Cervical Spine Causes for Referred Otalgia

Otolaryngology–Head and Neck Surgery (2008) 138, 479-485 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

innervation of the ear is supplied through a combination of OBJECTIVE: Present experience in diagnosis and treatment for four cranial nerves (CN V, VII, IX, and X) and two superior referred otalgia secondary to cervical spine degenerative disease cervical plexus nerves (C2 and C3). Presumably this com- (CSDD). plex innervation serves as an evolutionary advantage as STUDY DESIGN: A retrospective study of 123 patients with hearing is a necessary survival tool, and any pain perceived ear pain. SUBJECTS AND METHODS: All patients had a normal oto- in that area causes a heightened sense of alarm. The differ- logic examination and diagnosed with unspecified otalgia. The ential diagnosis is specifically related to the sensory inner- causes for referred otalgia were categorized into Group I: otalgia vation of the ear, and therefore it is imperative that the from non–cervical spine disease (n ϭ 72), and Group II: cervical otolaryngologist have a working knowledge of the complex spine disease–referred otalgia (n ϭ 51). Pain relief following neuroanatomic innervation of the external and middle ear. cervical spine physical therapy (CSPT) was assessed. Among all causes of referred otalgia, dental pathology, RESULTS: The most common cause for referred otalgia in which transmits referred otalgia via a branch of the trigem- Group I was Temporomandibular joint (TMJ) dysfunction (46%); inal nerve, is the most common source of nonotogenic most common cervical spine finding in Group II was CSDD pain.5 This was demonstrated by a previous study by the (88%). CSPT in those documented patients all reported subjective author (JPL), where the most common cause of referred pain relief. otalgia with a normal-appearing ear was dental (74%).6 CONCLUSION: As the population in America ages, CSDD in Furthermore, the cause of referred otalgia can also be re- the elderly will begin to emerge as a major etiologic source for referred otalgia. With a targeted medical history and physical ferred pain from the mouth, teeth, larynx, or thyroid gland; examination one can use directed studies to diagnose CSDD- neural, vascular, or lymphatic structures of neck; or the 7,8 referred otalgia, and this pain can be alleviated with CSPT. esophagus. However, with the aging population, physi- © 2008 American Academy of Otolaryngology–Head and Neck cians must also consider cervical spine degenerative disease Surgery Foundation. All rights reserved. (CSDD) as an increasingly common cause of referred otal- gia involving the upper cervical plexus (greater auricular talgia can be classified as otogenic (primary) or non- and lesser occipital nerve).9 In this retrospective study, we Ootogenic (referred).1-3 External and middle ear infec- have reviewed the complex neuroanatomic basis of non- tions are associated with primary otogenic pain, which most otogenic ear pain, the prevalences of various etiological otolaryngologists and primary care physicians are trained to causes that have elicited this type of pain among our patient diagnose. A negative otologic exam and persistent otalgia population, and presented our own experience in the diag- should suggest the possibility of referred otalgia. Referred nosis and treatment of referred otalgia secondary to CSDD. otalgia or pain that is sensed by the ear but originates from a nonotologic source poses a difficult diagnostic challenge Nerve Pathways and Etiologies in to even the most experienced otolaryngologist. Referred Referred Otalgia1-4,10 pain is an unpleasant sensation localized to an area separate from the site of the causative injury or other noxious stim- Auriculotemporal nerve (CN V). The auriculotemporal ulation. Often, referred pain is caused by nerve compression nerve derived from the mandibular division of the trigemi- or irritation. In this circumstance, the sensation of pain will nal nerve courses with the superficial temporal artery ante- generally be felt in the territory that the nerve serves (ie, riorly to the external ear. The auriculotemporal nerve sup- somatic dermatone) even though the damage originates plies sensory afferents to the tragus, anterior auricle, elsewhere (ie,visceral tissue).4 anterior wall of the external canal, and anterior portion of The ear is unique in that no other structure in the body of the lateral tympanic membrane. Due to the length and ex- comparable size is supplied by so many sensory nerves from tensive distribution of the auriculotemporal nerve, it is the so many neural segments. As shown in Figure 1, the sensory nerve that is most commonly involved in referred otalgia.

Received September 4, 2007; revised December 14, 2007; accepted December 28, 2007.

0194-5998/$34.00 © 2008 American Academy of Otolaryngology–Head and Neck Surgery Foundation. All rights reserved. doi:10.1016/j.otohns.2007.12.043 480 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 pathol- glossopharyngeal nerve may be secondary to lesions and/or ogies are associated with referred otalgia by way of the inflammatory processes of the nasopharynx, palatine tonsil, auriculotemporal nerve. soft palate, or posterior one-third of the tongue.

Posterior auricular nerve (CN VII). The posterior auricular Arnold’s nerve (CN X). Arnold’s nerve, the auricular branch nerve, which is the first extracranial branch of the facial from the vagus, divides into a superior branch, which sends nerve, sends sensory afferents that provide innervation of a small branch to the facial nerve sheath, and an inferior the posterior wall of the external auditory canal, posterior branch, which is joined by a small branch from the facial lateral surface of the tympanic membrane, and posterior nerve. The inferior branch provides sensation to the inferior skin of the auricle. Otalgia referred from the facial nerve and posterior aspects of the external auditory canal, to the may also occur following an outbreak of herpes zoster (prior concavity of the concha, and finally to the lateral surface of to vesicle eruption). the tympanic membrane. Thyroiditis, thyroid tumors, laryn- geal carcinomas, and gastroesophageal reflux can present as Jacobson’s nerve (CN IX). Jacobson’s nerve, a derivative referred otalgia secondary to irritation of the superior laryn- from the glossopharyngeal nerve, joins with the caroti- geal nerve, a branch of the vagus nerve. cotympanic branches from the sympathetic plexus to form the tympanic plexus. This plexus provides sensation to the Greater auricular and lesser occipital nerve (cervical plexus). middle ear, upper eustachian tube, and medial surface of The greater auricular and lesser occipital nerves, derivatives the tympanic membrane. Referred otalgia transmitted by the from C2 and C3 of the cervical plexus, course over the Jaber et al Cervical spine causes for referred otalgia . . . 481 sternocleidomastoid muscle to innervate the posterior auri- cause of their referred ear pain (n ϭ 51). A positive imaging cle and the skin overlying the mastoid bone and parotid study showing CSDD at or above C4 was assumed to be gland. Pathology of the cervical spine that may present as positive but did not exclude the diagnosis of CSDD based referred otalgia includes cervical spine degenerative dis- on clinical evidence. Age, gender, ethnicity, and ear pain eases (eg, osteoarthritis, cervical facet syndrome, spondy- location (right vs left) were analyzed between the two co- losis, disc herniation, and stenosis), whiplash injury, and horts. In addition two predictors, 1) a significant past med- cervical meningiomas. ical 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. METHODOLOGY Student paired t tests were used in testing for group differ- ences unless the expected number in any cell was less than Following approval by the Loyola Research Institutional 5, in which case Fisher exact test was used. Statistics 6.0 Review Board, a retrospective study and chart review of 133 from Statsoft (Tulsa, OK) was used for all tests. 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 con- ducted. Patients were selected based on a normal otoscopic RESULTS examination and given the initial diagnosis of unspecified otalgia, ICD-9 code 388.70. Exclusion criteria included The distributions of diagnosed etiologic causes for ear pain those patients who had undergone previous ear surgery (n ϭ with their respective sensory innervations are shown in 10). Table 1. All cranial and cervical ear sensory nerves are The distributions of all diagnosed etiologic causes for represented within our patient population, with the majority referred otalgia (n ϭ 123) with their respective nerve path- of patients experiencing subjective ear pain secondary to ways were categorized. In addition, patients were separated TMJ/dental disease (n ϭ 44, 37%) or cervical spine degen- into two cohorts. Group I consisted of those with referred erative disease (n ϭ 45, 37%). One patient was diagnosed otalgia from an etiologic source other than cervical spine with psychogenic otalgia. disease (n ϭ 72), and Group II included those with clinical Group I and Group II patient characteristics are outlined and/or radiographic evidence of cervical spine disease as the in Table 2. Both groups shared similar demographics, with

Table 1 (123 ؍ Distribution of referred nerve pathways and etiological causes (n 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. 482 Otolaryngology–Head and Neck Surgery, Vol 138, No 4, April 2008

Table 2 Table 3 Patient characteristics: Group I vs Group II Predictors of cervical spine causes for referred *(48 ؍ otalgia (n Group I Non– Group II cervical spine Cervical spine Positive Negative causes of causes of imaging imaging referred otalgia referred otalgia [n (%)] [n (%)] (n ϭ 72) (n ϭ 51) MRI, CT, or x-ray Age (y, Ϯ SD)* 53 Ϯ 17 64 Ϯ 14 All (n ϭ 48) 40 (83) 8 (17) Caucasian [n (%)]† 61 (85) 44 (86) CSDD† (n ϭ 42) 37 (88) 5 (12) Gender [n (%)]† Significant medical history Female 58 (81) 41 (80) All‡ Male 14 (19) 10 (20) (ϩ) history 28 (88) 4 (12) Pain location (Ϫ) history 12 (75) 4 (25) [n (%)]† CSDD§ Right 35 (49) 21 (41) (ϩ) history 28 (97) 1 (3) Left 28 (39) 24 (47) (Ϫ) history 9 (69) 4 (31) Bilateral 9 (12) 6 (12) Neck pain Allʈ *Student’s paired t test: P ϭ 0.002. (ϩ) pain 32 (89) 4 (11) †P value not significant between groups. (Ϫ) pain 8 (67) 4 (33) CSDD¶ (ϩ) pain 30 (97) 1 (3) (Ϫ) pain 7 (64) 4 (36) the majority of patients being of Caucasian origin and of *Three patients had previously documented CSDD and did female gender (4:1, female:male) with roughly an equal not undergo imaging. All tests were conducted using Fisher distribution of subjective ear pain location experienced exact P, two-tailed. among the two patient populations. However, one notable †CSDD, cervical spine degenerative disease; cervical degen- eration at C4 or above ϭ positive. difference exists between the two groups; age in Group II ‡P ϭ 0.41. was shown to be statistically higher, with a mean age of §P ϭ 0.02. 63.5 Ϯ 17.5 vs 53.2 Ϯ 17.1 in Group I (P ϭ 0.002, ʈP ϭ 0.09. Student’s paired t test). ¶P ϭ 0.01. Forty-eight patients in Group II underwent diagnostic imaging of their cervical spine, with 83% (n ϭ 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 dis- ease) 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: fibro- myalgia (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 pos- itive imaging study, subgroup analysis was warranted to elucidate pattern recognition for future diagnoses in this class of referred otalgia. Through a comprehensive retro- spective 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, cer- tain autoimmune diseases, musculoskeletal pain disorders; and 2) concomitant or recurrent neck pain on physical exam. Figure 2 Right foramenal stenosis (arrow) at C3 due to large Of those Group II patients who had a significant past med- osteophyte in a 69-year-old female with right-sided otalgia. ical history or neck pain, 88% (n ϭ 28) and 89% (n ϭ 32), Jaber et al Cervical spine causes for referred otalgia . . . 483 respectively, were found to have a positive imaging study. corticosteroid solution.9 In this current study we have Although these predictors correlated with a positive imag- shown that CSDD, diagnosed either through radiographic ing study, there was no statistical significance observed in or clinical evidence, is a major contributor to referred this group (P ϭ 0.41, significant history; and P ϭ 0.09, neck otalgia. CSDD-referred otalgia represented 37% of our pain, Fisher exact test, two-tailed). However, when the six patient population and was shown to be statistically non-CSDD patients were removed and a subgroup analysis higher in an elderly population (Group I vs Group II, P ϭ was conducted, a statistically significant association was 0.002). demonstrated between a positive imaging study and a sig- Imaging studies evaluate anatomy, rather than func- nificant medical history (97%, P ϭ 0.02) and/or neck pain tion, and are prone to false-positive and false-negative (97%, P ϭ 0.01). results. For example, Boden’s cervical MR study cites Cervical spine physical therapy (CSPT) was recom- abnormalities in nearly 20% of asymptomatic subjects.16 mended to all patients diagnosed with CSDD (n ϭ 45, Consequently, results of imaging studies must be inter- radiographic or clinical). Follow-up and compliance was preted within the context of each clinical case, with the difficult and consequently documentation for only 20 pa- converse being equally valid. Although both clinical and tients could be obtained. Nonetheless, all 20 individuals radiographic evidence were used to support the diagnosis expressed subjective pain relief following CSPT. 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 DISCUSSION otalgia. After ruling out non–cervical spine causes of referred ear pain, a targeted medical history of some type Despite published awareness regarding the many poten- of rheumatological disease, recurrent or concomitant tial causes of referred otalgia, diagnosis often eludes the neck pain coupled with a normal otologic exam highly most experienced physician.11 This may be due, in part, correlated with a positive imaging study of CSDD (P ϭ to the complex neuroanatomic innervation of the ear, 0.02, rheumatologic disease; P ϭ 0.01, neck pain). Kut- head, and neck, and therefore the inherent limitless tila et al have also described an association of several sources for referred ear pain. Two cohorts were catego- predictors, including and not limited to neck pain, gen- rized in this study, Group I (non–cervical spine causes of eral arthrosis, bruxism, age, and active need for TMJ referred otalgia) and Group II (cervical spine causes), in disease treatment, with secondary otalgia in an adult which we documented no fewer than 23 causes of re- population.17 Similar to this study, they reported that ferred otalgia representing all five nerve pathways (vide women presented with otalgia more often than men. This infra), with women reporting otalgia 4 times more fre- quently than men. These causes ranged from the benign published report very nicely outlines several general pre- etiology of whiplash (cervical spine nerves) to the more dictors in secondary otalgia similar to our observations serious mandibular tumor (CN V). The two most com- but falls short in implicating cervical spine causes as a mon nerve pathways for secondary otalgia were the tri- cause of ear pain. geminal nerve (n ϭ 56, 46%) and the superior cervi- The authors of this report believe that CSDD-referred cal plexus nerves (n ϭ 51, 42%). The most common otalgia is propagated through disease of the cervical etiology in Group I was TMJ dysfunction and in Group vertebrae and therefore is postural. This ear pain can be II, CSDD. Due to the length and extensive distribution ameliorated with physical therapy, and most studies sup- of the trigeminal nerve, it is not surprising that this port conservative treatment, such as cervicothoracic sta- nerve is most commonly involved in referred otalgia. bilization programs, combined with aerobic conditioning 18,19 This type of nonotogenic ear pain, especially involving in treating cervical spine disorders. With this in disorders of the temporal mandibular joint, is well doc- mind, we recommended outpatient physical therapy to all umented throughout oral surgery, otolaryngology, and our patients with CSDD-referred otalgia. Although doc- pain journals.12-14 umentation could be ascertained for only 20 patients, all Surprisingly, one group of patients with nonotogenic patients reported subjective pain relief. A prospective otalgia often overlooked are those diagnosed with cervi- study is currently underway at our institution to further cal spine sources, in particular CSDD.9,15 Referred otal- assess the long-term effects of CSPT for the treatment of gia due to cervical spine disease usually is described as referred otalgia due to degenerative changes in this ana- retroauricular or infra-auricular pain, which is constant tomic location. With the current study data in hand, a and often related to changes in neck position. As the diagnostic and treatment algorithm can be proposed and population in America ages, CSDD in the elderly will is outlined in Figure 3. If a female greater than 60 years begin to emerge as a major etiological source for referred of age with persistent otalgia and a negative otolaryngo- ear pain. A case report has been published implicating logic and dental work-up presents with similar charac- cervical spine arthritis with ear pain, which improved teristics outlined in this study, ie, rheumatologic disease with injection of the facet joint using a local anesthetic- and/or neck pain, a CT or MRI of the cervical spine has 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 IL; and the Center for Neuropharmacology and Neuroscience (Dr Feustel), source for her ear pain. In that case CSPT is indicated as Albany Medical College. a conservative and effective treatment strategy. 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 60153. E-mail address: [email protected]. CONCLUSION

The complex sensory innervation of the ear and the many etiological factors that can elicit nonotogenic ear pain may AUTHOR CONTRIBUTIONS result in a diagnostic challenge. Elderly citizens aged 65 and John P. Leonetti, major author, original designer of study, clinician; over constitute over 13% of the United States’ population James J. Jaber, chart review, analysis, and majority author; Amy Law- and as a consequence cervical spine degenerative diseases rason, chart review, minor author; Paul J. Feustel, statistical analysis, in the elderly will begin to emerge as a major etiological minor author. 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 FINANCIAL DISCLOSURE being secondary to CSDD. Conservative medical manage- ment involving cervical spine physical therapy can help None. improve or eliminate this type of referred otalgia. A pro- spective pilot study is currently underway to assess the current treatment strategy. REFERENCES

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