Eur J Clin Microbiol Infect Dis DOI 10.1007/s10096-014-2292-7

ARTICLE

Does cerumen have a risk for transmission of HIV? F. M. Hanege & M. T. Kalcioglu & F. Sargin & Z. Cetinkaya & M. Tekin & H. Vahaboglu

Received: 17 October 2014 / Accepted: 25 November 2014 # Springer-Verlag Berlin Heidelberg 2014

Abstract Human immunodeficiency virus (HIV) is mainly transmitted via sexual activity, mother-to-child transmission, and contact with body fluids, such as saliva and semen. Cerumen, however, has not been investigated for its capability to transmit HIV. The purpose of this study was to evaluate the potential of cerumen for transmission of HIV infection. This study was conducted among 42 treatment-naive HIV-infected patients with positive HIV RNA and 27 HIV-infected patients with negative HIV RNA receiving antiviral treatment. Simultaneous blood samples were studied as positive controls. Sixty-nine prospectively collected cerumen specimens were analyzed for the presence of HIV RNA by real-time polymerase chain reaction (PCR). None of the 69 cerumen specimens were positive for HIV RNA. These results conclude that cerumen in HIV-positive patients with or without antiretroviral therapy (ART) carry only an insignificant risk of transmission. However, standard infection control precautions should be applied carefully in all examinations and surgical operations of the ears.

Introduction

This study was presented at the International Union of Microbiological Societies Congress, Montréal, Canada, 27 July–1 August 2014.

Materials and methods

F. M. Hanege : M. T. Kalcioglu (*) : M. Tekin Department of Otorhinolaryngology, Göztepe Training and Research Hospital, School of Medicine, Istanbul Medeniyet University, Istanbul, Turkey e-mail: [email protected] F. Sargin : H. Vahaboglu Department of Infectious Diseases and Clinical Microbiology, Göztepe Training and Research Hospital, School of Medicine, Istanbul Medeniyet University, Istanbul, Turkey Z. Cetinkaya Department of Microbiology and Clinical Microbiology, Goztepe Training and Research Hospital, School of Medicine, Istanbul Medeniyet University, Istanbul, Turkey

Human immunodeficiency virus (HIV) infection is a worldwide public health problem [1]. In 2012, there were an estimated 35.4 million people living with HIV [2]. HIV is spread mainly by sexual activity, mother-to-child transmission, and contact with body fluids, such as saliva and semen [1, 3]. Cerumen, however, has not yet been investigated for its potential for transmission of HIV infection. Otorhinolaryngologists come into contact with cerumen during patient examination. In order to provide disease control and self-protection for healthcare providers, exploring cerumen’s transmission potential for HIV infection is of great importance. In our previous studies, hepatitis B virus (HBV) DNA was found in the cerumen of 27.5 % of HBV DNApositive patients. In another study, we have found that cerumen samples from hepatitis C virus (HCV) RNA-positive chronic hepatitis patients were negative for HCV RNA [4, 5]. In the current study, we aimed to investigate the transmission potential of cerumen by assessing the HIV RNA loads in blood and cerumen with polymerase chain reaction (PCR).

Study population and data collection The study protocol was approved by the Ethics Committee of Istanbul Medeniyet University (decision no. 28-08-13). Informed consent was obtained from all participants. We included HIV-positive patients who attended Istanbul Medeniyet University Hospital from July 2013 to April 2014. The patients were divided into two groups: group 1 consisted of 51 treatment-naive patients with a positive plasma HIV RNA assay, while group 2 consisted of 27 HIV-infected patients under treatment with a negative plasma HIV RNA assay. Nine patients in group 1 were excluded from the study because a cerumen

Eur J Clin Microbiol Infect Dis

sample could not be obtained. The study was then continued with 69 patients in total (7 females, 62 males). The average age of the patients was 36.73 (range 19–66) years. The transmission mode varied: 35 of them were men who have sex with men (MSM), 24 Table 1

subjects acquired infection through heterosexual contact, one patient through blood transfusion, and the transmission mode was unknown for nine patients. Cerumen samples from all subjects were collected carefully without blood contamination

Cerumen HIV RNA concentrations, transmission routes, and serological parameters in group 1

Patient no.

Gender

Age (years)

Transmission route

ART

CD4

Serum HIV RNA (IU)

Cerumen HIV RNA

1 2 3 4 5 6 7

M M M M M M M

34 28 22 26 34 35 32

MSM HETERO MSM MSM MSM MSM HETERO

Naive Naive Naive Naive Naive Naive Naive

345 195 420 368 845 197 720

24,020 136,514 236,991 915,465 100,791 17,372 96,854

Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected

8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25

M F M M M F F M M M M M M M M M F M

33 39 21 26 28 37 25 41 25 32 41 31 39 39 27 32 41 25

HETERO HETERO HETERO MSM MSM HETERO HETERO MSM MSM MSM HETERO Unknown MSM MSM MSM MSM HETERO MSM

Naive Naive Naive Naive Naive Naive Naive Naive Naive Naive Naive Naive Naive Naive Naive Naive Naive Naive

814 260 280 385 447 374 122 489 554 432 312 728 424 324 482 381 280 512

134,644 107,244 124,810 236,991 516,540 295,498 149,316 492,201 23,367 1,043,605 37,088 81,394 179,868 2,152,543 301,452 83,700 2670 218,123

Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected

26 27 28 29 30 32 32 33 34 35 36 37 38 39 40 41 42

M M M M M F M F M M M M M M M M M

41 22 19 32 33 25 30 28 64 29 33 29 26 36 47 61 29

MSM MSM MSM MSM Unknown HETERO Unknown HETERO MSM Unknown MSM HETERO Unknown MSM MSM Unknown MSM

Naive Naive Naive Naive Naive Naive Naive Naive Naive Naive Naive Naive Naive Naive Naive Naive Naive

1,153 384 323 713 76 680 518 856 259 531 609 330 447 853 341 688 840

14,100 52,460 13,730 56,200 113,600 32,600 10,870 15,450 175 648,515 155,622 373,564 119,752 200,847 183,000 149,316 338,690

Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected

M male, F female, ART antiretroviral therapy, MSM men who have sex with men, HETERO heterosexual

Eur J Clin Microbiol Infect Dis Table 2

Cerumen HIV RNA concentrations, transmission routes, and serological parameters in group 2

Patient no.

Gender

Age (years)

Transmission route

ART

CD4

Serum HIV RNA (IU)

Cerumen HIV RNA

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17

M M M M M M M M M M M M F M M M M

46 24 26 28 62 47 50 26 61 33 27 52 53 30 30 66 37

MSM MSM MSM HETERO Unknown MSM HETERO HETERO MSM HETERO HETERO HETERO HETERO MSM MSM MSM MSM

+ + + + + + + + + + + + + + + + +

720 445 434 123 221 432 151 462 868 738 798 462 429 836 610 474 1,100

Negative Negative Negative Negative Negative Negative Negative Negative Negative Negative Negative Negative Negative Negative Negative Negative Negative

Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected

18 19 20 21 22 23 24 25 26 27

M M M M M M M M M M

58 54 50 65 26 23 61 27 62 34

HETERO HETERO HETERO HETERO MSM MSM Unknown Unknown Transfusion HETERO

+ + + + + + + + + +

800 300 385 306 968 780 532 570 582 496

Negative Negative Negative Negative Negative Negative Negative Negative Negative Negative

Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected Non-detected

M male, F female, ART antiretroviral therapy, MSM men who have sex with men, HETERO heterosexual

by an expert otorhinolaryngologist and put into sterile Eppendorf tubes containing 1 ml saline and kept at −32 °C. A total of 69 cerumen specimens were studied by PCR for the presence of HIV RNA. Comparison was made against simultaneous blood HIV RNA results. Table 3 Studies on the prevalence of HIV RNA in different body fluids or secretions of serum HIV RNA-positive patients

Definitions: PCR diagnosis HIV RNA extraction from serum and cerumen samples was performed using an RNA extraction kit (QIAamp UltraSens, QIAGEN, Hilden, Germany), according to the manufacturer’s

Study

Serum HIV RNA-positive body fluid/secretion

Body fluid/secretion

Positive HIV RNA in body fluid/secretion, n (%)

Kantor et al., 2014 [8] Cotten et al., 2014 [10] Liuzzi et al., 1996 [11] Mohlala et al., 2005 [12] Mohlala et al., 2005 [12] Balamane et al., 2010 [13] Lourenço et al., 2014 [14] Han et al., 2011 [18] Current study

143 20 26 23 23 47 57 21 69

Genital secretion Feces Semen Amniotic fluid Fetal cord blood Saliva Saliva Tear fluid Cerumen

82 (57) 12 (60) 25 (96) 0 (0) 0 (0) 36 (77) 34 (60) 21 (100) 0 (0)

Eur J Clin Microbiol Infect Dis

instructions. HIV RNA concentrations were detected by realtime PCR using the RealArt HIV Rotor-Gene (RG) real-time PCR reagents containing a ready-to-use system for the detection of HIV RNA in the Rotor-Gene 2000/3000 (Corbett Research, Hamburg, Germany). The HIV RG master mix contains all reagents and enzymes for the reverse transcription and amplification of a 240-base-pair region of HIV genome. HIV primers and probes used in the HIV real-time PCR reagents were obtained by Artus (Bonn, Germany) for validation purposes. Amplification and detection were performed with the Rotor-Gene 3000 by using the following profile: one cycle of 50 °C for 10 min, 45 cycles of 95 °C for 8 s, 55 °C for 20 s, and 72 °C for 20 s.

Results HIV RNA was not detected in the cerumen samples from either 42 patients with positive serum HIV RNA or 27 patients with negative serum HIV RNA. The results of HIV RNA detection in serum and cerumen specimens and the demographic data of patients are shown in Tables 1 and 2 for groups 1 and 2, respectively.

Mohlala et al. reported that, in 23 HIV-positive medically and obstetrically non-complicated women who had received either zidovudine or nevirapine during late pregnancy and underwent elective cesarean section, HIV-1 RNA was not detected in either amniotic fluid samples or fetal cord blood collected during surgery [12]. In a study by Balamane et al., 36 of 47 plasma viremic patients had saliva HIV-1 RNA, while Lourenço et al. found that specimens of saliva collected from 57 subjects were seropositive in 34 patients [13, 14]. On the other hand, it is known that saliva has a much lower viral load than blood or genital fluid [15]. However, there have been reports of transmission of HIV infection from a HIV-positive partner by only oral sex, which explains how saliva is a transmission route for HIV [16, 17]. In their study, Han et al. found that patients who underwent long-term ART with undetectable plasma viral load had detectable HIV-1 load in tears [18]. In conclusion, this study showed that cerumen has only an insignificant risk for transmission of HIV infection, even in patients with high HIV RNA serum levels, unless it is contaminated with blood. Acknowledgments This research was supported by the Research Fund of Istanbul Medeniyet University, Istanbul, Turkey.

Discussion

Conflict of interest The authors declare that they have no conflict of interest.

Research on HIV vaccines is still in progress, though success has not yet been achieved [6]. Due to HIV-1 residual disease, antiretroviral therapy (ART) does not result in viral eradication [7]. The fact that some patients may not respond to ART emphasizes the importance of preventing exposure to HIV [8]. Various studies have reported that patients with negative plasma HIV RNA undergoing ART had HIV RNA-positive body fluids (feces, tears, saliva, gingival fluid, semen, and cervicovaginal secretion) [8–18] (Table 3). During our literature review, we observed that cerumen in HIV-positive patients has never been evaluated either among treated or untreated patients. In our study, we took 69 cerumen samples from 42 untreated patients with positive HIV RNA (Table 1) and 27 ART-treated patients with negative plasma HIV RNA (Table 2). All cerumen samples evaluated by the PCR method were negative for HIV RNA. These results show that cerumen in HIV-positive patients with or without ART has only an insignificant risk for transmission of HIV infection. Cotten et al. showed that 12 out of 20 feces samples were positive for HIV RNA [10]. Kantor et al. found 82 HIVpositive samples among 143 genital secretion samples [8]. Liuzzi et al. reported that semen was an important transmission route; HIV-1 RNA was detected in 25 out of 26 samples of semen, although the viral load in semen was significantly lower than in plasma [11]. Sexual transmission is one of the most common routes of HIV infection.

Ethical approval All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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Does cerumen have a risk for transmission of HIV?

Human immunodeficiency virus (HIV) is mainly transmitted via sexual activity, mother-to-child transmission, and contact with body fluids, such as sali...
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