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Human Immunodeficiency Virus in Otorhinoloaryngology - HIV in ENT
 
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Otorhinolaryngological Manifestations of Human Immunodeficiency Virus Infection in Bangalore City Population

Authors:   Chidananda Devasamudra1 and Wilma Delphine Silvia Chickballapur Rayappa2

Institution: 

(1) Assistant Professor, Dept of Otorhinolaryngology, Sapthagiri Institute of Medical Sciences & Research Center, Bengaluru -560090, Karnataka, India.
(2) Professor and Head, Department of Biochemistry, Sapthagiri Institute of Medical Sciences and Research Center, Bangaluru, 560090, Karnataka, India

Corresponding Author: 

Dr. Wilma Delphine Silvia CR. MD., DNB
Professor & Head of Department
Department of Biochemistry
Sapthagiri Institute of Medical Sciences and Research Center
#15, Chikkasandra, Hesaraghatta Main Road, Bangaluru 560090, Karnataka, India.
Email:  widel@rediffmail.com 

Abstract:

Human Immunodeficiency Virus (HIV) Infection is a complicated disorder of the body's defense system.  It is a fatal multisystem disease that causes breakdown of a part of the body’s immune system making it vulnerable to a variety of unusual life-threatening illnesses.  The objective of this study was to describe the various Otorhinolaryngological manifestations in HIV sero-positive patients.  100 cases were examined which had Otolaryngological and Head and Neck manifestations.  The most common age group with ENT manifestations of HIV was found to be between 4 to 56 years with the male-to-female ratio being 2.12:1.  Oral and Oropharyngeal manifestations of HIV were noted to be the most common in the study group at 41%, followed by otological manifestations at 21%.  Oral candidiasis was being the most frequent diagnosis, followed by with sensori-neural hearing loss at 11%.  Nose and paranasal sinus manifestations occured in 18% of patients, with nasopharyngeal lymphoid tissue hypertrophy noted to be the most common.  Neck manifestations occured in 16% of patients and herpetic infections in 4%.  Testing for HIV antibodies should be made mandatory in patients presenting with unusual ENT manifestations.  In HIV seropositive individuals, periodic ENT examination is required for early diagnosis, to monitor disease progression, to alleviate symptoms of opportunistic infections and improve the quality of life.

 
Introduction:

Human Immunodeficiency Virus Infection is a fatal illness, which reduces the body's immunity and leaves the victim vulnerable to life-threatening opportunistic infections, neurological disorders, or unusual malignancies.1

In HIV-infected adults, oral ulcers occur more frequently, last longer and produce more painful symptoms than in immunocompetent individuals.  Oral aphthous ulcers observed during the course of HIV infection and may be severe, resulting in significant morbidity in these patients.  Such manifestations may interfere with oral functions and alter patients' quality of life.2

Often, the otolaryngologist is the primary physician who diagnoses the HIV infection.  With the increase in the number of AIDS cases, it is important for otolaryngologists to become aware of the otolaryngological manifestations.  Early detection of clinically undiagnosed cases of HIV and timely intervention along with appropriate antiretroviral therapy, improve the quality of life and survival rates.3  Hence, the aim of the study was to determine the incidence of otolaryngological manifestations in undiagnosed cases of HIV.

Methods:

This was a prospective study conducted over a period of one and a half years.  A hundred patients of all age groups and both sexes, who were referred to the ENT out patient department (OPD) with a seropositive diagnosis of HIV, along with patients admitted to Victoria Hospital and Bowring & Lady Curzon Hospitall, were included in the study group. 

The HIV positive patients were determined based on WHO/NACO guidelines.4  A serum testing positive on all three rapid tests was reported positive.  Serum reactive in the first and second rapid and non-reactive in third test was considered equivocal/borderline.  Such individuals were retested after a couple of weeks.  The three rapid tests used for the diagnosis of HIV seropositivity were the: Coomb method, Capillus method, and Tridot method.  Ethical clearance was obtained from the institution and informed consent was obtained from the patients.

Patients with immunosuppressive disorders like diabetes mellitus, malignancy and immunosuppressive treatment and those who were on antiretroviral therapy were excluded from the study.  Antiretroviral therapy can alter the disease process and mask presenting symptoms.

In every case, a detail history was elicited, with emphasis on sexual habits, intravenous drug abuse, alcoholism and history of blood transfusion.  Family history and marital status were also noted.  Besides the history of presenting illness, any history of otolaryngological and head and neck complaints were also determined.

A detailed physical examination, including a complete ENT examination was carried out on each of the patients in the ENT OPD. The findings, thus, obtained were recorded in a specifically constructed proforma.  All the cases that were included in the study underwent the following relevant investigations:  HIV 1, 2 and 3, culture and sensitivity in relevant cases, X–ray of the paranasal sinuses, chest, neck and mastoid; CT Scan/MRI of the Head and neck, Fine Needle Aspiration Culture of lymph nodes, KOH preparation, biopsy for histopathological examination, audiometry, and upper GI endoscopy.

Statistical Analysis:   Data analysis was carried out using the Statistical Package for Social Science (SPSS) 17.0.

 
Results:

A hundred seropositive cases (Table 1) of HIV were included in this study with the male-to- female ratio being 2.12:1.  Oral and Oropharyngeal manifestations were noted to be the most common manifestations of HIV in the study group (41%), followed by otological manifestations (21%), nose and paranasal sinus manifestations (18%), neck manifestations (16%) and others (4%) - see Table 2. 

In the oral and oropharyngeal manifestations group of patients, oral candidiasis was found to be the most common.  Nasopharyngeal lymphoid tissue hypertrophy was noted to be the most common nose and paranasal sinus manifestation.  Among the otological manifestations, sensori-neural hearing loss was most frequently seen.  Atypical ENT manifestations such as temporal bone malignancy with facial nerve palsy and early onset oral cavity malignancy were found in association with some HIV seropositive individuals.  Presenting complaints of the patients studied have been depicted in Table 3.   

Table 1:  List of investigations carried out to confirm HIV infection Table 2:  Ear, Nose, Throat, Neck manifestations of HIV Table 3: Presenting complaints of HIV infected patients

Table 1:  List of investigations carried out to confirm HIV infection

Table 2: Ear, Nose, Throat, Neck manifestations of HIV

Table 3: Presenting complaints of HIV infected patients


Discussion:

The increased prevalence of HIV has resulted in a greater number of HIV infected patients presenting to Otolaryngologists.  HIV disease is associated with a variety of problems in the head and neck region.  As many as 70% of HIV infected patients eventually develop such conditions.  Marcusen, et al., in 1985, studied 899 patients with AIDS and found that 165 patients (41%) had symptoms related to Otolaryngology.5  Prasad, et al.3 (2006) studied 986 patients with HIV, found that 779 patients (79%) had symptoms related to Otolaryngology.  In the present study, the most common age group was 25-45 years, which comprised 78% of the total HIV positive patients.  This group comprises the most economically productive age group.  There was also a male-to-female ratio of 3:1.  In addition, we found that 68% of the patients were male (ratio of 2.12:1).  As with other studies, the present study also shows male preponderance.  Male patients are more prone to high-risk activities which predisposes them to HIV infection. 

The causes of most otolaryngologic manifestations of HIV disease fall into the following three categories:  Infections, neoplasms, and primary neurologic damage caused by HIV.  In the present study, oral candidiasis is the most common manifestation, followed by sensori-neural hearing loss and tonsillar hypertrophy.  One of the most common regions of the head and neck in which HIV–related pathology occurs is the oral cavity and oropharynx.  William, et al. in 1987, found that 80% of patients in their study group had oral and oropharyngeal manifestations.7

Figure. 1 Oral candidiasisIn conformity with the study by Deb, et al.,8 the present study shows 41% of HIV positive patients with oral and oropharyngeal manifestations (Figure 1: Oral Candidiasis - to the right).  Oral Candidiasis (thrush) is by far the most common oral condition of HIV infection. The prevalence of Candidiasis has been reported to be from 30% to 90% among HIV positive in various reported research studies.  Silverman, et al.9 in 1986, in their study reported oral candidiasis in 87% of HIV positive cases.

Gileva, et al.10 in 2004 and Prasad, et al.3 in 2006, noted Herpes Simplex in 15.4% and 3% of HIV positive cases, respectively.  The present study found 2% of HIV positive cases with oral Herpes Simplex.

Figure. 2 Apthus ulcerRecurrent aphthous ulcerations are one of the most painful and troublesome conditions of the oral cavity (Figure 2: Apthus Ulcer - to the right). HIV- infected patients frequently present with giant aphthous ulcerations (more than 2 centimeters in diameter), the cause of which is uncertain.6  Gileva, et al.10 (2004) reported that 2% of cases had aphthous ulcers.  Prasad, et al.3 (2006) reported 6% of cases with aphthous ulcerations.  The present study found 9% of HIV positive cases with aphthous ulcerations, which approximates the incidence observed by Prasad, et al.3  In the present study, out of 100 cases 5 cases were diagnosed as angular chelitis.  Tonsils and adenoids are part of the lymphoid system.  Lymphoid hyperplasia is common in the HIV population.  An increased incidence of tonsillar and adenoid hyperplasia has been shown to occur with HIV infection.  The study Figure 3: Hypertrophied tonsilsconducted by Buda, et al.11 looked at 6 HIV positive individuals who were referred for sleep evaluation, four had enlarged tonsils.11  In the present study, out of 100 HIV positive cases 10 cases of tonsillar hypertrophy were diagnosed (Figure 3: Hypertrophic Tonsils - to the right).
   

Several studies of patients infected with HIV have described a 30% to 68% prevalence of sinusitis.12  Prasad, et al.3 (2006) showed that 26% of patients had nasal and paranasal sinus manifestations, while, the present study found 18% of cases with nasal and paranasal sinus manifestations.

The incidence of “NPLT (nasopharyngeal lymphoid tissue) hypertrophy” is higher in patients with HIV-1 with persistent generalized lymphadenopathy (PGL) when cervical lymph nodes are also enlarged.13   In the present study, the incidence was 8%.

William, et al.7 in 1987 noted otological manifestation in 80% of HIV positive cases and Prasad, et al.3 in 2006, in 20% of HIV positive cases. The present study found 21% of HIV positive cases with otological manifestations, which is comparable with the study by Prasad, et al.3  Unilateral or bilateral SNHL occurs in 21% to 49% of HIV infected patients.14  Prasad, et al.3 (2006) found SNHL in 2% of HIV positive cases.  In the present study, 11 patients had sensorineural hearing loss (SNHL).  The possible etiology is a primary infection by HIV of either the central nervous system or peripheral auditory nerve.  Otitis media was found in 13% of HIV positive cases in the study conducted by Prasad, et al.3   In crontradistinction, the present study, only 2 cases of otitis media were found.  Prasad, et al.3 also reported otitis externa in 5% of HIV positive cases.  In comparison, the present study found otitis externa in 4% of HIV positive cases.  The prevalence of facial nerve palsy in patients with HIV infection is higher than in the general population.15  In the present study, 3 cases of facial paralysis were diagnosed.  However, only 12 cases of bilateral facial palsy among HIV infected patients have been reported worldwide over the last 20 years.16

The cause of neck masses in this population can be divided into four categories:  HIV lymphadenopathy, infectious processes, parotid disease and neoplasms17 (Figure 4, 5 and 6 - see below).  The most common finding in the neck is cervical lymphadenopathy.  Cervical lymphadenopathy is seen as a part of persistent generalized lymphadenopathy in AIDS patients.  Marcussen, et al.5 (1985) found 8% of cases with cervical lymphadenopathy.  In the present study, 12% of cases were found to have cervical lymphadenopathy, which is similar to the findings of Ndjolo A, et al.18    Ndjolo, et al.,18 (2004) also found that 8.23% of HIV positive cases had salivary gland disease, while, the present study found 4% of HIV positive cases with salivary gland disease.  In the present study, however, not a single case was found of homosexual mode of transmission and Kaposi’s Sarcoma. 

Figure. 4 Parotid swelling ( Lymphoepithelial cyst) Figure. 5 Tubercular lymphadenitis Figure. 6 Neck abscess (drained)
Figure. 4 Parotid swelling (Lymphoepithelial cyst) Figure. 5 Tubercular lymphadenitis Figure. 6 Neck abscess (drained)

  
Conclusion:

While some ENT findings are nearly exclusive to HIV seropositive individuals, many are also found in the general population.  However, HIV infected individuals often have an increased prevalence or severity, atypical presentation or difficulty in treatment.  Patients presenting with recurrent Oral Candidiasis and recurrent Rhinosinusitis (pansinusitis) to the OPD should raise a high index of suspicion for HIV seropositivity.  Testing for HIV antibodies should be made mandatory in patients presenting with unusual ENT manifestations.  Early onset malignancy should draw suspicion for HIV seropositivity.  In HIV seropositive individuals, periodic ENT examination is required for early diagnosis, to monitor disease progression, to alleviate symptoms of opportunistic infections and improve the quality of life.

 
References:

1. Sunita H, GB Doddamani, Pujari LL, Prasad CVB. Pleural Fluid Analysis in HIV-associated
tuberculosis Patients: A Retrospective Study. Indian Journal of Clinical Practice. 2012 June;23(1):22-25.   Download PDF

2. Kuteyi T, Okwundu CI. Topical treatments for HIV-related oral ulcers. Cochrane Database Syst Rev. 2012 Jan 18;1:CD007975. doi: 10.1002/14651858.CD007975.pub2.   View Abstract

3. Prasad HK, Bhojwani KM, Shenoy V, Prasad SC. HIV manifestations in otolaryngology. Am J Otolaryngol. 2006 May-Jun;27(3):179-85.   View Abstract

4. Antiretroviral therapy guidelines for HIV-Infected adults and adolescents including post-exposure Prophylaxis.  Accessed on 27/01/2013. http://www.ilo.org/wcmsp5/groups/public

5. Marcusen DC, Sooy CD. Otolaryngologic and head and neck manifestations of acquired immunodeficiency syndrome (AIDS). Laryngoscope. 1985 Apr;95(4):401-5.    View Abstract

6. Dichtel WJ Jr. Oral manifestations of Human Immunodefiency Virus infection. Otolaryngol Clin North Am 1992; 25:1211-26.  

7. Williams MA. Head and neck findings in pediatric acquired immune deficiency syndrome. Laryngoscope. 1987 Jun;97(6):713-6.  View Abstract

8. Deb T, Singh NB, Devi HP, Sanasam JC. Head and neck manifestations of HIV infection: a preliminary study. J Indian Med Assoc. 2003 Feb;101(2):93-5.  View Abstract

9. Silverman S Jr, Migliorati CA, Lozada-Nur F, Greenspan D, Conant MA. Oral findings in people with or at high risk for AIDS: a study of 375 homosexual males. J Am Dent Assoc. 1986 Feb;112(2):187-92.  View Abstract

10. Gileva OS, Sazhina MV, Gileva ES, Efimov AV, Scully C. Spectrum of oral manifestations of HIV/AIDS in the Perm region (Russia) and identification of self-induced ulceronecrotic lingual lesions. Med Oral. 2004 May-Jul;9(3):212-5.  View Abstract

11. Buda FB. Sleep disorders in HIV-positive patients: Curable causes of daytime fatigue and sleepiness. XI International Conference on AIDS, Vancouver, Canada, July 7-12, 1996. Abstract MoB301

12. Tami TA, Wawrose S.  Disease of the nose and paranasal sinuses in human immunodeficiency virus infected population. Otolaryngol Clin North Am 1992; 25:1199-1210.

13. Barzan L, Carbone A, Saracchini S, Vaccher G, Tirelli U, Comoretto R. Nasopharyngeal lymphatic tissue hypertrophy in HIV-infected patients. Lancet. 1989 Jan 7;1(8628):42-3.  View Abstract

14. Lalwani AK, Sooy CD. Otologic and neurotologic manifestations of acquired immunodeficiency syndrome. Otolaryngol Clin North Am 1992; 25:1183-97.

15. Bélec L, Gherardi R, Georges AJ, Schüller E, Vuillecard E, Di Costanzo B, Martin PM. Peripheral facial paralysis and HIV infection: report of four African cases and review of the literature. J Neurol. 1989 Oct;236(7):411-4.   View Abstract

16. Kleyberg RL, Kleynberg JL. Bilateral facial nerve paralysis and acute HIV -1 infection. International Journal of case reports and images 2011 Aug;2(8): 5-7.  Download PDF

17. Lee KC, Tami TA. Otolaryngologic manifestations of HIV.  Accessed on 29/01/2013. http://hivinsite.ucsf.edu/ 

18. Ndjolo A, Njock R, Ngowe NM, Ebogo MM, Toukam M, Nko'o S, Bengono G. Rev Laryngol Otol Rhinol (Bord). 2004;125(1):39-43.   View Abstract
 

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