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\begin{document}

\title{On skunk rabies and its prevention in North America}



\author[1]{Andres Velasco-Villa}%
\affil[1]{Center for Disease Control and Prevention}%


\vspace{-1em}



  
  \date{May 17, 2024}


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\selectlanguage{english}
\begin{abstract}
The case report by Navarro-Lopez et al., (2023) in this issue describes
a thorough differential diagnosis in an equine with acute neurological
disease. Rabies was confirmed by direct fluorescent antibody test (DFA).
Rabies virus (RABV) was isolated from brain tissue of the ill mare by
intracerebral inoculation in sucking mice. Sequencing and phylogenetic
inference allowed the identification of the rabies virus variant (RVV)
associated with this case. Thus, Navarro-Lopez et al., reported that the
rabid mare got infected with a rabies virus variant associated with
skunks. This clinical commentary elaborates on the seemingly rare skunk
rabies across North America (NA) highlighting its relevance in human and
animal health that have remained somehow neglected%
\end{abstract}%



\sloppy


\textbf{On skunk rabies and its prevention in North America}

Andres Velasco-Villa

Centers for Disease Control and Prevention, 1600 Clifton Rd. NE,
Atlanta, GA 30333

Disclaimer: The opinions and conclusions expressed in this report are
those of the authors and do not necessarily represent the official
position of the CDC or the US Department of Health and Human Services

The case report by Navarro-Lopez et al., (2023) in this issue describes
a thorough differential diagnosis in an equine with acute neurological
disease. Rabies was confirmed by direct fluorescent antibody test (DFA).
Rabies virus (RABV) was isolated from brain tissue of the ill mare by
intracerebral inoculation in sucking mice. Sequencing and phylogenetic
inference allowed the identification of the rabies virus variant (RVV)
associated with this case. Thus, Navarro-Lopez et al., reported that the
rabid mare got infected with a rabies virus variant associated with
skunks. This clinical commentary elaborates on the seemingly rare skunk
rabies across North America (NA) highlighting its relevance in human and
animal health that have remained somehow neglected.

Over the last two centuries, skunks have been one of the most common
wildlife rabid animals across NA (Gremillion-Smith et al., 1988; Ma et
al., 2023; Oertli et al., 2009). Early reports of skunk rabies
transmitted to humans, companion animals, and farm animals, date from
1826 in lower California (Johnson 1971), where most exposures were
associated with spotted skunks (\emph{Spilogale spp} ). Skunk rabies
across the Central Great Plains mainly involving striped skunks
(\emph{Mephitis mephitis} ) began to be observed during the second half
of the 19\textsuperscript{th} century (Hovey 1874).

Due to advances in molecular epidemiology, phylogenetics and notable
improvements on wildlife rabies surveillance (primarily passive both
laboratory-based and epidemiological), it is now known that the skunk
rabies epizootic is comprised by regional independent enzootics in which
RVVs with particular evolutionary histories predominate (Charlton et
al., 1988; Clark et al., 2015; Kuzmina et al., 2013). The north-central
skunk (NC SK), the California skunk (CA SK), the Baja California Sur
Mexico skunk (BCSMX SK), the Northwest Mexico skunk (NWMX SK), and the
Yucatan Mexico skunk (YUCMX SK) enzootics, maintain circulation of
specific RVVs that originated from long standing dog rabies epizootics
prevailing in their respective regions, Figure 1 (Barton et al., 2012;
Davis et al., 2013; Kuzmina et al., 2013; Velasco-Villa et al., 2002;
2005; 2008; 2017). Meanwhile, the South-central skunk (SC SK) and the
North-central Mexico skunk (NCMX SK) enzootics, maintain RVVs that
originated from ancestral bat rabies epizootics, Figure 1 (Barton et
al., 2012; Davis et al., 2013; Kuzmina et al., 2013; Velasco-Villa et
al., 2002; 2005; 2008; 2017).

Thus far, individuals of all skunk species in NA have been reported to
be rabid (\emph{Conepatus leuconotus} , \emph{Conepatus semistriatus}
,\emph{Mephitis mephitis} , \emph{Mephitis macroura} , \emph{Spilogale
gracillis} , \emph{Spilogale putorius} , \emph{Spilogale leucoparia}
and\emph{Spilogale yucatanensis} ), however only \emph{M. mephitis} and
some\emph{Spilogale spp} have been recognized as major rabies reservoir
hosts across NA (Aranda et al., 1999; Dragoo et al., 2004; 2006;
Gremillion-Smith et al., 1988; Oertli et al., 2009; Velasco-Villa et
al., 2002; 2005).

Albeit their divergent origins, all RVVs circulating in NA skunk
populations seem to be virulent and capable of causing rabies in any
sympatric mammal a rabid skunk may encounter (Barton et al., 2012;
Charlton et al., 1991; Hill et al., 1993). Rabies is a highly lethal
infectious disease for all mammals including the rabies reservoir hosts
-- \emph{i.e} ., mammal species in the Carnivore and Chiroptera orders
that play a central role in maintaining specific RVVs through
intraspecific transmission (Smith 1989). The most common mechanism of
rabies transmission is by direct contact through bites of sick animals
infected with RABV. However, rabies could be acquired through contact
with RABV infected/contaminated saliva or brain tissue from a rabid
animal in open wounds or mucosa (Fisher et al., 2018). The incubation
period for rabies in skunks varies from 21 to 117 days, which is similar
to that observed in most mammals (Gremillion-Smith et al., 1988; Oertli
et al., 2009; Borchering et al., 2012). A rabid skunk may stay alive for
up to 10 days after the onset of neurological signs (Charlton et al.,
1987). However, RABV shedding in saliva can occur up to 6 days before
the onset of neurological signs (Charlton et al., 1991), thereby, any
skunk bite should be considered as a rabies exposure, particularly if
the animal is not available for laboratory diagnosis. The most common
rabies signs in rabid skunks are abnormal behavior (active during
daytime), hyperesthesia, hypersensitiveness to light noise or movement,
incoordination, and extremely aggressive behavior (Gremillion-Smith et
al., 1988; Oertli et al., 2009). Rabid skunk attacks on people or
animals have been reported as incursions at animal enclosures, people's
homes and/or camping sites (Johnson 1971; Hovey 1874; Gremillion-Smith
et al., 1988; Oertli et al., 2009).

Skunk rabies occurs throughout the year with disease peaks during
spring, when males increase their regular home range for mating. Skunk
rabies epizootic cycles have been reported to occur every 4, 6, 8 or 20
years in the U. S. and Canada, depending on the region or the period of
observation (Charlton et al., 1991; Gremillion-Smith et al., 1988;
Oertli et al., 2009; Pybus 1988).

Understanding the current geographic distribution of rabies enzootics
and the main reservoir host species associated with them allows for a
better design of species targeted control, prevention, and elimination
strategies, as well as for tailored outreach campaigns aimed at the most
vulnerable populations (Fehlner-Gardiner et al., 2018; Pepin et al.,
2017; Wohlers et al., 2018). Striped skunks (\emph{M mephitis} ) are
considered generalist, while other species such as \emph{Conepatus spp
and Spilogale spp} could be more specialized inhabiting diverse
ecosystems, comprising high forests to plains and semi-desertic regions,
including transition areas. Unlike most skunk species, striped skunks
have successfully adapted across the urbanization gradient, including
densely populated areas (Harrington et al., 2017; Hass and Dragoo 2017;
Ramey et al., 2013). Skunks may be targeted for removal or exclusion,
due to the nuisance provoked by their pungent defense scent and the
occasional damage they cause to people properties or crops (Harrington
et al., 2018). In some instances, skunks may be removed through
poisoning or trapping. The latter is not considered practical, nor cost
effective or feasible in rural and farm areas (Harrington et al., 2018).
Skunk extermination or extirpation from certain areas often leads to
ecological imbalances and the emergence of pests, namely rodents and
some insects they predate on (Harrington et al., 2018; Hass and Dragoo
2017). Measures that combine oral rabies vaccination and humane
population control (such as hormone derived contraception or relocation
measures) may be more acceptable and effective to mitigate rabies
exposures to humans, companion and farm animals (Charlton et al., 1992;
Elmore et al., 2017; Feldhamer et al., 2003; Richards et al., 2019).

Skunk rabies rarely affects humans in the U. S. and Canada, with only
few cases reported in Mexico in the last three decades (Aranda et al.,
1999; Arechiga-Ceballos et al., 2022). Securing camping tent's entrances
and/or keeping doors closed at homes and stables may help prevent
incursions of rabid skunks (Gremillion-Smith et al., 1988; Hovey 1874;
Johnson 1971; Oertli et al., 2009). There is no accurate estimation of
the total number of rabies cases due to skunk RVVs or rabid skunk
exposures in domesticated and wildlife animals throughout NA (Ma et al.,
2023). Nonetheless, it would be recommended to be cautious of its
presence at regions known enzootic for skunk rabies (Fehlner-Gardiner et
al., 2018;). Economic losses due to skunk rabies in farm animals have
not been accurately estimated, but the loss of high-value breeders,
racehorses, or other farm animals due to skunk rabies have been reported
(Aranda et al., 1999; Arechiga-Ceballos et al., 2022; Velasco-Villa et
al 2002). Commonly available parenteral rabies vaccines labeled for use
in cattle, horses, and other farm animals, protect against all known
RVVs, including those present in rabid skunks (Green et al., 2011;
Wohlers et al., 2018). However, having pre-exposure vaccination
(receiving vaccine before an exposure to rabies occurs), both humans and
animals does not always warrant 100\% immunity after severe exposure to
a confirmed rabid animal (Larghi 2004; National Association of State
Public Health Veterinarians Committee 2008). If the viral entry location
(bites) is too close to the head or the spine, and a high RABV load has
been delivered by a rabid animal, RABV could potentially reach the
central nervous system (CNS) before the immune system can stop infection
at the periphery (Brunt et al., 2021; Green t al., 2011). Once RABV
reaches the CNS, rabies will be almost 100\% fatal, thereby it is highly
recommended to consult a veterinarian or a rabies medical expert to help
assess exposure levels and decide the pertinence to provide booster
vaccinations (Green et al., 2011; National Association of State Public
Health Veterinarians Committee 2008; Rupprecht et al., 2006).

Currently, there are no systematic oral vaccination campaigns to reduce
or eliminate the skunk rabies epizootic in NA (Elmore et al., 2017).
However, some efforts have been conducted in the U. S and Canada to
reduce or mitigate the associated risks that imply the expansion of
skunk rabies outbreaks, or the establishment of new RVVs in certain
skunk populations (Elmore et al., 2017; Fehlner-Gardiner et al., 2012;
Slate et al., 2005). Examples of outbreaks and the detection of none
skunk-associated RVVs in skunks include a skunk rabies outbreak in
Flagstaff Arizona, where skunk to skunk rabies transmission of a RVV
maintained by big brown bats lasted over consecutive years; and southern
Canada where intraspecific rabies transmission of the raccoon RVV in
skunk populations sparked a rabies outbreak among skunks (Elmore et al.,
2017).

Since skunks seem to have remarkable ecological plasticity and an
outstanding susceptibility to RABV from different origins, it would not
be surprising if new skunk rabies enzootic cycles appear (Elmore et al.,
2017; Fehlner-Gardiner et al., 2012; Slate et al., 2005). Rabies
vaccination should be considered to mitigate the effects of skunk
transmitted rabies in horses and all other rabies susceptible farm
animals when pertinent (Green et al., 2011; National Association of
State Public Health Veterinarians Committee 2008; Rupprecht et al.,
2006). Feasibility of oral rabies vaccination for skunks continues to be
explored, and ongoing research efforts include improvement of the uptake
(such as improved vaccine baits that could be more attractive for skunk
consumption), as well as formulations that evaluate different vectors,
and genetically modified RABVs and their concentrations (Elmore et al.,
2017; Fehlner-Gardiner et al., 2012; Slate et al., 2005).

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\textbf{Hosted file}

\verb`Distribution of skunk RABV variants in North America Clinical commentary.ppt`  available at \url{https://authorea.com/users/622602/articles/645658-on-skunk-rabies-and-its-prevention-in-north-america}

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