Role of Biodental Engineering Factors (BEF) in the Etiology of Root Caries John 0.Grippo, D.D.S., F.A.G.D.* James V. Masi, Ph.D.t

A preliminary study and hypothesis of the etiology of root caries is presented with appropriate data suggesting that biodental engineering factors (BEF)be introduced into the equation that is generally accepted in the formation of all caries. Principally, because of the rapid progression and location of root caries, BEF in addition to bacterial plaque and suitable substrate contribute to the development of these unique lesions. The dominant and most significant factors recognized by bioengineers are tooth flexure, stress concentration, stress corrosion, and piezcelectricity. All of these factors interplay during the dynamics of occlusal activity causing the loss of tooth substance. A new and revised model is being presented that provides a basis for the etiology of root caries.

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oot caries is a major oral health problem. Its bacterial etiology is unclear and its pathogenic mechanisms have not been defined. The purpose of this paper is to present several new factors in the complex multifactorial equation of root caries development. Research is presented on the etiology of root caries involving a variety of biomechanical, bioelectrical, and biochemical principles known as the biodental engineering factors, or BEF. Due to the paucity of information concerning the etiology of root caries, this article contains two sections, the known factors attributed to root caries and the results of several in uitro experiments in the determination of BEF. There is a prevalence, diversity of distribution, and pattern of root caries.2 After age 35, its incidence increases significantly, affecting 50 percent of the population between 40 and 49 years of age.2.3In subjects older than 50, nearly one of every five teeth with recession has root caries and, because of the increasing retention of teeth into adult years, the management of root caries will become a more important clinical service.4 The prevention, restoration, and control of these areas present a n ongoing challenge to the dental profession.

Root caries, also referred to as cemental, cervical, radicular, and senile caries, is a soft, progressive lesion affecting the cementum and dentin of the r ~ o t .These ~.~

*Senior Lecturer, School of Engineering, Bioengineering Program, Western New England College, Springfield. Massachusetts tProfessor, Department of Electrical Engineering and Coordinator of Bioengineering Program. Western New England College, SpringBeld, Massachusetts. Address reprlnt requests to John 0. Grippo, D.D.S.. 123 Dwight Rd., Longmeadow. MA 01 106. 01991 Decker Periodicals Publishing, Inc.

Figure 1. A diagrammatic representation of the primary (essential)factors in dental caries etiology. Concurrent interaction of the three factors over a period of time (overlapping circles) is essential for caries to develop. (After Keyes PH. The infectious and transmissible nature of experimental dental caries. Arch Oral Biol 1960; 1(4):304-320.) 71

JOURNAL OF ESTHETIC DENTISTRY/VOLUME 3, NUMBER 2 MarchlApril 1991

lesions occumng a t the cementoenamel junction involve plaque and subsequent bacterial invasion. Like coronal canes, root caries has been established to be a complex and multifactorial disease. This process involves three essential parameters: cariogenic microflora, susceptible teeth, and a suitable local substrate existing for a period of time (Fig. Actinornyces viscosus, a n acidogenic bacterium, is almost always present in the plaque overlying root lesions. We suggest that several new bioengineering factors are essential in the root caries process. These factors are ever present, unavoidable, and interplay during mastication, parafunction, or swallowing tooth contact. Interocclusal contact takes place 1,500 or more times each day during the act of chewing and ~wallowing.~ Parafunctional activities (bruxing. clenching) and gum chewing increase this number tremendously. The interaction of biomechanical, electrochemical, chemicometallurgical, and piezoelectrical forces are present during interocclusal contact and, by working in concert with the corrosive products of plaque, potentiate the root caries process. In 1965, Lehman and Meyer did photoelastic tests showing that mechanical stresses between teeth, e.g. at contact points or between natural teeth and partial denture clasp and rest, are contributory factors in caries formation.s Lebau in 1968 hypothesized that the loading of teeth preceded caries a c t i ~ i t i e s McCoy .~ reported on tooth flexure from masticatory loading and that tensile forces at the fulcra, usually found at the cementoenamel junction, are powerful enough to pull apart the enamel prisms and also cause cervical notch-

ing of the dentin. l o At these flexure points we have tensile forces concentrated on one side and a compressive force on the opposing surface. Since enamel has high compressive strength a n d low tensile strength, the resultant forces tend to cause hairline cracks and eventually fragment the highly crystalline enamel. Dentin, though having a higher tensile strength than enamel, is limited in its ability to withstand tensile stresses. Excessive tensile forces act on the dentin and disrupt the chemical bonds between the hydroxyapatite crystals resulting in the loss of tooth substance.12 The notches that appear a t the gingival margins are caused by eccentric occlusal loading forces. The consensus among a group of California engineers who viewed these effects was that they were seeing obvious examples of hard tissue fatigue.” These lesions a r e designated a n d classed as abfractions (breaking away).l3 McCoy observed that the fatigue depends on the resisting quality of the alveolar bone. If the resisting bone is dense, the fatigue will affect the coronal portions of the tooth. If, however, the bone is not dense, then the fatigue will cause deterioration of the alveolar bone. lo In this latter instance, the greater tensile forces in teeth are lowered from the cementoenamel junction to a more apical position. These are now the areas where root caries make their appearance. Rapid penetration and spreading of caries is due to the increased content of organic substance in the dentin matrix.14 Many factors come into play when we consider the r e s u l t a n t effects of interocclusal forces. The biomechanical loading factors that affect teeth are the magnitude, direction, frequency, location, and duration

Figure 2. Diagrammatic representation of the interplay between primary and secondary factors in caries etiology. The three primary factors, tooth, bacterial flora, and substrate are depicted by overlapping circles. Saliva. an important secondary, predisposing factor. is depicted by a concentric circle surrounding the three primary factors. Other secondaryfactors (arrows) that influence the tooth, flora. and substrate are also depictedJAfter Nikiforuk G . Understanding dental caries. Vol. I. New York: Karger Press, 1985:72-81.)

Figure 3. Revised diagrammatic representation of the interplay between primary and secondary factors in caries etiology. The three primary factors. tooth, bacterial flora, and substrate are depicted by overlapping circles. Secondaryfactors (arrows) that influence the tooth, flora, and substrate are also depicted [doublearrow). Biodental engineering factors (BEF) affect both primary and secondary factors.

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Table 1. Biodental Engineering Factors (BEF) Biomechanical: Biochemical: Bioelectrical:

gical engineering that corrosion is accelerated wherever tensile forces exist if corrosive elements are present. Stress corrosion is the engineering term used when static or stationary stresses are involved. If alternating or cyclic stresses are transmitted, the failure is designated as fatigue corrosion. The term identifies the nature of the stress.17 Tensile stresses are a basic requirement for stress or fatigue corrosion. During the act of chewing or bruxing, fatigue corrosion takes place and clenching would result in stress or static corrosion. both predicated on the presence of corrosive elements. We can see, from an engineering viewpoint, that corrosion or caries of susceptible teeth is unavoidable, continuous, and ever present wherever there is stress concentration coexisting with acidogenic organisms within plaque acting upon a suitable substrate producing acids. The consequent effect of tensile stresses greatly potentiate the dissolution of tooth structure when there is interplay of these forces in the presence of acids. Consider the teenager who consumes carbonated drinks, sweetened snacks, and chews sugared gum. If the teeth are caries-susceptible and oral hygiene-lacking, invariably, cervical demineralization followed by rampant caries is noticed. As people get older and bone loss and recession take place, caries will frequently appear on the radicular surface. Due principally to the prime components of collagen and hydroxyapatite, loading of teeth produces an electrical potential difference between portions of the teeth in tension and compression. This phenomenon is termed the piezoelectric effect, from the Greek word “piezen”meaning pressure. This electrical activity further exacerbates the loss of tooth substance.

Column loading Compressiveand tensile forces Stress concentration Stress and fatigue corrosion Ionic transport Saliva-ph, flow rate, buffering capacity Piezoelectric Electrochemical Potential difference between materials involved Electrolysis

of the forces. The chemical composition and crystalline morphology of teeth as we know from biochemical and histologic studies are also significant. A case in point is the existence of gnarled enamel, which makes the enamel more resistant to fracture. l4 Straight enamel rods cleave more readily than gnarled enamel. The cement or interprismatic substance is apparently weaker than the body of the rods, so that the line of cleavage usually follows this substance. In gnarled enamel where the bundles of rods do not lie parallel to each other, cleavage does not occur as readily, since the stronger bodies of the intertwined rods make a clean, straight fracture impossible. The morphology of the occlusal surface with its numerous inclined planes and fossae has to be considered. The misalignment could play a major role in determining how susceptible a tooth is to deformation. The composition, density, and other mechanical properties of the supporting bone are also considerations. Keyes in 1960 developed the first model depicting the primary or essential factors in the etiology of dental caries (see Fig. 1).6Subsequently, Nikiforuk expanded this model introducing the secondary factors that contribute to caries formation (Fig. 2).15Without dwelling on this representation and the explanations of susceptible teeth, bacterial flora, and suitable local substrate, it can easily be seen that there are some gaps in the present hypothesis regarding cause and effect with regard to dental caries. We propose that the biodental engineering factors be introduced into the equation of the caries process (Fig. 3).16These major factors affect the teeth, flora, and substrate, which are the primary factors. While BEFs play a role in the development of all caries, their contribution to the formation of root caries is relatively more significant (Table 1).

METHOD AND MEASUREMENTS The specific aims of our current research are to classifl and quantify cause and effect relationships between the total dynamic environment of the teeth and dental caries. The measurement of stress and cyclic fatigue corrosion and piezoelectric phenomena are prime factors that quantitatively set a basis for the proof of the hypothesis that root caries (and probably other forms of caries formation) are caused, in large part, by a n environment of dynamical loading and flexure of teeth in an electrochemicalenvironment, which highly favors ion transport fi-om teeth to the saliva.16 As previously stated, teeth experience mechanical deformation many times a day during static (clenching) and dynamic conditions (such a s chewing, bruxing, tongue thrusting, and swallowing). Flexion has been demonstrated and veriaed by using a strain gauge on a tooth mounted in a loading kame (Fig. 4A). The deformation of the tooth resulted in a resistance change in the strain gauge indicating the degree of strain (change in length per unit of length). Typical values obtained from stress/strain curve of a wet, in vitro tooth indicate

BEF The most important engineering factor that has never been specifically identified or introduced in dental literature is the principal of stress corrosionand how this phenomenon relates to the caries process, in particular root caries. It is a well-known fact in metallur73

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March/ApriZ 1991

Figure 6. Cyclic fatigue cracking (arrow depicts cracking). Figure 4A. Loading frame and strain gauge.

an average modulus of 1000 MPa, which translates to a strain of 0.1 percent at a stress of 1.0 MPa (Fig. 4B). Specimens of a variety of teeth were placed in a loading frame and tested in vitro in solutions of varying concentrations of citric acid (representing conditions found in the oral environment) at room temperature. Results showed accelerated corrosion rates for samples under tension and retarded corrosion for those under compression compared to unstressed samples (Fig. 5). Etch rates were determined by sectioning numerous samples, which were masked to show the depth of the step that was etched into the tooth material. Samples that were subjected to these citric acid solutions showed evidence of stress corrosion cracking in regions of high stress. Cyclic fatigue cracking (due to failure at the cementoenamel junction) was also observed because of the combined effects of stress and corrosion (Fig. 6). Piezoelectric effectswere observed on teeth that were loaded both statically and cyclically. The basics of piezoelectric behavior of materials shows that, dependent upon the crystalline orientation, a specimen shows a potential difference from end to end and side to side when it is flexed, put in tension, or put in compression. Voltage and charge were measured with a Keithley electrometer and a storage oscilloscope noting peak

STRESS [MPa)

0

0.2

0.e 0.6 STRAIN (%)

0.4

A

1

1.2

+ Seriee E

Series A

Figure 4B. Compressive stress/strain of dry and wet tooth

om.). ETCH RATE

[microns/min)

CHARGE(C)xlE-M

2

0

-

e

4

CITRIC ACID CONC.(%) Series A

+ Series B

;+-

Series

VOLTAGE(V)

200

5,

so0

0

VOLTAGE VS FORCE CHARGE VS FORCE I

; 100

zoo

300

FORCE (N)

-

C *PEAK ELECTROMETER AEADING

Figure 5. Typical etch rate of teeth.

Figure 7. Piezoelectric response. 74

Sorles A

400

600

Role of BEF

readings versus force. The results of measurements on a typical premolar are shown in Figure 7. These piezoelectric effects (in excess 10-14coulombs/newton) have been observed by the principal researchers of this project and are sufficient to transport calcium (Ca++) ions, thus resulting in the demineralization of teeth. Observations were also made on a storage oscilloscope and indicated peak voltages (dry)in the range measured previously by the electrometer. In vivo measurements on a volunteer (another dentist) indicated voltages in the range of tenths of volts on molars that were subjected to clenching (forcesin excess of 500 newtons or 125psi). Voltages were highest at the cementoenamel junction, or the portion of the tooth above the gingival margin. This is the region of greatest tooth flexure.

engineering factors, which are ever present and unavoidable, play a significant role in the root caries process. The literature is replete with studies relating to the microflora involved in plaque formation and enamel caries. On the other hand, only a few studies have considered the microbiota of an advanced dentinal lesion. Though both types of caries activity have been investigated from the microbiologic and chemical viewpoint, never in the literature has the stress corrosion principle been applied in its pathogenesis. It is our opinion that researchers should look beyond the bacterial flora and their various types, and recognize the role that engineering principles play in the development of caries. Unavoidable interocclusal contacts take place whether during chewing. swallowing, or parafunction (clenching or bruxing), and consequent loading forces are propagated throughout the teeth. The resultant tensile forces are greatest at the cementoenamel junction and apically to this juncture if bone loss has occurred. If acids are present at these points, then we must conclude that the dissolution of the tooth will take place. When these corrosive or cariogenic acids are coupled with either static or cyclic loading of teeth, the phenomena are correspondingly termed stress and fatigue corrosion. Both of these corrosions are major factors in the development of root caries. The piezoelectric effect provides for accelerated electrochemical transfer of ions from the teeth.

DISCUSSl0N From an engineering viewpoint, the location and rapid penetration of these root lesions can be explained by the fact that the greater the flexing, the more rapid the dissolution. We can expect that a lesion would accelerate as it deepens because of stress concentration resulting in stress corrosion. Consequently, as the lesion deepens, the greater the flexure. This is a sound basis on which to explain why root caries is so pervasive. The attendant piezoelectric effect has been measured in vivo and in vitro under loading. The long-term presence (dependent on the electrical properties of tooth and saliva) of piezoelectric voltages due to a variety of stresses on the teeth caused by chewing, swallowing, bruxism, clenching, eccentric loading, and traumatogenic occlusion provide for electrochemical transfer of ions from the teeth into the saliva. This electrical activity contributes to the demineralization, erosion, and caries activity of teeth and is especially significant in the formation of root caries. Biodental engineering research substantiates the need for a new approach in dental health and preventive dentistry. Dental practitioners can now better understand the caries process, more readily identify susceptible teeth, and correct and passivate this susceptibility to prevent root caries. More specifically, greater attention should be directed toward establishing harmonious occlusion through restorative dentistry, occlusal equilibration where indicated, and means of controlling bruxing and clenching habits. In addition, even noncarious abfracted areas should be considered for restoration at their earliest detection as these are susceptible to caries.

CONCLUSION The biodental engineering factors (BEF),an important mechanism in the etiology of root caries, have been presented based on accepted engineering principles. The principle of column loading causing flexure and the metallurgical principle of stress corrosion must be considered and cannot be ignored in dental research when root caries is investigated. The attendant piezoelectric effects exacerbate the migration of ions from teeth and accelerate the caries process on the radicular surfaces. A new and revised model was presented, which will make the caries process more readily understood and provides a sound basis for the etiology of root caries. It is the ardent desire of the authors to encourage other researchers to continue and expand on this investigation.

Acknowledgments The authors wish to thank the following for their contributions: Jan G . Stannard, Ph.D.. Tufts University School of Dental Medicine, Boston, MA; Donald R. Barber, B.A., President (Ret.), Heat Bath Corporation, Springfield, MA; Nicholas A. DiSalvo, D.D.S., Ph.D., Professor Emeritus, Chairman, Department of Orthodontics, Columbia University School of Dental a n d Oral Surgery, New York, Ny; Clyde E. Work, Ph.D.. Dean, School of Engineering, Westem New England College, Spring-

SUMMARY in uitro and Our p r e m q investigation the premise that biodental in uiUO observations 75

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15. NikiforukG.Understandingdental caries. Vol. 1. NewYork: Karger Press, 1985: 72-8 1. 16. Grippo J O , M a s i JV.The role of stress corrosion and piezoelectricity in the formation of root caries. Foster KR. ed. Proc 13th Ann N.E. Bioeng Conf Mar 12-13, 1987. University of Pennsylvania, Philadelphia, 93-95. 17. Fontana M, Greene ND. Corrosion engineering. New York McGraw Hill, 1978. 18. Watanabe A, et al. Surface electrokinetic phenomenon. Tokyo, Japan: Kyoritsa Co., 1969: 195.

field. MA; Maurice J. Dullea 111, D.D.S., Longmeadow, MA; and Kathleen Kolb, Secretary, Western New England College. Springfield, MA.

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Role of biodental engineering factors (BEF) in the etiology of root caries.

A preliminary study and hypothesis of the etiology of root caries is presented with appropriate data suggesting that biodental engineering factors (BE...
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