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Does Smallpox Vaccination Modify HIV Disease Progression Among ART-Naive People Living with HIV in Africa?

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Does Smallpox Vaccination Modify HIV Disease Progression Among ART-Naive People Living with HIV in Africa? Epidemiol. Infect. (2018), 146, 218–226. © Cambridge University Press 2017 doi:10.1017/S0950268817002795 Does smallpox vaccination modify HIV disease progression among ART-naive people living with HIV in Africa? A. DIOUF1,2,3*, H. TROTTIER2,3,T.J.YOUBONG1,N.F.NGOM-GUÉYE4, O. NDIAYE1,A.SECK5,D.SARR6,S.DIOP7,M.SEYDI1,S.MBOUP8, 2,9 10 V. K. NGUYEN AND A. JAYE 1 Department of Infectious Diseases/Regional Research and Training Center on HIV and Associated Diseases, Fann’s University Hospital Center, Dakar, Senegal; 2 School of Public Health, Department of Social and Preventive Medicine, Université de Montréal, Montreal, Canada; 3 Sainte-Justine University Hospital Research Center, 3175 Côte Sainte-Catherine, Montreal, Canada; 4 Ambolatory Treatment Center, Dakar, Senegal; 5 Pasteur Institute, Dakar, Senegal; 6 Health Promotion Center, Sida Service, Dakar, Senegal; 7 National Blood Transfusion Center, Dakar, Sénégal; 8 IRESSEF: Institut de Recherche en Santé, de Surveillance Épidémiologique et de Formation, Dakar, Sénégal; 9 Research Center of the Montreal University Hospital Center (CRCHUM), Montreal, Canada; 10 Medical Research Council Unit The Gambia, Banjul, Gambia Received 4 September 2017; Final revision 24 October 2017; Accepted 14 November 2017; first published online 13 December 2017 SUMMARY We examined the association between a history of smallpox vaccination and immune activation (IA) in a population of antiretroviral therapy-naïve people living with HIV (PLHIV). A cross- sectional study was conducted in Senegal from July 2015 to March 2017. Smallpox vaccination was ascertained by the presence of smallpox vaccine scar and IA by the plasma level of β-2- microglobulin (β2m). The association was analysed using logistic regression and linear regression models. The study population comprised 101 PLHIV born before 1980 with a median age of 47 years (interquartile range (IQR) = 42–55); 57·4% were women. Smallpox vaccine scar was present in 65·3% and the median β2m level was 2·59 mg/l (IQR = 2·06–3·86). After adjustment, the presence of smallpox vaccine scar was not associated with a β2m level 52·59 mg/l (adjusted odds ratio 0·94; 95% confidence interval 0·32–2·77). This result was confirmed by the linear regression model. Our study does not find any association between the presence of smallpox vaccine scar and the β2m level and does not support any association between a previous smallpox vaccination and HIV disease progression. In this study, IA is not a significant determinant of the reported non-targeted effect of smallpox vaccination in PLHIV. Key words: Africa, ART-naïve, immune activation, smallpox vaccination. INTRODUCTION and developments in synthetic biology have fed con- Smallpox was declared eradicated in 1980 by the World cerns about the risk that smallpox might return accord- Health Organization (WHO). The threat of bioterrorism ing to the Independent Advisory Group on Public Health Implications of Synthetic Biology Technology Related to Smallpox [1]. Hence in 2016, the Advisory * Author for correspondence: Dr A. Diouf, Department of Social Committee on Variola Virus Research (ACVVR) and Preventive Medicine, Université de Montréal, CHU recommended the maintenance of stocks of smallpox Sainte-Justine Research Center, 3175 Côte Ste-Catherine, Room B.17·002, Montreal, Qc, Canada. viruses, mainly for research purposes [2]. New smallpox (Email: [email protected]) vaccines have been developed and some are in different This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited. Downloaded from https://www.cambridge.org/core. IP address: 170.106.35.93, on 02 Oct 2021 at 12:36:04, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0950268817002795 Smallpox vaccination and HIV disease progression 219 phases in clinical trials. Higher efficacy and safety therapy (ART)-naïve PLHIV at the « Service des profiles than vaccinia virus (VACV) have been reported, Maladies Infectieuses et Tropicales/Centre Régional suggesting that newer vaccines could be administered de Recherche et de Formation à la Prise en Charge to immunosuppressed persons including people living du VIH et Maladies Associées (SMIT/CRCF) », with HIV (PLHIV) [2, 3]. In this context, it seems Dakar, Senegal. This is a West African country with important to study the epidemiological relationship a concentrated HIV epidemic: HIV prevalence is low between smallpox vaccination and HIV infection. (0·7%) in the general population, but high in key popu- A link between smallpox vaccination and HIV lations such as people who inject drugs, men who have infection has been suggested since the emergence of sex with men and female sex workers [14–17]. HIV epidemic. In vitro experiments have shown that A study population of 101 ART-naïve PLHIV was a previous smallpox vaccination could provide a cer- recruited from the principal HIV treatment sites in the tain protection against HIV infection or disease pro- country: the SMIT/CRCF and the « Centre de gression [4, 5]. Previous studies conducted in African Traitement Ambulatoire (CTA) » which are reference populations have also reported a positive effect on centres for the care of PLHIV, the « Centre de immune systems and on mortality [6, 7]. Promotion de la Santé (CPS) » which is a communal Recent data on the pathogenesis of HIV argue that health centre and the « Centre National de chronic immune activation (IA) is the main factor driv- Transfusion Sanguine (CNTS) » which is the national ing the progression of HIV infection [8]. IA can be blood transfusion centre where HIV screening was sys- influenced by several factors, including co-infections tematically performed for every donor. PLHIV from and the frequency of sexual exposure to HIV. High these sites were included in our study if they: (1) levels of IA are reported in sub-Saharan Africa, where were born before 1980, (2) were ART-naïve, (3) were the majority of PLHIV are found. IA also depends on not hospitalised at the time of the study and (4) signed non-specific immunity and it has recently been shown the inform consent form. that immunity due to the non-specific effect of a patho- The study protocol was approved by the institu- gen persists in humans and can confer strong and innate tional ethical and research review boards of the par- non-specific protection [9]. It has been suggested that ticipating institutions in Senegal: (Comité national smallpox vaccination could provide protection even in d’éthique pour la recherche en santé (CNERS) of the PLHIV. Moreover, some studies have shown that cellu- Ministry of Health) and in Canada (Research lar and humoral immunity of VACV could persist for Ethical Board of Sainte-Justine University Hospital, decades [10–12]. Montreal). We hypothesised that PLHIV who had previously received smallpox vaccination would have a lower level of IA and a slower disease progression than Data collection those who had not. Clinical data were collected during the medical visit Sub-Saharan Africa was the last WHO geograph- and results of laboratory tests were obtained from ical region to eradicate smallpox [13]. In Senegal, patient’s medical charts. These data were reported smallpox vaccine was administered until 1980, when on a case report form designed for the study. smallpox was declared eradicated. Senegal is a setting where IA levels are high and where one of the popula- tions with the most recent smallpox vaccination is pre- History of smallpox vaccination sent. This offers the opportunity to evaluate the The exposure variable was the history of smallpox epidemiological relationship between a previous vaccination. This was ascertained if smallpox vaccine smallpox vaccination and HIV disease progression scar was visible on medical visits. The smallpox vac- using the level of IA as a marker. cine scar presents specific characteristics: it is broken, with a smooth central area, a rough peripheral rim and lines from the centre to the periphery. This differ- METHODS entiates it from the Bacillus of Calmette and Guerin (BCG) vaccine scar. The BCG vaccine is a viable Study design and population avirulent attenuated strain of Mycobacterium tubercu- We conducted a cross-sectional study between July losis which confers protection against certain forms of 2015 and March 2017 on a population of antiretroviral tuberculosis. The BCG vaccine scar is located on the Downloaded from https://www.cambridge.org/core. IP address: 170.106.35.93, on 02 Oct 2021 at 12:36:04, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0950268817002795 220 A. Diouf and others upper left arm with a raised centre. Although both confidence intervals (CIs). Confounding was controlled scars can be round or oval, smallpox scar is usually using a 10% change in estimate method (variables that bigger with a diameter >10 mm, while BCG scar change the estimate by 5|10%| were included in the diameter is <10 mm. Two clinicians independently model) among the following potential confounders: assessed whether or not the smallpox vaccine scar age (35–45/46–55/56–66), sex (male vs female), marital was present, and only concordant cases (agreement status (single, married, divorced, widower), education on presence or absence) were retained. The number level (absence/elementary/high school/university), occu- of smallpox vaccine scars was specified as well as the pation (public or private sector executive, other public diameter of the biggest one. or private sector employee, informal worker, no current occupation), BMI (<18·5/18·5–24·9/525), presence of BCG vaccine scar, HIV serotype (HIV-1, HIV-2, β -2-Microglobulin measurement HIV-1+HIV-2 dual infection), WHO clinical stage The outcome variable was the β-2-microglobulin (stage 1 or 2, stage 3 or 4), estimated glomerular filtra- (β2m) level.
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