- Host Animals
- Hosts/Species Affected
- Systems Affected
- Distribution Table
- List of Symptoms/Signs
- Disease Course
- Impact: Economic
- Zoonoses and Food Safety
- Disease Treatment
- Prevention and Control
- Links to Websites
- Distribution Maps
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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- swine influenza
International Common Names
- English: hog flu; pig flu; SIV infection; swine flu; swine influenza, flu; swine influenzavirus infection
- French: grippe porcine; la grippe porcine
OverviewTop of page
Swine influenza (SI) is an acute viral respiratory disease of pigs caused by type A influenza viruses of the family Orthomyxoviridae. Influenza A virus contains a negative-sense RNA genome organized into eight individual segments, allowing for reassortment and production of novel viruses (Lamb et al., 2001). Based upon the major differences within the haemoagglutinin (HA) and Neuroaminidase (NA) of the external protein of the virus, 16 HA and 9 NA subtypes, naturally paired in different combinations, have been identified (Fouchier at al., 2005). Like other influenza A viruses, swine influenza virus is genetically unstable and able to accumulate antigenic changes. Influenza A viruses infect pigs, as well as humans, horses, wild and domestic poultry, waterfowl and some aquatic mammals, but the strains that cause disease in these various species differ. Type B and C influenza viruses are generally limited to humans and they are rare and insignificant in pigs (Brown et al., 1995b). Type B and C influenza viruses are generally limited to humans and they are rare and insignificant in pigs (Brown et al., 1995b).
Swine influenza was first observed in 1918 in the USA, Hungary and China (Chun, 1919; Koen, 1919; Beveridge, 1977), coincident with the devastating human influenza pandemic. The disease in humans and pigs was caused by closely related viruses (Taubenberger et al., 1997; Reid et al., 1999) and it remains uncertain whether the virus spread from humans to pigs or vice-versa. It was not until 1930 that the virus was isolated (Shope, 1931). Currently, swine influenza virus (SIV) is ubiquitous in swine-producing regions of the USA, Asia and Europe.
In its classic epizootic form, SI is characterised by high fever, dullness, loss of appetite, laboured abdominal breathing and coughing, but many subclinical infections also occur. Pigs can also play a role in the epidemiology of human influenza viruses (Webster et al., 1992).
Host AnimalsTop of page
|Animal name||Context||Life stage||System|
|Sus scrofa (pigs)||Domesticated host; Wild host||Pigs: All Stages|
Hosts/Species AffectedTop of page
SIV infection can also occur in feral pigs and in wild boars (Saliki et al., 1998; Markovska-Daniel and Pejsak, 1999), but information on factors that predispose pigs to disease is only available for domestic animals. Among the main factors are the immune status of pigs, management practices and climatic conditions, and intercurrent infections with other respiratory agents.
Clinically typical SI is generally limited to fully susceptible, antibody-negative pigs. In swine-dense regions, breeding animals are usually immune as a result of previous infections and young piglets are protected by maternally-derived immunity until the age of 10-12 weeks. Pigs between 15 and 18 weeks of age, therefore, are most frequently affected (Loeffen et al., 1999). However, in regions or herds that have not been previously exposed to SIV, disease may occur in pigs of all ages.
SIV infection occurs throughout the year, but is clinically most severe during the colder seasons, i.e. during autumn and winter. A whole series of management factors, such as number of pigs per unit, ventilation, etc, is thought to influence the clinical course of SIV infection, but confirmed data are difficult to find.
Intercurrent infections are important complicating factors of a SIV infection. SIV sets the stage for bacterial infections of the lungs, which may cause more severe and prolonged disease and even mortality. There is growing evidence that common respiratory virus infections such as porcine reproductive and respiratory syndrome virus (PRRSV) or porcine respiratory coronavirus (PRCV) often coincide with SIV infection (Laval et al., 1991; Groschup et al., 1993; Reeth and Pensaert, 1994a). In experimental infection studies, fever, respiratory disease and growth retardation were significantly more severe and long-lasting when the virus infections were followed by SIV as compared to each of the single virus infections (Reeth and Pensaert, 1994b; Reeth et al., 1996). All of these viruses, therefore, are considered key-agents in the so-called "porcine respiratory disease complex (PRDC)". Nevertheless, the effects of experimental combined infections with SIV and other viruses can vary from subclinical to extremely severe (Lanza et al., 1992; Pol et al., 1997), indicating that many unknown variables determine the final outcome of combined infections.
Systems AffectedTop of page
DistributionTop of page
Distribution TableTop of page
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.Last updated: 10 Jan 2020
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|-Andaman and Nicobar Islands||Present|
|United Kingdom||Present, Widespread|
|Canada||Present||Present based on regional distribution.|
|United States||Present||Original citation: Hinshaw et al. (1978)|
|-North Dakota||Present, Widespread|
|-South Dakota||Present, Widespread|
|Brazil||Present||Present based on regional distribution.|
|-Rio de Janeiro||Present|
PathologyTop of page
Macroscopic lesions exclusively involve the lungs. There is often extensive lung consolidation, with a sharp line of demarcation between the affected, red and firm lung parts and normal lung tissue. The characteristic histopathological lung lesions include detachment of large areas of bronchial/bronchiolar epithelium and accumulation of exudates containing initially necrotic epithelial cell debris and neutrophils in the air spaces, and later mostly monocytes (Done et al., 1996a, b; Reeth et al., 1999).
SIV infection has been associated with "proliferative and necrotizing pneumonia (PNP)" in pigs in Canada (Morin et al., 1990). Re-examinations of tissues from these cases, however, showed combinations of SIV and PRRSV.
DiagnosisTop of page
Laboratory diagnosis is required for confirmation of SIV infection. The virus can be readily demonstrated in lung tissue or nasal swabs, provided that samples are collected within 24-48 hours after the onset of clinical signs and handled appropriately. Immunofluorescence or immunohistochemical techniques can be applied to frozen lung tissue sections or to paraffin sections (Barigazzi et al., 1993; Haines et al., 1993; Vincent et al., 1997). These tests use an antiserum prepared against either the whole virus (polyclonal antibody) or a specific viral protein (monoclonal antibody) in combination with suitable fluorescent or enzymatic labels to visualise intracellular viral antigens. Depending on the nature of the antisera used one or several influenza virus subtypes can be detected. These tests are relatively rapid and results can be available the same day. Lung tissue samples should be taken at the borders of areas of consolidation, kept refrigerated and provided to the diagnostic laboratory within 24 h.
Virus isolation can be applied to both lung tissue homogenates and nasal secretions. Inoculation of ten-day-old embryonated chicken eggs is considered a gold-standard method, but use of cell lines could improve influenza virus detection from samples (Chiapponi et al., 2010). Viral detection is determined by detection of haemagglutinating activity from egg fluids and cells supernatants 3 days after inoculation. Virus isolation is slow, but remains the most sensitive diagnostic technique. Virus characterization using inhibition of haemoagglutination test is performed. Definitive antigenic characterisation of SIV also requires virus isolation and is generally done by a designated reference centre. If samples for virus isolation can be tested within 48 h after collection, they should be kept at 4°C. Otherwise, storage at –70°C is recommended. Nasal swabs should be suspended in a suitable transport medium or in physiological saline.
Other assays for virus detection include ELISA (Lee et al 1993b). A commercial enzyme immunoassay membrane test (Directigen FLU-A) has been reported to detect influenza A antigen in clinical specimens (Ryan-Poirier et al., 1992).
Detection of influenza A virus could be obtained also by biomolecular tests as RT-PCR and Real Time PCR (Schorr et al., 1994; Spackman et al., 2002; Slomka et al., 2010). Moreover a multiplex RT-PCR has been demonstrated to be useful also for identification of swine influenza virus subtype from samples and isolates (Choi et al., 2002; Lee et al., 2008; Chiapponi et al., 2012).
Serologic diagnosis of SI requires the use of paired sera, the first obtained during the acute phase of the disease and the second 3-4 weeks later. This way, an increase in antibodies can be demonstrated when tested against the appropriate antigens. The haemagglutination-inhibition test is most commonly used. ELISA tests have been developed (Lee et al., 1993a). Commercial diagnostic kits to detect antibody against influenza A (H1N1 and H3N2) virus in pig sera, are available. Serological diagnostic tests for field use are not available.
List of Symptoms/SignsTop of page
|Digestive Signs / Anorexia, loss or decreased appetite, not nursing, off feed||Pigs:Weaner,Pigs:Growing-finishing pig||Diagnosis|
|General Signs / Fever, pyrexia, hyperthermia||Pigs:Weaner,Pigs:Growing-finishing pig||Diagnosis|
|General Signs / Generalized lameness or stiffness, limping||Sign|
|General Signs / Generalized weakness, paresis, paralysis||Sign|
|General Signs / Lack of growth or weight gain, retarded, stunted growth||Pigs:Weaner,Pigs:Growing-finishing pig||Diagnosis|
|General Signs / Overweight, obese, weight gain||Sign|
|General Signs / Reluctant to move, refusal to move||Sign|
|General Signs / Trembling, shivering, fasciculations, chilling||Pigs:Weaner,Pigs:Growing-finishing pig||Sign|
|General Signs / Underweight, poor condition, thin, emaciated, unthriftiness, ill thrift||Sign|
|General Signs / Weight loss||Pigs:Weaner,Pigs:Growing-finishing pig||Sign|
|Nervous Signs / Dullness, depression, lethargy, depressed, lethargic, listless||Sign|
|Ophthalmology Signs / Lacrimation, tearing, serous ocular discharge, watery eyes||Sign|
|Ophthalmology Signs / Purulent discharge from eye||Sign|
|Reproductive Signs / Abortion or weak newborns, stillbirth||Pigs:Gilt,Pigs:Sow||Sign|
|Reproductive Signs / Female infertility, repeat breeder||Sign|
|Reproductive Signs / Small litter size||Sign|
|Respiratory Signs / Coughing, coughs||Pigs:Weaner,Pigs:Growing-finishing pig||Diagnosis|
|Respiratory Signs / Dyspnea, difficult, open mouth breathing, grunt, gasping||Pigs:Weaner,Pigs:Growing-finishing pig||Diagnosis|
|Respiratory Signs / Increased respiratory rate, polypnea, tachypnea, hyperpnea||Pigs:Weaner,Pigs:Growing-finishing pig||Diagnosis|
|Respiratory Signs / Mucoid nasal discharge, serous, watery||Pigs:Weaner,Pigs:Growing-finishing pig||Sign|
|Respiratory Signs / Purulent nasal discharge||Pigs:Weaner,Pigs:Growing-finishing pig||Sign|
|Respiratory Signs / Sneezing, sneeze||Pigs:Weaner,Pigs:Growing-finishing pig||Sign|
Disease CourseTop of page
Typical outbreaks of SI are characterised by a sudden onset of coughing, laboured jerky breathing, fever, anorexia, muscular weakness and weight loss. Morbidity is near to 100%, but mortality is usually less than 1%. Generally, recovery starts after 5-7 days and is almost as sudden and remarkable as the onset. In addition to clinical SI outbreaks, subclinical infections frequently occur. Conversely, secondary bacterial infections leading to pneumonia often increase disease severity and mortality rates. All three SIV subtypes have been associated with this clinical picture (Vandeputte et al., 1980; Haesebrouck et al., 1985; Brown et al., 1995a; Loeffen et al., 1999). SI is occasionally associated with abortion in pregnant sows. There are, however, no indications for transplacental infection and abortion most likely results from the fever associated with SI (Brown et al., 1982).
The typical clinical manifestations can be reproduced experimentally, but only under very specific conditions. Direct inoculation of high virus doses into the trachea of seronegative swine of all ages generally results in "swine flu" symptoms (Haesebrouck et al., 1985; Haesebrouck and Pensaert, 1986b; Reeth et al., 1999). Nonetheless, recovery is rapid, and symptoms persist only for 2 or 3 days. In contrast, inoculation of the same amount of virus by the less invasive oronasal route produces mild clinical signs or an asymptomatic infection (Lanza et al., 1992).
Infection with SIV is generally limited to the respiratory tract. In experimental infections, virus replication has been demonstrated in nasal mucosa, tonsils, trachea and lungs (Haesebrouck and Pensaert, 1986b; Lanza et al., 1992). Low virus titres have occasionally been isolated from serum (Brown et al., 1993a), but virus isolation from extra-respiratory sites has been negative. In the lungs, massive virus replication occurs in epithelial cells of bronchi, bronchioles and alveoli. Virus titres in the lungs may reach up to 8 log10 50% egg infectious doses (EID50)/gram lung tissue (Haesebrouck and Pensaert, 1986b; Reeth et al., 1999) and immunofluorescence studies may show infection of nearly 100% of the epithelial lining of bronchi/bronchioles. In most experimental studies, virus clearance was seen to be extremely rapid. SIV could not be isolated from lungs or other respiratory tract tissues on or after day 7 (Brown et al., 1993a). Influenza-specific antibodies have been detected in the serum and nasal swabs as early as 3 and 4 days post-infection, respectively. There is growing evidence that typical pro-inflammatory mediators, such as the cytokines interferon-alpha, tumour necrosis factor-alpha and interleukin-1, play an important role in symptom formation and lung pathology (Reeth et al., 1999).
EpidemiologyTop of page
SIV infects pigs exclusively via the respiratory tract; infected pigs shed large amounts of virus in their respiratory secretions for approximately 6-7 days (Reeth and Pensaert, 1994b). Virus transmission occurs primarily through direct contact with infected pigs, but airborne transmission between farms is common in densely populated pig regions. Once the infection has appeared in a swine breeding operation, the virus may persist at the farm level. This occurs particularly in larger farms, where successive litters of young piglets become infected as their maternal immunity wanes. In most instances, however, SIV temporarily disappears from an infected herd after an outbreak and becomes reintroduced at some later point.
Three different subtypes of SIV are currently circulating in pigs: H1N1, H3N2, H1N2, moreover, since 2009 also H1N1v pandemic is demonstrated to circulate in swine in 20 countries in the world (Torremorell et al., 2012). Infection or vaccination with one subtype generally fails to protect against another subtype. Consequently, fattening pigs frequently contract infections with two or more SIVs within their lifetime. To further complicate matters, antigenic variants exist within a given subtype. The H1N1 subtype, for example, contains classical and avian-like viruses. Classical H1N1 SIVs are related antigenically to human H1N1 influenza viruses implicated in the 1918-1919 human pandemic (Taubenberger et al., 1997; Reid et al., 1999). Avian-like H1N1 SIVs have been derived entirely from birds (Scholtissek et al., 1983). The prevailing subtypes and their antigenic characteristics are different in different parts of the world and there may be regional differences within a country or continent.
The epidemiology of SI has remained most stable in the USA (Sheerar et al., 1989), where influenza-like illness was already recognised in pigs in 1918 (Koen, 1919). From that time up until the 1990s, influenza among North American pigs has been due almost exclusively to infection with the classical H1N1 subtype (Chambers et al., 1991). In recent years, however, H3N2 infection appears to be on the increase. This subtype has been associated with disease outbreaks in Canada since 1991 (Bikour et al., 1995b) and in the USA since 1998 (Zhou et al., 1999). H3N2 viruses isolated in the USA in 1998 differ from those in Asia or Europe, and they probably arose by genetic recombination between human, swine and, in some cases, avian influenza viruses. Following reassortant events, viruses of the H1N2 subtype now also seem to be established in the North America pig population (Vincent et al., 2009).
In Asia, where pig husbandry practices differ widely in different countries, the SI situation is less clear. Classical H1N1 SIVs are apparently predominant and have been reported in Hong Kong, China, Taiwan, Thailand and Japan since the 1970s (Hsu et al., 1976; Shortridge and Webster, 1979; Kupradinun et al., 1991), though they have probably been prevalent since the 1918-1919 pandemic (Chun, 1919). Southern China may be the area in which human H3N2 viruses regularly cross into pigs (Kundin, 1970). Unlike in Europe, these "human-like" swine H3N2 viruses failed to form reservoirs in pigs in Asia and their association with respiratory disease is unproven (Nerome et al., 1995). H1N2 viruses, derived from classical H1N1 SIVs and "human-like" H3N2 SIVs, frequently cause infection and disease in pigs in Japan (Sugimura et al., 1981; Ouchi et al., 1996) but have not been reported in other Asian countries.
In Europe, H1N1 and H3N2 SIVs have been enzootic in a number of European countries for at least 15-20 years. Avian-like H1N1 viruses, which predominate over classical H1N1 strains in Europe (Brown et al., 1997) were introduced into European mainland pigs in 1979 (Pensaert et al., 1981), when continental Europe was hit by a series of swine flu epizootics, and into pigs in the UK in 1992 (Brown et al., 1993b). The H3N2 SIVs originate from variants of the human influenza virus that caused the "Hong Kong flu" pandemic in 1968. These "human-like" H3N2 viruses have formed a reservoir in European swine since the early 1970s, but it was not until 1984 that they were directly associated with respiratory disease (Haesebrouck et al., 1985). Genetic analyses of swine H3N2 viruses isolated in Italy between 1985 and 1989 have provided evidence of reassortment between the surface glycoprotein genes from human-like swine H3N2 viruses and the internal protein genes from avian-like swine H1N1 viruses (Castrucci et al., 1993). H1N2 viruses have more recently become established in the swine population in the UK, in Belgium (Brown et al., 1995a; Reeth et al., 2000) and in Italy (Moreno et al., 2012) and they have been associated with disease outbreaks in these countries. Interestingly, these viruses differ from H1N2 viruses isolated in Japan (Ito et al., 1998) or occasionally in France (Gourreau et al., 1994). They probably arose by multiple genetic reassortment events, involving human H1N1, human-like swine H3N2 and avian-like H1N1 viruses (Brown et al., 1998). The prevalence and significance of this subtype in other European countries remains to be examined.
Impact: EconomicTop of page
It is thought that the clinical signs of influenza in pigs can add up to 2 weeks to the time that it takes animals to reach market weight. However, exact data on the cost of swine flu outbreaks are difficult to find. The pig respiratory disease complex of which swine influenza is a contributory factor causes significant impact to most pig-producing regions.
Zoonoses and Food SafetyTop of page
Influenza A viruses do exhibit host specificity, but this restriction is not absolute. Most of the time influenza viruses in animal species evolve along separate paths, but occasionally there is interaction among viruses of different lineages (Webster et al., 1992). Pigs are unique in that they are susceptible to influenza viruses of both human and avian origin and they may function as intermediate hosts in transmission of avian influenza viruses to humans. When pigs become doubly infected with avian and human influenza viruses, new reassortant viruses can originate and cross back into humans. Such reassortants often originate in Southeast Asia, where pigs live in close proximity to their farmers. Avian-human reassortant viruses that originated in pigs appeared to be responsible for the human influenza pandemics in 1957 and 1967 in Asia (Webster et al., 1992). In 1976 an outbreak of severe respiratory disease among soldiers at Fort Dix, New Jersey, was determined to be caused by a swine H1N1 influenza virus (Kendal et al., 1977). Nevertheless, such pandemics occur rather infrequently. Occasionally, pigs can serve as direct sources for zoonotic transmission of SIV to humans. There are several documented cases of SIV spread from pigs to humans (Jong et al., 1988; Rota et al., 1989; Claas et al., 1994; Wentworth et al., 1994; Myers et al., 2007), but further person-to-person spread did not occur in any of these cases. In April 2009 H1N1 influenza A virus was isolated in humans in California, the virus showed HA and internal genes similar to those found in reassortant North American swine virus but NA and M genes were closely related to the Euro-Asian avian–like swine influenza lineage (Dawood F.S. et al., 2009). Transmission of SIV from pigs to turkeys has also been reported (Wright et al., 1992; Ludwig et al., 1994; Wood et al., 1997) and a few influenza outbreaks in pigs have been followed immediately by disease signs in turkeys (Mohan et al., 1981).
Because of the lack of a viraemic phase during SIV infection, there is little chance for virus contamination of meat. In addition, the virus is heat-labile and becomes readily inactivated in the tissues of dead animals.
Disease TreatmentTop of page
There is no specific therapy for swine influenza. Antiviral drugs that are used in human influenza patients at risk are too expensive to justify their use in swine. Antibiotics on the other hand may be useful to control concurrent or secondary bacterial infections.
Prevention and ControlTop of page
As SIV spreads readily by air, sanitary measures alone cannot prevent virus infection. Vaccination, on the other hand, is efficacious under certain conditions. Inactivated whole virus or split vaccines, containing an adjuvant, have been licensed in Europe and more recently in the USA. These vaccines are administered intramuscularly. Protection is based on the presence of haemagglutination-inhibiting antibodies in serum and vaccine strains should match antigenically with epidemic strains of SIV. In Europe, vaccines containing two (H1N1 and H3N2) subtypes and three (H1N1, H3N2 and H1N2) subtypes are available. In the USA because of the high variability of the swine influenza viruses involved in the outbreaks, mainly autogenous vaccines are used. The first vaccination should consist of two injections with a 3- or 4-week-interval. Experimentally, two doses of the European SI vaccine were shown to provide complete protection against infection and disease by H1N1 and H3N2 SIVs circulating in the mid 1980s (Haesebrouck and Pensaert, 1986b; Vandeputte et al., 1986). In contrast, the results of vaccination in the field may be disappointing and the cost-effectiveness of vaccination has not yet been proven. The timing of vaccination is one of the critical issues, as feeder pigs should be vaccinated when maternal antibodies have run out, but before infection occurs. The question whether antigenic drift of SIVs can contribute to vaccination breakthroughs needs further investigation.
ReferencesTop of page
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