Bioelectric stimulation and residual ridge resorption

ric stimulation Lance

P. Ortman,

DDS,

MS,a

and residual David

M. Casey,

DDS,b

ridge and

Mark

resorptio DeersC

University at Buffalo, School of Dental Medicine and State University of New York, Buffalo, N.Y. The use of exogenous pulsed electromagnetic fields (PEMF) to stimulate the healing of nonunions and other long bone defects is common in medicine. This investigation used the dog model and image analysis of standardarized radiographs to assess loss of residual ridge height following extractions. It demonstrates the effectiveness of intermittent PEMF to reduce the rate of residual ridge resorption. It further suggests there may be a causal relationship between residual ridge resorption and the alteration of endogenous biolelectric signals caused by the loss of teeth. (J PROSTHET DENT 1992;67:67-71.)

esidual ridge resorption (RRR) is a major disease entity that results in the functional impairment of the stomatognathic system. Furthermore, the socioeconomic consequeaces reIated to complex prosthetic t,reatment create a hardship for all edentulous and partially edentulous patients. The loss of bone following the extraction of teeth at the site of the edentulous ridge has been characterized as a long-term, cumulative, and irreversible process that often proceeds at an alarmingly rapid rate.’ Although proportionally the largest amount of bone is lost within the first 6 months, RRR continues for the rest of the patient’s life until all the alveolar bone is lost.2m4If the rate of RRR is rapid or the patient is edentulous for a long period of time, the remaining residual ridge may become so compromised that traditional complete denture treatment is impossible. Although numerous studies have attempted to characterize RRR, the cause of this phenomenon has remained elusive. The factors explored have included the viability of the osteogenic cell population,5-8 local tissue factors,g-ll systemic biochemical factors,12, l3 physical loading factors,14, l5 and prosthetic factors.16, l7 Although interesting, none of these studies has been successful in establishing a specific causal relationship with RRR. To date, the length of time the patient has been edentulous is the best predictor of the amount of alveolar ridge 10~s.‘~ The lack of a single or primary factor that can explain RRR has led to the conclusion that RRR is most likely a multifactorial problem with a number of interacting or coexisting factors that cause the alveolar bone loss. Furthermore, the concept of multiple factors and the complex interplay between them

Supported by NI?R grant No. IR03DE0827301. aAssociate Professor, Department of Removable Prosthodontics, University at Buffalo, School of Dental Medicine. bClinical Assistant Professor, Department of Removable Prosthodontics, University at Buffalo, School of Dental Medicine. CBiostatistician, University at Buffalo, State University of New York. 10/l/32701

has been thought to explain the wide individual variation in the rate of loss. An alternative scenario may explain the phenomenon of RRR. The ability of bone to produce electrical signals when stressed has been known since 1957, when it was first discovered by Fukada and Yasuda.lsTheir findings were later confirmed in the United States by Bassett and Becker.rg The relationship of these endogenous bioelectric signals to bone growth, remodelling, and repair has been investigated and tested in orthopedic clinical studies for the last 20 years. 20,21The use of exogenous bioelectric signals to stimulate healing in nonunions and pseudoarthrosis is supported in the medical literature .22,23 The bioelectric properties of dentin, enamel, cementum, and the tooth and periodontal complex have also been studied.24-30 The magnitude, polarity, and character of the bioelectric signals that resulted from tooth and alveolar bone loading are similar to those found in the long bone studies. Another important feature was the endogenous electric signal strength, related to the load placed on the tooth in a linear fashion. The last 15 years of dental research have suggested that exogenous bioelectric stimulation is effective in healing fractured jaws,31 in reducing RRR,32s33 in implant healing34, 35 and in treating osteoradionecrosis.36 This article discusses RRR in terms of the loss of bioelectric stimulation and presents new findings related to the use of intermittent pulsed electromagnetic field bioelectric stimulation (PEMF) in reducing RRR.

MATERIALS

AND

METHODS

Ten female adult purebred beagle dogs with complete, healthy dentitions were selected and were randomly assigned to the stimulated (treatment) group or to the unstimulat.ed (control) group. Each of the dogs was rendered unconscious using standard intravenous sedation and all the teeth were scaled and polished with prophylaxis paste. The first molar and canine teeth on the right mandible were prepared for ring crowns. The ring crown design was selected as it does not interfere with the dog’s natural

ORTMAN,

CASEY, AND DEERS

1. Cobalt/chrome fixture cemented in place. The two threaded holes permitted attachment of x-ray cassette and PEMF coil.

Fig.

Table

I

Table

Frequency 10 Hz Peak 10 mV Pulse duration 2 msec Heat 2 mW Induced field 2 mV/cm

occlusion. Traditional rubber base impressions were made of the maxillae and mandible in custom trays and were poured in die stone. The third and fourth premolars were removed from the master cast and a chrome/cobalt fixed partial denture with two threaded holes for attachment of the PEMF coil and x-ray alignment device was fabricated on the master cast. When the prosthesis was completed, the dogs were scheduled for extraction of the third and fourth premolars. Care was taken to extract the teeth in a simple manner to minimize the trauma to the adjacent alveolar bone. The fourth premolar is a double divergent rooted tooth. The crown of the tooth was sectioned to facilitate simple extraction. Immediately following extraction and hemostatis, the fixed prosthesis was cemented as illustrated in Fig. 1. The occlusion was checked to ensure that there was no occlusal contact on the prosthesis and that the dog’s natural occlusion was not altered. A standardized x-ray film was then made of the edentulous region. The custom film cassette was positioned so a portion of the second premolar and the first molar were included in the x-ray image to act as landmarks. The x-ray films were made according to a standardized technique, as described by Ortman et a1.,37which assures reproducible image geometry. In addition, the PEMF coil was attached to the fixed prosthesis and was activated for the treatment group for 1 hour and 68

II Control

group

PEMF Doax

Dog 180 days

NO.

180 days

NO.

269

1.20

272

(died)

264

0.78

265

0.29

276

0.98

274

0.63

275

1.59

277

0.29

270

1.73

273

0.78

x = 1.25 PEMF,

group

Pulsed electromagnetic

x = 0.49 fields.

was then removed. During the study all dogs received a PEMF coil, but only the stimulated group had the coil attached to a power source. The dogs were then put on a S-day week, 1 hour/day PEMF schedule. No sedation was necessary for this procedure, as the dogs were very passive during attachment and stimulation, The coils, circuitry, and resulting PEMF were identical to those used by Van der Kuij et a1.,33since they had been shown to be effective in retarding RRR (Table I). The dogs were anesthetized at the 180-day interval and the standardized x-ray films were repeated. Bone changes over time were determined for all edentulous sites by using a Magiscan image analysis system (MSA) (Magiscan Joyce-Loebl, Gateshead, England) and custom software in a double-blind manner.38 X-ray images were loaded into the image analysis memory, aligned, checked for proper alignment by subtraction radiography, and were then measured by the computer for changes in bone height at the mid third of the edentulous ridge site. This area was selected because it is the site farthest from the adjacent

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III Naof dogs

control group PEMF

group

5 4

X

S

SE

1.2560 0.4975

0.401 0.247

0.179 0.124

S, Sum of squares; SE, standard error; other abbreviations as in Table II. df = 7; t value = 3.29; p = 0.0015 (one-tailed-pooled variance).

teeth and is thus less likely to be affected by their naturally arising bioeiectric signals. One dog from each group was sacrificed and a gross block section of the mandible in the region of the extracted premolars was removed. The block section was decalcified, prepared for sectioning, and the sections were stained with a standard hematoxylin and eosin preparation. The sections were examined for qualitative histologic differences. RESULTS The 180-daytime interval was examined for differences in mean responses between the stimulated PEMF (treatment) and unstimulated (control) groups. The radiographs were coded to ensure blindness and were examined using the MSA Bone Program two separate times. The results for each bone site were averaged (Table II) and were then analyzed with Student’s t test (one-tailed, pooled variance). The results (Table III) indicated a significant difference in the residual ridge height between the PEMF group and the control groups at the 1% level of significance (p 0.0015). The histogram for the mean residual ridge loss demonstrates the results of the statistical analysis (Fig. 2). Tbe prepared histologic material in Fig. 3 was examined in a blind manner for qualitative comparison only because the limited amount of specimens-only one from each group-prohibited quantitative comparison. The most evident overall feature is one of endosteal activity in the PEMF-stimulated dogs and a lack of similar activity in the control dogs. The crest of the PEMF residual ridge and the endosteal bone are characterized as active healing bone. There is no evidence of an inflammatory or traumatic response to heat. An important feature is the generous amount of supporting vasculature for this endosteal activity. The boney trabeculae have numerous adjacent blood vessels. In contrast, the control specimen shows very little endosteal activity. There is an overall cellular quiescence. There is very little evidence of any bone remodelling or turnover. The marrow is fibrofatty and is more mature than that of the PEMF specimen. There is also a marked decrease in the amount of supporting blood vessels compared with those of the PEMF specimen. DIScUSSION The presence of endogenous stress-generated electric signals and steady-state potentials in bone has been well documented. In addition, the ability of exogenous bioelec-

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2 2 i! mo E E 1

0

180Da Fig. 2. Histogram of results.

tric signals to induce osteogenesis and to influence bone healing has been repeated in many clinical studies. The combination of these two facts can lead to the hypothesis that the endogenously generated signals combine to form the stimulation and feedback mechanism that controls the remodelling events in bone. Although the cellular mechanism of bioelectric stimulation is not fully understood, changes in membrane potentials as well as increased proteoglycan systhesis, alkaline phosphatase content, matrix calcification, and proliferation have been implicated.3g,40 Additionally, the magnetic fields may act on calcium crystal formation and increase the crystalline perfection and density of the population of calcium crystal seeds41 Bassett40 stated that the electrical activity in bone caused by functional stresses appears to be the most promising candidate as the primary feedback control mechanism. Likewise, the dentoalveolar complex may function as a mechanical-electrical transducer that converts the loading to the teeth and alveolar bone into electrical signals. The electrical signal then influences the cellular events that determine the remodelling of the alveolus. Furthermore, each tooth and periodontal complex would have influence over the immediately adjacent alveolar bone. The loss of the tooth would significantly change the bioelectric events in the immediate area (edentulous site) that would result in triggering RRR. This would explain the enigma of the solitary tooth that is immediately surrounded by alveolar bone while the adjacent edentulous region is undergoing RRR. The results of this study and the results of the study by Van der Kuij et a1.33support this hypothesis. An important distinction between this study and theirs is the application of the PEMF stimulation. Their study used 24-hour continuous stimulation, whereas this study used intermittent stimulation (that is, 1 hour per day). Intermittent stimulation mimics the natural loading of the teeth and periodontal complex. Brewer42 showed that masticatory and swallowing contacts between dentures average less than 15 69

ORTMAN,

CASEY,

AND

DEERS

Fig. 3. A, Hematoxylin and eosin stained cross section of mandibular residual ridge of control dog (original magnification x200). B, Hematoxylin and eosin stained cross section of mandibular residual ridge of PEMF stimulated dog (original magnification x200).

minutes per day. 42 Loads on the teeth and periodontium from an interposing bolus or from clenching/bruxing amount to 1 hour or less.*” The duration of the PEMF stimulation time necessary to simulate functional forces is considerably less than indicated in the study by Van der Kuij et a1.33The importance of the effectiveness of intermittent stimulation is that it makes the therapy possible on an outpatient schedule or a home care basis. The effectiveness of PEMF in reducing RRR in humans has not yet been demonstrated. The early animal research in the long bone studies has been successfully extrapolated to humans and there is every expectation that this PEMF technique will show similar results. If it proves effective in humans, dentistry has gained a potent treatment modality. Future applications may include the ability to control the resorption and accelerate the healing so a more predictable 70

result in mandibular fracture healing or orthognathic surgery can be achieved. The bone mass of edentulous ridge sites may be able to be better maintained following extraction. Postextraction treatment would result in better sites for subsequent implant procedures. In addition, the healing period for implant procedures may be significantly shortened and made more predictable by the application of PEMF immediately following fixture placement.

SUMMARY This research project demonstrates the ability of intermittent PEMF to significantly reduce RRR at edentulous ridge sites in the dog model. The ability to prevent the rapid bone loss of alveolar bone at an edentulous ridge site has important prosthodontic implications. The effectiveness of PEMF in reducing RRR also supports the concept

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that the primary cause of RRR may be the alteration of the normal endogenous activity resulting from the loss of the tooth and periodontal complex. REFERENCES 1. Atwood DA. The reduction of residual ridges. A major oral disease entity. J PROSTHET DENT 1971;26:266-79. 2. Carlsson GE, Persson G. Morphologic changes of the mandible after

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24. Braden M, B&stow AG, Beider I, Ritter BG. Electrical and piezoelectrical properties of dental hard tissues. Nature 1966;212:1565-6. 25. Mumford JM, Newton AV. Transduction of hydrostatic pressure to electric potential in human teeth. J Dent Res 1969;48:226-9. 26. Liboff AR, Shamos MH. Piezoelectric effect in dentin. J Dent Res 1971;50:516. 27. Cochran G, Pawluk R, Bassett C. Stress-generated electric potential in the mandible and teeth. Arch Oral Biol 1967;12:917-29. 28. Cochran G, Pawluk R, Bassett C. Electromechanical characteristics of bone under physiologic moisture conditions. Clin Orthop Rel Res 1968;58:249-70. 29. Zengo A, Pawlut R, Bassett C. Stress-induced bioelectric potentials in the dentoalveolar complex. Am J Orthod 1973;64:17-27. 30. Zengo A, Pawlut R, Bassett C, Prountzos G. In viva bioelectric potentials in the dentoalveolar complex. Am J Orthod 197$66:130-g. 31. Masureik C, Eriksson C. A clinical evaluation of the effect of small electrical currents on the healing of jaw fractures. J Dent Res 1976;55:294300. 32. Van der Kuij P. Reducing residual ridge reduction. An experimental investigation into the effects of electromagnetic stimulation on reduction of alveolar ridges in dogs. Thesis. Free University, Amsterdam, 1981. 33. Van der Kuij P, Vingerling P, de Grott K, Sillivis Smitt P. Electromagnetic reduction of resorption rate of extraction wounds. Electrical properties of bone and cartilage. New York: Grune & Stratton, 1979: 333-40. 34. Buch F, Albrektsson T, Herbst E. Direct current influence on bone formation in titanium implants. Biomaterials 1984;5:341-6. 35. Shimizu T, Zerwekh J, Videman T, et al. Bone ingrowth into porous calcium phosphate ceramics: influence of pulsing electromagnetic field. J Orthop Res 1988;6:248-58. 36. Barak S, Rosenblum I, Czerniak P, Arieli J. Treatment of osteoradionecrosis combined with pathologic fracture and osteomyelitis of the mandible with electromagnetic stimulation. Int J Oral Maxillofac Surg 1988;17:253-6. 31. Ortman L, Dunford R, MeHenry K, Hausmann E. Subtraction radiography and computer assisted densitometric analyses of standardized radiographs. J Periodont Res 1985;20:644-7. 38. Hausmann E, Christersson I,, Dunford R, Wikesjo U, Phyo J, Genco R. Usefulness of subtraction radiography in the evaluation of periodontal therapy. J Periodont 1985;57(special issue):l-4. 39. Peck W. Bone and mineral research 4. Chapt. 5. Cellular response and mechanisms of action of electrically induced osteoginesis. Amsterdam: Elsevier Science Publr BV, 1986213-37. 40. Bassett CAL. Low energy pulsing electromagnetic fields modify biomedical processes. Bioessays 1987;6:36-42. 41. Madronero A. Influence of magnetic fields on calcium salts crystal formation: an explanation of the pulsed electromagnetic field technique for bone healing. J Biomed Eng 1990;12:410-14. 42. Brewer AA. Prosthodontic research in progress at the School of Aerospace Medicine. J PROSTHET DENT 1963;13:49-69. 43. Glickman I, Pameijer J, Roeber F, Brion M. Functional occlusion as revealed by miniaturized radio transmitters. Dent Clin North Am 1969;13:667-79. Reprint requests to: DR. LANCE F. ORTMAN 222 SQKJIREHALL SCHOOL OF DENTAL MEDICINE, SUNYAB BUFFALO, NY 14214

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