Once a small fishing village, the East African port city of Dar es Salaam, Tanzania, has become a major trading port, and today is a vibrant, bustling city of 3 million people. But the AIDS epidemic also affects this city; approximately 9% of the population has been infected with the human immunodeficiency virus (HIV). Some of those infected are likely noting problems with their hearing.
When the HIV epidemic began in the early 1980s, clinicians noted that some patients with HIV had ear and hearing problems. These patients complained of hearing loss, ear pain, tinnitus, and ear drainage. Some patients had severe otitis media, while others had cryptococcus and cytomegalovirus infections of the inner ear. At the time, these ear problems seemed minor compared to a life-threatening HIV infection.
Today, HIV medication advances have reduced the disease to a serious—but not necessarily fatal—infection. Yet the hearing problems haven't gone away. Researchers wondered whether there could be a connection, and several small-scale studies (Chandrasekhar et al., 2000; Khoza & Ross, 2002; Marra et al., 1997) confirmed that many patients with HIV have hearing complaints and abnormal hearing tests.
HIV and Hearing Loss
Early reports suggested that people with HIV experienced problems throughout the hearing system from the middle ear to the brain (Michaels, Soucek, & Liang, 1994; Soucek & Michaels, 1996). Otoscopic exams and tympanometry tests sometimes revealed otitis media. Several studies of people with HIV reported a high rate of abnormal audiogram results, and revealed abnormal ABR tests (Matas, Leite, Magliaro, & Goncalves, 2006; Matas, Santos Filha, Juan, Pinto, & Goncalves, 2010).
There are several possible reasons for these results. HIV-positive patients are more susceptible to ear infections, which could lead to hearing loss. The HIV virus—and some other infections associated with HIV—can affect the brain directly, and so might affect hearing pathways in the brain. Many patients with HIV take a large number of medications, which could potentially damage the ear.
But understanding how frequently hearing problems occurred in HIV-positive patients, and where in the hearing system these problems arose, requires a comprehensive study on hearing problems in people with HIV.
The Tanzania Project
We proposed our project, "Hearing impairment in HIV-infected and HIV/TB-coinfected individuals in Tanzania," in response to a National Institute on Deafness and Other Communication Disorders call for research. The project is a team effort with Odile Clavier and her colleagues at Creare, Inc.—an engineering research and development company—and audiology researchers Brenda Lonsbury-Martin of Loma Linda University and Frank Musiek of the University of Connecticut.
We took advantage of the long-standing relationship between our institution, The Geisel School of Medicine at Dartmouth, and the Infectious Disease Center in Dar es Salaam. Ford von Reyn from Dartmouth conducted a tuberculosis vaccine trial at this site, and worked with a cohort of HIV-positive patients who were dedicated to research. Dartmouth pediatrician and researcher Paul Palumbo ran the Dartmouth Pediatric Program for children with HIV at the same site. The combination of this cohort of patients, with a comprehensive laptop-based hearing testing system, forms the basis for our study.
Our team—Dartmouth, Creare, Musiek, and Lonsbury-Martin—had prior experience designing hearing testing systems for field settings. One of our projects had been to build a hearing testing system for use on the International Space Station. The goal of that project was to develop a small, lightweight system that could work in environments with background noise—such as a space station—and provide feedback to the user on the quality of the test. The system was designed to measure noise in the ear canal, so the user would know if the noise level in the ear canal was too high for an accurate threshold-based audiological test.
Although the system never made it into orbit, its features made it a good choice for use in the developing world, where access to sound booths is limited. It is a laptop-based, hearing testing system that measures audiometric thresholds, distortion product otoacoustic emissions (DPOAEs), and of course, in-ear noise.
Before starting in Tanzania, we needed to test our methods. James Saunders, an otolaryngologist at Dartmouth who works extensively in the developing world, agreed to use the testing system in a study of miners in Nicaragua, gathering data while exposing the equipment to a field setting. Although the study went well and the technology was deemed effective, we also learned how important a comprehensive, consistent, easily understood, and efficient questionnaire could be. The questionnaire was essential for gathering information on individuals' subjective assessment of their hearing, and on their exposure to confounding factors such as noise and medications.
Also, we learned how challenging it is to perform a quick, but accurate, gap detection test in a field setting. We knew that in Tanzania we would need to work hard to perform a comprehensive, detailed assessment without making the test battery so long that participants would lose interest and focus.
With these experiences in mind, we modified our system by developing a video questionnaire in Kiswahili. This questionnaire was designed to automate data gathering, and to ensure that all subjects were asked a defined set of questions in their native language, in a consistent way. This protocol also helped with patients who can't read well, because they listened to the questions from the video.
We again worked with Frank Musiek and Creare, Inc., along with Towson University audiologist Stephanie Nagle, an expert in central auditory processing testing, to refine our gap detection algorithm. This work resulted in a test battery that includes an otoscopic exam, tympanometry, questionnaire administration, threshold audiometry, DPOAEs, and gap detection. Although many of our patients are new to computers and haven't had a hearing test before, it is only the rare patient who cannot complete the protocol successfully.
Gains and Progress
Under the direction of physician and public health expert Isaac Maro at the Infectious Disease Center in Dar es Salaam, the study has tested 499 adults so far—346 of them HIV-positive, 153 HIV-negative, average age 40 years. Pediatric data collection is underway. We have tested an additional 100 HIV-negative adults in the United States. The adult study in Tanzania includes 173 men, 326 women, 244 people with HIV and undergoing antiretroviral therapy (ART), and 102 people with HIV but not on ART.
Although full analysis of the data is in progress, early indications suggest the hearing problems people with HIV experience may have more to do with interpreting speech rather than detecting sounds. People with HIV and on ART are more likely to report difficulty hearing speech in background noise. They are also more likely to say that they hear sounds normally but don't understand speech, and they have higher gap detection thresholds.
During our five-year study, participants return every six months for a hearing evaluation. Over time, we will be able to see if patients starting ART begin to develop hearing problems, and we will learn how the audiological findings differ between children and adults. For now, our study seems to confirm that HIV is associated with hearing problems, but these problems may have more to do with the brain than with the ear.