The Potential Risk of Infectious Disease Dissemination Via Artificial Insemination in

Reprod Dom Anim 46 (Suppl 2), 64–67 (2011); doi: 10.1111/j.1439-0531.2011.01863.x
ISSN 0936-6768
Plenary Article
The Potential Risk of Infectious Disease Dissemination Via Artificial Insemination in
Swine
GC Althouse1 and K Rossow2
1
Department of Clinical Studies, New Bolton Center, School of Veterinary Medicine, University of Pennsylvania, Kennett Square, PA; 2Minnesota
Veterinary Diagnostic Lab, University of Minnesota, St. Paul, MN, USA
Contents
Infectious Diseases of Concern
Artificial insemination (AI) is one of the most widely used
assisted reproductive technologies in swine. To maintain a
healthy semen trade, it is crucial that diligence be given to
managing and minimizing the chance of extended semen
playing an epidemiological role in the transmission of
infectious disease. In swine, pathogens of primary importance, which may be transmitted through semen include
Aujeszky’s disease, brucellosis, chlamydophilosis, porcine
circovirus type 2, classical swine fever, Japanese encephalitis,
leptospirosis, parvovirus, porcine reproductive and respiratory syndrome, rubulavirus, foot-and-mouth disease and
swine vesicular disease. This paper will summarise the
current state of knowledge pertaining to these pathogens
in relation to swine AI.
Bacteria
There are few infectious bacteria that are of concern in
relation to swine AI, and include brucellosis, chlamydophilosis and leptospirosis (Table 1). Even so, it is
important to realise that some bacterial species are a
normal component in a boar ejaculate (Althouse and Lu
2005). These bacteria, along with others, which can
contaminate a sample during semen collection, analysis
or processing, can potentially have a significant impact
on herd reproductive performance through their negative effect on the extended semen product (Althouse
et al. 2000). Good stud hygiene and sanitation (Althouse 2008), along with effective antimicrobial control
in the extender, can work effectively in controlling these
type of contaminants (Althouse et al. 2008). There are
many popular antimicrobials used in semen extenders
(i.e. aminocyclitols, aminoglycosides, ß-lactams, lincosamides and macrolides), yet, are irregular in their
effectiveness against infectious pathogens of concern
(Althouse and Lu 2005).
Brucellosis, caused primarily by Brucella suis (biovars
1, 2, 3) in swine, can be a major cause of reproductive
failure in certain areas of the world (e.g. Africa, Asia
and South America). Even though prevalence may be
low in other areas globally, most countries monitor for
its presence in the domestic herd. A true pathogen of the
reproductive tract, the pathogenesis of brucellosis in
infected boars includes localising in the genital organs
(e.g. accessory sex glands, testes and epididymides).
Subsequently, Brucella sp. has been identified in the
ejaculates of infected boars (Lord et al. 1997). Brucella
organisms appear to be relatively hearty in liquid media
such as milk and water (Timoney et al. 1988), lending
support of the possibility of its transmission via AI
through extended semen. There is or should be no
tolerance for the establishment of this pathogen in a
stud. Diagnostic serology and direct culture under acute
infectious conditions can be quite effective in identifying
suspect carriers and introducing only negative animals
into stud.
Chlamydophilosis in boars can cause disturbances to
the urogenital system, although its preference is to
colonise the intestinal tract, with many pigs being
asymptomatic (Althouse 2007). Although epidemiological data on the distribution of this disease among the
Introduction
Today, artificial insemination (AI) is one of the most
widely used assisted reproductive technologies in
swine. In many countries, AI accounts for the
majority of litters conceived. Key advantages that
lead to its broad application in the swine industry
were the accelerated propagation and amplification of
genetic merit, economic savings, delineated reproductive management and disease control. Ironically, many
of these same advantages can be looked upon as
disadvantages in that AI can propagate and amplify
genetic defects and the spread of infectious disease. It
is the latter of which is the focus of this current
review. Prior reviews on this topic particular to swine
have been published (Thacker et al. 1984; Guerin and
Pozzi 2005; Maes et al. 2008), and one would be
remiss if consultation of these additional works were
not included as part of developing a critical knowledge base.
Because AI can introduce disease into a herd, the
importance of controlling the introduction of pathogenic organisms into a stud can not be overemphasized.
The most common route of disease introduction into a
stud is through direct or close boar-to-boar contact,
which is facilitated by the normally high (40–100%)
boar turnover in a stud. Depending upon the pathogen,
other less likely but equally important routes of disease
introduction into a stud can be via long distance
aerosolisation, fomites, people, insect vectors, birds
and mammals.
2011 Blackwell Verlag GmbH
Infectious disease via artificial insemination in swine
65
Table 1. Selected swine diseases that have been identified in semen and
those verified to have been transmitted via artificial insemination (AI)
Diseases
Aujeszky’s disease
(Pseudorabies)
Brucellosis
Chlamydophilosis
Circovirus type 2 (PCV2)
Classical swine
fever (Hog Cholera)
Foot-and-mouth disease
Japanese encephalitis
Leptospirosis
Parvovirus
Reproductive and
respiratory syndrome
Rubulavirus
(blue eye disease)
Vesicular disease
AI transmission
OIE listed
disease*
Yes
Yes (Madson et al. 2009)
Yes (de Smit et al. 1999)
Yes
No
No
Yes
Yes (Lucas et al. 1974)
Yes (Prieto et al. 1997)
Yes
Yes
Yes
No
Yes
No
Yes
*Source: http://www.oie.int
world’s swine population are sparse, it does appear that
the disease is widespread. Direct evidence has demonstrated the shedding of chlamydophila in semen from
boars standing at stud (Kauffold et al. 2006). Given the
stability of chlamydophila elementary bodies, disease
transmission through AI is a risk. Culture, PCR and
histopathology methodologies have been used to identify this contaminant (Kauffold et al. 2006). Because of
the lack of complete knowledge on this pathogen in
relation to reproductive performance, definitive control
measures remain elusive at this time.
Leptospirosis, caused by Leptospira interrogans, is a
common bacterial disease of swine that can contribute to
reproductive inefficiencies. It is widely distributed
throughout the world, having multiple serovars, some
of zoonotic importance. Leptospirae can localise in the
susceptible boar’s urogenital tract (Ellis et al. 1986),leading to a chronic carrier and shedding state. Acute
bacteremia may result in semen shedding. Strong evidence
supports the transmission of leptospirae in neat and ⁄ or
diluted semen in many species (Kiktenko et al. 1976;
Vinodh et al. 2008), including epizootiological support in
swine (Boqvist et al. 2002). Because of the widespread
nature and potential for economic loss in a swine herd,
effective bacterins are commercially available, which can
be used to control infection in a stud. Leptospira are most
commonly found in wet ⁄ warm climates, therefore, avoidance of surface water use and appropriate treatment of
drinking water can greatly aid in controlling the introduction of this pathogen into a stud. Vaccination can be
effective as part of a stud’s control program.
Viruses
Unlike bacteria, there appear to be numerous viral
pathogens that can interfere with boar fertility, and may
even use semen in its disease transmission (Table 1).
Pathogens that appear to have a global swine industry
presence include porcine circovirus type 2 (PCV2),
porcine parvovirus (PPV) and porcine reproductive
and respiratory syndrome (PRRS). Other viral pathogens of regional concern are Aujeszky’s disease ⁄ pseudo 2011 Blackwell Verlag GmbH
rabies, classical swine fever ⁄ hog cholera, Japanese
encephalitis, rubulavirus ⁄ blue eye disease, foot-andmouth disease and swine vesicular disease.
Although investigations are being conducted looking
at stimulating protective antiviral immunity in the male
reproductive tract (Christopher-Hennings et al. 2008),
current control of viral pathogens should follow along a
plan similar to that outlined earlier with bacterial
pathogens.
Aujeszky’s disease (pseudorabies), caused by suid
herpesvirus type 1, is an important disease globally that
spreads predominantly through animal contact. Primarily a disease which is introduced and then colonises the
respiratory system, viral replication can occur in the
boar genital tract, thus, being found in semen (Medveczky and Szabo 1981; Selivanov and Sedov 1986).
Additionally, under viremic conditions, infected white
blood cells can be shed in the semen, causing an
infectious leucospermia. Herpesviridae are quite stable
in a variety of environments, including liquid media.
They are known to become latent, allowing for periodic
recrudescence and shedding by events such as stress.
Although this virus is not a common cause of primary
reproductive tract infections, it does have epithelial
tropism, allowing for the potential for transmission
through AI. Serologic screening and selection of negative boars is a valuable management tool for keeping
this pathogen out of a stud. Vaccination programmes
may be of value in controlling ⁄ eradicating the disease.
Porcine circovirus type 2 (PCV2) is known to cause a
variety of disease conditions throughout all stages of pig
production, including affecting reproductive performance (West et al. 1999). It is found worldwide and
can be assumed that most if not all herds ⁄ studs have
PCV2 present. Boars have been found to shed PCV2 in
their semen (Larochelle et al. 2000), albeit usually in low
numbers either in leucocytes or free virus in semen.
Recently, reproductive failure was experimentally induced in sows through AI using PCV2-spiked doses
(Madson et al. 2009). It appears that PCV2 can be
intermittently shed and is relatively stable in environments. With the availability of effective vaccines, PCV2
is not commonly tested for in boars and does not appear
to be a pathogen of primary concern in studs.
Classical swine fever, or hog cholera, is a highly
contagious swine disease. Although eradicated in many
parts of the world, in other areas, it remains endemic,
especially in those regions supporting feral hog populations. This relatively stable virus has been found in
boar semen (Choi and Chae, 2003), and has subsequently been found to have been spread through AI in
the Netherlands (de Smit et al. 1999). Infected leucocytes may also be shed in semen, allowing for its
transmission. A mutable RNA virus of high consequence, only test-negative boars originating from negative herds, should be introduced at stud. Vaccines can
be of value in controlling ⁄ eradicating the disease.
Foot-and-mouth disease (FMD) is a highly contagious
and invasive virus. Along with swine, all other artiodactyls can be natural hosts of FMD. The virus generally
enters the body through the respiratory route, followed
by dissemination in tissues (i.e. genital tract) throughout
the body, where it may replicate in epithelial cells.
66
GC Althouse and K Rossow
Shedding of FMD is occurs through excretions and
secretions, including semen (McVicar et al. 1978).
Although sharing similar clinical signs, swine vesicular
disease has a slightly different pathogenesis. Both FMD
and SVD are OIE List A reportable diseases. Both
diagnostic screening and other preventable measures are
available to minimise the introduction of these diseases
into a stud.
Japanese encephalitis (JE) is a mosquito-borne disease
that can cause reproductive failure in swine. Once a boar
is infected, the virus can cause genital tract inflammation
(i.e. orchitis) leading to viral shedding in the semen
(Ogasa et al. 1977). The disease resides throughout
much of the Australasian region and has zoonotic
potential. Diagnostic testing and appropriate vaccine
use may aid in minimising the transmission of this
disease through AI use.
Porcine parvovirus is a highly stable virus, which is
ubiquitous in swine globally. Before effective vaccination programmes were in place, PPV was a common
source of swine reproductive problems. A relatively
thermostable virus, PPV usually infects boars through
the oronasal route. Once infected, colonisation of the
boar’s genital tract can follow, leading to viral shedding
in the semen (Cartwright and Huck 1967). Infection can
occur with PPV inoculation into the uterus (Lucas et al.
1974). Management should establish protocols to ensure
natural exposure of the boar during development in
conjunction with appropriate and regular vaccination.
Porcine reproductive and respiratory syndrome is one
of the primary aetiologic agents responsible for swine
reproductive failure today. Transmission of the disease
can occur through a variety of routes, including
insemination with infected semen (Prieto et al. 1997).
Excretion of PRRS virus via semen appears to occur
most frequently during the acute phases of the infection.
Duration of excretion in semen appears to vary, with
persistent or intermittent excretion occurring days to
months after infection (Christopher-Hennings et al.
1996). A mutable RNA virus with serious health issues
if spread downstream, the presence of this virus in a stud
should not be tolerated. Vaccination does not appear to
offer full protection against re-infections and shedding.
Modified live vaccines are known to be shed in semen
(Madsen et al. 1998; Amonsin et al. 2009). Most semen
sold ⁄ used in the United States has representative
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Author contributions
Dr. Althouse contributed to all aspects of this publication, from
conceptualization through preparation of the final draft. Dr. Rossow
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Conflict of interest
Neither of the authors of this manuscript have any financial or
otherwise conflict of interest to report in relation to being named as an
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Submitted: 8 April 2011; Accepted: 14 June
2011
Author’s address (for correspondence): GC
Althouse, Department of Clinical Studies,
New Bolton Center, School of Veterinary
Medicine, University of Pennsylvania, Kennett Square, Pennsylvania, USA. E-mail:
[email protected]