Experimentally induced masseter-pain changes masseter but not sternocleidomastoid muscle-related activity during mastication
Introduction
Mastication is a rhythmic motor behavior involving a coordinated action of masticatory and neck muscles, tongue, lips and cheeks. In this process, food is mechanically reduced to smaller particles and prepared for swallowing (Lund, 1991, Lund and Kolta, 2005). The close functional connection of craniocervical and jaw systems have been widely referred and explained by the convergence of trigeminal and cervical afferents in the brainstem sensory trigeminal nuclear complex (Eriksson et al., 2000, Zafar et al., 2000a). Furthermore, these systems are linked by chains of interconnecting muscles, tendons, ligaments and fascia (Corrêa and Bérzin, 2004, Ciuffolo et al., 2005).
These neuroanatomical and biomechanical connections have been supported by evidence as the increase of sternocleidomastoid EMG amplitude during clenching (Svensson et al., 2004, Ciuffolo et al., 2005, Ferrario et al., 2006, Giannakopoulos et al., 2013) and the fact that the occlusal interferences affect their EMG pattern during the dental clenching (Ferrario et al., 2003). Indeed, concomitant activation of the SCM muscle in response to increased chewing load (increased food volume and texture) was observed. It has been suggested that this coactivation may play a role in stabilizing the head in space while jaw muscles move the mandible to get an appropriate pattern of movement, coordination and strength (Häggman-Henrikson et al., 2013).
Pain in the masticatory muscles is one of the main symptoms of temporomandibular disorder (TMD) (Svensson and Graven-Nielsen, 2001, Mujakperuo et al., 2010). Studies indicate that pain may trigger neuromuscular control in the jaw–neck motor system. Pain and TMD have been associated with a decrease in muscle recruitment (Svensson et al., 2004, Wang et al., 2010, Castroflorio et al., 2012) and imbalance between the pairs of masticatory muscles during clenching (Ries et al., 2008, Tartaglia et al., 2008, De Felício et al., 2012) and mastication (Ries et al., 2008). The cervical spine dysfunctions (Bevilaqua-Grossi et al., 2007, Ries et al., 2008, Armijo-Olivo et al., 2010), also it has been related to pain myogenic TMD. But the complexity of the somatosensory interaction mechanisms between the cervical spine and jaw as well as the differences between research clinical and experimental still make this a controversial subject.
Clinical studies (Ries et al., 2008, Pasinato et al., 2011, De Felício et al., 2013, Weber et al., 2013) have tried to clarify the motor adaptations associated with TMD. However, psychosocial and anatomo-occlusal variables, the dysfunction severity, and the fluctuation of the painful condition cannot be appropriately controlled for studies conducted with patients (Svensson and Graven-Nielsen, 2001, Lobbezoo et al., 2006). For this reason, chemical induction techniques, such as intramuscular injection of glutamate solution, have been used to experimentally produce jaw-muscle pain in healthy individuals (Castrillon et al., 2008, Sae-Lee et al., 2008, Baad-Hansen et al., 2009, Castroflorio et al., 2012, Wiesinger et al., 2013). Thus, human experimental-pain models allow for the assessment the effects of muscle pain on the somatosensory system and motor function under standardized conditions (Svensson and Graven-Nielsen, 2001).
Results of experimental studies (Svensson et al., 1996, Svensson et al., 1997) are consistent with the pain-adaptation model. According to this model, the inputs are mediated at the spinal cord or brainstem and when nociceptive afferents are excited, the motor reorganization involves decreased electromyographic activity of the agonist muscles accompanied by increased activity of the antagonist muscles (Svensson et al., 1998, Svensson et al., 2004, Castroflorio et al., 2012). These changes are usually associated with reduced amplitude and speed of movements (Svensson and Graven-Nielsen, 2001, Svensson, 2007). Nevertheless, changes in motor control caused by pain are not always predictable or adequately explained, such as the maintenance of force when motoneuron discharge is reduced (Hodges and Tucker, 2011) or that masticatory function may suffer cortical modulation and respond differently to acute and chronic pain (Sessle, 2006).
Studies have been conducted using electromyographic assessment of jaw and neck elevator muscles mainly during dental clenching (Svensson et al., 2004, Svensson et al., 2005, Gonçalves et al., 2007, Pasinato et al., 2011, Ballenberger et al., 2012). Dynamic situations, although less functional, such as repeated jaw-opening (Zafar et al., 2000b, Baad-Hansen et al., 2009, Wiesinger et al., 2013), and the simultaneous bilateral isotonic contraction (non-habitual mastication) have also been previously analyzed (Ries et al., 2008, Briesemeister et al., 2012). However, the effects of pain on the activation pattern of jaw and neck muscles during chewing is unclear. Moreover, there is no description in the literature of the effects of experimental muscle-pain on the symmetry of jaw- and neck-muscle activation during mastication.
Considering that motor adaptations caused by muscle pain are task-dependent (Hodges and Tucker, 2011), distinct effects can be expected on masticatory (masseter) and neck (SCM) muscles during a dynamic activity such as mastication. A better understanding of these effects may provide new insights for early pain-management practices, as well as for general assessments of orofacial motor function in general and of mastication in particular.
The aim of the present study was to investigate the effects of experimental pain induced by glutamate injection into the masseter muscle of healthy volunteers on the amplitude and symmetry of electromyographic activity of the masseter and SCM muscles during mastication. The effects of pain on coactivation between masseter e SCM were also analyzed.
Section snippets
Volunteers
Twenty-eight male volunteers, aged 18–27 years (mean age ± SD = 20.6 ± 2.0) recruited among the students at the University of Brasília, participated in this study. The exclusion criteria were: presence of TMD, pain in the shoulder, cervical region, or headache; missing teeth (except for the third molars), open bite, crossbite, Angle Class II or III (Ferrario et al., 2006); self-reported bruxism or mouth breathing; dolichofacial or brachyfacial types of face; atypical mastication, and body mass index
Induced pain intensity
Isotonic saline injection into the masseter muscle was associated with very low scores. The peak perceived pain intensity on the VAS after saline injection was 7.69 ± 8.72 (range 0–36.72 mm). On the other hand, glutamate solution injection evoked pain with moderate to high intensity, with peak on the VAS at 58.1 ± 16.6 mm (range 19.2–84.9 mm) during the glutamate injection. Of note, during mastication recording, glutamate-evoked pain sensation remained stable, after which it gradually decreased,
Discussion
The present study showed the effects of experimentally-induced pain in the masseter muscle on the EMG activity of the masseter and SCM muscles. Symmetry and coactivation during mastication were analyzed in healthy individuals. We expected to see changes in both masseter and SCM muscles; instead, provoked acute pain in the masseter caused no effect in the ECM. This pattern brings into question the overall cranio-cervical strategy of adaptation to orofacial acute pain.
Perceived pain by the
Conclusion
The results of this study suggest that experimentally-induced acute pain caused a decrease in the amplitude of muscular activation of the masseter-muscle on the working side during the active period of the masticatory cycle, with a reduction of the physiological asymmetry between the two sides. No significant changes could be detected on the SCM-muscle electromyographic activity or on the masseter and SCM muscles coactivation during mastication, except for the working side (particularly
Acknowledgements
We extend our sincere thanks to the students, volunteers and other collaborators of the University of Brasília. Geovana P. Bolzan, is acknowledged by support in the screening of volunteers; Marcus R. Giannetti and Lilian G.K. Ries, special thanks for assistance with data analysis.
Fernanda Pasinato is Physical Therapist (PT). Master Degree and Ph.D in Human Communication Disorders from the Federal University of Santa Maria, Brazil. Her research focus involves clinical and experimental research in surface electromyography of masticatory and cervical muscles in healthy subjects and patients with temporomandibular disorders.
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Fernanda Pasinato is Physical Therapist (PT). Master Degree and Ph.D in Human Communication Disorders from the Federal University of Santa Maria, Brazil. Her research focus involves clinical and experimental research in surface electromyography of masticatory and cervical muscles in healthy subjects and patients with temporomandibular disorders.
Clarissa Cardoso dos Santos C. Paz is Physical Therapy (PT), Professor of the Physical Therapy Course at the University of Brasília, Brazil, since 2012, Master of Science (MSc) in 2005 from the Federal University of Minas Gerais (UFMG), Brazil and Ph.D. in Neuroscience (UFMG), Brazil, since 2012. Her research focus involves clinical research in biomechanics aspects, including sit to stand, gait and reaching in stroke, multiple sclerosis, Down syndrome and healthy subjects.
Jorge Luis Lopes Zeredo is a Dental Surgeon (DDS) with a PhD in Orthodontics. He received his PhD from Tokyo Medical and Dental University (2003) and worked as an Assistant Professor for the Department of Department of Developmental and Reconstructive Medicine of Nagasaki University, Japan (2003–2008). He is currently a professor of Basic Sciences and Health at the University of Brasília, Brazil (2008-present). In his research, Dr. Zeredo has studied extensively the effects of orthodontic treatment, pain, and emotional stress on oral and maxillofacial function in both animal and human models.
Sérgio Bruzadelli Macedo is Oral and Maxillofacial Surgeon, professor of the Oral and Maxillofacial Surgery at the University of Brasília (UnB), Brazil. Master of Degree and PhD in OMFS. His research focus radio and chemo necrosis of the jaws. Actually, coordinate a clinic at University Hospital to treat pacients with these desease, using Ozone and Surgery.
Eliane Castilhos Rodrigues Corrêa is Physical Therapist (PT), Associate professor at Federal University of Santa Maria, Brazil, with Master Degree (M.S.) in Human Communication Disorders from the Federal University of Santa Maria, Brazil and Ph.D. in Oral-Dental Biology from State University of Campinas, Brazil. She is adviser at Graduate Program of Human Communication Disorders with research focusing on surface electromyography of masticatory and cervical muscles, temporomandibular disorders, mouth-breathing syndrome and ventilatory function.