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Outbreak of Influenza A (H3N2) Variant Virus Infection among Attendees of an Agricultural Fair, Pennsylvania, USA, 2011

Karen K. Wong , Adena Greenbaum, Maria E. Moll, James Lando, Erin L. Moore, Rahul Ganatra, Matthew Biggerstaff, Eugene Lam, Erica E. Smith, Aaron D. Storms, Jeffrey R. Miller, Virginia Dato, Kumar Nalluswami, Atmaram Nambiar, Sharon A. Silvestri, James R. Lute, Stephen Ostroff, Kathy Hancock, Alicia Branch, Susan C. Trock, Alexander Klimov, Bo Shu, Lynnette Brammer, Scott Epperson, Lyn Finelli, and Michael A. Jhung

Author affiliations: Centers for Disease Control and Prevention, Atlanta, Georgia, USA (K.K. Wong, A. Greenbaum, R. Ganatra, M. Biggerstaff, E. Lam, A.D. Storms, J.R. Miller, K. Hancock, A. Branch, S.C. Trock, A. Klimov, B. Shu, L. Brammer, S. Epperson, L. Finelli, M.A. Jhung); Pennsylvania Department of Health, Harrisburg, Pennsylvania, USA (M.E. Moll, E.E. Smith, J.R. Miller, V. Dato, K. Nalluswami, A. Nambiar, J.R. Lute, S. Ostroff); Allegheny County Health Department, Pittsburgh, Pennsylvania (J. Lando, S.A. Silvestri); and Pennsylvania Department of Agriculture, Harrisburg (E.L. Moore)
Suggested citation for this article

Abstract
During August 2011, influenza A (H3N2) variant [A(H3N2)v] virus infection developed in a child who attended an agricultural fair in Pennsylvania, USA; the virus resulted from reassortment of a swine influenza virus with influenza A(H1N1)pdm09. We interviewed fair attendees and conducted a retrospective cohort study among members of an agricultural club who attended the fair. Probable and confirmed cases of A(H3N2)v virus infection were defined by serology and genomic sequencing results, respectively. We identified 82 suspected, 4 probable, and 3 confirmed case-patients who attended the fair. Among 127 cohort study members, the risk for suspected case status increased as swine exposure increased from none (4%; referent) to visiting swine exhibits (8%; relative risk 2.1; 95% CI 0.2–53.4) to touching swine (16%; relative risk 4.4; 95% CI 0.8–116.3). Fairs may be venues for zoonotic transmission of viruses with epidemic potential; thus, health officials should investigate respiratory illness outbreaks associated with agricultural events.
Triple reassortant swine influenza A viruses have circulated in swine herds in North America since 1998 (1–3). On the rare occasions that these viruses infect humans, they are called influenza A variant viruses (4). Viruses resulting from reassortment of swine influenza A (H3N2) virus and influenza A(H1N1)pdm09 (pH1N1) virus have emerged among US swine (4–6), and similar viruses have been identified among swine outside the United States (7,8). During August 2011, the first known human infection with influenza A (H3N2) variant [A(H3N2)v] virus containing the pH1N1 matrix (M) gene was reported in the United States (9). The pH1N1 M gene is implicated in increasing influenza transmissibility in animal models (10,11), and there was concern that this new A(H3N2)v virus could be efficiently transmitted among humans. Because these viruses contain a novel combination of genes, little is known about the epidemiologic and clinical characteristics of human infections.

During August 2011, a child who had attended an agricultural fair in Pennsylvania (Fair A) attended by ≈70,000 persons became ill; the Centers for Disease Control and Prevention (CDC) confirmed infection with A(H3N2)v virus in the child 6 days after Fair A closed and immediately began an investigation with the Pennsylvania Department of Health (PA DOH), the Allegheny County Health Department, and the Pennsylvania Department of Agriculture (PDA) to determine the extent of A(H3N2)v virus transmission and to identify illness risk factors among Fair A attendees.

Methods
Case Finding
We identified cases through multiple methods. First, 1–2 weeks after Fair A closed, PDA investigators conducted open-ended interviews with swine exhibitors to determine whether they or their household members had become ill; exhibitors were identified though a list provided by fair organizers. Ill exhibitors or their surrogates were interviewed by CDC/PA DOH to assess whether their illness met suspected case criteria. Second, members of a national children’s agricultural club who participated in activities in the county where Fair A occurred were interviewed about illness occurring in their households after attendance at Fair A and/or swine exposure. Third, investigators went to another fair (Fair B), which occurred 3 weeks after Fair A ≈20 miles away in the same county, to enroll a convenience sample of Fair B attendees. Investigators enrolled Fair B attendees as they visited the health department booth, food service areas, exhibit halls, rides, and games. Fair B enrollees were subsequently asked during a phone interview whether they or their household members had become ill after attending Fair A. Fourth, media sources, including newspapers, television, and websites, encouraged community members to contact PA DOH if they became ill with influenza-like symptoms after attending Fair A. Fifth, clinicians were encouraged to obtain respiratory specimens from patients with suspected influenza virus infection who had recent swine or agricultural fair exposure and to refer such patients to PA DOH for interview. Sixth, state and county influenza surveillance supported prospective detection of persons with test results positive for influenza. Seventh, ill contacts of case-patients were interviewed by investigators.

If close contacts of case-patients became ill, they were offered testing for influenza virus infection regardless of whether they attended Fair A. Testing was done only if specimens could be collected <7 days after symptom onset; nasopharyngeal swab samples were used for testing.

Retrospective Cohort Study
We conducted a retrospective cohort study among a systematic random sample of members of a children’s agricultural club (Club X) who resided in the county where Fair A occurred and who attended Fair A. Club members were children who conducted projects, such as raising livestock, for exhibition at Fair A. From a list of 994 Club X members, every fourth name was selected, yielding a cohort of 247 children. Using a standard questionnaire, we queried the parents of Club X members about illness occurring since Fair A; animal exposures at Fair A, home, work, and/or school; influenza vaccination history; and underlying medical conditions. If no adult was reached after 3 telephone attempts, the household members were considered nonrespondents. Interviews were conducted 3–4 weeks after Fair A concluded. Levels of swine exposure were categorized as 1) no exposure (attending Fair A but not visiting a swine exhibit); 2) indirect exposure (visiting a swine exhibit but not touching swine at Fair A); and 3) direct exposure (touching swine at Fair A). Risk for illness was estimated from the beginning of Fair A through 7 days after its conclusion.

Case Definitions
A suspected case-patient was a person with >1 sign/symptom of influenza virus infection from >2 of 4 categories occurring <7 days after attending Fair A. Categories were: 1) fever (temperature >38C°) or subjective fever; 2) respiratory (cough, sore throat, or runny nose); 3) gastrointestinal (vomiting or diarrhea); and 4) constitutional (fatigue, muscle aches, or joint pain). At least 1 category was required to be fever or respiratory.

A broad clinical case definition was used because the clinical characteristics of A(H3N2)v virus infections were not well understood. Suspected case-patients were reclassified as noncase-patients if respiratory specimens obtained <7 days after symptom onset had real-time reverse transcription PCR (rRT-PCR) or genomic sequencing results negative for A(H3N2)v virus or if convalescent-phase serology results were negative for A(H3N2)v virus infection.

A probable case-patient was a person <4 years of age (explained below) who met suspected case-patient criteria and who was seropositive for A(H3N2)v virus. A confirmed case-patient was a person who had rRT-PCR and genomic sequencing results positive for A(H3N2)v virus infection; RNA from a respiratory specimen was used for genomic sequencing (12).

Influenza Diagnostic Testing
Respiratory Specimens
Respiratory specimens were obtained <7 days after symptom onset. We used rRT-PCR with the Human Influenza Virus Real-Time RT-PCR Diagnostic Panel (CDC, Atlanta, GA, USA) to test specimens. Specimens positive for influenza A were subtyped, and amplified RNA from specimens with results consistent with A(H3N2)v virus infection (positive for InfA, pdmInfA, and H3 markers) or with indeterminate results underwent partial genome sequencing as described (12,13).

Serologic Testing
We asked suspected case-patients <13 years of age to participate in serologic testing. We chose this age group for testing because it is assumed that children have limited prior exposure to viruses similar to A(H3N2)v virus and therefore fewer cross-reactive antibodies. A convalescent-phase serum sample was obtained from participating suspected case-patients 3–5 weeks after illness onset. Serum samples were tested by microneutralization and hemagglutination inhibition (HI) for antibodies to variant strains A/Minnesota/11/2010 (H3N2) and A/Indiana/08/2011 (H3N2). The outbreak strain could not be used as an antigen because viable virus was not isolated from any of the case-patients. Microneutralization and HI tests were performed as described (14).

Preliminary testing of serum samples collected in 2007–2008 and in 2010 indicates that no children <4 years of age have antibodies to A(H3N2)v virus, but some children 4–13 years of age have cross-reactive antibodies (15). Therefore, test results for children <4 years of age were considered seronegative if HI titers to the variant strains were <10, indeterminate if titers were 10 to <40, and seropositive if titers were >40. Test results for children 4–13 years of age were considered seronegative if titers to the variant strains were <10 and indeterminate if titers were >10. Children with seronegative test results were reclassified as noncase-patients, and those with seropositive results were reclassified as probable case-patients. Children with indeterminate results retained suspected case-patient status.

Animal Investigation
PDA veterinarians routinely inspected all swine at Fair A. In addition, veterinarians called Fair A swine exhibitors 1–2 weeks after Fair A closed to ask whether signs of illness developed in any swine during or shortly after Fair A.

Data Analysis
We entered data into a Microsoft Access 2010 database (Microsoft, Redmond, WA, USA) and analyzed it by using SAS version 9.3 (SAS Institute, Cary, NC, USA). Relative risks and exact 95% CIs, determined by using the Farrington-Manning method (16), are reported for selected exposures.

Ethical Considerations
This investigation was determined to be a response to a public health threat; in accordance with Federal human subjects’ protection regulations, it was not considered to be human subjects research. Participation in interviews was voluntary; parents or guardians were interviewed for subjects <18 years of age. Parents or guardians consented to collection of respiratory and serum samples from subjects <18 years of age. Minors >7 years of age assented to collection of respiratory and serum samples.

Results
Case Finding
Figure


Figure. . . Epidemic curve, by date of illness onset and case status, for 88 cases of influenza A (H3N2) variant virus infection associated with agricultural Fair A, Pennsylvania, 2011. Day 0...
We identified 3 confirmed, 4 probable, and 82 suspected cases, including the index case. No A(H3N2)v virus infections were identified by state or county influenza surveillance or by clinicians among persons who did not attend Fair A. Of the confirmed, probable, and suspected cases, 19 (21%) were identified from Fair A swine exhibitor households, 29 (33%) were identified from Club X households, 4 (4%) were identified among Fair B attendees who also attended Fair A, 34 (38%) were identified among persons who called PA DOH to report illness, 10 (11%) were identified by another case-patient, and 2 (2%) were detected by state influenza surveillance; persons could be identified by >1 method. The median age of all case-patients was 12 years (range 6 months–60 years); 39 (44%) were male (Table 1). Dates of illness onset ranged from day 0–13, where day 0 was the opening day for Fair A (Figure). Most case-patients had illness onset within 4 days after either the swine show or swine auction, and no cases were identified >6 days after the fair ended. Of 87 case-patients for whom medical history was known, 18 (21%) reported at least 1 underlying medical condition. Case-patients reported spending a median of 6 days (range 1–10 days) at Fair A, and 29 (33%) of 89 reported that their household owned swine. Of 87 case-patients for whom swine exposure was known, 80 (92%) reported direct or indirect swine exposure at Fair A.

The first confirmed case occurred in a previously healthy girl <4 years of age who touched swine at Fair A (case-patient 1); fever, cough, and rhinorrhea developed 4 days after she had contact with swine. The second confirmed case occurred in a previously healthy girl in the 4- to 13-year-old age group who exhibited swine at Fair A and had subjective fever and vomiting without respiratory symptoms (case-patient 2). The third confirmed case occurred in a girl in the 4- to 13-year-old age group who had a preexisting medical condition (case-patient 3); the girl had contact with swine at Fair A and was hospitalized for respiratory distress. Of 3 confirmed and 4 probable case-patients, 2 (29%) were male and all were <13 years of age. All confirmed and probable case-patients attended Fair A on or after day 3 of the fair (Table 2). All except case-patient 2 had fever and respiratory symptoms, and all recovered. All 7 confirmed and probable case-patients visited the swine exhibit at Fair A, and 6 (86%) touched swine.

Illness developed in contacts of 4 case-patients (3 suspected and 1 confirmed case-patient); the contacts had not attended Fair A <7 days before illness onset. Respiratory specimens were obtained from 3 of these 4 contacts, including the contact of the confirmed case-patient, <7 days after illness onset; all tested negative for influenza by rRT-PCR, and 1 contact tested positive for rhinovirus. One person declined testing for influenza.

Laboratory Results
Respiratory specimens from case-patients 1 and 3 were positive for InfA, H3, and pdmInfA markers by rRT-PCR, and the specimen from case-patient 2 was InfA positive. Phylogenetic analysis of the 3 specimens showed that the genome contained the M gene from pH1N1 and 7 gene segments (hemagglutinin, neuraminidase, polymerase PB1, polymerase PB2, polymerase PA, nucleocapsid protein, nonstructural protein) similar to those from North American swine H3N2 subtype viruses and variant viruses that previously caused infection in humans (13).

Convalescent-phase serum samples were obtained from 6 (40%) of 15 persons <4 years of age who initially met suspected case-patient criteria; 4 (67%) of the 6 samples were seropositive for A(H3N2)v virus (HI geometric mean titers >57), and 2 (33%) were seronegative. Convalescent-phase serum samples were obtained from 18 (47%) of 38 persons 4–13 years of age who initially met suspected case-patient criteria; 4 (22%) of the 18 samples were seronegative for A(H3N2)v, and 14 (78%) had indeterminate results.

Retrospective Cohort Study
We were able to contact 139 (56%) of the 247 Club X members; 127 (91%) of those contacted agreed to be interviewed. The median age of Club X members was 13 years (range 4–19 years); 47 (37%) were male (Table 3). Of 124 members, 19 (15%) reported >1 underlying medical condition. Members spent a median of 9 days at the fair (range 1–10 days), and 75/125 (60%) exhibited animals at Fair A; 34/125 (27%) exhibited swine. Of 125 families, 83 (66%) owned livestock and 33 (26%) owned swine.

Of 127 Club X members, 15 initially met the suspected case definition. Serologic testing was performed for 3 members: 1 was seronegative for A(H3N2)v virus and was reclassified as a noncase-patient, and 2 had indeterminate results. Thus, 14 (11%) of the 127 Club X members were suspected case-patients. Respiratory specimens were not obtained from any club members.

The risk for suspected case status increased as exposure to swine increased from no exposure (referent) to indirect exposure (relative risk [RR] 2.1; 95% CI 0.2–53.4) to direct exposure (RR 4.4; 95% CI 0.8–116.3; p = 0.07 by Cochran-Armitage trend test); however, these differences were not statistically significant (Table 4). Exhibiting swine was not associated with suspected case-patient status (RR 1.1; 95% CI 0.2–3.2). Suspected case-patient status was more common, but not statistically significantly so, among persons whose families owned swine and among persons who fed or bathed swine or who cleaned the swine pen during the fair (Table 4).

Animal Investigation
The PDA veterinarian inspected >150 swine on day 3 of Fair A. All swine were healthy-appearing at inspection, although fever had developed in 1 pig, and that pig had already been removed from the fair. The febrile pig was housed with other swine at the fair for ≈24 hours before removal; it was not tested for influenza. Another pig died after a seizure on the last day of the fair; the cause of death was unknown.

No other illness in swine was reported to PDA during the fair. After the fair ended, PDA veterinarians attempted to call 135 households of swine exhibitors and reached 80 (59%). Of those 80 households, 8 (10%) reported that the swine they exhibited had signs of respiratory illness during or shortly after the fair. Ill swine had recovered or had been slaughtered before these interviews. No swine were tested for influenza.

Discussion
We describe an outbreak of respiratory illness, including 3 confirmed infections with a variant influenza A virus not identified in humans before August 2011. The outbreak occurred during a large agricultural fair, where humans and animals had opportunities for repeated and/or prolonged contact.

Outbreaks of variant influenza A viruses at agricultural events have been described, and these events may be key settings for zoonotic influenza transmission (17–24). Triple reassortant H3N2 subtype viruses containing the pH1N1 M gene were first identified among swine in the United States in 2009 and have been detected among swine in multiple states, including Pennsylvania (25,26). During July–November 2011, 13 human infections with A(H3N2)v virus containing the pH1N1 M gene were identified, and 5 were linked to agricultural fairs (24). Although the frequency of zoonotic influenza transmission at agricultural events is unknown, these events provide opportunities for swine influenza viruses to infect humans who have contact with infected swine. Human and swine influenza viruses may circulate at these events, creating opportunities for virus reassortment and the emergence of novel strains.

This investigation suggests that swine contact during Fair A was a risk factor for illness. Persons reporting direct contact with swine were more likely to report illness. Most case-patients became ill within 4 days after the swine show or auction, suggesting a temporal relationship between human–swine contact and onset of human illness within <4 days. The epidemic curve, which suggests that case-patients were exposed to a common infectious source that was present for several days, is consistent with the hypothesis that infected swine were present for the duration of the fair. Prior investigations of human variant influenza virus infections have documented contact with infected swine (17,21), and cases have also occurred after contact with apparently healthy swine (4,23). No swine were tested for influenza during this investigation because swine at Fair A had either been slaughtered or had recovered before the first human case was reported; however, triple reassortant H3N2 subtype viruses containing genetic material from pH1N1 have been detected in swine (4–6).

Because of limited diagnostic testing, the extent and distribution of illness caused by A(H3N2)v virus among Fair A attendees are unknown; however, two thirds of children <4 years of age who were tested were seropositive for A(H3N2)v virus. This finding suggests that illness in at least some suspected case-patients can be attributed to A(H3N2)v virus infection. Suspected case-patients had illness onset dates and symptoms similar to those for probable and confirmed case-patients. Symptoms were similar to those of seasonal influenza (27), but no seasonal influenza was circulating at the time in Pennsylvania.

Although we cannot rule out human-to-human transmission of A(H3N2)v virus at or after Fair A, enhanced surveillance after Fair A through the beginning of the typical influenza season detected no additional cases of A(H3N2)v virus infection in the community; this suggests that the virus did not exhibit efficient or sustained human-to-human transmission. However, A(H3N2)v virus infection has occurred with limited human-to-human transmission among persons who reported no swine contact (4).

This investigation is subject to a number of limitations. First, interviews occurred when media sources began reporting “swine flu” linked to Fair A. Persons who became ill after attending Fair A may therefore have been more likely to report swine exposure, thus biasing toward an association between illness and swine exposure. Second, testing for influenza was not conducted for most case-patients. The timing of the investigation allowed for collection of few respiratory specimens and only convalescent-phase rather than paired serum samples. Serologic testing was further limited to young children because cross-reactive antibodies in older age groups made interpretation of test results for convalescent-phase serum samples difficult. Because only convalescent serum samples were obtained and baseline serologic studies for A(H3N2)v were conducted in a different population, it is possible that elevated HI titers among probable case-patients reflect exposure to A(H3N2)v virus before Fair A. Third, because all members of a household would often attend Fair A together, it was rare to identify ill contacts of case-patients who did not also attend Fair A. This made it difficult to evaluate human-to-human transmission in this population. Fourth, case-patients in the cohort study likely include some persons without A(H3N2)v virus infection, and some persons with mild or asymptomatic A(H3N2)v virus infection may have been considered noncase-patients; the resulting misclassification may have caused underestimation of any association between exposures and illness. One person identified during this investigation had rhinovirus infection identified by rRT-PCR testing, and it is possible that noninfluenza respiratory viruses circulated at Fair A and caused illness in some suspected case-patients. Fifth, the small sample size of the cohort limited our ability to detect statistically significant associations between exposures and case status. Last, we were unable to confirm influenza virus infection among swine at Fair A; therefore, the source of the A(H3N2)v virus cannot be confirmed.

Novel influenza A viruses will continue to emerge sporadically, but steps can be taken to reduce risks to human and animal health. Our findings suggests that swine contact increases risk for A(H3N2)v virus infection; therefore, advising fair attendees, especially those at high risk for complications from influenza, to avoid or limit swine contact may help prevent A(H3N2)v virus infections at agricultural events (28). Agricultural club members and others with prolonged swine exposure should also be educated about the risk of zoonotic influenza transmission and actions they can take to reduce transmission risk, such as using personal protective equipment when they or their animals are ill (29). We found simultaneous illness in humans and swine at the fair; this finding supports those from prior studies showing that transmission of influenza virus occurs from swine to humans and vice versa (30–32). Preventing seasonal influenza in humans who have contact with swine (e.g., through annual influenza vaccination) can reduce reassortment opportunities in swine that become co-infected with swine and human influenza viruses. Prompt and thorough investigations should be conducted of all novel influenza virus outbreaks among humans and animals. Investigations can be more timely if patients with influenza-like symptoms inform clinicians of recent swine exposure and if clinicians consider variant influenza virus infection in patients with influenza-like symptoms and recent swine or agricultural fair exposure. Clinicians should work with public health officials to test respiratory specimens by rRT-PCR when they suspect variant influenza virus infection. This investigation was limited by the lack of influenza testing in swine. Representative and timely influenza surveillance among swine, especially during fair season in states where swine are present at agricultural events, would facilitate future investigations.

This outbreak of A(H3N2)v virus infections among persons attending an agricultural fair was likely associated with swine contact. We did not identify sustained human-to-human transmission of A(H3N2)v virus during this investigation; however, the identification of ≈300 human A(H3N2)v virus infections in multiple states during 2011 and 2012 and the occurrence of limited human-to-human transmission in small clusters (33,34) demonstrate that variant influenza viruses remain a public health concern for animals and humans who may infect each other at venues such as agricultural fairs. Collaboration among public health officials with responsibilities for human and animal health is critical to determining the transmissibility and pandemic potential of variant influenza viruses, such as A(H3N2)v virus, and the epidemiologic features of illnesses caused by them.

Dr Wong is an Epidemic Intelligence Service officer in the Influenza Division at the Centers for Disease Control and Prevention in Atlanta, Georgia. Her research interests include influenza and infectious disease modeling.

Acknowledgments
We thank James Rankin, Enzo Campagnolo, Owen Simwale, Larry Sundberg, Marian Lech, Maxine Kopiec, Artis Hall, Judi Sedivy, Tracy Lahew, George Kruckvich, Cynthia Rost, Collene Musho, Ellen Donahue, Patricia Begg, Pauline Ostrowski, Nanette Hanshaw, Craig Shultz, David Truxell, Michael Gronostaj, Megan Casey, Jim Davidson, Zack Moore, Nicole Lee, Loretta Haddy, Grace Chen, Jacqueline Katz, Stephen Lindstrom, Shannon Emery, Erin Burns, Doug Jordan, Paul Gargiullo, and Thomas Gomez for their contributions to the investigation.

This work was supported by the US Centers for Disease Control and Prevention, the Pennsylvania Departments of Health and Agriculture, and the Allegheny County Department of Health. The CDC Experience fellowship in applied epidemiology (to R.G.) was made possible by a public–private partnership supported by a grant to the CDC Foundation from External Medical Affairs, Pfizer Inc.

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30.Forgie SE, Keenliside J, Wilkinson C, Webby R, Lu P, Sorensen O, Swine outbreak of pandemic influenza A virus on a Canadian research farm supports human-to-swine transmission. Clin Infect Dis. 2011;52:10–8. DOIPubMed31.Olsen CW, Brammer L, Easterday BC, Arden N, Belay E, Baker I, Serologic evidence of H1 swine influenza virus infection in swine farm residents and employees. Emerg Infect Dis. 2002;8:814–9. DOIPubMed32.Terebuh P, Olsen CW, Wright J, Klimov A, Karasin A, Todd K, Transmission of influenza A viruses between pigs and people, Iowa, 2002–2004. Influenza Other Respir Viruses. 2010;4:387–96. DOIPubMed33.Centers for Disease Control and Prevention. Limited human-to-human transmission of novel influenza A (H3N2) virus—Iowa, November 2011. MMWR Morb Mortal Wkly Rep. 2011;60:1615–7.PubMed34.Centers for Disease Control and Prevention. Evaluation of rapid influenza diagnostic tests for influenza A (H3N2)v virus and updated case count—United States, 2012. MMWR Morb Mortal Wkly Rep. 2012;61:619–21.PubMedFigure
Figure. . . Epidemic curve, by date of illness onset and case status, for 88 cases of influenza A (H3N2) variant virus infection associated with agricultural Fair A, Pennsylvania, 2011. Day...
Tables
Table 1. Characteristics of case-patients with suspected, probable, or confirmed A(H3N2)v virus infection after attending agricultural Fair A, Pennsylvania, 2011
Table 2. Characteristics of case-patients with confirmed or probable A(H3N2)v virus infection after attending an agricultural Fair A, Pennsylvania, 2011
Table 3. Characteristics of Club X cohort members who attended agricultural Fair A during an outbreak of A(H3N2)v virus infection, Pennsylvania, 2011
Table 4. Characteristics of Club X cohort members, by case status, who attended agricultural Fair A during an outbreak of A(H3N2)v virus infection, Pennsylvania, 2011
Suggested citation for this article: Wong KK, Greenbaum A, Moll ME, Lando J, Moore EL, Ganatra R, et al. Outbreak of influenza A (H3N2) variant virus infection among attendees of an agricultural fair, Pennsylvania, USA, 2011. Emerg Infect Dis [Internet]. 2012 Dec [date cited]. http://dx.doi.org/10.3201/eid1812.121097

DOI: 10.3201/eid1812.121097

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PostPosted: Fri Sep 21, 2012 6:35 am 
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Rport discussed last night

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PostPosted: Fri Sep 21, 2012 8:07 pm 
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Sep 21, 2012 (CIDRAP News) – An investigation of one of the first swine-origin H3N2 influenza cases detected in the United States in 2011 suggests that for each confirmed case, there may be many more that go undetected.

The investigation, triggered by a case related to a Pennsylvania fair in August 2011, revealed 3 confirmed cases, 4 probable cases, and 82 suspected cases of variant H3N2 (H3N2v), all of them in people who had attended the fair, according to a report published yesterday in Emerging Infectious Diseases.

The virus could not be confirmed in most cases because most of those with suspected infections had recovered before the investigation, the report says. But among six children under age 4, an age-group in which retrospective serologic testing for novel flu viruses is more useful than for older groups, four tested positive for antibodies to the virus.

"This finding suggests that illness in at least some suspected case-patients can be attributed to A(H3N2v) virus infection," says the report by investigators from the Centers for Disease Control and Prevention (CDC), the Pennsylvania departments of health and agriculture, and the Allegheny County Health Department in Pittsburgh.

The investigators also found signs that greater exposure to pigs increased the risk of having a suspected case, though this finding was not statistically significant. They found no clear evidence of efficient or sustained human-to-human transmission of the virus.

The three confirmed cases discussed in the report were among 12 that were identified in 2011. So far this year more than 300 cases have been found, nearly all of them over the summer in people who had exposure to pigs at county and state fairs. Also, a few cases of variant H1N2 and one case of variant H1N1 have cropped up recently, also associated with fairs.

All of these variant strains have picked up the M (matrix) gene from the 2009 H1N1 virus.

Casting a wide net
The first infection in the 2011 Pennsylvania cluster was confirmed by the CDC 6 days after the fair closed, and it prompted the CDC and state and local officials to launch a hunt for other cases and possible risk factors, according to the new report.

The investigators cast a wide net to find possible cases. They interviewed swine exhibitors at the fair and members of a national children's agricultural club in the county where the fair occurred. They used the media to encourage people to contact the state health department if they were sick after attending the fair. Also, they encouraged clinicians to obtain samples from patients with flu-like illness after swine or fair exposure.

In addition, the researchers questioned sick contacts of case-patients, and they interviewed visitors at another, later fair in the same county to find out if they had gotten sick after attending the earlier fair. Finally, they used regular flu surveillance to find cases.

The team defined a suspected case-patient as a person who, within 7 days after attending the fair, had one or more flu signs or symptoms from at least two categories, such as fever, respiratory, gastrointestinal, and "constitutional" (fatigue, joint pain). Confirmation of a case was based on reverse-transcriptase polymerase chain reaction (RT-PCR).

Serologic (antibody) testing of suspected case-patients was used to define probable cases. Children age 13 and younger were asked to undergo such testing, because it was assumed they would have little previous exposure to viruses like H3N2v and therefore fewer cross-reactive antibodies, which make results hard to interpret. Previous studies indicated that no children younger than 4 have antibodies to H3N2v, but some children between 4 and 13 have cross-reactive antibodies, the report says.

Consequently, a probable case-patient was defined as a suspected case-patient younger than 4 who had an H3N2v antibody titer over 40. Because of possible cross-reactive antibodies, children between 4 and 13 were considered seronegative if they had an antibody titer under 10 and indeterminate if titers were higher than that.

On this basis, the investigation yielded 3 confirmed, 4 probable, and 82 suspected cases. The three confirmed cases included the initial case and are included in the official total of 12 H3N2v cases the CDC has listed for 2011, said Michael Jhung, MD, a medical epidemiologist in the CDC's Influenza Division and senior author of the study.

Of the 89 total case-patients, 19 (21%) were from households of exhibitors at the original fair, 29 (33%) were from households of ag club members, 4 (4%) had attended both the earlier and the later fair, 34 (38%) had called the state health department to report an illness, 10 (11%) were identified by another case-patient, and 2 (2%) were found through state flu surveillance. Some were identified by more than one method.

Illnesses followed swine exposure
The patients ranged in age from 6 months to 60 years, with a median of 12 years. Most of them got sick within 4 days after the swine show or the swine auction at the fair. The patients spent a median of 6 days at the fair, and 80 of 87 patients with available information reported direct or indirect exposure to swine there.

Of the three confirmed case-patients, one was a girl under age 4 and the others were girls between 4 and 13 years old. One of the latter had a preexisting medical condition and was hospitalized for respiratory distress but recovered, according to the CDC. All seven of the confirmed and probable case-patients attended the swine exhibit at the fair.

Karen Wong, MD, a CDC Epidemic Intelligence Service officer and first author of the study, declined to identify the preexisting condition in the girl who was hospitalized. But she said it was among those that are known to be risk factors for flu complications.

In the serologic investigation, convalescent-phase samples were obtained from 6 of 15 suspected case-patients under 4 years old, and 4 of the 6 were seropositive for H3N2v. Serum samples were gathered from 18 suspected case-patients between ages 4 and 13, four of whom tested negative and 14 of whom had indeterminate results.

One contact of each of four case-patients (3 suspected and 1 confirmed) had flu-like illness, though none had attended the fair within 7 days before their illness. For three of the contacts, respiratory samples were obtained within the first week of illness and tested, and all were negative for flu, though one had a rhinovirus.

The investigators interviewed 127 ag club members, 14 (11%) of whom qualified as suspected case-patients. In this cohort, the risk of having a suspected case increased with the degree of swine exposure: no exposure, 4% risk; visiting swine exhibits, 8%; touching swine, 16%. But wide confidence intervals showed that these findings were not statistically significant.

Few sick pigs
An inspection by a veterinarian on the third day of the fair found no visibly sick pigs, though one had been removed earlier because of a fever, the report says. But in a post-fair survey of swine exhibitors, 8 of 80 households said their swine had shown signs of respiratory illness during or shortly after the fair. All of them had recovered or been slaughtered by the time of the survey. No pigs were tested for flu.

Though flu was not confirmed in any of pigs, the investigation suggests that contact with pigs during the fair was a risk factor for illness, the report says. "Persons reporting direct contact with swine were more likely to report illness," and most patients got sick within 4 days after the swine show or auction.

The report says two findings suggest that at least some of the suspected H3N2v cases were real: 4 of 6 children under age 4 had antibodies to the virus, and suspected case-patients had illness-onset dates and symptoms similar to those of the probable and confirmed patients.

Jhung said it is difficult to say whether the H3N2v cases identified in recent months have been just the tip of the iceberg or if most cases have been detected, thanks to increased awareness and surveillance.

"I think it's reasonable to assume that we have not identified every case that has occurred since July 2012, but it's difficult to tell how many cases may have gone undetected," he told CIDRAP News via e-mail.

"What I can say is that surveillance for variant influenza in the 10 affected states has been enhanced substantially since the first few cases were identified, and that awareness of H3N2v among public health, animal health (and I suspect the general population, due to media reports) is high."

Jhung said in an interview that more recent and ongoing investigations of H3N2v cases by the CDC and state health departments have come up with results generally similar to this one.

"We're finding pretty much the same thing, that there's an association with swine in an agricultural fair setting, which is why we recommend that people at increased risk for complications of influenza avoid swine," he said. "We're also seeing very rare instances of limited human-to-human transmission during the current outbreak. Notably, what we're not seeing is any evidence of efficient or sustained human-to-human transmission."

He commented that there has been "a pretty dramatic decrease" in new H3N2v cases recently, as most county and state fairs have ended. But a few states have fairs scheduled in October and even into November, he said.

Jhung said he thinks official messages reminding people to watch for signs of respiratory illness in pigs have been effective. "I think people are being extremely careful about that and removing pigs that appear to be ill from the fairs," he said.

In this week's flu surveillance update, the CDC reported no new swine-origin variant flu cases, for the first time since the summer outbreak surfaced in July. The number of confirmed H3N2v cases remained at 305.

Wong KK, Greenbaum A, Moll ME, et al. Outbreak of influenza A(H3N2) variant virus infection among attendees of an agricultural fair, Pennsylvania, USA, 2011. Emerg Infect Dis 2012 December (Early online publication) [Full text]

See also:

Sep 2, 2011, CIDRAP News story on first H3N2v cases

Sep 21 CDC flu update

http://www.cidrap.umn.edu/cidrap/conten ... swine.html

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PostPosted: Mon Sep 24, 2012 1:04 pm 
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Published Date: 2012-09-23 17:05:24
Subject: PRO/AH/EDR> Influenza (90): USA H3N2v, human cases under-estimated
Archive Number: 20120923.1305983

INFLUENZA (90): USA H3N2V, HUMAN CASES UNDERESTIMATED
*****************************************************
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Date: Fri 21 Sep 2012
Source: CIDRAP News [abridged, edited]
http://www.cidrap.umn.edu/cidrap/conten ... swine.html


An investigation of one of the 1st swine-origin H3N2 influenza cases detected in the United States in 2011 suggests that for each confirmed case, there may be many more that go undetected. The investigation, triggered by a case related to a Pennsylvania fair in August 2011, revealed 3 confirmed cases, 4 probable cases, and 82 suspected cases of variant H3N2 (H3N2v), all of them in people who had attended the fair, according to a report published yesterday [20 Sep 2012] in Emerging Infectious Diseases [ref. below]. The virus could not be confirmed in most cases because most of those with suspected infections had recovered before the investigation, the report says. But among 6 children under age 4, an age-group in which retrospective serologic testing for novel flu viruses is more useful than for older groups, 4 tested positive for antibodies to the virus. "This finding suggests that illness in at least some suspected case-patients can be attributed to A(H3N2v) virus infection," says the report by investigators from the Centers for Disease Control and Prevention (CDC), the Pennsylvania departments of health and agriculture, and the Allegheny County Health Department in Pittsburgh. The investigators also found signs that greater exposure to pigs increased the risk of having a suspected case, though this finding was not statistically significant. They found no clear evidence of efficient or sustained human-to-human transmission of the virus.

The 3 confirmed cases discussed in the report were among 12 that were identified in 2011. So far this year [2012], more than 300 cases have been found, nearly all of them over the summer in people who had exposure to pigs at county and state fairs. Also, a few cases of variant H1N2 and one case of variant H1N1 have cropped up recently, also associated with fairs. All of these variant strains have picked up the M (matrix) gene from the 2009 H1N1 virus.

The 1st infection in the 2011 Pennsylvania cluster was confirmed by the CDC 6 days after the fair closed, and it prompted the CDC and state and local officials to launch a hunt for other cases and possible risk factors, according to the new report. The investigators cast a wide net to find possible cases. They interviewed swine exhibitors at the fair and members of a national children's agricultural club in the county where the fair occurred. They used the media to encourage people to contact the state health department if they were sick after attending the fair. Also, they encouraged clinicians to obtain samples from patients with flu-like illness after swine or fair exposure.

In addition, the researchers questioned sick contacts of case-patients, and they interviewed visitors at another, later fair in the same county to find out whether they had gotten sick after attending the earlier fair. Finally, they used regular flu surveillance to find cases.

The team defined a suspected case-patient as a person who, within 7 days after attending the fair, had one or more flu signs or symptoms from at least 2 categories, such as fever, respiratory, gastrointestinal, and "constitutional" (fatigue, joint pain). Confirmation of a case was based on reverse-transcriptase polymerase chain reaction (RT-PCR). Serologic (antibody) testing of suspected case-patients was used to define probable cases. Children aged 13 and younger were asked to undergo such testing, because it was assumed they would have little previous exposure to viruses like H3N2v and, therefore, fewer cross-reactive antibodies, which make results hard to interpret. Previous studies indicated that no children younger than 4 have antibodies to H3N2v, but some children between 4 and 13 have cross-reactive antibodies, the report says. Consequently, a probable case-patient was defined as a suspected case-patient younger than 4 who had an H3N2v antibody titer over 40. Because of possible cross-reactive antibodies, children between 4 and 13 were considered seronegative if they had an antibody titer under 10 and indeterminate if titers were higher than that. On this basis, the investigation yielded 3 confirmed, 4 probable, and 82 suspected cases. The 3 confirmed cases included the initial case and are included in the official total of 12 H3N2v cases the CDC has listed for 2011, said Michael Jhung, MD, a medical epidemiologist in the CDC's Influenza Division and senior author of the study.

Of the 89 total case-patients, 19 (21 percent) were from households of exhibitors at the original fair, 29 (33 percent) were from households of ag club members, 4 (4 percent) had attended both the earlier and the later fair, 34 (38 percent) had called the state health department to report an illness, 10 (11 percent) were identified by another case-patient, and 2 (2 percent) were found through state flu surveillance. Some were identified by more than one method.

Illnesses followed swine exposure: The patients ranged in age from 6 months to 60 years, with a median of 12 years. Most of them got sick within 4 days after the swine show or the swine auction at the fair. The patients spent a median of 6 days at the fair, and 80 of 87 patients with available information reported direct or indirect exposure to swine there. Of the 3 confirmed case-patients, one was a girl under age 4, and the others were girls between 4 and 13 years old. One of the latter had a preexisting medical condition and was hospitalized for respiratory distress but recovered, according to the CDC. All 7 of the confirmed and probable case-patients attended the swine exhibit at the fair.

One contact of each of 4 case-patients (3 suspected and one confirmed) had flu-like illness, although none had attended the fair within 7 days before their illness. For 3 of the contacts, respiratory samples were obtained within the 1st week of illness and tested, and all were negative for flu, although one had a rhinovirus.

An inspection by a veterinarian on the 3rd day of the fair found no visibly sick pigs, though one had been removed earlier because of a fever, the report says. But in a post-fair survey of swine exhibitors, 8 of 80 households said their swine had shown signs of respiratory illness during or shortly after the fair. All of them had recovered or been slaughtered by the time of the survey. No pigs were tested for flu.

[Byline: Robert Roos]

--
Communicated by:
ProMED-mail Rapporteur Kunihiko Iizuka

[The Abstract of the paper "Outbreak of Influenza A (H3N2) Variant Virus Infection among Attendees of an Agricultural Fair, Pennsylvania, USA, 2011" by Karen K. Wong et al. in Emerg Infect Dis 2012 December (Early online publication) http://wwwnc.cdc.gov/eid/article/18/12/ ... rticle.htm, reads as follows:

"During August 2011, influenza A (H3N2) variant [A(H3N2)v] virus infection developed in a child who attended an agricultural fair in Pennsylvania, USA; the virus resulted from reassortment of a swine influenza virus with influenza A(H1N1)pdm09. We interviewed fair attendees and conducted a retrospective cohort study among members of an agricultural club who attended the fair. Probable and confirmed cases of A(H3N2)v virus infection were defined by serology and genomic sequencing results, respectively. We identified 82 suspected, 4 probable, and 3 confirmed case-patients who attended the fair.

Among 127 cohort study members, the risk for suspected case status increased as swine exposure increased from none (4 percent; referent) to visiting swine exhibits (8 percent; relative risk 2.1; 95 percent CI 0.2-53.4) to touching swine (16 percent; relative risk 4.4; 95 percent CI 0.8-116.3). Fairs may be venues for zoonotic transmission of viruses with epidemic potential; thus, health officials should investigate respiratory illness outbreaks associated with agricultural events."

Subsequent to this investigation, for the 1st time since the summer outbreak began in July 2012, the CDC reported no new swine-origin variant flu cases, and the number of confirmed H3N2v cases remained at 305. - Mod.CP

A HealthMap/ProMED-mail map can be accessed at: http://healthmap.org/r/1hiS.]

See Also

Influenza (88): USA (MN) H3N2v, human cases 20120918.1299231
Influenza (87): USA, H3N2, H1N2, H1N1, human cases 20120917.1297468
Influenza (83): USA (MN) A(H1N2)v human infection 20120908.1286721
Influenza (82): USA A(H3N2)v, 1st human death 20120901.1276404
Influenza (80): USA (WN) A(H3N2)v 20120831.1275553
Influenza (79): USA (MN) human infection, correction 20120831.1275374
Influenza (79): USA (MN) human infection 20120830.1273921
Influenza (77): (USA) A(H3N2)v 20120826.1264634
Influenza (76): (North America), A(H3N2)v 20120821.1255415
Influenza (74): USA, A(H3N2)v, more states affected 20120820.1252968
Influenza (73): USA (PA), A(H3N2)v 20120819.1251882
Influenza (72): A(H3N2)v, asymptomatic pigs 20120819.1251848
Influenza (70): A(H3N2)v update 20120817.1249415
Influenza (69): A(H3N2)v, CDC update 20120811.1239668
Influenza (68): A(H3N2)v, age-related seroprotection 20120810.1238403
Influenza (67): USA (IN, OH), A(H3N2)v, more cases 20120809.1236861
Influenza (66): USA (OH), A/(H3N2)v, infected pigs 20120807.1232623
Influenza (65): swine influenza, A/(H3N2)v, OIE status 20120806.1229963
Influenza (64): USA, A/(H3N2)v, CDC report 20120805.1228593]
.................................................cp/msp/mpp

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PostPosted: Thu Sep 27, 2012 5:59 pm 
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PostPosted: Thu Sep 27, 2012 6:04 pm 
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niman wrote:
Image

Note that the only CONFIRMED H3N2v cases in this figure are PEOPLE, not swine.

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PostPosted: Thu Oct 11, 2012 3:14 pm 
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Commentary

http://www.recombinomics.com/News/10111 ... Human.html

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PostPosted: Thu Oct 11, 2012 4:38 pm 
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Published Date: 2012-10-11 15:35:27
Subject: PRO/AH/EDR> Influenza (98): human-animal interface, WHO
Archive Number: 20121011.1337739

INFLUENZA (98): HUMAN-ANIMAL INTERFACE, WHO
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Date: Mon 1 Oct 2012
Source: WHO, Programmes and Projects [edited]
http://www.who.int/influenza/human_anim ... index.html


A. Human infection with avian influenza A(H5N1) virus and associated animal health events:
-----------------------------------------------------
From 2003 through 1 Oct 2012, 608 laboratory-confirmed human cases with avian influenza A(H5N1) virus infection have been officially reported to WHO from 15 countries, of which 359 died. Since January 2012, 30 human cases of influenza A(H5N1) virus infection have been reported to WHO. Since the last update [10 Sep 2012], no new laboratory-confirmed human cases with influenza A(H5N1) virus infection have been reported to WHO. Public health risk assessment for avian influenza A(H5N1) viruses: The public health risk for the virus remains unchanged.

B. Human infection with other non-human influenza viruses
---------------------------------------------------------
A(H3N2) variant virus infection
-------------------------------
The United States of America (USA) reported few additional human cases of influenza A(H3N2)v, and no additional deaths. The large majority of cases have been associated with swine exposure, though instances of likely human-to-human transmission have been identified. No sustained human-to-human transmission has been reported.

Limited serological studies [1-4] indicate that adults may have some pre-existing immunity to this virus but children do not. Seasonal vaccines do not provide cross protection against A (H3N2)v infection. WHO has identified several candidate vaccine viruses specific for A(H3N2)v that could be used to produce an (H3N2)v vaccine if needed [5].

Overall public health risk assessment for influenza A(H3N2)v viruses:
Further human cases and small clusters may be expected as this virus is circulating in the swine population in the USA and people may continue to be exposed, especially through the autumn. Close monitoring of the situation is warranted as schools have started again and changing weather conditions may favor influenza transmission.

A(H1N1) variant virus infections
--------------------------------
As a result of enhanced surveillance around the agricultural fairs, a case of human infection with H1N1 variant influenza virus was detected and reported from the USA [6]. The case occurred in August 2012 in a previously healthy woman. She was not hospitalized and recovered from her illness. The person had direct contact with swine at a State Fair. No further cases were identified. This is the 2nd case of infection with this H1N1v virus in the USA; the previous case occurred in 2011.

Canada also reported a case of human infection with influenza A(H1N1)v in an adult male with underlying risk factors. He developed symptoms at the end of August [2012] and was hospitalized with pneumonia in September. He had occupational exposure to swine. No additional cases have been reported.

The influenza A(H1N1)v viruses isolated from patients in the USA and Canada have an haemagglutinin similar to human seasonal influenza viruses circulating very recently in people, which might suggest some existing population immunity except in young children. Current seasonal vaccines would provide cross protection against these viruses. Available data indicates that the virus would be susceptible to antivirals (neuraminidase inhibitors; oseltamivir and zanamivir).

Overall public health risk assessment for influenza A(H1N1)v viruses:
Further human cases and small clusters of human infection with these viruses may be expected as they are circulating in swine populations. No human-to-human transmission with this virus has been reported. It is expected that the human populations are largely protected by existing immunity except for young children and by the seasonal influenza vaccine.

Because influenza viruses evolve constantly and change characteristics and behavior unpredictably, WHO continues to stress the importance of global monitoring of variant influenza viruses and recommends to all Member States to strengthen routine surveillance activities.

All human infections with non-human influenza viruses as such are reportable to WHO under IHR (2005). More information on influenza at the human-animal interface is available from WHO (http://www.who.int/influenza/human_animal_interface/en/); additional information on influenza in animals is available from OIE (http://www.oie.int/animal-health-in-the ... influenza/) and FAO (http://www.fao.org/avianflu/en/index.html), and OFFLU (http://www.offlu.net).

References
----------
1. CDC. Antibodies cross-reactive to influenza A(H3N2) variant virus and impact of 2010-11 seasonal influenza vaccine on cross-reactive antibodies -- United States. MMWR 2012; 61(14): 237-41; [available at http://www.cdc.gov/mmwr/preview/mmwrhtml/mm6114a1.htm].
2. Skowronski, et al. Cross-reactive antibody to swine influenza A(H3N2)subtype virus in children and adults before and after immunisation with 2010/11 trivalent inactivated influenza vaccine in Canada, August to November 2010. Euro Surveillance 2012; 17(4); available at http://www.eurosurveillance.org/ViewArt ... leId=20066.
3. Waalen et al. Age-dependent prevalence of antibodies cross-reactive to the influenza A(H3N2) variant virus in sera collected in Norway in 2011; Euro Surveillance 2012; 17(19); available at http://www.eurosurveillance.org/ViewArt ... leId=20170.
4. Danuta Skowronski, et al. Cross-reactive and vaccine-induced antibody to emerging swine influenza A(H3N2)v, JID 2012; available at http://jid.oxfordjournals.org/content/e ... l.pdf+html.
5. WHO. Candidate vaccine viruses for variant influenza A(H3N2); available at http://www.who.int/influenza/vaccines/v ... index.html.
6. CDC. H1N2 variant virus detected in Minnesota; available at http://www.cdc.gov/flu/spotlights/h1n2v-cases-mn.htm.

Relevant links
--------------
- WHO table: cumulative number of confirmed human cases of avian influenza A/(H5N1) reported to WHO: http://www.who.int/influenza/human_anim ... 1cases.pdf
- WHO table: H5N1 avian influenza: timeline of major events http://www.who.int/influenza/human_anim ... update.pdf
- WHO archive: avian influenza situation updates: http://www.who.int/influenza/human_anim ... index.html
- World Organisation of Animal Health (OIE) webpage: web portal on avian influenza: http://www.oie.int/animal-health-in-the ... influenza/
- Food and Agriculture Organization of the UN (FAO) webpage: avian influenza: http://www.fao.org/avianflu/en/index.html
- Updated unified nomenclature system for the highly pathogenic H5N1 avian influenza viruses: http://www.who.int/influenza/gisrs_labo ... index.html

--
communicated by:
ProMED-mail rapporteur Marianne Hopp

[This document includes an epidemiological curve of avian influenza H5N1 cases in humans by country and month of onset, and a useful map of avian influenza H5N1 cases in humans for 2012. Readers are recommended to view these illustrations, which can be accessed, via the source URL above. - Mod.CP]


See Also

Influenza (97): USA & worldwide, CDC update 20121004.1324516
Influenza (95): USA (OH) H3N2v, hospitalizations 20120930.1316697
Influenza (94): WHO Update 20120928.1314640
Influenza (93): Canada (ON) H1N1v, sequence data 20120928.1312982
Influenza (91): Canada (ON) H1N1v, human case 20120926.1311060
Influenza (90): USA H3N2v, human cases under-estimated 20120923.1305983
Influenza (88): USA (MN) H3N2v, human cases 20120918.1299231
Influenza (87): USA, H3N2, H1N2, H1N1, human cases 20120917.1297468
Influenza (85): USA: (MN) swine H1N2 influenza, human cases 20120911.1290389
Influenza (83): USA (MN) A(H1N2)v human infection 20120908.1286721
Influenza (82): USA A(H3N2)v, 1st human death 20120901.1276404
Influenza (81): WHO update 20120831.1275624]
.................................................cp/mj/sh

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