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Epidemiology and Transmission of Kaposi's Sarcoma

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Epidemiology and Transmission of Kaposi's Sarcoma Viruses 2014, 6, 4178-4194; doi:10.3390/v6114178 OPEN ACCESS viruses ISSN 1999-4915 www.mdpi.com/journal/viruses Review Epidemiology and Transmission of Kaposi’s Sarcoma-Associated Herpesvirus Veenu Minhas † and Charles Wood * Nebraska Center for Virology, School of Biological Sciences, University of Nebraska, Morrison Center, 4240 Fair Street, Lincoln, NE 68583, USA; E-Mail: [email protected] † Present Address: Department of Epidemiology, College of Public Health, University of Nebraska Medical Center, Omaha, NE 68198, USA. * Author to whom correspondence should be addressed; E-Mail: [email protected]; Tel.: +1-402-472-4559; Fax: +1-402-472-3323. External Editor: Zhi-Ming Zheng Received: 2 September 2014; in revised form: 14 October 2014 / Accepted: 23 October 2014 / Published: 4 November 2014 Abstract: This review summarizes the current knowledge pertaining to Kaposi sarcoma-associated herpesvirus (KSHV) epidemiology and transmission. Since the identification of KSHV twenty years ago, it is now known to be associated with Kaposi’s sarcoma (KS), primary effusion lymphoma, and multicentric Castleman’s disease. Many studies have been conducted to understand its epidemiology and pathogenesis and their results clearly show that the worldwide distribution of KSHV is uneven. Some geographical areas, such as sub-Saharan Africa, the Mediterranean region and the Xinjiang region of China, are endemic areas, but Western Europe and United States have a low prevalence in the general population. This makes it imperative to understand the risk factors associated with acquisition of infection. KSHV can be transmitted via sexual contact and non-sexual routes, such as transfusion of contaminated blood and tissues transplants, or via saliva contact. There is now a general consensus that salivary transmission is the main route of transmission, especially in children residing in endemic areas. Therefore, there is a need to better understand the sources of transmission to young children. Additionally, lack of animal models to study transmission, gold standard serological assay and the lack of emphasis on endemic KS research has hampered the efforts to further delineate KSHV transmission in order to design effective prevention strategies. Viruses 2014, 6 4179 Keywords: KSHV; HHV-8; epidemiology; transmission 1. Introduction Human herpesviruses are large double stranded DNA viruses that are ubiquitous in nature. Of the eight known human herpesviruses two have been implicated to be the etiologic agents for a number of cancers, Epstein-Barr virus, and the Kaposi sarcoma-associated herpesvirus (KSHV). Since its identification in 1994, KSHV is known to be associated with all forms of Kaposi’s sarcoma (KS) primary effusion lymphoma and multicentric Castleman’s disease [1–4]. KS is an AIDS-defining illness and is the most common malignancy present in HIV-1 infected patients [5]. One of the earliest indicators of the upcoming HIV/AIDS epidemic was the sudden appearance of KS and high-grade non-Hodgkin’s lymphoma in young men having sex with men (MSM) [6]. Since KSHV DNA cannot be detected in all infected individuals, a serological assay to detect the presence of antibodies against KSHV is the method of choice to investigate KSHV prevalence in a population. Unlike EBV, global seroprevalence of KSHV varies greatly and is generally high in areas where non-HIV associated forms of KS (classic or endemic forms) have been common [7]. These areas include African and Mediterranean regions, where KSHV seroprevalence ranges from 20% to 80% in the adult populations, whereas seroprevalence in the United States and Northern Europe is generally low (<10%) [8–14]. In South America, the Amerindians have also been identified as a hyperendemic population for KSHV infection [15]. Interestingly, the prevalence in the non- Amerindians is significantly lower. de Souza et al. have recently reported that >70% of children (four to nine years) were positive for KSHV and the prevalence increased with age (>90% in >40 year age group) [16]. This pattern is strikingly similar to Africa, where infection seems to occur in early childhood. In contrast, KS incidence is uncommon and KSHV prevalence is low in most Asian countries [17]. However, in China, KSHV prevalence varies considerably between different regions of the country and is between 7.3% percent and 16.1 percent in adults in different provinces [18–21]. In particular, the prevalence was found to be high in the Xinjiang province, which is located in the northwestern region of China. Interestingly, cases of both classic KS and AIDS-associated KS are found mostly in the Uyghurs and the Kazakh ethnicities [20,21]. The reasons for such geographical and population variations of KS and KSHV distribution remain to be addressed. Our laboratory has conducted extensive cohort studies in Zambia, a sub-Saharan African country. Zambia has been considered as part of the “KS belt”, where endemic KS was prevalent and where significant increase in KS incidence in adults and children has coincided with the emergence of the HIV-1 epidemic [22–24]. This increase in KS incidence is significant because, by 1992, KS accounted for approximately 25% of all childhood cancers diagnosed in Lusaka, the capital of Zambia [25]. This review summarizes some of the results of our cohort studies in Zambia, together with those from other significant studies that have contributed to further our understanding of KSHV transmission and pathogenesis, and, more importantly, explore some of the questions that still remain unanswered and warrant further research. Viruses 2014, 6 4180 2. Modes of Transmission Primary KSHV infection can occur during childhood and as an adult and can be transmitted via both sexual and non-sexual routes. KSHV can be found in the peripheral blood mononuclear cells (PBMCs), saliva, oropharyngeal mucosa, semen, cervico-vaginal secretions, and prostate glands, which may represent the source of both vertical and horizontal transmission [26–29]. The modes of transmission of KSHV may vary in different parts of the world, depending on the endemicity of that region. In non-endemic areas, especially in adults, sexual transmission (homosexual and heterosexual) of KSHV may be the route of transmission [30–32]. However, there is limited information about this route and further extensive studies are needed. Studies have shown that sexual transmission, particularly among MSMs, may play a major role in transmission in non-endemic areas, such as the United States and Western Europe, because the seroprevalence among MSMs is significantly higher as compared to the general population. In the San Francisco Mens Health Study, the prevalence of KSHV infection was reported to be high among MSMs (37.6%) when compared to heterosexual men (no prevalence in this group) [31]. They also reported an association of KSHV prevalence with the number of sexual partners. Other studies have reported that besides the number of sex partners, syphilis infection and hepatitis B infection are also risk factors for acquisition of infection [27,31,33,34]. However, the possibility of sexual transmission among heterosexual individuals remains unclear. Different studies have been inconsistent about the evidence of transmission through heterosexual contact. This can be explained in part by the populations that were investigated. Two African studies have been conducted in commercial sex workers in Nigeria and Kenya, and clearly suggest sexual transmission occurring in the adult population [35,36]. Another study conducted in truckers in Kenya also suggest that there is ongoing sexual transmission during adulthood [37]. However, there are other studies that do not observe any evidence of sexual transmission [38,39]. One of them is a study conducted by Malope et al., in South Africa. This is an interesting study because it had a large sample size and sampling was conducted from miners, sex workers, and other residents of the city. This study did not find any association of KSHV prevalence with sexual behavior. In addition, our study conducted in a group of female sex workers in China showed KSHV prevalence of 10%, which is similar to the general women population, even though the prevalence of other sexually transmitted infections (STI), such as HSV-2 and syphilis, were higher than the general women population. Our study suggested that heterosexual transmission may not be a dominant route for KSHV, at least among Chinese women [40]. Another important issue while investigating sexual transmission is that both kissing and salivary exchange during hetero and homosexual contact is common. This makes it harder to delineate whether the transmission was sexual or oral through saliva. Additionally, it is important to consider that all these studies were cross-sectional in design. Longitudinal cohort studies that can follow individuals for seroconversion and incident infection are needed to truly understand the impact of this route of transmission. Besides sexual transmission, another possible horizontal transmission route is via KSHV contaminated blood transfusion because viral DNA may be detected in 10–15 percent of PBMCs of healthy KSHV seropositive individuals [41,42]. Transmission of KSHV via this route is likely to be inefficient because of the cell associated nature of the virus, and viremia is uncommon, even in KSHV infected individuals. However, blood transfusion has recently been investigated in an elegant study by Viruses 2014, 6 4181 Hladik et al., where they provided strong evidence that
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