Audiological assessment of children with HIV/AIDS: a meta-analysis

Bentivi, Janaina Oliveira; Azevedo, Conceição de Maria Pedrozo e Silva de; Lopes, Monique Kelly Duarte; Rocha, Savya Cybelle Milhomem; Silva, Paula Cristina Ribeiro e; Costa, Valeria Maciel; Costa, Ana Beatriz Sousa

doi:10.1016/j.jped.2019.11.003

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Review articles • J. Pediatr. (Rio J.) 96 (5) • Sep-Oct 2020 • https://doi.org/10.1016/j.jped.2019.11.003 copy

Audiological assessment of children with HIV/AIDS: a meta-analysis^☆ ☆ Please cite this article as: Bentivi JO, Azevedo CM, Lopes MK, Rocha SC, Silva PC, Costa VM, et al. Audiological assessment of children with HIV/AIDS: a meta-analysis. J Pediatr (Rio J). 2020;96:537-45. , ^☆☆ ☆☆ Study conducted at Federal University of Maranhão, São Luís, MA, Brazil.

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

Objective:

To analyze the results of the audiological evaluation of children with HIV and AIDS.

Data collection:

Systematic review carried out in May 2019 in the Web of Science, PubMed, SciELO, and Scopus databases. Case reports and original articles were included, with no limitationsregarding country or year of publication.

Data synthesis:

278 articles were identified; 26 were included, in which HIV/AIDS was shown to be a risk factor for hearing loss (OR = 5.364; p = 0.00). The studies used different audiological exams, with varying methodologies. There was no difference regarding the type of hearing loss (p = 0.119).

Conclusion:

Longitudinal studies using the same type of examination at all stages are suggested, to allow better monitoring of the effects of HIV on the child's hearing,and studies that provide more methodological details. The knowledge of the influence of HIV on the child's auditory system may lead to the promotion of measures that minimize the prevalence of hearing loss, allow an early diagnosis and timely rehabilitation, so as not to compromise child development.

KEYWORDS
Human immunodeficiency virus; AIDS; Audiology; Hearing loss

Authors/year	Country	n	Sample	Audiological exams
Bastos et al., 2010³¹31 Bastos FN, Fleig R, Nascimento IB. Hearing abilities and analysis in an oralized hearing-impaired child with HIV: a case study. Rev CEFAC. 2010;12:700-8.	Brazil	1	7 years	Pure tone audiometry
				Behavioral tests
Buriti et al., 2013²⁹29 Buriti AK, Oliveira SH, Muniz LF. Hearing loss in children with HIV/AIDS. CoDAS. 2013;25:513-20.	Brazil	23	2 years-10 years and 11 months	Pure tone audiometry
				Acoustic immittance measures
Buriti et al., 2014²⁸28 Buriti AK, Oliveira SHS, Muniz LF, Soares MJ. Evaluation of hearing health in children with HIV/AIDS. Audiol Commun Res. 2014;19:105-11.	Brazil	23	2 years-10 years and 11 months	Pure tone audiometry
				Acoustic immittance measures
Chao et al., 2012²2 Chao CK, Czechowicz JA, Messner AH, Alarcón J, Kolevic RL, Rodriguez MM, et al. High prevalence of hearing impairment in HIV-infected Peruvian children. Otolaryngol Head Neck Surg. 2012;146:259-65.	Peru	139	4-19 years	Pure tone audiometry
				Acoustic immittance measures
Chidziva et al., 2016¹⁷17 Chidziva C, Matsekete J, Bandason T, Shamu S, Dzongodza T, Matinhira N. Hearing impairment and deafness among HIV infected children and adolescents in Harare, Zimbabwe. Cent Afr J Med. 2015;61:56-61.	Zimbabwe	380	5-17 years	Pure tone audiometry (359)
Christopher et al., 2013⁵5 Christopher N, Edward T, Sabrina BK, Agnes N. The prevalence of hearing impairment in the 6 months - 5 years HIV/AIDS-positive patients attending paediatric infectious disease clinic at Mulago Hospital. Int J Pediatr Otorhinolaryngol. 2013;77:262-5.	Uganda	370	6-60 months	ABR
				Tympanogram
Christensen et al., 1998²⁶26 Christensen LA, Morehouse CR, Powell TW, Alchediak T, Silio M. Antiviral therapy in a child with pediatric human immunodeficiency virus (HIV): case study of audiologic findings. J Am Acad Audiol. 1998;9:292-8.	United States	1	Three evaluations: at 21, 34, and 43 months	21 months: VRA, OAE-TE, ABR
				34 months: ABR
				43 months: VRA, ABR, tympanogram
Govender et al., 2011¹⁵15 Govender R, Eley B, Walker K, Petersen R, Wilmshurst JM. Neurologic and neurobehavioral sequelae in children with human immunodeficiency virus (HIV-1) infection. J Child Neurol. 2011;26:1355-64.	South Africa	78	3 months-12 years	ABR (based on clinical suspicion)
Hrapcak et al., 2016²⁵25 Hrapcak S, Kuper H, Bartlett P, Devendra A, Makawa A, Kim M, et al. Hearing loss in HIV-infected children in Lilongwe, Malawi. PLoS One. 2016;11:e0161421.	Malawi	380	4-14 years	Pure tone audiometry (372)
				VRA (7)
				Tympanometry
				OAE-TE
Knox et al., 2018²⁴24 Knox J, Arpadi SM, Kauchali S, Craib M, Kvalsvig JD, Taylor M, et al. Screening for developmental disabilities in HIV positive and HIV negative children in South Africa: results from the Asenze Study. PLoS One. 2018;13:e0199860.	South Africa	61	4-6 years	OAE-DP
Makar et al., 2012²⁰20 Makar SK, Dhara S, Sinha AK, Chatterjee I, Dutta P. Nature and onset of communication disorder in pediatrics with HIV. Int J Ped Otorhinolaryngol. 2012;76:1065-6.	India	67	4-16 years	Pure tone audiometry
				Acoustic immittance measures
Maro et al., 2016²²22 Maro II, Fellows AM, Clavier OH, Gui J, Rieke CC, Wilbur JC, et al. Auditory impairments in HIV-infected children. Ear Hear. 2016;37:443-51.	Tanzania	131	1.3-18 years	Tympanometry
			113 HIV-negative controls	Pure tone audiometry (75)
				OAE-DP (97)
				Gap detection test (48)
				ABR (90)
Martins et al., 2001³⁴34 Martins RH, Batista L, Souza AC, Costa GA, Zuliani A, OlbrichNeto J. Otolaryngologicmanifestations in children with AIDS. Braz J Otorhinolaryngol. 2001;67:204-11.	Brazil	22	8 months-12 years	Pure tone audiometry
				Behavioral tests
				Acoustic immittance measures
Matas et al., 2000²¹21 Matas CG, Sansone AP, Iorio MC, Succi RC. Avaliação Audiológica emcrianças nascidas de mãessoropositivas para o vírus da imunodeficiênciahumana. Braz J Otorhinolaryngol. 2000;66:317-24.	Brazil	18	18 months-2 years and 6 months	Behavioral tests
			Controls:	VRA
			- Exposed: 34	Acoustic immittance measures
			- Sero-reverted: 91
Matas et al., 2006⁴4 Matas CG, Leite RA, Magliaro FC, Gonçalves IC. Audiological and electrophysiological evaluation of children with acquired immunodeficiency syndrome (AIDS). Braz J Infect Dis. 2006;10:264-8.	Brazil	51	3-10 years	Pure tone audiometry
			50 HIV-negativecontrols	Acoustic immittance measures
				ABR
Matas et al., 2008⁶6 Matas CG, Iorio MC, Succi RC. Auditory disorders and acquisition of the ability to localize sound in children born to HIV-positive mothers. Braz J Infect Dis. 2008;12:10-4.	Brazil	18	1-30 months	Behavioral audiometry
			Controls:	VRA
			- Exposed: 34 (<18 months)	Acoustic immittance measures
			- Sero-reverted: 91
Matas et al., 2010²⁷27 Matas CG, Santos Filha VA, Juan KR, Pinto FR, Gonçalves IC. Manifestaçõesaudiológicasemcrianças e adultoscom AIDS. Pro Fono. 2010;22:269-74.	Brazil	51	3 years-10 years and 11 months	Pure tone audiometry
			50 HIV-negative controls	Vocal audiometry
				Acoustic immittance measures
				ABR
Nakku et al., 2017¹⁶16 Nakku D, Nyaiteera V, Llowet E, Nanseera D, Nakalema G, Westerberg B, et al. HIV status and hearing loss among children between 6 and 12 years of age at a large urban health facility in South Western Uganda. Int J Pediatr Otorhinolaryngol. 2017;101:172-7.	Uganda	148	6-12 years	Pure tone audiometry
			79 HIV-negative controls
Palacios et al., 2008¹⁹19 Palacios GC, Montalvo MS, Fraire MI, Leon E, Alvarez MT, Solorzano F. Audiologic and vestibular findings in a sample of human immunodeficiency virus type-1-infected Mexican children under highly active antiretroviral therapy. Int J Pediatr Otorhinolaryngol. 2008;72:1671-81.	Mexico	23	5 months-17 years	ABR
				Pure tone audiometry (> 4 years: 12)
				Speech discrimination test
Rezende et al., 2004³⁶36 Rezende CE, Rodrigues RE, Haddad L, Yoshimura R, Rapoport PB. Manifestaçõesotológicasemcriançacomsíndrome da imunodeficiênciaadquirida. Braz J Otorhinolaryngol. 2004;70:430-4.	Brazil	1	10 years	Pure tone audiometry
				Vocal audiometry
				Acoustic immittance measures
Romero et al., 2017³²32 Romero AC, Alfaya LM, Gonçalves AS, Frizzo AC, Isaac ML. Auditory alterations in children infected by human immunodeficiency virus verified through auditory processing test. Int Arch Otorhinolaryngol. 2017;21:86-91.	Brazil	15	8-9 years	Pure tone audiometry
				Vocal audiometry
				Acoustic immittance measures
				Behavioral tests
Smith et al., 2017¹⁸18 Smith AF, Ianacone DC, Ensink RJ, Melaku A, Casselbrant ML, Isaacson G. Prevalence of hearing-loss among HAART-treated children in the Horn of Africa. Int J Pediatr Otorhinolaryngol. 2017;98:166e170.	Ethiopia	107	7-20 years	Pure tone audiometry
Taipale et al., 2011³³33 Taipale A, Pelkonen T, Taipale M, Roine I, Bernardino L, Peltola H, et al. Otorhinolaryngological findings and hearing in HIV-positive and HIV-negative children in a developing country. Eur Arch Otorhinolaryngol. 2011;268:1527-32.	Angola	78	9-178 months	Pure tone audiometry
			78 HIV-negative controls	ABR
Torre et al., 2012³⁰30 Torre P, Zeldow B, Hoffman HJ, Buchanan A, Siberry GK, Rice M, et al. Hearing loss in perinatally human immunodeficiency virus-infected and human immunodeficiency virus-exposed but uninfected children and adolescents. Pediatr Infect Dis J. 2012;31:835-41.	United States and Puerto Rico	145	7-17 years	Pure tone audiometry
			86 HIV-negative controls	Tympanometry
Torre et al., 2015²³23 Torre P, Cook A, Elliott H, Dawood G, Laughton B. Hearing assessment data in HIV-infected and uninfected children of Cape Town, South Africa. AIDS Care. 2015;27:1037-41.	South Africa	37	4-14 years	Tympanometry
			24 HIV-negative controls	OAE-DP
				Pure tone audiometry
Torre et al., 2015¹⁴14 Torre P, Yao TJ, Zeldow B, Williams P, Hoffman HJ, Siberry GK. Distortion product otoacoustic emission data in perinatally HIV-infected and HIV-exposed but uninfected children and adolescents in the pediatric HIV/AIDS cohort study. Pediatr Infect Dis J. 2015;34:276-8.	United States and Puerto Rico	89	7-16 years	OAE-DP
			83 HIV-negative controls

Study	Tympanogram (ears)	Acoustic reflex
Buriti et al., 2013²⁹29 Buriti AK, Oliveira SH, Muniz LF. Hearing loss in children with HIV/AIDS. CoDAS. 2013;25:513-20.	Type A (10.9%), Type B (67.4%), Type As/Ar (10.9%), Type C (8.7%), Type Ad (2.2%)	Absent in 65.2%
Buriti et al., 2014²⁷27 Matas CG, Santos Filha VA, Juan KR, Pinto FR, Gonçalves IC. Manifestaçõesaudiológicasemcrianças e adultoscom AIDS. Pro Fono. 2010;22:269-74.	Type A (10.9%), Type B (67.4%), Type As/Ar (10.9%), Type C (8.7%), Type Ad (2.2%)	Absent in 65.2%
Chao et al., 2012²2 Chao CK, Czechowicz JA, Messner AH, Alarcón J, Kolevic RL, Rodriguez MM, et al. High prevalence of hearing impairment in HIV-infected Peruvian children. Otolaryngol Head Neck Surg. 2012;146:259-65.	Abnormal in 46.3%.	-----
Hrapcak et al., 2016²⁵25 Hrapcak S, Kuper H, Bartlett P, Devendra A, Makawa A, Kim M, et al. Hearing loss in HIV-infected children in Lilongwe, Malawi. PLoS One. 2016;11:e0161421.	84% of ears with hearing loss had alterations (majority Type B)	-----
	21% of the ears without hearing loss had alterations
Makar et al., 2012²⁰20 Makar SK, Dhara S, Sinha AK, Chatterjee I, Dutta P. Nature and onset of communication disorder in pediatrics with HIV. Int J Ped Otorhinolaryngol. 2012;76:1065-6.	32.8% not Type A	Absent in 47/67
Maro et al., 2016²²22 Maro II, Fellows AM, Clavier OH, Gui J, Rieke CC, Wilbur JC, et al. Auditory impairments in HIV-infected children. Ear Hear. 2016;37:443-51.	25% abnormal	-------
Martins et al., 2001³⁴34 Martins RH, Batista L, Souza AC, Costa GA, Zuliani A, OlbrichNeto J. Otolaryngologicmanifestations in children with AIDS. Braz J Otorhinolaryngol. 2001;67:204-11.	Type C (13.6%)	-------

Study	Otoscopy (% ears)
Chao et al., 2012²2 Chao CK, Czechowicz JA, Messner AH, Alarcón J, Kolevic RL, Rodriguez MM, et al. High prevalence of hearing impairment in HIV-infected Peruvian children. Otolaryngol Head Neck Surg. 2012;146:259-65.	Abnormal otoscopy (59.7%): tympanic perforation (13.7%), cerumen (17.3%) and tympanic inflammation
Chidziva et al., 2016¹⁷17 Chidziva C, Matsekete J, Bandason T, Shamu S, Dzongodza T, Matinhira N. Hearing impairment and deafness among HIV infected children and adolescents in Harare, Zimbabwe. Cent Afr J Med. 2015;61:56-61.	Abnormal otoscopy (61%): cerumen (37.2%), chronic suppurative otitis media (10.4%) inactive chronic otitis media (5.2%), otitis media with effusion (16%), acute otitis media (3%), tympanic retraction (2.2%)
Hrapcak et al., 2016²⁵25 Hrapcak S, Kuper H, Bartlett P, Devendra A, Makawa A, Kim M, et al. Hearing loss in HIV-infected children in Lilongwe, Malawi. PLoS One. 2016;11:e0161421.	Cerumen (25.5%), otorrhea (5.4%), tympanic perforation (6.3%), fungal otitis (1.3%), tympanic inflammation (2.9%), changes in the appearance of the tympanic membrane (31.3%), tympanum not evaluated (10.8%)
Makar et al., 2012²⁰20 Makar SK, Dhara S, Sinha AK, Chatterjee I, Dutta P. Nature and onset of communication disorder in pediatrics with HIV. Int J Ped Otorhinolaryngol. 2012;76:1065-6.	Cerumen and fungal otitis (56.7%), chronic suppurative otitis media (16.4%)
Martins et al., 2001³⁴34 Martins RH, Batista L, Souza AC, Costa GA, Zuliani A, OlbrichNeto J. Otolaryngologicmanifestations in children with AIDS. Braz J Otorhinolaryngol. 2001;67:204-11.	Thickening of ear drum (31.8%), red/bulgingear drum (9.1%), perforated ear drum (4.5%)
Matas et al., 2000²¹21 Matas CG, Sansone AP, Iorio MC, Succi RC. Avaliação Audiológica emcrianças nascidas de mãessoropositivas para o vírus da imunodeficiênciahumana. Braz J Otorhinolaryngol. 2000;66:317-24.	Tympanic retraction and thickening (31.8%), red/bulging eardrum (9.1%), perforated eardrum (4.5%), neomembrane (4.5%)
Palacios et al., 2008¹⁹19 Palacios GC, Montalvo MS, Fraire MI, Leon E, Alvarez MT, Solorzano F. Audiologic and vestibular findings in a sample of human immunodeficiency virus type-1-infected Mexican children under highly active antiretroviral therapy. Int J Pediatr Otorhinolaryngol. 2008;72:1671-81.	Tympanic perforation (4.3%)
Rezende et al., 2004³⁶36 Rezende CE, Rodrigues RE, Haddad L, Yoshimura R, Rapoport PB. Manifestaçõesotológicasemcriançacomsíndrome da imunodeficiênciaadquirida. Braz J Otorhinolaryngol. 2004;70:430-4.	Tympanic perforation
Smith et al., 2017¹⁸18 Smith AF, Ianacone DC, Ensink RJ, Melaku A, Casselbrant ML, Isaacson G. Prevalence of hearing-loss among HAART-treated children in the Horn of Africa. Int J Pediatr Otorhinolaryngol. 2017;98:166e170.	Tympanic perforation (17.75%), otorrhea (8.41%), other abnormal findings (16.82%)
Taipale et al., 2011³³33 Taipale A, Pelkonen T, Taipale M, Roine I, Bernardino L, Peltola H, et al. Otorhinolaryngological findings and hearing in HIV-positive and HIV-negative children in a developing country. Eur Arch Otorhinolaryngol. 2011;268:1527-32.	Acute otitis media (10%), chronic otitis media (27%), tympanic perforation (9%), cerumen (21%), retraction (2%)

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[1] * Corresponding author. E-mail: Corresponding author. janabentivi.orl@gmail.com (J.O. Bentivi).