Am
J Otolaryngol
11:3w-369,199O
Otologic Pathophysiology in Patients With Human Immunodeficiency Virus KYLE
E. RAREY,
PHD
During the initial phase of clinical diagnosis and treatment of the manifestations of acquired immunodeficiency syndrome, involvement of the ear appeared minor. In the past several years, however, otologic disorders increasingly have been reported in individuals with human immunodeficiency virus (HIV), as well as in retrospective studies of such patients. The otologic data appear quite variable. Functionally, conductive hearing loss, unilateral and bilateral sudden or progressive sensorineural hearing losses, vertigo, and tinnitus have been reported. In addition, tissue responses in each division of the ear have been observed. Based on collective serologic and immunologic diagnostic assays, clinical histories, and temporal bone histopathology, otologic symptoms may not be the direct effect of HIV alone, but rather a combination of the effects of HIV infection coupled with that of opportunistic microorganisms and/or possible ototoxic effects of certain therapeutic agents. It is within this context that otologic findings in this population of subjects will be discussed. AM J OTOLARYNGOL 11:366-369. 0 1990 by W.B. Saunders Company. Key words: otologic disease, human immunodeficiency virus, acquired immunodeficiency syndrome, hearing loss, vertigo.
cipally T-helper cells, as well as a neurotropic virus. As a result, AIDS is characterized by an underlying suppression of cell-mediated response leading to the development of opportunistic infections and/or malignant tumors. Infections and tumors of the central nervous system are the chief complications of AIDS. It is not surprising, therefore, that reports identify the brain as the most frequently infected tissue.l*‘p4 The majority of patients with AIDS have been categorized into four major risk groups? sexually active homosexuals and bisexuals (65% to 75%), intravenous drug abusers (12% to 17%), Haitians (6%), and hemophiliacs (0.3% to 1%). While the preponderance of reported patients with HIV are adults, the number of cases of pediatric AIDS is no less impressive when compared with other pediatric diseases.5*6 The presentation of patients with HIV is consistent with their immunocompromised status. Initially, these patients are observed to have fever, malaise, weight loss, cough, and dyspnea. A diffuse lymphadenopathy is often noted. Based on laboratory analyses, these presenting symptoms and signs are the result of one or more secondary opportunistic infections. Opportunistic infections commonly seen in patients with HIV are caused by relatively nonviru-
Since the first diagnosis of acquired immunodeficiency syndrome (AIDS) in the early 198Os, the number of cases has grown exponentially, and the mortality of this disease continues to be of The Centers for Disease paramount concern.‘*’ Control has defined AIDS as a disease suggestive of an underlying immunodeficiency at the cellular level in persons who have no known underlying cause of such an immunodeficiency or any other cause of marked reduced resistance.’ The human immunodeficiency virus (HIV) is strongly considered to be the etiologic agent of AIDSzP3: HIV antibody has been consistently identified in patients with AIDS. A retrovirus, HIV has the enzyme reverse transcriptase, which functions to transcribe viral RNA to DNA, which is then incorporated into the genetic makeup of target cells. Human immunodeficiency virus has been shown to be a lymphotropic virus, attacking prinReceived May 16,1990,from the Departments of Anatomy and Cell Biology and Surgery (Division of Otolaryngology), College of Medicine, University of Florida, Gainesville, FL. Accepted for publication June 9, 1990. Address correspondence and reprint requests to Kyle E. Rarey, PhD, Box JI235, Department of Anatomy and Cell Bioloev. 1. Hillis Miller Health Science Center, Universitv of Florida, Gainesville, FL 32610. 0 1990 by W.B. Saunders Company. 0196-0709/90/1106-0001$5.00/O UI
I
366
367
RAREY
lent pathogens; however, in immunosuppressed individuals, such pathogens cause severe lifethreatening infections. Such agents include Pneumocystis carinii, Candida albicans, herpes simplex virus, varicella zoster, cytomegalovirus, Streptococcus pneumonia, Staphylococcus aureus, Mycobacterium tuberculosis, and Toxoplasma gondii. P carinii is the most common infection identified in patients with AIDS, and is the major listed cause of death in 50% of AIDS fatalities. OTOLARYNGOLOGIC MANIFESTATIONS IN PATIENTS WITH HUMAN IMMUNODEFICIENCY VIRUS It has been reported that between 41% and 71% of all manifestations of HIV are seen in the head and neck region.3 Among these are head and neck masses, sinusitis, nasal obstruction, dysphagia, chronic cough, difficulty in breathing, facial droop, and otologic disorders.““ Such problems are often found to be due to one or more of the following entities: Kaposi’s sarcoma (cutaneous and oral lesions), cervical lymphadenopathy, non-Hodgkin’s lymphoma, candidal infections (oral, laryngeal, pharyngeal, and/or esophageal), P carinii pneumonia, Mycobacterium, and fungal infections. Reported Otologic Features. Hearing loss, otalgia, otorrhea, vertigo, and tinnitus are among the chief otologic complaints of patients with AIDS.3’g Otologic diagnoses chiefly include otitis externa, otitis media, conductive hearing loss, sensorineural hearing loss (SNHL), mastoiditis, tympanic membrane perforation, and/or cholesteatoma. It appears that while most pathologies
TABLE 1. in Patients
Reported Cases of Otologic Manifestations With Human
Immunodeficiency
Virus
No. OF REPORT
Kohan et al9 Real et al” Gherman et al“’ Breda et alI3 Langford-Kuntz et-al* Poole et allo Hart et alI5 Smith and Canalis” Atkins (personal communication)
CASES
OTOLOCIC FEATURES
26
SNHL (n = 7);otitis (n = 17) Unilateral SNHL Unilateral mixed hearing loss Otic polyps Nondescriptive deafness
1
1 2 2 1 1 5
30
Otitis media Central, brain stem Bilateral SNHL (n = 4); unilateral SNHL otosyphilis (n = I] Low-frequency SNHL (n = 14);high-frequency SNHL (n = 10)
of the external and middle ear were reported to resolve or to return to normal limits after treatment and/or surgical intervention, those with SNHL remained unchanged. Both conductive and sensorineural losses have been documentedg-15 (Table 1). Conductive hearing loss has been reported to be less frequent than SNHL in patients with HIV.3 Causes of conductive hearing loss include external otitis, Kaposi’s sarcoma, polyps in the external ear canal, and various subtypes of otitis media.g,‘3,14 The list of etiologic agents of SNHL in patients with HIV is less well defined than that established for conductive hearing loss. Given the basic premise that the causes of SNHL are multifactorial previously, this new epidemic of HIV infections has added another suspicious etiologic agent. It is difficult to determine whether SNHL is caused by HIV infection and/or by other microorganisms in the peripheral auditory and vestibular endorgans, or in more central regions. The characteristics of SNHL in patients with HIV are not uniformly defined. The degree of hearing loss, range of loss, and even incidence appear variable. Some of the variability in the degree of SNHL may be due to the criteria used to evaluate the condition. In general, a threshold shift 220 dB has been a standard criterion. Hearing loss in the high frequencies was more commonly reported than low-frequency hearing losses in patients with HIV. Assessment of hearing loss has been performed by traditional audiometry, including brain stem audiometry. Delayed latencies of brain stem auditory-evoked responses have been observed in patients with HIV, suggesting neuropathies of the central auditory and vestibular regions.15 The incidence of SNHL in patients with HIV ranges from 23% to 49%.3,g The degree of variability in the incidence of SNHL in this group also may be due to the possible ototoxicity of antiviral and antibiotic agents. Preliminary studies involving the culture of ear tissues have demonstrated the presence of viral antigens as well as bacterial and fungal microorganisms in patients diagnosed with HIV, but with no noticeable hearing disorder (Davis and Rarey, personal communication]. It may not be surprising that in patients who are HIV-positive and otologically asymptomatic, the presence of HIV antigens and/or histopathologic changes would be identified in postmortem ear tissues. Postmortem neuropathologic changes have been reported in over two thirds of patients who tested positive with HIV; however, neurologic findings were detectable in only approximately one third. Various virulent and nonvirulent organisms have long been implicated in hearing impairment
OTOLOGIC PATHOPHYSIOLOGY
368
and/or vestibular disequilibrium. Viral agents have been implicated in SNHL for several decades,16-29 but the evidence for such viralinduced hearing loss principally has been circumstantial. Traditionally, the difficulty in determining the role of viral agents in the pathophysiology of the ear is that, because in many cases they were not also the cause of death, substantial time had elapsed between the episode of virus-associated ear dysfunction and tissue analysis; furthermore, an excessive interval between death and the harvesting of ear tissues often resulted in poorly preserved tissue specimens inadequate for electron microscopy. Using the new immunocytochemistry techniques, our ability to associate functional and/or structural alterations in ear tissues to viruses through the detection of viral antigens in ear tissues from patients with HIV certainly will be enhanced. The role of the DNA family of viruses has been the least understood of all viruses in the pathophysiology of hearing and equilibrium. Measles, varicella, herpes simplex virus (types I and II), Epstein-Barr virus, adenovirus, cytomegalovirus, and papovaviruses have the ability to exist in latent forms for long periods of time.30,31 Interestingly, multiple viral agents were positively identified in single serum samples by serologic analysis in approximately 50% of patients diagnosed with idiopathic sudden hearing 10~s.‘~ Djupesland et al” reported the identification of viral infection in 12 subjects from a group of 34 patients who were diagnosed with SNHL. Normal middle ear function was noted in each of the 12 subjects. A moderate high-frequency hearing loss was detected in seven subjects; varicella zoster infection was identified in six of these subjects, and herpes infection in one. A low-frequency hearing loss was measured in the other five subjects, of whom varicella zoster infections were identified in three and mumps infection in the other two. Such data underline the complexity of determining the cause of ear disorders when multiple viruses may be present within the ear tissues of patients with HIV. In summary, otologic manifestations will continue to be identified in patients with HIV. Only by the assimilation of serologic, morphologic, physiologic, immunologic, and laboratory data will the primary causative agents of such manifestations in patients with HIV be identified and appropriate clinical management and treatment provided. Acknowledgment. The helpful comments of Drs Lynn Larkin and Chris Post in the preparation of this manuscript are gratefully acknowledged.
OF HIV
References 1. Snider WD, Simpson DM, Nielsen S, et al: Neurological complications of acquired immune deficiency syndrome: Analysis of 50 patients. Ann Neurol, 1983; 14:403-418 2. Levy RM, Bredesen DE, Rosenblum ML: Neurological manifestations of the acquired immunodeficiency syndrome [AIDS]: Experience at UCSF and review of the literature. J Neurosurg 1985; 62:475-495 3. Sooy CD: The impact of AIDS on otolaryngology-head and neck surgery. Otolaryngol Head Neck Surg 1987; l:l-28 4. Ho DD, Rota TR, Schooley RT, et al: Isolation of HTLV-III from cerebrospinal fluid and neural tissues of patients with neurologic syndromes related to the acquired immunodeficiency syndrome. N Engl J Med 1987; 313:1493-1497 5. Williams MA: Head and neck findings in pediatric acquired immune deficiency syndrome. Laryngoscope 1987; 97:713-716 6. Marcusen
DC, Sooy CD: Otolaryngologic and head and neck manifestations of acquired immunodeficiency syndrome (AIDS]. Laryngoscope 1985; 95:401-405 7. Rosenberg RA, Schneider KL, Cohen NL: Head and neck presentations of acquired immunodeficiency syndrome. Laryngoscope 1984; 94:642-646 8. Langford-Kuntz A, Reichart P, Pohle HD: Impairment of crania-facial nerves due to AIDS: Report of 2 cases. Int J Oral Maxillofac Surg 1988; 17:227-229 9. Kohan D, Rothstein SG, Cohen NL: Otologic disease in patients with acquired immunodeficiency syndrome. Ann Otol Rhino1 Laryngol 1988; 97:636-640 10. Poole MD, Postma D, Cohen MS: Pyogenic otorhinologic infections in acquired immune deficiency syndrome. Arch Otolaryngol 1984; 110:130-131 11. Real R, Thomas M, Gerwin JM: Sudden hearing loss and acquired immunodeficiency syndrome. Otolaryngol Head Neck Surg 1987; 97:409-412 12. Smith ME, Canalis RF: Otologic manifestations of AIDS: The otosyphilis connection. Laryngoscope 1989; 99:365-372 13. Breda SD, Hammerschlag PE, Gigliotti F, et al: Pneumocystis carnii in the temporal bone as a primary manifestation of the acquired immunodeficiency syndrome. Ann Otol Rhino1 Laryngol 1988; 97:427-431 14. Gherman CR, Ward RR, Bassis ML: Pneumocystis carinii otitis media and mastoiditis as the initial manifestation of the acquired immunodeficiency syndrome. Am J Med 1988; 85:250-252 15. Hart CW, Cokely CG, Schupbach
J, et al: Neurotologic findings of a patient with acquired immune deficiency syndrome. Ear Hear 1989; 10:68-76 16. Bordley LE, Brookhouser PE, Worthington EL: Viral infections and hearing: A critical review of the literature, 19691970. Laryngoscope 1972; 82:557-577 17. Davis LE: Infections of the labyrinth, in Cummings C (ed): Otolaryngology-Head and Neck Surgery. St Louis, MO, 1986, pp 3137-3147 18. Davis LE, Johnsson LG: Viral infections of the inner ear: Clinical, virologic, and pathologic studies in humans and animals. Am J Otolaryngol 1983; 4:347-362 19. Igarashi M, Weber SC, Alford BR, et al: Temporal bone findings in cryptococcal meningitis. Arch Otolaryngol 1975; 101:577-583 20. Jaffe BF: Sudden
deafness-An otologic emergency. Arch Otolaryngol 1967; 86:81-86 21. Lindsay JR: Viral labyrinthitis-Histopathologic characteristics. Acta Otolaryngol (Stockh) 1967; 63:138-143 22. Djupesland G, Flottorp G, Degre M, et al: Cochlear hearing loss and viral infection. Acta Otolaryngol (Stockh) 1979; 87:247-254 23. Veltri RW, Wilson WR, Sprinkle
PM, et al: The implication of viruses in idiopathic sudden hearing loss (ISHL): Primary infection or reactivation of latent vi&es? Otolaryngol Head Neck Surg 1981; 89:137-141 24. Karmody CS: Viral labyrinthitis: Early pathology in the human. Laryngoscope 1983; 93:1527-1533
369
RAREY
25. Aubry M, Pialoux P: Involvement of the ear and of the vestibular-labyrinthine tract in viral infections, in Debre R, Celers ,\ I (edsl: Clinical Virolosrv. The Evaluation & Manaaement of Human Viral Infections. Philadelphia, PA, Saunders, 1970,~~ 751-758 26. Davis GL: Cytomegalovirus in the inner ear. Case report and electron microscopic study. Ann Otol Rhino1 Laryngol 1969; 78:1179-1188 27. Davis LE, Fiber F, James CG, et al: Cytomegalovirus isolation from a human inner ear. Ann Otol 1979; 88:424-426 I
..,
J Otolaryngol
11:3w-369,199O
Otologic Pathophysiology in Patients With Human Immunodeficiency Virus KYLE
E. RAREY,
PHD
During the initial phase of clinical diagnosis and treatment of the manifestations of acquired immunodeficiency syndrome, involvement of the ear appeared minor. In the past several years, however, otologic disorders increasingly have been reported in individuals with human immunodeficiency virus (HIV), as well as in retrospective studies of such patients. The otologic data appear quite variable. Functionally, conductive hearing loss, unilateral and bilateral sudden or progressive sensorineural hearing losses, vertigo, and tinnitus have been reported. In addition, tissue responses in each division of the ear have been observed. Based on collective serologic and immunologic diagnostic assays, clinical histories, and temporal bone histopathology, otologic symptoms may not be the direct effect of HIV alone, but rather a combination of the effects of HIV infection coupled with that of opportunistic microorganisms and/or possible ototoxic effects of certain therapeutic agents. It is within this context that otologic findings in this population of subjects will be discussed. AM J OTOLARYNGOL 11:366-369. 0 1990 by W.B. Saunders Company. Key words: otologic disease, human immunodeficiency virus, acquired immunodeficiency syndrome, hearing loss, vertigo.
cipally T-helper cells, as well as a neurotropic virus. As a result, AIDS is characterized by an underlying suppression of cell-mediated response leading to the development of opportunistic infections and/or malignant tumors. Infections and tumors of the central nervous system are the chief complications of AIDS. It is not surprising, therefore, that reports identify the brain as the most frequently infected tissue.l*‘p4 The majority of patients with AIDS have been categorized into four major risk groups? sexually active homosexuals and bisexuals (65% to 75%), intravenous drug abusers (12% to 17%), Haitians (6%), and hemophiliacs (0.3% to 1%). While the preponderance of reported patients with HIV are adults, the number of cases of pediatric AIDS is no less impressive when compared with other pediatric diseases.5*6 The presentation of patients with HIV is consistent with their immunocompromised status. Initially, these patients are observed to have fever, malaise, weight loss, cough, and dyspnea. A diffuse lymphadenopathy is often noted. Based on laboratory analyses, these presenting symptoms and signs are the result of one or more secondary opportunistic infections. Opportunistic infections commonly seen in patients with HIV are caused by relatively nonviru-
Since the first diagnosis of acquired immunodeficiency syndrome (AIDS) in the early 198Os, the number of cases has grown exponentially, and the mortality of this disease continues to be of The Centers for Disease paramount concern.‘*’ Control has defined AIDS as a disease suggestive of an underlying immunodeficiency at the cellular level in persons who have no known underlying cause of such an immunodeficiency or any other cause of marked reduced resistance.’ The human immunodeficiency virus (HIV) is strongly considered to be the etiologic agent of AIDSzP3: HIV antibody has been consistently identified in patients with AIDS. A retrovirus, HIV has the enzyme reverse transcriptase, which functions to transcribe viral RNA to DNA, which is then incorporated into the genetic makeup of target cells. Human immunodeficiency virus has been shown to be a lymphotropic virus, attacking prinReceived May 16,1990,from the Departments of Anatomy and Cell Biology and Surgery (Division of Otolaryngology), College of Medicine, University of Florida, Gainesville, FL. Accepted for publication June 9, 1990. Address correspondence and reprint requests to Kyle E. Rarey, PhD, Box JI235, Department of Anatomy and Cell Bioloev. 1. Hillis Miller Health Science Center, Universitv of Florida, Gainesville, FL 32610. 0 1990 by W.B. Saunders Company. 0196-0709/90/1106-0001$5.00/O UI
I
366
367
RAREY
lent pathogens; however, in immunosuppressed individuals, such pathogens cause severe lifethreatening infections. Such agents include Pneumocystis carinii, Candida albicans, herpes simplex virus, varicella zoster, cytomegalovirus, Streptococcus pneumonia, Staphylococcus aureus, Mycobacterium tuberculosis, and Toxoplasma gondii. P carinii is the most common infection identified in patients with AIDS, and is the major listed cause of death in 50% of AIDS fatalities. OTOLARYNGOLOGIC MANIFESTATIONS IN PATIENTS WITH HUMAN IMMUNODEFICIENCY VIRUS It has been reported that between 41% and 71% of all manifestations of HIV are seen in the head and neck region.3 Among these are head and neck masses, sinusitis, nasal obstruction, dysphagia, chronic cough, difficulty in breathing, facial droop, and otologic disorders.““ Such problems are often found to be due to one or more of the following entities: Kaposi’s sarcoma (cutaneous and oral lesions), cervical lymphadenopathy, non-Hodgkin’s lymphoma, candidal infections (oral, laryngeal, pharyngeal, and/or esophageal), P carinii pneumonia, Mycobacterium, and fungal infections. Reported Otologic Features. Hearing loss, otalgia, otorrhea, vertigo, and tinnitus are among the chief otologic complaints of patients with AIDS.3’g Otologic diagnoses chiefly include otitis externa, otitis media, conductive hearing loss, sensorineural hearing loss (SNHL), mastoiditis, tympanic membrane perforation, and/or cholesteatoma. It appears that while most pathologies
TABLE 1. in Patients
Reported Cases of Otologic Manifestations With Human
Immunodeficiency
Virus
No. OF REPORT
Kohan et al9 Real et al” Gherman et al“’ Breda et alI3 Langford-Kuntz et-al* Poole et allo Hart et alI5 Smith and Canalis” Atkins (personal communication)
CASES
OTOLOCIC FEATURES
26
SNHL (n = 7);otitis (n = 17) Unilateral SNHL Unilateral mixed hearing loss Otic polyps Nondescriptive deafness
1
1 2 2 1 1 5
30
Otitis media Central, brain stem Bilateral SNHL (n = 4); unilateral SNHL otosyphilis (n = I] Low-frequency SNHL (n = 14);high-frequency SNHL (n = 10)
of the external and middle ear were reported to resolve or to return to normal limits after treatment and/or surgical intervention, those with SNHL remained unchanged. Both conductive and sensorineural losses have been documentedg-15 (Table 1). Conductive hearing loss has been reported to be less frequent than SNHL in patients with HIV.3 Causes of conductive hearing loss include external otitis, Kaposi’s sarcoma, polyps in the external ear canal, and various subtypes of otitis media.g,‘3,14 The list of etiologic agents of SNHL in patients with HIV is less well defined than that established for conductive hearing loss. Given the basic premise that the causes of SNHL are multifactorial previously, this new epidemic of HIV infections has added another suspicious etiologic agent. It is difficult to determine whether SNHL is caused by HIV infection and/or by other microorganisms in the peripheral auditory and vestibular endorgans, or in more central regions. The characteristics of SNHL in patients with HIV are not uniformly defined. The degree of hearing loss, range of loss, and even incidence appear variable. Some of the variability in the degree of SNHL may be due to the criteria used to evaluate the condition. In general, a threshold shift 220 dB has been a standard criterion. Hearing loss in the high frequencies was more commonly reported than low-frequency hearing losses in patients with HIV. Assessment of hearing loss has been performed by traditional audiometry, including brain stem audiometry. Delayed latencies of brain stem auditory-evoked responses have been observed in patients with HIV, suggesting neuropathies of the central auditory and vestibular regions.15 The incidence of SNHL in patients with HIV ranges from 23% to 49%.3,g The degree of variability in the incidence of SNHL in this group also may be due to the possible ototoxicity of antiviral and antibiotic agents. Preliminary studies involving the culture of ear tissues have demonstrated the presence of viral antigens as well as bacterial and fungal microorganisms in patients diagnosed with HIV, but with no noticeable hearing disorder (Davis and Rarey, personal communication]. It may not be surprising that in patients who are HIV-positive and otologically asymptomatic, the presence of HIV antigens and/or histopathologic changes would be identified in postmortem ear tissues. Postmortem neuropathologic changes have been reported in over two thirds of patients who tested positive with HIV; however, neurologic findings were detectable in only approximately one third. Various virulent and nonvirulent organisms have long been implicated in hearing impairment
OTOLOGIC PATHOPHYSIOLOGY
368
and/or vestibular disequilibrium. Viral agents have been implicated in SNHL for several decades,16-29 but the evidence for such viralinduced hearing loss principally has been circumstantial. Traditionally, the difficulty in determining the role of viral agents in the pathophysiology of the ear is that, because in many cases they were not also the cause of death, substantial time had elapsed between the episode of virus-associated ear dysfunction and tissue analysis; furthermore, an excessive interval between death and the harvesting of ear tissues often resulted in poorly preserved tissue specimens inadequate for electron microscopy. Using the new immunocytochemistry techniques, our ability to associate functional and/or structural alterations in ear tissues to viruses through the detection of viral antigens in ear tissues from patients with HIV certainly will be enhanced. The role of the DNA family of viruses has been the least understood of all viruses in the pathophysiology of hearing and equilibrium. Measles, varicella, herpes simplex virus (types I and II), Epstein-Barr virus, adenovirus, cytomegalovirus, and papovaviruses have the ability to exist in latent forms for long periods of time.30,31 Interestingly, multiple viral agents were positively identified in single serum samples by serologic analysis in approximately 50% of patients diagnosed with idiopathic sudden hearing 10~s.‘~ Djupesland et al” reported the identification of viral infection in 12 subjects from a group of 34 patients who were diagnosed with SNHL. Normal middle ear function was noted in each of the 12 subjects. A moderate high-frequency hearing loss was detected in seven subjects; varicella zoster infection was identified in six of these subjects, and herpes infection in one. A low-frequency hearing loss was measured in the other five subjects, of whom varicella zoster infections were identified in three and mumps infection in the other two. Such data underline the complexity of determining the cause of ear disorders when multiple viruses may be present within the ear tissues of patients with HIV. In summary, otologic manifestations will continue to be identified in patients with HIV. Only by the assimilation of serologic, morphologic, physiologic, immunologic, and laboratory data will the primary causative agents of such manifestations in patients with HIV be identified and appropriate clinical management and treatment provided. Acknowledgment. The helpful comments of Drs Lynn Larkin and Chris Post in the preparation of this manuscript are gratefully acknowledged.
OF HIV
References 1. Snider WD, Simpson DM, Nielsen S, et al: Neurological complications of acquired immune deficiency syndrome: Analysis of 50 patients. Ann Neurol, 1983; 14:403-418 2. Levy RM, Bredesen DE, Rosenblum ML: Neurological manifestations of the acquired immunodeficiency syndrome [AIDS]: Experience at UCSF and review of the literature. J Neurosurg 1985; 62:475-495 3. Sooy CD: The impact of AIDS on otolaryngology-head and neck surgery. Otolaryngol Head Neck Surg 1987; l:l-28 4. Ho DD, Rota TR, Schooley RT, et al: Isolation of HTLV-III from cerebrospinal fluid and neural tissues of patients with neurologic syndromes related to the acquired immunodeficiency syndrome. N Engl J Med 1987; 313:1493-1497 5. Williams MA: Head and neck findings in pediatric acquired immune deficiency syndrome. Laryngoscope 1987; 97:713-716 6. Marcusen
DC, Sooy CD: Otolaryngologic and head and neck manifestations of acquired immunodeficiency syndrome (AIDS]. Laryngoscope 1985; 95:401-405 7. Rosenberg RA, Schneider KL, Cohen NL: Head and neck presentations of acquired immunodeficiency syndrome. Laryngoscope 1984; 94:642-646 8. Langford-Kuntz A, Reichart P, Pohle HD: Impairment of crania-facial nerves due to AIDS: Report of 2 cases. Int J Oral Maxillofac Surg 1988; 17:227-229 9. Kohan D, Rothstein SG, Cohen NL: Otologic disease in patients with acquired immunodeficiency syndrome. Ann Otol Rhino1 Laryngol 1988; 97:636-640 10. Poole MD, Postma D, Cohen MS: Pyogenic otorhinologic infections in acquired immune deficiency syndrome. Arch Otolaryngol 1984; 110:130-131 11. Real R, Thomas M, Gerwin JM: Sudden hearing loss and acquired immunodeficiency syndrome. Otolaryngol Head Neck Surg 1987; 97:409-412 12. Smith ME, Canalis RF: Otologic manifestations of AIDS: The otosyphilis connection. Laryngoscope 1989; 99:365-372 13. Breda SD, Hammerschlag PE, Gigliotti F, et al: Pneumocystis carnii in the temporal bone as a primary manifestation of the acquired immunodeficiency syndrome. Ann Otol Rhino1 Laryngol 1988; 97:427-431 14. Gherman CR, Ward RR, Bassis ML: Pneumocystis carinii otitis media and mastoiditis as the initial manifestation of the acquired immunodeficiency syndrome. Am J Med 1988; 85:250-252 15. Hart CW, Cokely CG, Schupbach
J, et al: Neurotologic findings of a patient with acquired immune deficiency syndrome. Ear Hear 1989; 10:68-76 16. Bordley LE, Brookhouser PE, Worthington EL: Viral infections and hearing: A critical review of the literature, 19691970. Laryngoscope 1972; 82:557-577 17. Davis LE: Infections of the labyrinth, in Cummings C (ed): Otolaryngology-Head and Neck Surgery. St Louis, MO, 1986, pp 3137-3147 18. Davis LE, Johnsson LG: Viral infections of the inner ear: Clinical, virologic, and pathologic studies in humans and animals. Am J Otolaryngol 1983; 4:347-362 19. Igarashi M, Weber SC, Alford BR, et al: Temporal bone findings in cryptococcal meningitis. Arch Otolaryngol 1975; 101:577-583 20. Jaffe BF: Sudden
deafness-An otologic emergency. Arch Otolaryngol 1967; 86:81-86 21. Lindsay JR: Viral labyrinthitis-Histopathologic characteristics. Acta Otolaryngol (Stockh) 1967; 63:138-143 22. Djupesland G, Flottorp G, Degre M, et al: Cochlear hearing loss and viral infection. Acta Otolaryngol (Stockh) 1979; 87:247-254 23. Veltri RW, Wilson WR, Sprinkle
PM, et al: The implication of viruses in idiopathic sudden hearing loss (ISHL): Primary infection or reactivation of latent vi&es? Otolaryngol Head Neck Surg 1981; 89:137-141 24. Karmody CS: Viral labyrinthitis: Early pathology in the human. Laryngoscope 1983; 93:1527-1533
369
RAREY
25. Aubry M, Pialoux P: Involvement of the ear and of the vestibular-labyrinthine tract in viral infections, in Debre R, Celers ,\ I (edsl: Clinical Virolosrv. The Evaluation & Manaaement of Human Viral Infections. Philadelphia, PA, Saunders, 1970,~~ 751-758 26. Davis GL: Cytomegalovirus in the inner ear. Case report and electron microscopic study. Ann Otol Rhino1 Laryngol 1969; 78:1179-1188 27. Davis LE, Fiber F, James CG, et al: Cytomegalovirus isolation from a human inner ear. Ann Otol 1979; 88:424-426 I
..,
