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The Path from Studying Masticatory Function to Managing TMD and Pain: A Personal Journey

Dept. of Oral and Maxillofacial Surgery, School of Dentistry, Oral Pathology and Maxillofacial Surgery, Catholic University Leuven, Kapucijnenvoer 7, B-3000 Leuven, Belgium; antoon.delaat{at}med.kuleuven.ac.be

KEY WORDS: temporomandibular disorders • reflexes • trigeminal

	INTRODUCTION

TOP INTRODUCTION THE INITIAL PLAN: DENTISTRY A FIRST TASTE OF... A YEAR OF TRAVEL,... PAIN COMES INTO FOCUS,... CONCLUSIONS REFERENCES

 
Over the last 25 years, many changes took place in the field of oral physiology, temporomandibular disorders (TMD), and related pain in the masticatory system. While in the late ’70s, the etiology, diagnosis, and treatment of TMD were especially governed by biomechanical theories—i.e., the influence of dental occlusion and articulation—newer insights progressively shifted the focus to biological factors, the (sometimes disturbed) balance between adaptation and overload, and a biopsychosocial approach, primarily aimed at reducing pain before improving normal function. Since, traditionally, techniques like electromyography, psychophysics, and jaw tracking were used in the study of trigeminal neurophysiology but were also tested for their application in the diagnosis of dysfunction and pain, these topics were incorporated into the scope of the IADR Neuroscience Group. As a result of the increasing importance of pain treatment in general, the Group’s agenda shifted more from the study of trigeminal sensory and motor function to research on the etiology, diagnosis, and management of pain and dysfunction.

I was fortunate to experience and be part of important evolutions in our field, and in this invited essay, I will try to highlight some of the landmarks.

	THE INITIAL PLAN: DENTISTRY

TOP INTRODUCTION THE INITIAL PLAN: DENTISTRY A FIRST TASTE OF... A YEAR OF TRAVEL,... PAIN COMES INTO FOCUS,... CONCLUSIONS REFERENCES

 
During my last years in high school, the array of choices for my future profession narrowed to two areas of interest: mathematics (civil engineer) or biomedical sciences. I probably chose dentistry because in this way I could realize that drive to care for people without, however, the need to be available 24 hours per day (as, in my mind, the physicians did): Indeed, I wanted to be sure that I could schedule time outside my profession, to continue my intense involvement in social organizations, to pursue my hobbies like music and gardening, and to secure enough time for my (future) family.

At first, studying at University did not seem to be an option because of the costs, but happily, in Belgium, grants are issued to every student, proportionate to the family income. Our budget was always very tight, and I think that this situation still pops up every time a discussion is raised on asking for or spending a grant, deciding on an important investment, and so on. In addition, the support for University students lasted only as long as one successfully passed one’s exams, which was an extra motivation to work as hard as possible: to fail would mean to stop. So I entered the School of the Catholic University of Leuven, preparing to be a fine dentist in my home town. The studies were very intense, and little time was left outside class hours, which was probably one of the reasons I fell in love with a classmate. Thanks to her, my professional and personal life changed completely: She motivated me to undertake post-graduate studies, and the initial plan to return to my home town and "cocoon" in private practice lasted only a few years on a half-time basis, to finance the specialty studies.

	A FIRST TASTE OF RESEARCH

TOP INTRODUCTION THE INITIAL PLAN: DENTISTRY A FIRST TASTE OF... A YEAR OF TRAVEL,... PAIN COMES INTO FOCUS,... CONCLUSIONS REFERENCES

 
In addition to my (future) wife, another person became very influential in my (and many other colleagues’) career: Daniel van Steenberghe, just returned from his doctoral studies in Amsterdam, became professor of periodontology at our School in 1979, and we were the first class to enjoy his enthusiasm, his lectures, and his vision of oral health care research. Together with three other classmates, we were the first group to stay with him and study periodontology as a three-year post-graduate specialty. He has an encyclopedic mind and always had a "feeling" for new tracks to follow, new ideas to implement, and the contagious enthusiasm to motivate people. All his assistants had to spend at least 20% of their time in research, which at that time was a "revolution" in a School with a very good tradition in educating good clinicians, but where research activity had only recently changed from zero to a small nucleus. A Laboratory of Oral Physiology was initiated, and, consequently, I could spend half a day per week (as well as a lot of evenings and weekends) there. Other researchers were Bert van der Glas (a biologist), Jan Weytjens (an MD), and, later, Carine Carels (an orthodontist). Initially, the plan was to continue the original work from Amsterdam on jaw tremor, but the tracking machine for these studies needed to be duplicated. Consequently, we decided to do some electromyography studies in the meantime. The literature was contradictory regarding the silent period and its potential use in the diagnosis of pain and dysfunction of the masticatory system, mostly because of a lack of standardization of the experimental set-up and the way to interpret the electromyographic signal. In our studies on masseteric reflexes, a custom-made pendulum system provided standardized and silent taps to a single tooth, while the subjects kept a constant clenching level by means of visual feedback through a periscope. In addition, a computer program allowed for unbiased determination of the beginnings and end-points of the various reflex components occurring as a result of the stimulus. Surprisingly, not only an (inhibitory) silent period was observed, but also excitatory periods, eventually interrupted by a second silent period. This sequence of inhibitory and excitatory components was called the Post-stimulus EMG Complex (PSEC) (for review, see van Steenberghe et al., 1989).

The receptors mediating the PSEC were systematically identified: In addition to the periodontal receptors, inner ear receptors were also found to be responsible, probably stimulated via bone conduction. With higher clenching levels increasing the motoneuronal drive, the whole reflex response became shorter and relatively smaller. Especially during the second part of the reflex, occurring at longer latencies, many influences could be documented: Jaw position could alter these periods as well as induced jaw muscle fatigue. Also, groups of patients with myofascial pain or exhibiting bruxist behavior were tested. Surprisingly, a second inhibition, which was observed in most symptom-free subjects, was clearly absent in these patient groups. The findings of these studies formed an important part of my thesis (De Laat, 1985) and became a new personal challenge of research direction, after some years of a combination of private practice and specialty studies in periodontics.

In addition to the electromyography studies, which aroused my interest in pain and dysfunction, other investigations were also undertaken on the etiology of TMD. Analyzing occlusal and articular parameters and interpreting them in a statistically correct way (De Laat et al., 1986) stressed the difference between a simple correlation and a causal relationship, which of course had important consequences for the old etiological concepts linking occlusion to TMD.

While finishing the doctoral thesis, I also wrote a literature review on reflexes and jaw function (De Laat, 1987) that drew the attention of many, among whom was Harold Perry, who later asked later me to join him as associate editor of the Journal of Craniomandibular Disorders, Facial and Oral Pain (currently the Journal of Orofacial Pain).

After finishing my thesis, one year was left from my University grant. I used that year to broaden my practical knowledge on pain and dysfunction, because—even if I was still in training as a periodontologist—I felt that my future would be in pain and TMD, not periodontology.

	A YEAR OF TRAVEL, GATHERING KNOWLEDGE, AND MAKING FRIENDS

TOP INTRODUCTION THE INITIAL PLAN: DENTISTRY A FIRST TASTE OF... A YEAR OF TRAVEL,... PAIN COMES INTO FOCUS,... CONCLUSIONS REFERENCES

 
As mentioned earlier, my knowledge of TMD and pain was more theoretical: I studied a lot, did some research on reflexes as a diagnostic tool, but was not trained to manage these patients. A comprehensive approach to TMD patients was certainly lacking at our School, so I decided to visit the centers that were famous in this regard. I had some initial training with Tore Hansson in Amsterdam, and with Gunnar Carlsson and Martti Helkimo in Sweden. The Scandinavians were famous for their epidemiological research, and for documenting the results of a conservative approach (including the use of splints and occlusal grinding) over longer periods of time. Later on, I was allowed to spend time with Daniel Laskin (Richmond, VA), who coined the term "Myofascial Pain Dysfunction" and attributed the signs and symptoms to psychophysiological disturbances and stress, rather than to abnormal occlusal and articular relations. Together with Charles Greene, he certainly introduced critical thinking and appropriate research designs in this field of dentistry. Finally, like many others, I enjoyed Michigan Dental School and Major Ash: His personal approach to patients as well as the way to organize the time for research and study were very beneficial. All these visits lasted for just a few months, enabling me to compare the different viewpoints and experiences, and to melt them down to my own ‘approach’. This was a fantastic time to learn, with ample time for work and study and for building friendships. Most of the graduate or post-doctoral students I encountered during these periods have now grown into respected leaders in our field. I still feel very grateful both to the University for the opportunity to travel, and to the generous hosts who allowed me to visit. I think that international exposure is crucial for everyone pursuing an academic career, and the excellent opportunities I enjoyed have been instrumental in opening the doors of my current working environment to the many international guests who have visited Leuven since then.

In the summer of 1986, after long discussions, it was decided to host the new TMD Clinic in the Department of Oral and Maxillofacial Surgery and not in the Prosthodontics Department. Did this already reflect the changes the TMD area faced regarding diagnosis and management?

The research activities on trigeminal reflexes dropped in intensity, both because of people leaving the Lab, but also since an international ‘allergy’ toward the coupling of reflexes and diagnostics had occurred. In the United States particularly, people claimed ‘diagnostic’ properties for EMG and jaw-tracking, even if sound studies indicated a clear lack of specificity, reproducibility, and validity in TMD problems (for review, see Lund et al., 1995). As a result, my own findings regarding the differences in PSEC morphology in patients with pain or masticatory hyperactivity were not developed further.

Even being half-time at the School, I could continue my international contacts and became active in many international societies: e.g., the IADR Neuroscience Group, the American and European Academies of Craniomandibular Disorders, and the Society of Oral Physiology. The drive to be active in social organizations, so apparent during my high school days, had regained its strength, but at an international level.

	PAIN COMES INTO FOCUS, BOTH IN THE CLINIC AND IN RESEARCH

TOP INTRODUCTION THE INITIAL PLAN: DENTISTRY A FIRST TASTE OF... A YEAR OF TRAVEL,... PAIN COMES INTO FOCUS,... CONCLUSIONS REFERENCES

 
Over the years, as a result of both teaching efforts with students and local study clubs, the patient population at our TMD Clinic shifted: less myofascial pain and clicking joints, more chronic orofacial pain in all its diversity. Around the world, dentists became valid co-workers in multidisciplinary approaches to studying these complicated orofacial pains. The research community developed better diagnostic criteria for TMD and implemented better study designs, resulting in higher-quality research. In this way, dentistry could contribute significantly to the new developments regarding the etiology, pathophysiology, and management of pain. Continuous progress was made in our understanding of peripheral and central sensitization and the pathophysiology of pain (Sessle, 1999). More and more, it became apparent that, in these patients, disturbed function or limitation of movement is the result, rather than the cause, of pain (Lund et al., 1991). These developments led not only to a better understanding and better management of pain (Stohler and Zarb, 1999), but also to a shift in attention in the research field. Since then, the content of the meetings of the Neuroscience Group or the Society of Oral Physiology (Store Kro) centered more around pain than on the traditional sensory and motor functions of the masticatory system.

In 1994, a young and bright Italian dentist, Guido Macaluso, joined me in Leuven to prepare a Master’s thesis on H-reflexes in the trigeminal system. The standardization of both the stimulation and recording techniques was investigated and implemented, and we found that, upon stimulation of the masseteric nerve, a heteronymous H-reflex was present in the temporalis muscle. Its amplitude reached a steady state while increasing the stimulation intensity, and thus could be used as a measure for motoneuronal excitability (Macaluso and De Laat, 1995a,b,c). Later, after Dr. Macaluso’s return to Parma University, where he now chairs the periodontal department, we continued to work with short-latency reflexes and were able to enjoy the hospitality and the excellent facilities of Lars-Arendt Nielsen and Peter Svensson at the Centre for Sensori-Motor Interaction in Aalborg (Denmark). In Aalborg, we showed that experimental pain did not have a significant influence on short-latency reflexes (Svensson et al., 1998).

Parallel to the electromyography research, a new line of experiments, focusing on pressure pain thresholds (PPT) and psychophysics, was initiated, which led to a successful doctoral thesis of Hans Isselee. In line with the growing evidence that gender is one of the important factors in the etiology and pathophysiology of pain (Dao and LeResche, 2000), he could show, for example, that the PPT was influenced by hormonal fluctuations both in symptom-free women and in patients with myofascial pain (Isselee et al., 1997, 2002). While in general, myofascial pain tends to "fade out" over longer periods of time, apparently it regularly increases again to higher levels, especially during the peri-menstrual periods.

Service to national and international organizations continued. Here in Belgium, I could initiate the project on the establishment of multidisciplinary pain clinics as president of the Belgian Pain Society, and Barry Sessle, who became editor-in-chief of the Journal of Orofacial Pain and President of the International Association for the Study of Pain, asked me to found the Special Interest Group on Orofacial Pain, which has since grown to a multidisciplinary group of over 200 colleagues.

	CONCLUSIONS

TOP INTRODUCTION THE INITIAL PLAN: DENTISTRY A FIRST TASTE OF... A YEAR OF TRAVEL,... PAIN COMES INTO FOCUS,... CONCLUSIONS REFERENCES

 
For some years now, I have been back full-time at the School of Dentistry, Oral Pathology and Maxillofacial Surgery, at the same University where I studied, graduated, and specialized. With the stimulating enthusiasm of mentors like Daniel van Steenberghe, Guido Vanherle, and others, the School has grown into an internationally renowned clinical and research center featuring leaders in the fields of dental materials, osseointegration, implant prosthodontics, bacterial adhesion, and other areas. For myself, the different tasks as teacher, researcher, clinician, journal editor, organizer, and initiator have melted together into a vibrant and challenging professional life and career. My present situation is completely different from the one I projected while starting my dental studies, and I am very grateful to all of the colleagues and friends who crossed my path and made this all possible.

It is time to continue, and perhaps the current developments in psychophysics and quantitative sensory testing will allow us, finally, to ‘objectify’ pain (and dysfunction) better; maybe even reflexes will play a role again.

Looking back over the last 25 years, however, I must admit that I could not honor one of my important initial reasons to choose ‘dentistry’: I still do not have enough time for music, my garden, or my family!

Received July 18, 2002; Accepted October 1, 2002

	REFERENCES

TOP INTRODUCTION THE INITIAL PLAN: DENTISTRY A FIRST TASTE OF... A YEAR OF TRAVEL,... PAIN COMES INTO FOCUS,... CONCLUSIONS REFERENCES

 
Dao TT, LeResche L (2000). Gender differences in pain. J Orofac Pain 14:169–184.[ISI][Medline]

De Laat A (1985). Masseteric reflexes and their relationship towards occlusion and temporomandibular joint dysfunction (thesis). Leuven: Catholic University Leuven, Acco.

De Laat A (1987). Reflexes elicitable in jaw muscles and their role during jaw function and dysfunction: a review of the literature. Part I–III. J Craniomandib Pract 5:139–151, 246–253, 333–343.

De Laat A, van Steenberghe D, LeSaffre E (1986). Occlusal relationships and temporomandibular joint dysfunction. Part II: Correlations between occlusal and articular parameters and symptoms of TMJ dysfunction by means of stepwise logistic regression. J Prosthet Dent 55:116–121.[ISI][Medline]

Isselee H, De Laat A, Lesaffre E, Lyssens R (1997). Short-term reproducibility of pressure pain thresholds in masseter and temporalis muscles of symptom-free subjects. Eur J Oral Sci 105:583–587.[ISI][Medline]

Isselee H, De Laat A, De Mot B, Lysens R (2002). Pressure-pain threshold variation in temporomandibular disorder myalgia over the course of the menstrual cycle. J Orofac Pain 16:105–117.[ISI][Medline]

Lund JP, Donga R, Widmer CG, Stohler CS (1991). The pain-adaptation model: a discussion of the relationship between chronic musculoskeletal pain and motor activity. Can J Physiol Pharmacol 69:683–694.[ISI][Medline]

Lund JP, Widmer CG, Feine JS (1995). Validity of diagnostic and monitoring tests used for temporomandibular disorders. J Dent Res 74:1133–1143.[Abstract/Free Full Text]

Macaluso GM, De Laat A (1995a). The influence of stimulating techniques on the masseteric and temporal M-responses in man. Arch Oral Biol 40:521–524.[ISI][Medline]

Macaluso GM, De Laat A (1995b). H-reflexes in masseter and temporalis muscles in man. Exp Brain Res 107:315–320.[ISI][Medline]

Macaluso GM, De Laat A (1995c). The influence of the position of surface recording electrodes on the relative uptake of the masseteric and temporal M-responses in man. Eur J Oral Sci 103:345–350.[ISI][Medline]

Sessle BJ (1999). The neural basis of temporomandibular joint and masticatory muscle pain. J Orofac Pain 13:238–245.[ISI][Medline]

Stohler CS, Zarb GA (1999). On the management of temporomandibular disorders: a plea for a low-tech, high prudence therapeutic approach. J Orofac Pain 13:255–261.[ISI][Medline]

Svensson P, De Laat A, Graven-Nielsen T, Arendt-Nielsen L (1998). Experimental jaw-muscle pain does not change heteronymous H-reflexes in the human temporalis muscle. Exp Brain Res 121:311–318.[ISI][Medline]

van Steenberghe D, van der Glas HW, De Laat A, Weytjens J, Carels C, Bonte B (1989). The masseteric poststimulus EMG complex (PSEC) in man: methodology, underlying reflexes and clinical perspectives. In: Electromyography of jaw reflexes in man. van Steenberghe D, De Laat A, editors. Leuven: University Press, pp. 269–288.

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