Tuberculosis Incidence Is High in HIV-Infected African Children But Is Reduced by Co-Trimoxazole & Time on Antiretroviral Therapy

BACKGROUND:

There are few data on tuberculosis (TB) incidence in HIV-infected children on antiretroviral therapy (ART). Observational studies suggest co-trimoxazole prophylaxis may prevent TB, but there are no randomized data supporting this. The ARROW trial, which enrolled HIV-infected children initiating ART in Uganda and Zimbabwe and included randomized cessation of co-trimoxazole prophylaxis, provided an opportunity to estimate the incidence of TB over time, to explore potential risk factors for TB, and to evaluate the effect of stopping co-trimoxazole prophylaxis.

METHODS:

Of 1,206 children enrolled in ARROW, there were 969 children with no previous TB history. After 96 weeks on ART, children older than 3 years were randomized to stop or continue co-trimoxazole prophylaxis; 622 were eligible and included in the co-trimoxazole analysis. Endpoints, including TB, were adjudicated blind to randomization by an independent endpoint review committee (ERC). Crude incidence rates of TB were estimated and potential risk factors, including age, sex, center, CD4, weight, height, and initial ART strategy, were explored in multivariable Cox proportional hazards models.

RESULTS:

After a median of 4 years follow-up (3,632 child-years), 69 children had an ERC-confirmed TB diagnosis. The overall TB incidence was 1.9/100 child-years (95 % CI, 1.5-2.4), and was highest in the first 12 weeks following ART initiation (8.8/100 child-years (5.2-13.4) versus 1.2/100 child-years (0.8-1.6) after 52 weeks). A higher TB risk was independently associated with younger age (<3 years), female sex, lower pre-ART weight-for-age Z-score, and current CD4 percent; fewer TB diagnoses were observed in children on maintenance triple nucleoside reverse transcriptase inhibitor (NRTI) ART compared to standard non-NRTI + 2NRTI. Over the median 2 years of follow-up, there were 20 ERC-adjudicated TB cases among 622 children in the co-trimoxazole analysis: 5 in the continue arm and 15 in the stop arm (hazard ratio (stop: continue) = 3.0 (95 % CI, 1.1-8.3), P = 0.028). TB risk was also independently associated with lower current CD4 percent (P <0.001).

CONCLUSIONS:

TB incidence varies over time following ART initiation, and is particularly high during the first 3 months post-ART, reinforcing the importance of TB screening prior to starting ART and use of isoniazid preventive therapy once active TB is excluded. HIV-infected children continuing co-trimoxazole prophylaxis after 96 weeks of ART were diagnosed with TB less frequently, highlighting a potentially important role of co-trimoxazole in preventing TB.

Below:  Tuberculosis incidence over time after antiretroviral therapy initiation

Full article at:   http://goo.gl/vd6abn

By:  Crook AM1, Turkova A2, Musiime V3,4, Bwakura-Dangarembizi M5, Bakeera-Kitaka S4,6, Nahirya-Ntege P7, Thomason M2, Mugyenyi P3, Musoke P4,8,Kekitiinwa A6, Munderi P7, Nathoo K5, Prendergast AJ9, Walker AS2, Gibb DM2; ARROW Trial Team.

• 1MRC Clinical Trials Unit at UCL, London, UK. angela.crook@ucl.ac.uk.
• 2MRC Clinical Trials Unit at UCL, London, UK.
• 3Joint Clinical Research Centre, Kampala, Uganda.
• 4Makerere University College of Health Sciences, Kampala, Uganda.
• 5Department of Paediatrics and Child Health, University of Zimbabwe Medical School, Harare, Zimbabwe.
• 6Baylor College of Medicine Children's Foundation, Kampala, Uganda.
• 7MRC/UVRI Uganda Research Unit on AIDS, Entebbe, Uganda.
• 8MU-JHU Care Ltd, Kampala, Uganda.
• 9Blizard Institute, Queen Mary University of London, London, UK. 
• BMC Med. 2016 Mar 23;14(1):50. doi: 10.1186/s12916-016-0593-7.

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HIV-Infected Presumptive Tuberculosis Patients Without Tuberculosis: How Many Are Eligible for Antiretroviral Therapy in Karnataka, India?

For certain subgroups within people living with the human immunodeficiency virus (HIV) [active tuberculosis (TB), pregnant women, children <5 years old, and serodiscordant couples], the World Health Organization recommends antiretroviral therapy (ART) irrespective of CD4 count. Another subgroup which has received increased attention is "HIV-infected presumptive TB patients without TB". 

In this study, we assess the proportion of HIV-infected presumptive TB patients eligible for ART in Karnataka State (population 60 million), India. This was a cross-sectional analysis of data of HIV-infected presumptive TB patients diagnosed in May 2015 abstracted from national TB and HIV program records. 

Of 42,585 presumptive TB patients, 28,964 (68%) were tested for HIV and 2262 (8%) were HIV positive. Of the latter, 377 (17%) had active TB. Of 1885 "presumptive TB patients without active TB", 1100 (58%) were already receiving ART. Of the remaining 789 who were not receiving ART, 617 (79%) were assessed for ART eligibility and of those, 548 (89%) were eligible for ART. About 90% of "HIV-infected presumptive TB patients without TB" were eligible for ART. 

This evidence supports a public health approach of starting all "HIV-infected presumptive TB patients without TB" on ART irrespective of CD4 count in line with global thinking about 'test and treat'.

Full article at:   http://goo.gl/TBg0pA

By:  Kumar AM1, Singarajipura A2, Naik B3, Guddemane DK3, Patel Y3, Shastri S2, Kumar S4, Deshmukh R5, Rewari BB5, Harries AD6.

• 1International Union Against Tuberculosis and Lung Disease (The Union), South-East Asia Regional Office, New Delhi, India. Electronic address: akumar@theunion.org.
• 2State TB Cell, Directorate of Health Services, Bangalore, Karnataka, India.
• 3World Health Organization Country Office, New Delhi, India.
• 4Karnataka State AIDS Prevention Society, Bangalore, Karnataka, India; National AIDS Control Organization, Ministry of Health and Family Welfare, New Delhi, India.
• 5National AIDS Control Organization, Ministry of Health and Family Welfare, New Delhi, India.
• 6International Union Against Tuberculosis and Lung Disease (The Union), Paris, France; London School of Hygiene and Tropical Medicine, London, United Kingdom. 
• J Epidemiol Glob Health. 2016 Jan 25. pii: S2210-6006(15)30080-0. doi: 10.1016/j.jegh.2015.12.002.

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Prevalence of Tuberculosis, HIV & TB-HIV Co-Infection among Pulmonary Tuberculosis Suspects in a Predominantly Pastoralist Area, Northeast Ethiopia

BACKGROUND:

TB-HIV co-infection is one of the biggest public health challenges in sub-Saharan Africa. Although there is a wealth of information on TB-HIV co-infection among settled populations in Africa and elsewhere, to our knowledge, there are no published reports on TB-HIV co-infection from pastoral communities. In this study, we report the prevalence of TB, HIV and TB-HIV co-infection among pulmonary TB suspects in the Afar Regional State of Ethiopia.

DESIGN:

In a cross-sectional study design, 325 pulmonary TB suspects were included from five health facilities. Three sputum samples (spot-morning-spot) were collected from each participant. Sputum samples were examined for the presence of acid fast bacilli using Ziehl-Neelsen staining method, and culture was done on the remaining sputum samples. Participants were interviewed and HIV tested.

RESULTS:

Of the 325 pulmonary TB suspects, 44 (13.5%) were smear positive, and 105 (32.3%) were culture positive. Among smear-positive patients, five were culture negative and, therefore, a total of 110 (33.8%) suspects were bacteriologically confirmed pulmonary TB patients. Out of 287 pulmonary TB suspects who were tested for HIV infection, 82 (28.6%) were HIV positive. A significantly higher proportion of bacteriologically confirmed pulmonary TB patients [40 (40.4%)] were HIV co-infected compared with patients without bacteriological evidence for pulmonary TB [42 (22.3%)]. However, among ethnic Afar pastoralists, HIV infections in smear- and/or culture-negative pulmonary TB suspects [7 (7.6%)] and bacteriologically confirmed pulmonary TB patients [4 (11.8%)] were comparable. On multivariable logistic regression analysis, Afar ethnicity was independently associated with low HIV infection [OR=0.16 (95% CI: 0.07-0.37)], whereas literacy was independently associated with higher HIV infection [OR=2.21 (95% CI: 1.05-4.64)].

CONCLUSIONS:

Although the overall prevalence of TB-HIV co-infection in the current study is high, ethnic Afars had significantly lower HIV infection both in suspects as well as TB patients. The data suggest that the prevalence of HIV infection among Afar pastoralists is probably low. However, population-based prevalence studies are needed to substantiate our findings.

Full article at:   http://goo.gl/DEjK5U

By:   Belay M1,2, Bjune G3, Abebe F3.

• 1Aklilu Lemma Institute of Pathobiology, Addis Ababa University, Addis Ababa, Ethiopia.
• 2Department of Community Medicine, Institute of Health and Society, Faculty of Medicine, University of Oslo, Oslo, Norway; mulg2002@yahoo.com.
• 3Department of Community Medicine, Institute of Health and Society, Faculty of Medicine, University of Oslo, Oslo, Norway. 

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TB-HIV Co-Infection among Pregnant Women in Karnataka, South India: A Case Series

Tuberculosis (TB) is a significant contributor to mortality in HIV-infected patients. Concurrent TB infection is also a significant contributing factor to maternal mortality in human immunodeficiency virus (HIV)-infected pregnant women. Studies addressing the outcomes of TB and HIV co-infection among pregnant women are generally infrequent. 

Although limited, the records maintained by the Revised National Tuberculosis Control Programme (RNTCP) and the National AIDS Control Programme (NACP) in Karnataka State, Southern India provide information about the numbers of pregnant women who are co-infected with TB and HIV and their pregnancy outcomes. We reviewed the data and conducted this study to understand how TB-HIV co-infection influences the outcomes of pregnancy in this setting. We sought to determine the incidence and treatment and delivery outcomes of TB-HIV co-infected pregnant women in programmatic settings in Karnataka State in southern India. 

The study participants were all the HIV-infected pregnant women who were screened for tuberculosis under the NACP from 2008 to 2012. For the purposes of this study, the program staff in the field gathered the data regarding on treatment and delivery outcomes of pregnant women. A total of seventeen pregnant women with TB-HIV co-infection were identified among 3,165,729 pregnant women (for an incidence of 5.4 per million pregnancies). 

The median age of these pregnant women was 24 years, and majority were primiparous women with WHO HIV stage III disease and were on a stavudine-based ART regimen. The maternal mortality rates were 18% before delivery and 24% after delivery. The abortion rate was 24%, and the neonatal mortality rate was 10%. The anti-tuberculosis treatment and anti-retroviral treatment outcome mortality rates were 30% and 53%, respectively. 

Although the incidence of TB among the HIV-infected pregnant women was marginally less than that among the non-HIV-infected women, the delivery outcomes were relatively poorer. 

The current strategy for the management of TB among the HIV-positive pregnant women needs urgent review.

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By:   Suresh S1, Sharath BN2, Anita S3, Lalitha R4, Jaya Prasad T5, Rewari BB6.

• 1State Tuberculosis Office, Bangalore, India.
• 2ESIC Medical College and PGIMSR, Bangalore, India. Electronic address: sharathbn@yahoo.com.
• 3St. John's Medical College Hospital, Bangalore, India.
• 4Karnataka State AIDS Prevention Society, Bangalore, India.
• 5School of Public Health, Post Graduate Institute of Medical Education and Research (PGIMER), Chandigarh, India.
• 6National AIDS Control Organization, New Delhi, India. 

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Tuberculosis Disease in HIV-Infected Patients

Excerpted From PowerPoint Slide Deck At:  http://goo.gl/JNjfqx

Via:  http://goo.gl/oXJhGQ

The Impact of HIV Status & Antiretroviral Treatment on TB Treatment Outcomes of New Tuberculosis Patients Attending Co-Located TB & ART Services in South Africa

Background

The implementation of collaborative TB-HIV services is challenging. We, therefore, assessed TB treatment outcomes in relation to HIV infection and antiretroviral therapy (ART) among TB patients attending a primary care service with co-located ART and TB clinics in Cape Town, South Africa.

Methods

In this retrospective cohort study, all new TB patients aged ≥ 15 years who registered and initiated TB treatment between 1 October 2009 and 30 June 2011 were identified from an electronic database. The effects of HIV-infection and ART on TB treatment outcomes were analysed using a multinomial logistic regression model, in which treatment success was the reference outcome.

Results

The 797 new TB patients included in the analysis were categorized as follows: HIV- negative, in 325 patients (40.8 %); HIV-positive on ART, in 339 patients (42.5 %) and HIV-positive not on ART, in 133 patients (16.7 %). Overall, bivariate analyses showed no significant difference in death and default rates between HIV-positive TB patients on ART and HIV-negative patients. Statistically significant higher mortality rates were found among HIV-positive patients not on ART compared to HIV-negative patients (unadjusted odds ratio (OR) 3.25; 95 % confidence interval (CI) 1.53–6.91). When multivariate analyses were conducted, the only significant difference between the patient categories on TB treatment outcomes was that HIV-positive TB patients not on ART had significantly higher mortality rates than HIV-negative patients (adjusted OR 4.12; 95 % CI 1.76–9.66). Among HIV-positive TB patients (n = 472), 28.2 % deemed eligible did not initiate ART in spite of the co-location of TB and ART services. When multivariate analyses were restricted to HIV-positive patients in the cohort, we found that being HIV-positive not on ART was associated with higher mortality (adjusted OR 7.12; 95 % CI 2.95–18.47) and higher default rates (adjusted OR 2.27; 95 % CI 1.15–4.47).

Conclusions

There was no significant difference in death and default rates between HIV-positive TB patients on ART and HIV negative TB patients. Despite the co-location of services 28.2 % of 472 HIV-positive TB patients deemed eligible did not initiate ART. These patients had a significantly higher death and default rates.

Full article at:  http://goo.gl/BJYJ5I

By:  Mweete D. Nglazi^123*, Linda-Gail Bekker¹, Robin Wood¹ and Richard Kaplan¹

¹The Desmond Tutu HIV Centre, Institute of Infectious Disease and Molecular Medicine and the Department of Medicine, Faculty of Health Sciences, University of Cape Town, Cape Town, South Africa

²International Union against Tuberculosis and Lung Disease, Paris, France

³Burden of Disease Research Unit, South African Medical Research Council, Cape Town, Tygerberg, South Africa

 

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Optimizing Mycobacterial Culture in Smear-Negative, Human Immunodeficiency Virus-Infected Tuberculosis Cases

Tuberculosis (TB) is a significant public health problem and the diagnosis in human immunodeficiency virus (HIV)—infected individuals is challenging. The use of mycobacterial culture remains an important complementary tool and optimizing it has important benefits. We sought to determine the effect of an increase in the number of specimens evaluated, addition of nutritional supplementation to the culture medium, sputum appearance and volume on diagnostic yield and time to detection of pulmonary TB among smear-negative, HIV-infected adults.

In this prospective study conducted at the Tshwane District Hospital and Academic TB Laboratory, Pretoria, South Africa we collected three sputum specimens an hour apart from presumptive TB cases at an antiretroviral treatment site. We analysed specimens from 236 patients. Specimen appearance and volume were recorded. All specimens were processed for culture using both standard and supplemented media.

A single specimen identified 79% of PTB cases using standard media; the second and third specimens added 12.5% and 8.3% respectively. Media supplementation, sputum appearance and specimen volume had no effect on culture yield or contamination rates. The mean time to detection was reduced from 19.8 days in standard cultures to 11.8 days in nutrient supplemented cultures (p = 0.002). For every 1 ml increase in sputum volume, time to detection was decreased by a factor of 0.797 (p = 0.011).

Use of an inexpensive culture supplement substantially reduced time to detection and could contribute to reducing treatment delay among HIV-infected cases.

Below:  Proportion of cultures positive by time in days of standard and supplemented cultures

Full article at: http://goo.gl/TMCKNf

By:

N. A. Ismail

Department of Medical Microbiology, Faculty of Health Science, University of Pretoria, Pretoria, South Africa

N. A. Ismail, H. M. Said, S. V. Omar

Centre for Tuberculosis, National Institute for Communicable Diseases, Johannesburg, South Africa

H. M. Said

Department of Medical Microbiology, University of Free State, Bloemfontein, South Africa

Z. Pinini

TB/HIV Directorate, Gauteng Department of Health, Johannesburg, South Africa

N. Beyers, P. Naidoo

Desmond Tutu TB Centre, Department of Paediatrics and Child Health, Stellenbosch University, Cape Town, South Africa

  

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Management of Drug Resistant TB in Patients with HIV Co-Infection

Multidrug-resistant and extensively drug-resistant tuberculosis (MDR- and XDR-TB) are major public health concerns worldwide. Their association with HIV/AIDS infection has contributed to the slowing down of TB incidence decline over the last two decades, therefore representing one of the most important barriers to reach TB elimination. Areas covered: 

The aim of this manuscript is to critically review the recent scientific evidence on the management of drug-resistant TB (essentially MDR- and XDR-TB) in subjects coinfected with HIV, focusing on the two new recently-approved anti-TB drugs delamanid and bedaquiline. The medical search-engine PubMed was used, selecting the time-period January 2013 - February 2015, and using the following Keywords: drug-resistant TB, multidrug resistant TB (or MDR-TB), extensively drug-resistant TB (or XDR-TB), delamanid and bedaquiline. 

Expert opinion: The TB/HIV co-epidemic can be faced by implementing the 12 TB/HIV collaborative activities recommended by the World Health Organization. They are focused on the systematic screening of individuals to detect the Mycobacterium tuberculosis infection in HIV-positives, as well as HIV infection in TB patients in order to ensure a rapid initiation of the anti-retroviral therapy (ART). The clinical and public health management of HIV-positive individuals with MDR-TB is complex and expensive, given the cost of second line anti-TB drugs (including the new drugs, delamanid and bedaquiline) and ART. Political commitment and more investment to identify shorter, cheaper and effective anti-TB and HIV regimens as well as better diagnostics and, hopefully, a vaccine will contribute to boost the efforts to eliminate TB.

Purchase full article at: http://goo.gl/F6d33H

By: Pontali E1, Sotgiu G2, Centis R3, D'Ambrosio L3, Spanevello A4,5, Migliori GB3.

• 1 Department of Infectious Diseases , Galliera Hospital, Mura delle Cappuccina, 14 , 16128 Genova , Italy.
• 2 Clinical Epidemiology and Medical Statistics Unit, Department of Biomedical Sciences , University of Sassari - Research, Medical Education and Professional Development Unit, AOU Sassari, via Padre Manzella, 4 , 07100 , Sassari , Italy.
• 3 WHO Collaborating Centre for TB and Lung Diseases , Fondazione S. Maugeri, Care and Research Institute , via Roncaccio 16, 21049 Tradate , Italy.
• 4 Pneumology Unit , Fondazione Maugeri, IRCCS , via Roncaccio 16, 21049 Tradate , Italy.
• 5 Department of Clinical and Experimental Medicine , University of Insubria , via Guicciardini 9, 21100 Varese , Italy.

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Prevalence & Determinants of HIV in TB Patients in Wuxi City, Jiangsu Province, China: A Cross-Sectional Study

At least one-third of the 34 million people living with human immunodeficiency virus (HIV) worldwide are infected with latent tuberculosis (TB). The aim of this study was to determine the rate of HIV infection in TB patients and its determinants in Wuxi City, China. 

TB patients attending health institutions (12 selected sites) for TB diagnoses and treatment were enrolled in this study. TB diagnoses, treatment and HIV testing were done according to the national guidelines. Blood samples were collected for anonymous HIV testing. Among the TB patients, the HIV-positive rate was 13.66% (1493/10,926). 

Multivariate analysis showed that gender, age, education, marital status, per capita monthly income, patient residence, family size, distance from a health institution, knowledge of HIV-TB co-infection, and knowledge of HIV may be risk factors for HIV-TB co-infection (all: odds ratio > 1, p < 0.05). The prevalence of TB in HIV infected was higher among the study participants. Improving public awareness of HIV-TB co-infection, regularly screening and improved follow-up can reduce the occurrence of HIV-TB co-infection.

Purchase full article at:  http://goo.gl/04bqMf

By: Chen J1, Cao W2, Chen R3, Ren Y4, Li T5.

• 1Department of Nursing, Wuxi No.5 People's Hospital, Wuxi, Jiangsu, P.R. China.
• 2Department of Tuberculosis, Wuxi No.5 People's Hospital, Wuxi, Jiangsu, P.R. China.
• 3Department of Infectious Diseases, Wuxi No.5 People's Hospital, Wuxi, Jiangsu, P.R. China.
• 4Department of Red ribbon Care Center, Wuxi No.5 People's Hospital, Wuxi, Jiangsu, P.R. China renyong196847@163.com.
• 5Department of Medical affairs, the Lixin People's Hospital, Bozhou, Anhui, P.R. China.  

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Treatment Outcomes in Multidrug Resistant Tuberculosis-Human Immunodeficiency Virus Co-Infected Patients on Anti-Retroviral Therapy at Sizwe Tropical Disease Hospital Johannesburg, South Africa

Multidrug resistant-tuberculosis (MDR-TB) is a threat to global tuberculosis control which is worsened by human immune-deficiency virus (HIV) co-infection. There is however paucity of data on the effects of antiretroviral treatment (ART) before or after starting MDR-TB treatment. This study determined predictors of mortality and treatment failure among HIV co-infected MDR-TB patients on ART.

A retrospective medical record review of 1200 HIV co-infected MDR-TB patients admitted at Sizwe Tropical Disease Hospital, Johannesburg from 2007 to 2010 was performed. Chi-square test was used to determine treatment outcomes in HIV co-infected MDR-TB patients on ART. Multivariable logistic regression and Poisson models were used to determine predictors of mortality and treatment failure respectively.

Mortality was higher (21.8 % vs. 15.4 %) among patients who started ART before initiating MDR-TB treatment compared with patients initiated on ART after commencing MDR-TB treatment (p = 0.013). Factors significantly associated with mortality included: the use of ART before starting MDR-TB treatment, severely-underweight and underweight, cavities on chest x-rays at baseline, presence of other opportunistic infectionsand presence of other co-morbidities. Factors predicting failure were severe anaemia, other co-morbidities and modified individualised regimen at baseline.

High mortality among patients already on ART before initiating MDR-TB treatment is a worrisome development. Management of adverse-events, opportunistic infections and co-morbidities in these patients is important if the protective benefits of being on ART are to be maximized. There is the need to intensify intervention programmes targeted at early identification of MDR-TB, treatment initiation, drug monitoring and increasing adherence among HIV co-infected MDR-TB patients.

Full article at: http://goo.gl/xgL37Z

By: Teye Umanah¹, Jabulani Ncayiyana¹², Xavier Padanilam³ and Peter S. Nyasulu^14*

¹Division of Epidemiology and Biostatistics, School of Public Health, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa

²Department of Epidemiology, Gillings School of Global Public Health, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA

³Sizwe Tropical Disease Hospital, Gauteng Department of Health, Sandringham, Johannesburg

⁴Department of Public Health, School of Health Sciences, Monash University, 144 Peter Road, Johannesburg, Rumsuig, South Africa

   

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Childhood Tuberculosis & Human Immunodeficiency Virus Status in Brazil: A Hierarchical Analysis

Human immunodeficiency virus (HIV) infection may impact tuberculosis (TB) diagnosis, clinical presentation and treatment outcomes in children as the signs and symptoms of both diseases overlap.

To compare the sociodemographic and clinical profiles of childhood TB according to HIV status in Brazil.

This was a cross-sectional study of data on subjects aged <15 years retrieved from the Brazilian National Electronic Disease Registry (Sistema de Informação de Agravos de Notificação) database on TB to compare TB-HIV coinfected patients and patients with TB only registered between 2007 and 2011. A hierarchical logistic regression model was applied.

Of 6091 cases analysed, 780 (12%) were TB-HIV patients, while 5311 (87%) presented with TB only. TB-HIV patients were more likely to be institutionalised, to present with relapsed TB and be readmitted after treatment default. They were also more likely to have unfavourable outcomes, including default, death due to TB and death from other causes.

Our study highlights the challenges of using national registers for research into childhood TB

Purchase full article at: http://goo.gl/fnsHs3

By: Dos Santos Dias E1, do Prado TN2, da Silva Guimarães AL1, Ramos MC3, Sales CM2, de Fátima Almeida Lima E3, Sant'Anna CC4, Sanchez M5, Maciel EL6

• 1Laboratory of Epidemiology, Federal University of Espírito Santo, Vitória, Espírito Santo, Rio de Janeiro, Brazil; School of Nursing, Federal University of Espírito Santo, Vitória, Espírito Santo, Rio de Janeiro, Brazil.
• 2Laboratory of Epidemiology, Federal University of Espírito Santo, Vitória, Espírito Santo, Rio de Janeiro, Brazil; School of Nursing, Federal University of Espírito Santo, Vitória, Espírito Santo, Rio de Janeiro, Brazil; Post-Graduate Programme in Infectious Diseases, Federal University of Espírito Santo, Vitória, Espírito Santo, Brazil.
• 3School of Nursing, Federal University of Espírito Santo, Vitória, Espírito Santo, Rio de Janeiro, Brazil.
• 4Faculty of Medicine^, Federal University of Rio de Janeiro, Rio de Janeiro, Rio de Janeiro, Brazil.
• 5Department of Public Health, University of Brasilia, Brasilia DF, Brazil.
• 6Laboratory of Epidemiology, Federal University of Espírito Santo, Vitória, Espírito Santo, Rio de Janeiro, Brazil; School of Nursing, Federal University of Espírito Santo, Vitória, Espírito Santo, Rio de Janeiro, Brazil; Post-Graduate Programme in Infectious Diseases, Federal University of Espírito Santo, Vitória, Espírito Santo, Brazil; Post-Graduate Program in Public Health, Federal University of Espírito Santo, Vitória, Espírito Santo, Brazil.  

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