Bovine Vaccinia: Insights into the Disease in Cattle
Bovine vaccinia (BV), caused by Vaccinia virus (VACV), is a zoonosis characterized by exanthematous lesions in the teats of dairy cows and the hands of milkers and is an important public health issue. Severe VACV-induced lesions in the teats and udder of cows and buffaloes could lead to mastitis and other secondary infections, thereby reducing productivity and resulting in economic losses to the dairy industry. In Brazil, BV re-emerged in the late 1990s and is now endemic in most of the Brazilian territory. In the last 15 years, much effort has been made to know more about this disease and its epidemiology, etiologic agents, and interactions with the host and the environment. In this review, we describe the known dynamics of VACV infection in cattle and the viral shedding routes, as well as the relevance of BV for animal and public health.
Poxviruses infect many invertebrate and vertebrate species, causing diseases that are of great veterinary and public health concern. The genus Orthopoxvirus includes at least 10 antigenically related species with a wide geographical distribution and variable spectra of vertebrate hosts [1,2]. With the exception of Variola virus (VARV), the smallpox etiologic agent, which is a strictly human pathogen, orthopoxviruses that are pathogenic to humans and animals include Cowpox virus (CPXV), Monkeypox virus (MPXV), and Vaccinia virus (VACV) [2].
Smallpox was a devastating disease, responsible for hundreds of millions of cases worldwide, with a mortality rate of one-fifth or more of infected people, until the middle of the twentieth century [3,4]. Highly effective cross-protection among orthopoxviruses enabled the use of CPXV and, later, VACV in the 19th and 20th centuries to prevent smallpox infection, leading to the term “vaccination” [3]. VACV has had an important role in human history owing to its highly effective use as an immunizing agent in the smallpox vaccination campaign, resulting in the global eradication of this deadly disease in 1980 [3].
After the cessation of VACV vaccination, the human population without immunity against smallpox and all other zoonotic orthopoxvirus infections has increased, and zoonotic orthopoxviruses have emerged worldwide [5]. Notable examples include the emergence of CPXV in Europe, MPXV in many African countries, and VACV in India and Brazil [6,7].
Buffalopox is an emerging contagious zoonosis associated with sporadic outbreaks in Asian buffalo (Bubalus bubalis) herds in India, Egypt, Pakistan, Nepal, Bangladesh, and Italy [8,9]. A phylogenetic analysis based on three genes confirmed that the buffalopox virus is closely related to VACV and it was taxonomically identified as a VACV strain [8]. Additionally, on the basis of sequence and phylogenetic analyses of the A56R gene, isolates from cows presenting poxvirus-compatible lesions in 2002–2006 throughout India were more closely related to VACV strains than to CPXV [10].
In Brazil, VACV was initially studied in the 1960s during a Brazilian government effort to survey rural regions for virus circulation, when the first Brazilian VACV was isolated from a wild rodent (Oryzomysgenus) captured in the Brazilian Amazon basin [11]. From that date, or even previously, the occurrence of exanthematous zoonotic disease affecting humans and dairy cows was reported, although in a sporadic manner, and the etiological diagnosis was generally not performed, resulting in a lack of important epidemiological information about VACV circulation in the country [12,13]. However, since the late 1990s, reports of an exanthematous disease affecting cattle and humans have increased [12,13,14,15,16,17,18,19,20,21,22,23,24,25] and have reached endemic proportions in many regions of Brazil. The VACV outbreaks in Brazil are associated with dairy cows and the dairy workers who have direct contact with sick cows. This zoonotic disease was named bovine vaccinia (BV).
There are controversies about the origins of the Brazilian VACV strains. One hypothesis is that these strains originated as an independent, distinct lineage of New World Orthopoxviruses [26,27]. In contrast, there is the hypothesis that the Brazilian VACV strains are derived from the vaccine strain IOC, which was widely used during the smallpox eradication vaccination campaign in Brazil [28,29]. In this last case, it is proposed that the Brazilian VACV strains are derived from an “escaped vaccine strain” originated from an ancient vaccine strain related to the horsepox virus, that established an epidemiological cycle in domestic and/or wild animals after its escape to nature [28,29]. So far, the available data suggest that there is circulation of two different Brazilian VACV lineages, which probably have a distinct evolutionary history [26,27,28,29].
These two genetically distinct groups (Group 1 and Group 2) [26,30] have shown differences in pathogenesis and virulence when inoculated in mice and/or rabbits [25,31,32,33,34]. Mouse and rabbit VACV infection models have demonstrated variation in pathogenesis and virulence among strains as well as a systemic infection in which viral DNA could be detected in urine, feces, saliva, and nasal secretions [25,31,32,33,34]. Infections caused by VACV strains belonging to Group 1 do not cause systemic clinical signs in infected mice, whereas the strains belonging to Group 2 cause clinical signs that may lead to death [25,31]. Despite the existence of both groups in Brazil, Group 1 viruses are isolated more frequently than Group 2 viruses. In particular, 92% of the isolated clones are classified as Group 1, whereas only 8% belong to Group 2 on the basis of an analysis of the A56R gene [25].
Among other South American countries, cutaneous lesions associated with VACV infection have only been described in dairy farmworkers in Colombia [35]. However, VACV circulation in cattle has been detected by serological and molecular diagnosis in Argentina [36] and Uruguay [37], although no clinical signs related to VACV infections have been reported in cattle or in humans in these countries.
In addition to the public health impact, it is also important to emphasize that infectious animal diseases are estimated to be responsible for about 20% of losses in animal production worldwide [38]. According to the Food and Agriculture Organization of the United Nations (FAO), the global demand for animal proteins (i.e., milk, eggs, and meat) is expected to increase by 70% by 2050 [38]. In cattle and buffalo herds, VACV infections are characterized by severe local lesions affecting the udder and teats of lactating animals, leading to mastitis and other secondary infections in more than 40% of affected animals [13]. These infections reduce the productivity of milk by 40–80% and impact milk and cheese producers, mainly the small ones, and the dairy industry [6,13]. Additionally, in farms in which suckling calves are in direct contact with the cows, it is common to observe sick calves presenting lesions in the mouth, which reduce food intake, leading to weight loss [13,18].
BV in Brazil re-emerged in the late 1990s and is currently endemic in most of the Brazilian territory. In this review, we describe VACV infection in cattle, the known viral shedding routes, and the importance of BV for animal and public health.
No comments:
Post a Comment