Ralph R Steinman DDS, Emeritus Professor, School of Dentistry, Loma Lina University, Loma Linda, California
Compend Contin Educ Dent, Vol V, No 9, pp 722-728, October 1984
It is well established that certain strains of bacteria are associated with the carious process. In clinical dentistry, a major portion of practice is spent repairing the damage cause by caries. The introduction to the section on infectious diseases in The Merck Manual states "a healthy individual lives in harmony with his normal body flora, but this balance may be disturbed by disease."(1) One dictionary defines disease as disturbed or abnormal condition of the organism or physiological action in the living organism as a whole or in one of its parts." Dental caries, by definition, is an infectious disease caused by microbes which are members of the normal oral flora. Is the presence of dental caries associated with normal function? Is the presence of dental caries associated with disturbed physiologic activity within the tooth, and is the normal response of the teeth to bacterial invasion similar to the response of other tissues to attack? This paper will report on a number of studies which have considered these and other questions.
Disease and Malfunction in the Hydraulic System
A reduction in the blood supply to a tissue may be associated with disease. A disturbance of fluid transport in a tissue may result in disease. The failure of endocrine glands is often associated with an increased susceptibility to disease. Could any of these conditions adversely affect the health and physiologic activity of the teeth?
In fact, the hydraulic system of the tooth could be affected by these conditions. The system can be compared to a pipe that connects two sections - dentin and enamel - and which is open at both ends and filled with fluid which can move in either direction or not move at all. The dentin end is in contact with the pulp fluid, while the enamel end is is in contact with either saliva or plaque fluid. In this system, the odontoblasts act as gatekeepers or directors of traffic.
Whether there is fluid movement in this imaginary pipe depends largely on the enamel. The enamel is porous. The pore size of the enamel is 5 nanometers(2), which is large enough to permit the passage of molecules the size of methyline blue(3), or acriflavine hydrochloride. ? percent by volume of the enamel is mobile water(5). This volume is not bound, but rather is free to move in either direction, depending upon the forces applied to it. Normally, the enamel fluid moves from the dentin-enamel junction toward the surface of the tooth(6,7).
The normal hydraulic system of the tooth is important because the dentin requires an active transport, without which its rate of metabolism would not be possible(8). The pulp is designed to support this hydraulic system. The rate of' blood flow in the pulp of the tooth is four time the rate of blood flow in resting muscle(9). The capillaries adjacent to the odontoblasts are fenestrated(10). Such capillaries are found in areas of rapid exchange, such as the kidneys or the villi of the intestines. It is obvious that the teeth are designed to facilitate a rapid exchange between the blood vessels and the adjacent tooth structure.
Restriction of the blood supply to the teeth
Ligating the major blood vessels to the teeth could adversely affect the hydraulics, the nutrient supply, and the availability of hormones for pulpal regulation. This observation stems from an experiment which resulted in a significant increase in the amount of caries in the teeth of rats whose blood supply was restricted(11). Further study revealed that the associated surgery did not adversely affect salivary gland function(12). This increase in caries could be explained most logically as resulting from some effect upon the pulp or adjacent tissue of the tooth.
A recent report showed that when the pulp vascularization of hamsters had been hindered, there was an increase incidence of caries, compared to that of teeth with normal blood flow in the same animal. It stated further that "a positive correlation between caries score and the pulp inflammation grade was observed."(13)
Alteration in Fluid Transport in the Dentin and Associated Increase in Caries
A malfunction in the hydraulics of the tooth can be imposed by an intraperitoneal administration of bradykinin, a tissue hormone. When administered to rats, it was found to cause an inward movement of fluid: from the plaque, through the enamel, through the dentin, and into the pulp of the molars(14) (Figures 1A and 1B). When administered regularly to young rats fed a non-cariogenic diet, the imposed disturbance was associated with a highly significant increase in caries(14,15). It was also demonstrated that the administration of bradykinin caused a decrease in pulpal blood flow(16).
Another technique that produced a malfunction in the hydraulics of the tooth, with a reversal in the normal direction of fluid transport was the administration of hydrogen peroxide to rats by stomach tube(17). With this procedure, dye placed in the oral cavity penetrated through the tips of the cusps of the molars. The tips of the cusps of rat molars have no enamel protection (Figures 2A and 2B). Although bacteria are usually present on this surface and there is occasional invasion of the tubules, usually no caries is present(18). However, when the administration of hydrogen peroxide was continued regularly to young rats, it was associated with dental caries in the tips of the cusps, the area of' penetration(19). Logically, it could be assumed that the caries was due to the inward movement of fluid. The authors suggest that the absence of caries normally is the result of the fluid transport in the dentin. Thus, reversal in the normal direction of fluid through the teeth is associated with a dramatic increase in caries, strongly suggesting the role of fluid transport in the health of the teeth.
Effect of a High-Sucrose Cariogenic Diet on the Hydraulic System of the Teeth.
A study of the movement in dentin of acriflavine hydrochloride, a fluorescent dye, showed that the dye did not move to the dentinoenamel junction as readily in the molars of rats fed a high-sucrose cariogenic diet as it did in animals fed a non-cariogenic diet(20,21) (Figures 3A and 3B). This was true in both germ-free animals and those with conventional oral flora(22).
The accumulation of tryptan blue in the dentin of rat molars following the intraperitoneal injection of the dye was also less in the teeth of rats fed the high-sucrose cariogenic diet than in the teeth of rats fed the non-cariogenic diet. This was true in both crowned and uncrowned teeth(23). Thus, malfunction of the pulp-dentin hydraulic complex can be imposed through alteration in diet. There is also, of course, a concomitant increase in the incidence of dental caries with a high-sucrose cariogenic diet.
Stasis of the hydraulic system of the teeth is found in endodontically-treated teeth. There is no inward fluid movement beneath the plaque, which may help to explain why endodontically-treated teeth have a lower incidence of caries that intact teeth in the same oral cavity(24-27). Passive diffusion would be the mode of penetration beneath the plaque into these teeth.
The Effects of a Reduced Rate of Fluid Transport in Teeth on their External Environment.
Concomitant with reduced dentinal fluid movement is a movement from outside the tooth beneath the plaque into the tooth. This is a reversal in the normal direction of fluid transport in the tooth. It is demonstrated by the movement of methylene blue from the oral cavity beneath the plaque through the enamel into the dentin (28) (Figures 4A and 4B), compared with little or no inward movement of dye into animal teeth that are caries free.
The presence are inflammatory cells in the pulp of human teeth beneath early caries would suggest that an inward movement of fluid is occurring with the carious process(29). The marked increase in ninhydrin reaction beneath the carious process in human teeth also may be evidence for this inward movement(30) (Figures 5A. and 5B). The lack of ninhydrin reaction beneath erosion would suggest that no inward movement is associated with erosion (figure 5C).
The suppressed rate of fluid transport in the dentin of animals fed the high-sucrose cariogenic diet is thought to be due to the suppression of the hypothalamic-parotid gland endocrine axis. The hypothalamus releases into the bloodstream a factor which stimulates the carotid gland, in turn, to release into the bloodstream the parotid hormone. This hormone stimulates the transport system in the dentin of the teeth(31,32). Thus, the removal of the salivary glands may adversely affect the health of the teeth, both through the absence of saliva on the external surfaces of the teeth and through the absence of hormonal stimulation of the fluid transport within the teeth(27).
Stimulating the Rate of Fluid Transport
Can the suppressed rate of dentinal fluid transport be stimulated in animals fed the high-sucrose cariogenic diet? How would this procedure affect the incidence of caries?
The administration of a parasympathetic stimulus was found to increase the rate of dentinal fluid transport in the teeth of animals fed the high-sucrose cariogenic diet. There was also a corresponding decrease in the incidence of dental caries(14,15).
The subcutaneous administration of urea was also found to significantly increase the rate of dentinal fluid transport in the teeth of animals fed the cariogenic diet. Again, there was a corresponding decrease in caries(21).
When infused intravenously, several compounds of the urea cycle have been found to stimulate the rate of fluid movement in the dentin of rats fed the high-sucrose cariogenic diet(33). When one of these compounds, carbamyl phosphate, was added to the cariogenic diet in minimal amounts, a significant decrease in caries was observed(34). Thus, when normal function of the hydraulic system was restored, a reduction in caries was observed. Furthermore, the addition of certain trace elements to this diet was found to enhance the effect of carbamyl phosphate and result in a further reduction in the incidence of caries. However, enriching the diet was only effective in reducing the incidence of caries in intact teeth of intact animals(27).
It is thought that compounds like carbamyl phosphate restore normal fluid transport in the teeth of animals fed the high-sucrose cariogenic diet by releasing hormones of the hypothalamic-parotid gland endocrine axis(31,32). The restoration of the normal rates of fluid transport in turn restores normal function in the pulp-dentin complex, thus resulting in a reduction in the incidence of dental caries. The oral flora are still eating the high-sucrose diet, although the caries rate has been reduced.
Reversing Induced Malfunction
If one malfunction has been the induced in the teeth of younger animals, can it be reversed, and what would be the result of such reversal?
After one week of eating the high-sucrose cariogenic diet, young animals often demonstrate demineralization at the dentin-enamel junction. If the animals are then fed a non-cariogenic diet, these areas often will re-mineralize(35,36). In addition, the caries process is arrested when the malfunction is corrected by an improvement in the nutritional value of the diet.
A number of years ago, Boyd and Dain, working with diabetic children at the Children's Hospital of the State University of Iowa, observed that when the diets of these children were corrected and the diabetes brought under control the caries was arrested(37). Again, if the underlying problem of malfunction is corrected caries may be arrested.
The Effect of Enrichment of the Diet on the Acid Production of Plaque
Food saliva incubation studies would suggest that the nutritional improvement of the diet in no way reduces the ability of the bacteria to produce acid(38,39). In fact, the foods with the greater micronutrient content produced significantly more acid than did an equal caloric amount of sucrose, glucose, or starch. It would be well to remember that when foods are consumed they nourish both the host and the bacteria of plaque.
An American Dental Association Health Foundation Research Report stated that "plaque pH methods using human plaque specimens have been used to give the measure of the acidity at the plaque tooth interface when food is eaten, but this is a measure of the plaque vicinity and not cariogenic city, per se."(40) It is safe to conclude that went wherever any food, saliva, and bacteria in accumulate in the oral cavity, as it may be produced in destructive amounts. It should not be interpreted from this conclusion that acid is unimportant in the carious process; it may be essential.
The Biological Response of Teeth to Bacterial Invasion
It is well-established that certain strains of bacteria are essential in the carious process. Other tissues subject to bacterial invasion respond to the challenge in an active matter. Antibodies are produced which move into the area in an effort to defend the body. There is also an effort to isolate and wall off the invading organisms. These defense reactions are not always successful, and the bacteria may spread further into the body.
What is the response of the tooth to bacterial invasion? When the bacterial invasion reaches the dentin-enamel junction, immunoglobulins are "physiologically localized in the dentin in response to the destruction to the destructive stimuli of caries."(41) (Figure 6). These antibodies are arranged in the dentin in a defensive formation. The source of these antibodies is the blood supply of the pulp. They are apparently transported to their defensive position under the influence of the odontoblasts.
Another response of the tooth to bacterial invasion involves the mineral component. Hiper-calcification may be found between the pulp and the area of invasion. Also, secondary dentin is formed to further protect the pulp from a direct invasion of bacteria (Figure 7). This process is an effort by nature to wall off the area are of infection from the rest of the tooth. If these measures are not successful, the infection may spread to the pulp into the rest of the body.
All activities of the body, whether calcification, nerve impulses, fluid transport, muscle contraction, or brain function, require energy. This energy usually is supplied in the form of adenosine triphosphate (ATP). The more ATP in a tissue, the greater that tissue's capacity for work. In one study, the ATP levels were measured in various layers of dentin beneath both caries and fillings in human teeth(42). Beneath caries confined to the enamel, there was a significant increase in ATP in the dentin. When the caries reach the dentin or when the a filling was placed, there was a 100% increase in ATP compared with the same areas when the caries was confined to the enamel. While these changes in ATP content were occurring in the dentin, no significant differences in ATP levels in the pulp were observed(43). Also reported was increased phosphoesterase activity in the pre-pulpal dentin layer under incipient carious changes in the dentin(44). Apparently, the dentin is already responding both anabolically and catabolically in the early stages of caries. What happens if the tooth fails to prevent the ingress of noxious material from the plaque? The pulp of the tooth also is adversely affected by the carious process. Changes were observed in the pulp beneath the white spots of the enamel before cavitation. The most common changes were an impairment of odontoblastic layer and an accumulation of exudate cells(29). Thus, the entire thickness of the teeth -- the pulp, the dentin, and the enamel -- is affected by the caries attack.
Summary
It should be clear from all that has been presented in this paper that the tooth is not a helpless appendage in a destructive environment; rather, it is a living vital organ capable of resistance repair, and a vital response to attack. In order to maintain its integrity, it is necessary that it be supplied with the correct nutrients and that its physiological processes be supported, not suppressed. The tooth is a vital part of the body, and what affects the body for good or ill may also affect the teeth to a greater or lesser degree. If the patient has a mouth full of caries, there is probably more wrong with the patient that holes in his or her teeth. The patient may need more than having cavities filled or purchasing a new toothbrush. In order to restore the tooth to health, the dentist may have to consider more than the surface of the tooth. Unless the underlying malfunction is corrected the restoration may fail.