James J. Jaber, MD, PhD, John P. Leonetti, MD, Amy E. Lawrason, and Paul J. Feustel, PhD, Maywood, IL; and Albany, NY
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1 Otolaryngology Head and Neck Surgery (2008) 138, ORIGINAL RESEARCH GENERAL OTOLARYNGOLOGY Cervical spine causes for referred otalgia James J. Jaber, MD, PhD, John P. Leonetti, MD, Amy E. Lawrason, and Paul J. Feustel, PhD, Maywood, IL; and Albany, NY OBJECTIVE: Present experience in diagnosis and treatment for referred otalgia secondary to cervical spine degenerative disease (CSDD). STUDY DESIGN: A retrospective study of 123 patients with ear pain. SUBJECTS AND METHODS: All patients had a normal otologic examination and diagnosed with unspecified otalgia. The causes for referred otalgia were categorized into Group I: otalgia from non cervical spine disease (n 72), and Group II: cervical spine disease referred otalgia (n 51). Pain relief following cervical spine physical therapy (CSPT) was assessed. RESULTS: The most common cause for referred otalgia in Group I was Temporomandibular joint (TMJ) dysfunction (46%); most common cervical spine finding in Group II was CSDD (88%). CSPT in those documented patients all reported subjective pain relief. CONCLUSION: As the population in America ages, CSDD in the elderly will begin to emerge as a major etiologic source for referred otalgia. With a targeted medical history and physical examination one can use directed studies to diagnose CSDDreferred otalgia, and this pain can be alleviated with CSPT American Academy of Otolaryngology Head and Neck Surgery Foundation. All rights reserved. Otalgia can be classified as otogenic (primary) or nonotogenic (referred). 1-3 External and middle ear infections are associated with primary otogenic pain, which most otolaryngologists and primary care physicians are trained to diagnose. A negative otologic exam and persistent otalgia should suggest the possibility of referred otalgia. Referred otalgia or pain that is sensed by the ear but originates from a nonotologic source poses a difficult diagnostic challenge to even the most experienced otolaryngologist. Referred pain is an unpleasant sensation localized to an area separate from the site of the causative injury or other noxious stimulation. Often, referred pain is caused by nerve compression or irritation. In this circumstance, the sensation of pain will generally be felt in the territory that the nerve serves (ie, somatic dermatone) even though the damage originates elsewhere (ie,visceral tissue). 4 The ear is unique in that no other structure in the body of comparable size is supplied by so many sensory nerves from so many neural segments. As shown in Figure 1, the sensory innervation of the ear is supplied through a combination of four cranial nerves (CN V, VII, IX, and X) and two superior cervical plexus nerves (C2 and C3). Presumably this complex innervation serves as an evolutionary advantage as hearing is a necessary survival tool, and any pain perceived in that area causes a heightened sense of alarm. The differential diagnosis is specifically related to the sensory innervation of the ear, and therefore it is imperative that the otolaryngologist have a working knowledge of the complex neuroanatomic innervation of the external and middle ear. Among all causes of referred otalgia, dental pathology, which transmits referred otalgia via a branch of the trigeminal nerve, is the most common source of nonotogenic pain. 5 This was demonstrated by a previous study by the author (JPL), where the most common cause of referred otalgia with a normal-appearing ear was dental (74%). 6 Furthermore, the cause of referred otalgia can also be referred pain from the mouth, teeth, larynx, or thyroid gland; neural, vascular, or lymphatic structures of neck; or the esophagus. 7,8 However, with the aging population, physicians must also consider cervical spine degenerative disease (CSDD) as an increasingly common cause of referred otalgia involving the upper cervical plexus (greater auricular and lesser occipital nerve). 9 In this retrospective study, we have reviewed the complex neuroanatomic basis of nonotogenic ear pain, the prevalences of various etiological causes that have elicited this type of pain among our patient population, and presented our own experience in the diagnosis and treatment of referred otalgia secondary to CSDD. Nerve Pathways and Etiologies in Referred Otalgia 1-4,10 Auriculotemporal nerve (CN V). The auriculotemporal nerve derived from the mandibular division of the trigeminal nerve courses with the superficial temporal artery anteriorly to the external ear. The auriculotemporal nerve supplies sensory afferents to the tragus, anterior auricle, anterior wall of the external canal, and anterior portion of the lateral tympanic membrane. Due to the length and extensive distribution of the auriculotemporal nerve, it is the nerve that is most commonly involved in referred otalgia. Received September 4, 2007; revised December 14, 2007; accepted December 28, /$ American Academy of Otolaryngology Head and Neck Surgery Foundation. All rights reserved. doi: /j.otohns
2 480 Otolaryngology Head and Neck Surgery, Vol 138, No 4, April 2008 Figure 1 Complex sensory innervation of the ear and periauricular structures and various etiological causes in referred otalgia. Temporomandibular joint (TMJ) disease and dental pathologies are associated with referred otalgia by way of the auriculotemporal nerve. Posterior auricular nerve (CN VII). The posterior auricular nerve, which is the first extracranial branch of the facial nerve, sends sensory afferents that provide innervation of the posterior wall of the external auditory canal, posterior lateral surface of the tympanic membrane, and posterior skin of the auricle. Otalgia referred from the facial nerve may also occur following an outbreak of herpes zoster (prior to vesicle eruption). Jacobson s nerve (CN IX). Jacobson s nerve, a derivative from the glossopharyngeal nerve, joins with the caroticotympanic branches from the sympathetic plexus to form the tympanic plexus. This plexus provides sensation to the middle ear, upper eustachian tube, and medial surface of the tympanic membrane. Referred otalgia transmitted by the glossopharyngeal nerve may be secondary to lesions and/or inflammatory processes of the nasopharynx, palatine tonsil, soft palate, or posterior one-third of the tongue. Arnold s nerve (CN X). Arnold s nerve, the auricular branch from the vagus, divides into a superior branch, which sends a small branch to the facial nerve sheath, and an inferior branch, which is joined by a small branch from the facial nerve. The inferior branch provides sensation to the inferior and posterior aspects of the external auditory canal, to the concavity of the concha, and finally to the lateral surface of the tympanic membrane. Thyroiditis, thyroid tumors, laryngeal carcinomas, and gastroesophageal reflux can present as referred otalgia secondary to irritation of the superior laryngeal nerve, a branch of the vagus nerve. Greater auricular and lesser occipital nerve (cervical plexus). The greater auricular and lesser occipital nerves, derivatives from C2 and C3 of the cervical plexus, course over the
3 Jaber et al Cervical spine causes for referred otalgia sternocleidomastoid muscle to innervate the posterior auricle and the skin overlying the mastoid bone and parotid gland. Pathology of the cervical spine that may present as referred otalgia includes cervical spine degenerative diseases (eg, osteoarthritis, cervical facet syndrome, spondylosis, disc herniation, and stenosis), whiplash injury, and cervical meningiomas. METHODOLOGY Following approval by the Loyola Research Institutional Review Board, a retrospective study and chart review of 133 adults diagnosed with unspecified ear pain at a tertiary-level academic medical center and seen by the senior author (JPL) between January 2002 and November 2006 was conducted. Patients were selected based on a normal otoscopic examination and given the initial diagnosis of unspecified otalgia, ICD-9 code Exclusion criteria included those patients who had undergone previous ear surgery (n 10). The distributions of all diagnosed etiologic causes for referred otalgia (n 123) with their respective nerve pathways were categorized. In addition, patients were separated into two cohorts. Group I consisted of those with referred otalgia from an etiologic source other than cervical spine disease (n 72), and Group II included those with clinical and/or radiographic evidence of cervical spine disease as the cause of their referred ear pain (n 51). A positive imaging study showing CSDD at or above C4 was assumed to be positive but did not exclude the diagnosis of CSDD based on clinical evidence. Age, gender, ethnicity, and ear pain location (right vs left) were analyzed between the two cohorts. In addition two predictors, 1) a significant past medical history of some type of rheumatologic disease, and/or 2) concomitant or recurrent neck pain, and their association with positive imaging study were analyzed in Group II. A P value less than or equal to 0.05 was selected as significant. Student paired t tests were used in testing for group differences unless the expected number in any cell was less than 5, in which case Fisher exact test was used. Statistics 6.0 from Statsoft (Tulsa, OK) was used for all tests. RESULTS The distributions of diagnosed etiologic causes for ear pain with their respective sensory innervations are shown in Table 1. All cranial and cervical ear sensory nerves are represented within our patient population, with the majority of patients experiencing subjective ear pain secondary to TMJ/dental disease (n 44, 37%) or cervical spine degenerative disease (n 45, 37%). One patient was diagnosed with psychogenic otalgia. Group I and Group II patient characteristics are outlined in Table 2. Both groups shared similar demographics, with Table 1 Distribution of referred nerve pathways and etiological causes (n 123) Referred nerve pathway, n (%) Etiological causes in referred otalgia, n (%) Auriculotemporal nerve (CN V), 56 (46%) TMJ dysfunction, 33 (28) Dental, 11 (9) Trigeminal neuralgia, 4 (3) Mandibular osteomyelitis/tumor, 4 (3) Parotid tumor/infection, 4 (3) Posterior auricular nerve (CN VII), 3 (2%) Acoustic neuroma, 2 (2) Herpes zoster, 1 (1) Jacobson s nerve (CN IX), 8 (7%) Tonsillitis/pharyngitis, 2 (2) Sinusitis, 4 (3) Pharyngeal tumor, 1 (1) Glossopharnygeal neuroma, 1 (1) Arnold s nerve (CN X), 4 (3%) LPR, 2 (2) Cricopharyngeal spasm, 1 (1) Vagal stimulator, 1 (1) Greater auricular, lesser occipital nerve (C2, C3), 51 (42%) CSDD, 45 (37) Cervical root cysts, 1 (1) Arnold-Chiari type I, 1 (1) Whiplash, 2 (2) Vascular, 1 (1) Fibromyalgia, 1 (1) Other, 1 (1%) Psychogenic, 1 (1) TMJ, temporal mandibular joint; LPR, laryngeal pharyngeal reflux; CSDD, cervical spine degenerative disease; C2,C3, cervical plexus.
4 482 Otolaryngology Head and Neck Surgery, Vol 138, No 4, April 2008 Table 2 Patient characteristics: Group I vs Group II Group I Non cervical spine causes of referred otalgia (n 72) Group II Cervical spine causes of referred otalgia (n 51) Age (y, SD)* Caucasian [n (%)] 61 (85) 44 (86) Gender [n (%)] Female 58 (81) 41 (80) Male 14 (19) 10 (20) Pain location [n (%)] Right 35 (49) 21 (41) Left 28 (39) 24 (47) Bilateral 9 (12) 6 (12) *Student s paired t test: P P value not significant between groups. the majority of patients being of Caucasian origin and of female gender (4:1, female:male) with roughly an equal distribution of subjective ear pain location experienced among the two patient populations. However, one notable difference exists between the two groups; age in Group II was shown to be statistically higher, with a mean age of vs in Group I (P 0.002, Student s paired t test). Forty-eight patients in Group II underwent diagnostic imaging of their cervical spine, with 83% (n 40) showing positive findings for some type of cervical spine pathology that can be attributed to their nonotogenic ear pain: 37, cervical spine degenerative disease (eg, disc changes and herniation, osteophytes, spinal/foramen stenosis, facet disease) with radiographic changes at C4 and above (Fig 2); 1, cervical root cyst; 1, Arnold-Chiari I; and 1, vascular, with the majority undergoing magnetic resonance imaging (85% MRI, 9% x-ray, 6% CT, Table 3). Of the eight negative imaging studies the following diagnoses were made: fibromyalgia (1), whiplash following a motor vehicle accident (2), CSDD based on clinical evidence (1), and probable CSDD with evidence of lower cervical spine pathology on imaging (4). Three patients had previously documented CSDD and did not undergo any diagnostic imaging study. With the majority of patients in Group II having a positive imaging study, subgroup analysis was warranted to elucidate pattern recognition for future diagnoses in this class of referred otalgia. Through a comprehensive retrospective chart review, including documented visits to other medical disciplines, two identifying factors appeared to correlate with a positive imaging study: 1) a significant past medical history of rheumatologic disease, eg, arthritis, certain autoimmune diseases, musculoskeletal pain disorders; Figure 2 Right foramenal stenosis (arrow) at C3 due to large osteophyte in a 69-year-old female with right-sided otalgia. Table 3 Predictors of cervical spine causes for referred otalgia (n 48)* Positive imaging [n (%)] Negative imaging [n (%)] MRI, CT, or x-ray All (n 48) 40 (83) 8 (17) CSDD (n 42) 37 (88) 5 (12) Significant medical history All ( ) history 28 (88) 4 (12) ( ) history 12 (75) 4 (25) CSDD ( ) history 28 (97) 1 (3) ( ) history 9 (69) 4 (31) Neck pain All ( ) pain 32 (89) 4 (11) ( ) pain 8 (67) 4 (33) CSDD ( ) pain 30 (97) 1 (3) ( ) pain 7 (64) 4 (36) *Three patients had previously documented CSDD and did not undergo imaging. All tests were conducted using Fisher exact P, two-tailed. CSDD, cervical spine degenerative disease; cervical degeneration at C4 or above positive. P P P P and 2) concomitant or recurrent neck pain on physical exam. Of those Group II patients who had a significant past medical history or neck pain, 88% (n 28) and 89% (n 32),
5 Jaber et al Cervical spine causes for referred otalgia respectively, were found to have a positive imaging study. Although these predictors correlated with a positive imaging study, there was no statistical significance observed in this group (P 0.41, significant history; and P 0.09, neck pain, Fisher exact test, two-tailed). However, when the six non-csdd patients were removed and a subgroup analysis was conducted, a statistically significant association was demonstrated between a positive imaging study and a significant medical history (97%, P 0.02) and/or neck pain (97%, P 0.01). Cervical spine physical therapy (CSPT) was recommended to all patients diagnosed with CSDD (n 45, radiographic or clinical). Follow-up and compliance was difficult and consequently documentation for only 20 patients could be obtained. Nonetheless, all 20 individuals expressed subjective pain relief following CSPT. DISCUSSION Despite published awareness regarding the many potential causes of referred otalgia, diagnosis often eludes the most experienced physician. 11 This may be due, in part, to the complex neuroanatomic innervation of the ear, head, and neck, and therefore the inherent limitless sources for referred ear pain. Two cohorts were categorized in this study, Group I (non cervical spine causes of referred otalgia) and Group II (cervical spine causes), in which we documented no fewer than 23 causes of referred otalgia representing all five nerve pathways (vide infra), with women reporting otalgia 4 times more frequently than men. These causes ranged from the benign etiology of whiplash (cervical spine nerves) to the more serious mandibular tumor (CN V). The two most common nerve pathways for secondary otalgia were the trigeminal nerve (n 56, 46%) and the superior cervical plexus nerves (n 51, 42%). The most common etiology in Group I was TMJ dysfunction and in Group II, CSDD. Due to the length and extensive distribution of the trigeminal nerve, it is not surprising that this nerve is most commonly involved in referred otalgia. This type of nonotogenic ear pain, especially involving disorders of the temporal mandibular joint, is well documented throughout oral surgery, otolaryngology, and pain journals Surprisingly, one group of patients with nonotogenic otalgia often overlooked are those diagnosed with cervical spine sources, in particular CSDD. 9,15 Referred otalgia due to cervical spine disease usually is described as retroauricular or infra-auricular pain, which is constant and often related to changes in neck position. As the population in America ages, CSDD in the elderly will begin to emerge as a major etiological source for referred ear pain. A case report has been published implicating cervical spine arthritis with ear pain, which improved with injection of the facet joint using a local anestheticcorticosteroid solution. 9 In this current study we have shown that CSDD, diagnosed either through radiographic or clinical evidence, is a major contributor to referred otalgia. CSDD-referred otalgia represented 37% of our patient population and was shown to be statistically higher in an elderly population (Group I vs Group II, P 0.002). Imaging studies evaluate anatomy, rather than function, and are prone to false-positive and false-negative results. For example, Boden s cervical MR study cites abnormalities in nearly 20% of asymptomatic subjects. 16 Consequently, results of imaging studies must be interpreted within the context of each clinical case, with the converse being equally valid. Although both clinical and radiographic evidence were used to support the diagnosis of referred otalgia from cervical spine causes (Group II), we also analyzed Group II independently for positive predictors in only those who had undergone imaging studies implicating cervical spine causes for referred otalgia. After ruling out non cervical spine causes of referred ear pain, a targeted medical history of some type of rheumatological disease, recurrent or concomitant neck pain coupled with a normal otologic exam highly correlated with a positive imaging study of CSDD (P 0.02, rheumatologic disease; P 0.01, neck pain). Kuttila et al have also described an association of several predictors, including and not limited to neck pain, general arthrosis, bruxism, age, and active need for TMJ disease treatment, with secondary otalgia in an adult population. 17 Similar to this study, they reported that women presented with otalgia more often than men. This published report very nicely outlines several general predictors in secondary otalgia similar to our observations but falls short in implicating cervical spine causes as a cause of ear pain. The authors of this report believe that CSDD-referred otalgia is propagated through disease of the cervical vertebrae and therefore is postural. This ear pain can be ameliorated with physical therapy, and most studies support conservative treatment, such as cervicothoracic stabilization programs, combined with aerobic conditioning in treating cervical spine disorders. 18,19 With this in mind, we recommended outpatient physical therapy to all our patients with CSDD-referred otalgia. Although documentation could be ascertained for only 20 patients, all patients reported subjective pain relief. A prospective study is currently underway at our institution to further assess the long-term effects of CSPT for the treatment of referred otalgia due to degenerative changes in this anatomic location. With the current study data in hand, a diagnostic and treatment algorithm can be proposed and is outlined in Figure 3. If a female greater than 60 years of age with persistent otalgia and a negative otolaryngologic and dental work-up presents with similar characteristics outlined in this study, ie, rheumatologic disease and/or neck pain, a CT or MRI of the cervical spine has
6 484 Otolaryngology Head and Neck Surgery, Vol 138, No 4, April 2008 Figure 3 Diagnostic and treatment algorithm for cervical spine degenerative disease referred otalgia. been shown to implicate degenerative changes as a source for her ear pain. In that case CSPT is indicated as a conservative and effective treatment strategy. CONCLUSION The complex sensory innervation of the ear and the many etiological factors that can elicit nonotogenic ear pain may result in a diagnostic challenge. Elderly citizens aged 65 and over constitute over 13% of the United States population and as a consequence cervical spine degenerative diseases in the elderly will begin to emerge as a major etiological source for referred ear pain. Our review clearly shows that with a targeted medical history and physical examination, one can use directed studies to elucidate the cause of pain as being secondary to CSDD. Conservative medical management involving cervical spine physical therapy can help improve or eliminate this type of referred otalgia. A prospective pilot study is currently underway to assess the current treatment strategy. AUTHOR INFORMATION From Loyola University Medical Center, Department of Otolaryngology Head and Neck Surgery (Drs Jaber and Leonetti), Maywood, IL; Loyola University Chicago, Stritch School of Medicine (Ms Lawrason), Chicago, IL; and the Center for Neuropharmacology and Neuroscience (Dr Feustel), Albany Medical College. Corresponding author: John P. Leonetti, MD, Loyola University Medical Center, Department of Otolaryngology-Head and Neck Surgery, 2160 S. First Ave, Maguire Building, Maywood, IL address: jleonet@lumc.edu. AUTHOR CONTRIBUTIONS John P. Leonetti, major author, original designer of study, clinician; James J. Jaber, chart review, analysis, and majority author; Amy Lawrason, chart review, minor author; Paul J. Feustel, statistical analysis, minor author. FINANCIAL DISCLOSURE None. REFERENCES 1. Shah RK, Blevins NH. Otalgia. Otolaryngol Clin North Am 2003;36: Olsen KD. The many causes of otalgia. Infection, trauma, cancer. Postgrad Med 1986;80:50 2., 55 6, Thaller SR. Otalgia with a normal ear. Am Fam Physician 1987;36:
7 Jaber et al Cervical spine causes for referred otalgia Powers WH, Britton BH. Nonotogenic otalgia: diagnosis and treatment. Am J Otol 1980;2: Kreisberg MK, Turner J. Dental causes of referred otalgia. Ear Nose Throat J 1987 Oct;66: Leonetti JP, Li J, Donzelli J. Otalgia in a normal appearing ear [poster]. Otolaryngol Head Neck Surg 117:P Scarbrough TJ, Day TA, Williams TE, et al. Referred otalgia in head and neck cancer: a unifying schema. Am J Clin Oncol 2003;26:e Yanagisawa K, Kveton JF. Referred otalgia. Am J Otolaryngol 1992; 13: Tamer TJ. Ear pain due to cervical spine arthritis: treatment with cervical facet injection. Headache 199;31: Wazen JJ. Referred otalgia. Otolaryngol Clin North Am 1989;22: Janetta PJ. Pain problems of significance in the head and face, some of which often are misdiagnosed. Curr Probl Surg 1973; Keersmaekers K, De Boever JA, Van Den Berghe L. Otalgia in patients with temporomandibular joint disorders. J Prosthet Dent 1996; 75: Kuttila S, Kuttila M, Le Bell Y, et al. Aural symptoms and signs of temporomandibular disorder in association with treatment need and visits to physician. Laryngoscope 1999;109: Ciancaglini R, Loreti P, Radalli G. Ear, nose and throat symptoms in patients with TMD: the association of symptoms according to severity of arthropathy. J Orofac Pain 1994;8: Danish, SF, Zager EL. Cervical spine meningioma presenting as otalgia: case report. Neurosurgery 2005;56(3):E Boden SD, McCowin PR, Davis DO, et al. Abnormal magneticresonance scans of the cervical spine in asymptomatic subjects. A prospective investigation. J Bone Joint Surg Am 1990;72: Kuttila SJ, Kuttila MH, Niemi PM, et al. Arch Otolaryngol Head Neck Surg 2001;127: Saal JS, Saal JA, Yurth EF. Nonoperative management of herniated cervical intervertebral disc with radiculopathy. Spine 1996;21: Grant RN, McKenzie RA. Mechanical diagnosis and therapy for cervical and thoracic spine. In: Grant R, editor. Physical therapy of the cervical and thoracic spine. New York: Churchill Livingstone; p
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