pm microspheres) tracers, are similar


M. G. Path

and M. W. Meyel

(Meyer, 1970; Path and Meyer, 1977). However. in dogs experimented on with the thorax intact (Meyer, 1970), and for other teeth such as the incisors and molars (Path and Meyer. 1977), blood flows determined by the 15- and 25-pm microspheres were higher than those determined by the diffusible tracers. If heterogeneity of flow exists, in the regions of high flow the diffusible tracers may no longer be tlowlimited; this would result in a lower fractional uptake of the tracers within the entire pulp. Experiments using the 7-lo-pm microspheres (Path and Meyer. 1977) show that pulp blood flow as calculated by the uptake of the lS+m microspheres is twice as large as that obtained using smaller spheres. If both sizes are distributed as flow, then vascular shunts with a diameter of about IO-pm must exist. The existence of these vascular shunts in particular regions of the pulp are responsible for heterogeneity of the flow. The anatomical arrangement of the blood vessels and heterogeneous distribution of flow may influence the flow measured by a particular method. Using several methods simultaneously or sequentially could expand our knowledge of circulatory physiology of the dental pulp. Acknowledyc,,nrrlt~This study grant number DE 02212.

was supported



Boling L. R. 1942. Blood Rec. 82, 25 31.

vessels of the dental



C‘heng T. C. and Provenza D. V. 1959. Histologic observations on the morphology of the blood vessels of canine and human tooth pulp. .I. dent. Res. 38, 552-557. Corpron R. E.. Avery J. K. and Lee S. D. 1974. Ultrastructure of terminal pulpal blood vessels in mouse molars. Anut. Rec. 179, 527-542. Edwall L. 1972. Nervous control of blood circulation in the dental pulp and the periodontal tissues. In: Oral Physiology (Edited by Emmelin N. and Zotterman Y.) pp. 1% 149. Pergamon Press, Oxford. Fisher A. K. 1967. Respiratory variations within the normal dental pulp. J. drrlt. Res. 46, 424428. Fisher A. K. and Schwabe C. 1961. The endogenous respiratory quotient of bovine dental pulp. J. dcwt. Rrs. 40, 346351. Klingsberg J.. Carvellaro L. and Butcher E. 0. 1959. A capillary network in the odontoblastic layer of developing teeth. J. dent. Rrs. 38, 419. Kramer 1. R. H. 1960. The vascular architecture of the human dental pulp. Archs orcrl Biol. 2, 177-189. Meyer M. W. 1970. Distribution of cardiac output to oral tissues in dogs. J. drnt. Rex 49, 787-794. Meyer M. W. and Sha R. S. 1968. Isotope clearance and blood flow in the dental pulp. Internat. Ass. for Dent. Res. Preprinted abstracts. 46th General Meeting, Abstract 524. Path M. G. and Meyer M. W. 1977. Quantification of pulpal blood flow in developing teeth of dogs. J. dent. Rex 50, 1245-1254. Sapirstein L. A. 1958. Regional blood flow by fractional distribution of indicators. Am J. Physiol. 193, 161-168. Stiisseck K. 1970. Hydrogen exchange through the pial vesscl wall and its meaning for the determination of the local cerebral blood tlow. Pfliigrrs Arch. 320, I I l- 119. Tandrr K. J. H. and Aukland K. 1975. Blood flow in the dental pulp in dogs measured by local H, gas desaturation technique. Archs orul Bid. 20, 73--76.