Exposure was common in urban and rural areas and remains a potential risk factor for human infection.
To investigate human exposure to live poultry and changes in risk perception and behavior after the April 2013 influenza A(H7N9) outbreak in China, we surveyed 2,504 urban residents in 5 cities and 1,227 rural residents in 4 provinces and found that perceived risk for influenza A(H7N9) was low. The highest rate of exposure to live poultry was reported in Guangzhou, where 47% of those surveyed reported visiting a live poultry market
The novel influenza A(H7N9) virus was identified in early 2013; as of March 31, 2014, a total of 404 laboratory-confirmed cases of human infection had been reported. These cases included 394 in mainland China, 2 in Taiwan, 7 in Hong Kong, and 1 in Malaysia (
Previously published studies have reported that most human infections appear to have occurred as a result of exposure to live poultry, particularly through visits to live poultry markets (LPMs) in urban areas (
We collected information on human exposure to poultry, risk perception and psychological responses to the outbreak, preventive behaviors, and attitudes toward control measures, including closure of LPMs. We used 2 approaches to collect these data. In urban areas, we conducted telephone surveys because access to mobile telephones is high, making the approach feasible. In rural areas, where telephone accessibility is lower, we conducted door-to-door surveys.
We selected 5 large cities for our study to represent diverse levels of socioeconomic development and geographic location: Chengdu, Guangzhou, Shanghai, Shenyang, and Wuhan (
Geographic distribution of urban locations (red stars) and rural locations (blue triangles) selected for population survey to determine human exposure to live poultry and attitudes and behavior toward influenza A(H7N9) in China, 2013. Black dots indicate geographic locations of laboratory-confirmed cases of H7N9 through October 31, 2013. Shading indicates population density (persons per square kilometer). The 5 selected urban locations were Chengdu, capital of Sichuan Province in western China, population 10 million; Guangzhou, capital of Guangdong Province in southern China, population 13 million; Shanghai, a municipality in eastern China, population 23 million; Shenyang, capital of Liaoning Province in northeastern China, population 8 million; and Wuhan, capital of Hubei Province in central China, population 10 million. The 4 rural areas were Dawa County (Panjin city, Liaoning Province), Zijin County (Heyuan city, Guangdong Province), Nanzhang County (Xiangfan city, Hubei Province), and Pengxi County (Suining city, Sichuan Province).
Although we had planned to use the same telephone survey approach in rural areas, a pilot study revealed it was not feasible because the survey would occur during the busy farming season, when residents would not be readily available by telephone. Instead, in rural areas we conducted door-to-door surveys. In mainland China, some cities/counties that are administrated as rural regions actually include semiurban areas, such as towns in a county, and rural areas, such as villages in a town/county. The living conditions and lifestyle of residents in semiurban areas are similar to those of urban residents, whereas residents in rural areas live in a different environment, with low population density and a more self-sustainable life, mainly dependent on farming. We used convenience sampling to choose 4 counties from rural rather than semiurban areas. Rural sites were selected on the basis of the level of economic development (measured by gross domestic product per capita) and the overall incidence of infectious diseases in 2012. Given the tiers of administration levels in mainland China, including province, city, county, town, and village, we selected a city from each of the 4 provinces with mid-level gross domestic product per capita compared with other cities in the province and with an incidence of notifiable infectious diseases above the provincial average. Within each province, we then selected a rural county from each of the 4 cities areas. As a result, we chose Dawa County (Panjin city, Liaoning Province), Zijin County (Heyuan city, Guangdong Province), Nanzhang County (Xiangfan city, Hubei Province), and Pengxi County (Suining city, Sichuan Province) for the study (
After the initial selections, all towns within a county were stratified into high, middle, and low levels of socioeconomic status on the basis of census data (
The urban surveys were conducted in May and June 2013 and the rural surveys in July and August 2013. Ethical approval was obtained from the Institutional Review Board of the Chinese Center for Disease Control and Prevention before the survey was conducted.
All surveys in urban and rural areas were conducted by using the same questionnaire, which was based on an instrument used during the outbreaks of severe acute respiratory syndrome (SARS) in 2003 (
We investigated exposure to live poultry in backyards and in LPMs, which are defined as markets where the public can buy live chickens, ducks, pigeons, and other birds. Because LPMs are rare in rural areas and rural residents seldom visit LPMs, we did not ask rural respondents about exposures to live poultry in LPMs, only about backyard poultry exposure. In urban areas, we asked respondents about frequency of visits to LPMs and behaviors in LPMs (i.e., frequency of purchases, practice of picking up birds before purchasing, location where purchased live poultry were slaughtered). We asked all respondents about perception of risk for influenza A(H7N9) infection and perceived severity of such an infection, preventive practices in general and specifically in response to influenza A(H7N9), and attitudes toward influenza A(H7N9) and closure of LPMs.
Statistical analyses were conducted in R version 2.13.0 (R Foundation for Statistical Computing, Vienna, Austria). We performed descriptive analyses of responses in each location and compared responses between urban areas with and without laboratory-confirmed cases of influenza A(H7N9) by using χ2 tests. For the subset of respondents who reported purchasing live poultry in LPMs during the previous year, we used a multivariate logistic regression model to estimate the associations of age, sex, educational level, and geographic location with attitudes toward closure of LPMs and changes in habits of buying live poultry after public health authorities announced the first human influenza A(H7N9) case on March 31, 2013 (
In the 5 urban areas, 81,266 unique telephone numbers were dialed, and the overall response rate was 8% (number of participants [2,504] divided by number of calls with eligible respondents [29,919]) (
Flowcharts for recruitment of participants for telephone surveys and face-to-face interviews to determine human exposure to live poultry and attitudes and behavior toward influenza A(H7N9) in China, 2013. A) Flowchart for telephone surveys conducted in 5 urban areas: Chengdu (capital of Sichuan Province), Guangzhou (capital of Guangdong Province), Shanghai municipality, Shenyang (capital of Liaoning Province), and Wuhan (capital of Hubei Province). B) Flowchart for face-to-face interviews conducted in 3 rural areas: Dawa county (Panjin city, Liaoning Province), Zijin county (Heyuan city, Guangdong Province), Nanzhang county (Xiangfan city, Hubei Province), and Pengxi county (Suining city, Sichuan Province). CATI, computer-assisted telephone interview; SES, socioeconomic status.
Respondents in urban areas tended to have white-collar jobs or were unemployed, were younger, had more education and higher income, and were less likely to be married than those in rural areas (
| Characteristic | No. (%) persons | |
|---|---|---|
| Urban, n = 2,504 | Rural, n = 1,227 | |
| Male sex | 1,288 (51.4) | 626 (51.0) |
| Age group, y | ||
| 18–44 | 1,938 (77.5) | 685 (55.8) |
| 45–64 | 415 (16.6) | 405 (33.0) |
|
| 147 (5.9) | 137 (11.2) |
| Educational attainment | ||
| No formal education | 38 (1.5) | 86 (7.0) |
| Primary school | 191 (7.6) | 259 (21.1) |
| Middle school | 391 (15.6) | 464 (37.9) |
| High school | 593 (23.7) | 268 (21.9) |
| College and above | 1,291 (51.6) | 148 (12.1) |
| Occupation | ||
| Service workers and shop sales workers | 601 (24.0) | 164 (13.4) |
| Professionals | 504 (20.1) | 66 (5.4) |
| Retired | 293 (11.7) | 61 (5.0) |
| Unemployed | 678 (27.1) | 195 (15.9) |
| Full-time students | 232 (9.3) | 111 (9.0) |
| Homemakers | 96 (3.8) | 86 (7.0) |
| Agricultural and fishery workers | 100 (4.0) | 544 (44.3) |
| Marital status | ||
| Single | 941 (38.1) | 269 (22.0) |
| Married | 1,458 (59.0) | 923 (75.4) |
| Divorced/separated | 35 (1.4) | 12 (1.0) |
| Widowed | 36 (1.5) | 20 (1.6) |
| Average household income, in renminbi* | ||
| No income | 65 (3.0) | 83 (6.8) |
| <3,000 | 368 (17.0) | 748 (61.2) |
| 3,001–6,000 | 627 (28.9) | 264 (21.6) |
| 6,001–10,000 | 408 (18.8) | 80 (6.5) |
| 10,001–50,000 | 396 (18.2) | 28 (2.3) |
| Not sure | 307 (14.1) | 20 (1.6) |
| Recent history of travel away from home | ||
| Yes | 479 (19.1) | 117 (9.6) |
*6.1 Chinese renminbi = $1 US.
We assessed exposures to live poultry and visits to LPMs in the 5 cities. In total, 33% of respondents reported visiting LPMs during the preceding year, the highest proportion in Guangzhou; notable differences were found between cities (
| Exposure | No. (%) persons | p value | ||||
|---|---|---|---|---|---|---|
| Chengdu, n = 500 | Guangzhou, n = 500 | Shanghai, n = 500 | Shenyang, n = 504 | Wuhan, n = 500 | ||
| Frequency of LPM visits in the previous year | <0.001 | |||||
|
| 183 (36.6) | 237 (47.4) | 161 (32.2) | 97 (19.2) | 151 (30.2) | |
| No. live poultry bought in the previous year† | <0.001 | |||||
| 1–2/y | 33 (18.0) | 32 (13.5) | 25 (15.5) | 35 (36.1) | 25 (16.6) | |
| 3–5/y | 31 (16.9) | 27 (11.4) | 30 (18.6) | 23 (23.7) | 28 (18.5) | |
| 6–11/y | 27 (14.8) | 25 (10.5) | 23 (14.3) | 4 (4.1) | 23 (15.2) | |
| 1–3/mo | 33 (18.0) | 56 (23.6) | 32 (19.9) | 10 (10.3) | 29 (19.2) | |
| 1–2/wk | 19 (10.4) | 49 (20.7) | 20 (12.4) | 2 (2.1) | 19 (12.6) | |
| 3–5/wk | 2 (1.1) | 8 (3.4) | 2 (1.2) | 0 | 2 (1.3) | |
| Almost every day | 2 (1.1) | 4 (1.7) | 2 (1.2) | 0 | 2 (1.3) | |
| Almost none | 36 (19.7) | 36 (15.2) | 27 (16.8) | 23 (23.7) | 23 (15.2) | |
| Pick up live poultry before buying‡ | <0.001 | |||||
| Yes | 120 (81.6) | 136 (67.7) | 94 (69.6) | 38 (51.4) | 97 (75.8) | |
| Where did you slaughter the live poultry?§ | 0.601 | |||||
| In LPM | 123 (83.7) | 175 (87.1) | 119 (88.1) | 66 (89.2) | 113 (88.3) | |
| In household | 22 (15.0) | 23 (11.4) | 15 (11.1) | 6 (8.1) | 13 (10.2) | |
| Other places | 2 (1.4) | 3 (1.5) | 1 (0.7) | 2 (2.7) | 2 (1.6) | |
| Not buying or buying less since March 2013¶ | <0.001 | |||||
| Yes | 101 (68.7) | 139 (69.2) | 123 (91.1) | 59 (79.7) | 104 (81.3) | |
| Views toward closure of LPMs# | 0.06 | |||||
| Agree | 37 (25.2) | 54 (26.9) | 53 (39.3) | 25 (33.8) | 35 (27.3) | |
| Closure caused any inconvenience** | ||||||
| More inconvenient | NA | NA | 45 (31.5) | NA | NA | |
| Distance of nearest LPM from home, km | <0.001 | |||||
|
| 12 (13.3) | 39 (31.0) | 21 (18.9) | 5 (13.5) | 6 (15.0) | |
| 0.51–1.00 | 23 (25.6) | 42 (33.3) | 32 (28.8) | 4 (10.8) | 10 (25.0) | |
| 1.01–2.00 | 16 (17.8) | 20 (15.9) | 16 (14.4) | 6 (16.2) | 7 (17.5) | |
| >2.00 | 39 (43.3) | 25 (19.8) | 42 (37.8) | 22 (59.5) | 17 (42.5) | |
| Backyard poultry exposure | 73 (14.6) | 76 (15.2) | 34 (6.8) | 37 (7.3) | 54 (10.8) | <0.001 |
*LPM, live poultry market; NA, not applicable. †Respondents who bought live poultry ≥1/year were further asked about the number of live poultry bought in the previous year, picking up poultry or not before buying, locations where poultry was slaughtered, and changes in poultry purchase behavior since influenza A(H7N9) outbreak. ‡Respondents who answered always/usually to the question “Did you pick up poultry for examination before deciding to buy it?” were categorized as “Yes.” §Respondents who stated that they always/usually have live poultry slaughtered in LPMs were categorized as “In LPM,” whereas those who answered always/usually in household were categorized as “in household.” ¶Respondents who answered not buying since then/still buying but less than before to the question “Has your habit of buying live poultry changed since H7N9 was identified in China in March 2013?” were categorized as “Yes.” #Respondents who answered strongly agree/agree to the question “Would you agree to permanent closure of live poultry markets in order to control avian influenza epidemics?” were categorized as “Agree.” **Respondents who reported that market closure caused great/some inconvenience were categorized as “More inconvenient.” This question was only asked of respondents in Shanghai because Shanghai was the only area where LPMs were closed at the time of the survey.
Age- and sex-specific patterns in exposures to live poultry markets in 5 urban areas of China, 2013. A) Chengdu; B) Guangzhou; C) Shanghai; D) Shenyang; E) Wuhan.
We further analyzed exposures in LPMs among urban residents on the basis of responses from the 829 (33%) of 2,504 participants who visited LPMs
During the study period, the general anxiety level among urban respondents (measured by the State Trait Anxiety Inventory) was low to moderate, but levels varied substantially between cities; the lowest mean scores were seen in Wuhan and Shenyang (
| Characteristic | Chengdu, n = 500 | Guangzhou, n = 500 | Shanghai, n = 500 | Shenyang, n = 504 | Wuhan, n = 500 | p value† |
|---|---|---|---|---|---|---|
| Mean STAI scores (95% CI) | 1.89 (1.85–1.94) | 1.80 (1.75–1.84) | 1.82 (1.78–1.86) | 1.73 (1.69–1.77) | 1.74 (1.71–1.78) | <0.001 |
| Self-perceived susceptibility to influenza A(H7N9)‡ | <0.001 | |||||
| High | 13 (2.6) | 9 (1.8) | 14 (2.8) | 1 (0.2) | 5 (1.0) | |
| Even | 61 (12.2) | 98 (19.6) | 61 (12.2) | 54 (10.7) | 90 (18.0) | |
| Low | 426 (85.2) | 393 (78.6) | 425 (85.0) | 449 (89.1) | 405 (81.0) | |
| Perceived susceptibility to influenza A(H7N9) compared with others§ | 0.431 | |||||
| High | 5 (1.0) | 5 (1.0) | 9 (1.8) | 4 (0.8) | 7 (1.4) | |
| Even | 40 (8.0) | 52 (10.4) | 39 (7.8) | 32 (6.3) | 50 (10.0) | |
| Low | 455 (91.0) | 443 (88.6) | 452 (90.4) | 468 (92.9) | 443 (88.6) | |
| ILI symptoms induced worry¶ | <0.001 | |||||
| More | 105 (21.0) | 151 (30.2) | 140 (28.0) | 113 (22.4) | 107 (21.4) | |
| Same as usual | 197 (39.4) | 198 (39.6) | 192 (38.4) | 165 (32.7) | 233 (46.6) | |
| Less | 198 (39.6) | 151 (30.2) | 168 (33.6) | 226 (44.8) | 160 (32.0) | |
| Infection with influenza A(H7N9) in next week# | 0.004 | |||||
| Worry | 64 (12.8) | 68 (13.6) | 68 (13.6) | 49 (9.7) | 53 (10.6) | |
| Think about it but no worry | 77 (15.4) | 57 (11.4) | 104 (20.8) | 92 (18.3) | 78 (15.6) | |
| Never think about it | 359 (71.8) | 375 (75.0) | 328 (65.6) | 363 (72.0) | 369 (73.8) | |
| Relative severity of influenza A(H7N9) compared with** | ||||||
| Seasonal influenza | 313 (62.6) | 319 (63.8) | 290 (58.0) | 361 (71.6) | 312 (62.4) | <0.001 |
| Avian influenza A(H5N1) | 159 (31.8) | 163 (32.6) | 170 (34.0) | 203 (40.3) | 156 (31.2) | 0.028 |
| SARS | 52 (10.4) | 57 (11.4) | 54 (10.8) | 45 (8.9) | 51 (10.2) | 0.779 |
| Distance, km†† | 804 | 383 | – | 601 | 233 | |
*Values are no. (%) persons except as indicated. STAI, State Trait Anxiety Inventory; ILI, influenza-like illness; SARS, severe acute respiratory syndrome. †Differences between groups was examined with the Kruskal Wallis Test (assuming nonhomogeneous variances). ‡Respondents who answered certain/very likely/likely to the question “How likely do you think it is that you will contract H7N9 avian flu over the next 1 month?” were categorized as “High”; those who answered never/very unlikely/unlikely were categorized as “Low.” §Respondents who answered certain/much more /more to the question “What do you think is your chance of getting infected with H7N9 avian flu over the next 1 month compared to other people outside your family of a similar age?” were categorized as “High”; those who answered not at all/much less/less were categorized as “Low.” ¶Respondents who answered extremely concerned/concerned much more than normal/concerned more than normal to the question “If you were to develop ILI symptoms tomorrow, would you be…?” were categorized as “More”; those who answered not at all concerned/much less concerned than normal/ concerned less than normal were categorized as “Less.” #Respondents who answered worried about it all the time/worried a lot/worried a bit to the question “Did you worry about H7N9 in the past week?“ were categorized as “Worry.” **Respondents who answered much higher/a little higher regarding the severity of influenza A(H7N9) compared with seasonal influenza, avian influenza A(H5N1), and SARS. ††Distance between the survey location and the nearest area in which influenza A(H7N9) case(s) were reported.
In rural areas, as in urban areas, the mean State Trait Anxiety Inventory was low to moderate (
| Characteristic | Dawa, n = 310 | Zijin, n = 308 | Nanzhang, n = 308 | Pengxi, n = 301 | p value |
|---|---|---|---|---|---|
| Mean STAI scores (95% CI) | 1.52 (1.47–1.57) | 1.85 (1.80–1.90) | 1.66 (1.62–1.70) | 1.54 (1.48–1.61) | <0.001† |
| Self-perceived susceptibility to influenza A(H7N9)‡ | <0.001 | ||||
| Higher | 2 (0.6) | 1 (0.3) | 1 (0.3) | 9 (3.0) | |
| Even | 29 (9.4) | 41 (13.3) | 21 (6.8) | 31 (10.3) | |
| Lower | 279 (90.0) | 266 (86.4) | 286 (92.9) | 261 (86.7) | |
| Perceived susceptibility to influenza A(H7N9) compared with others§ | <0.001 | ||||
| Higher | 0 | 1 (0.3) | 2 (0.6) | 8 (2.7) | |
| Even | 10 (3.2) | 25 (8.1) | 3 (1.0) | 36 (12.0) | |
| Lower | 300 (96.8) | 282 (91.6) | 303 (98.4) | 257 (85.4) | |
| Worry induced by ILI symptoms¶ | <0.001 | ||||
| More | 69 (22.3) | 79 (25.6) | 118 (38.4) | 49 (16.3) | |
| Same as usual | 73 (23.5) | 113 (36.7) | 118 (38.4) | 113 (37.5) | |
| Less | 168 (54.2) | 116 (37.7) | 71 (23.1) | 139 (46.2) | |
| Infection with influenza A(H7N9) in next week# | <0.001 | ||||
| Worry | 32 (10.3) | 75 (24.4) | 71 (23.1) | 51 (16.9) | |
| Think about it but no worry | 51 (16.5) | 42 (13.7) | 20 (6.5) | 33 (11.0) | |
| Never think about it | 227 (73.2) | 190 (61.9) | 217 (70.5) | 217 (72.1) | |
| Severity of influenza A(H7N9) compared with** | |||||
| Seasonal influenza | 201 (64.8) | 181 (58.8) | 224 (72.7) | 182 (60.5) | 0.001 |
| Avian influenza A(H5N1) | 105 (33.9) | 112 (36.4) | 67 (21.8) | 92 (30.6) | <0.001 |
| SARS | 51 (16.5) | 63 (20.5) | 30 (9.7) | 44 (14.6) | 0.003 |
| Distance, km†† | 482 | 2448 | 351 | 665 | |
| Raising backyard poultry | 141 (45.5) | 135 (43.8) | 166 (53.9) | 168 (49.7) | 0.067 |
| Type of backyard poultry raised | |||||
| Chicken | 120 (38.7) | 134 (43.5) | 162 (52.6) | 161 (53.5) | <0.001 |
| Ducks | 49 (15.8) | 45 (14.6) | 20 (6.5) | 65 (21.6) | <0.001 |
| Geese | 34 (11.0) | 17 (5.5) | 2 (0.6) | 43 (14.3) | <0.001 |
| Median no. live poultry raised | 6 | 20 | 13 | 12 | <0.001 |
*Values are no. (%) persons except as indicated. STAI, State Trait Anxiety Inventory; ILI, influenza-like illness; SARS, severe acute respiratory syndrome. †Differences between groups were examined with the Kruskal Wallis Test (assuming nonhomogeneous variances). ‡Respondents who answered certain/very likely/likely to the question “How likely do you think it is that you will contract H7N9 avian flu over the next 1 month?” were categorized as “High”; those who answered never/very unlikely/unlikely were categorized as “Low.” §Respondents who answered certain/much more /more to the question “What do you think is your chance of getting infected with H7N9 avian flu over the next 1 month compared to other people outside your family of a similar age?” were categorized as “High”; those who answered not at all/much less/less were categorized as “Low.” ¶Respondents who answered extremely concerned/concerned much more than normal/concerned more than normal to the question “If you were to develop ILI symptoms tomorrow, would you be…?” were categorized as “More”; those who answered not at all concerned/much less concerned than normal/ concerned less than normal were categorized as “Less.” #Respondents who answered worried about it all the time/worried a lot/worried a bit to the question “Did you worry about H7N9 in the past week?“ were categorized as “Worry.” **Respondents who answered much higher/a little higher regarding the severity of influenza A(H7N9) compared with seasonal influenza, avian influenza A(H5N1), and SARS. ††Distance between the survey location and the nearest area in which influenza A(H7N9) case(s) were reported.
Among respondents in urban areas who visited LPMs
| Characteristic | Odds ratio (95% CI) | |
|---|---|---|
| Support closure of LPMs | Change purchase behavior | |
| Sex | ||
| F | 1.19 (0.84–1.68) | |
| M | Referent | Referent |
| Age group, y | ||
| 18–24 | 0.73 (0.37–1.45) | 0.70 (0.36–1.36) |
| 25–34 | 1.36 (0.85–2.17) | 0.81 (0.49–1.34) |
| 35–44 | Referent | Referent |
| 45–54 | 1.43 (0.72–2.83) | 0.62 (0.3–1.26) |
| 55–64 | 0.86 (0.39–1.9) | |
|
| 1.42 (0.51–3.97) | |
| Educational attainment | ||
| Primary or below | Referent | Referent |
| Secondary | 1.80 (0.92–3.50) | |
| Tertiary or above | 1.78 (0.90–3.53) | 1.79 (0.91–3.51) |
| Urban sites | ||
| Chengdu | Referent | Referent |
| Guangzhou | 1.13 (0.69–1.85) | 0.99 (0.62–1.60) |
| Shanghai | ||
| Shenyang | 1.40 (0.74–2.64) | 1.95 (0.97–3.95) |
| Wuhan | 1.07 (0.62–1.86) | |
*Odds ratios were estimated by adjustment for all variables shown. Boldface indicates significance (p<0.05).
On average, across the 5 cities, 30% of respondents reported that they would support the closure of LPMs to control the epidemic; the proportion in support of closures was highest in Shanghai (39%) and lowest in Guangzhou (27%) and Chengdu (25%) (
We have reported empirical information on human exposures to live poultry, perception of risk for influenza A(H7N9), and behavioral responses to the 2013 influenza A(H7N9) outbreak in China. We found that exposure to LPMs in urban areas is common: 20%–50% of urban residents report
We found that men in the 55–64-year age group had more exposures to live poultry than women in that age group, but no difference by sex among the small number of respondents ≥65 years of age in Shanghai (
A minority of respondents reported willingness to accept LPM closures in the event of future outbreaks of influenza A(H7N9). During the winter 2013–14 influenza season, in some areas where human cases of influenza A(H7N9) had been reported, local governments implemented short-term LPM closures; other administrations, including that of Shanghai, closed LPMs for longer periods. However, such interventions can have serious economic consequences. Given the lack of public support for LPM closure and the related economic concerns, whether to make additional closures should be considered carefully. Regular rest days (i.e., days on which live poultry are not sold and stalls must be disinfected and left empty of live birds) and bans on overnight retention of live poultry in markets have been successful in controlling the transmission of avian influenza viruses in LPMs in Hong Kong (
Although almost all cases of influenza A(H7N9) cases have been identified in areas within or surrounding large cities, about half of the laboratory-confirmed avian influenza A(H5N1) cases in China were identified in rural residents, which indicates that avian influenza viruses can reach backyard poultry flocks and pose a risk to human health (
Perception of risk for influenza A(H7N9) infection by respondents to our surveys was generally low, as might be expected given the small number of laboratory-confirmed cases in China. However, low perception of risk could pose difficulties for policy measures such as closure of LPMs. Indeed, we found generally low levels of public support for long-term closure of LPMs (
Our study has several limitations. First, the cross-sectional study design did not enable us to identify changes over time in risk perception or preventive behaviors. Having access to data on live poultry exposures before the identification of influenza A(H7N9) virus infections would have been helpful because the epidemic may have led to changes in exposure patterns by the time our survey was conducted. Second, because the survey was conducted by telephone in urban areas and face-to-face in rural areas, our results may have been affected by selection bias. We did attempt multiple calls to unanswered telephone numbers in an attempt to mitigate this bias, but the overall response rate for the telephone survey was low. Also, because the respondents self-reported their behaviors, the results might be affected by response biases (e.g., if respondents had incomplete recollection of past visits to LPMs). In particular, results could have been affected by social desirability bias if respondents felt uncomfortable reporting true patterns of poultry exposure or attitudes toward government interventions and preferred to report what they perceived to be ideal or most acceptable.
Third, our analyses did not explore in depth the social or psychological factors underlying behavioral responses to influenza A(H7N9), such as the effect of perceived risk or severity. This area might be productive for further investigation. Fourth, similar to other cross-sectional knowledge–attitude–behavior studies, our survey could only provide descriptive data on live poultry exposure, risk perception, and behavioral changes. Inferences on the associations between different psychobehavioral factors will require further study. Furthermore, we did not investigate seasonal variation in poultry-purchasing behaviors, which could also be studied in longitudinal surveys.
In conclusion, exposures to live poultry are common in many areas of China. If influenza A(H7N9) virus were to become more prevalent among poultry, the number of human exposures could be substantial in the absence of control measures. Our findings highlight possible problems in the structure of the live poultry trade in China and the potential for improved protection of human and animal health (
English and Chinese language versions of the questionnaire used for the telephone survey conducted in 5 cities in China to determine human exposure to live poultry and attitudes and behavior toward influenza A(H7N9), 2013.
These authors contributed equally to this article.
We thank Hang Zhou and Zhibin Peng for questionnaire preparation and Qiaohong Liao, Hui Jiang, Xiang Ren, Vicky Fang, Michael Ni, and Hoi Wa Wong for technical assistance.
This study was funded by the US National Institutes of Health (Comprehensive International Program for Research on AIDS grant U19 AI51915); the China–US Collaborative Program on Emerging and Re-emerging Infectious Diseases; and grants from the Ministry of Science and Technology, China (2012 ZX10004-201); the Harvard Center for Communicable Disease Dynamics from the National Institute of General Medical Sciences (grant no. U54 GM088558); the Research Fund for the Control of Infectious Disease, Food and Health Bureau, Government of the Hong Kong Special Administrative Region (grant no. HKU-13-06-01); and the Area of Excellence Scheme of the Hong Kong University Grants Committee (grant no. AoE/M-12/06). The funding bodies had no role in study design, data collection and analysis, preparation of the manuscript, or the decision to publish.
L.W., B.J.C., P.W., G.M.L., and H.Y. designed the study; L.W., J.Y., F.L., and L.Z. collected data; and L.W., B.J.C., P.W., and J.Y. analyzed data. L.W. and B.J.C. wrote the first draft of this article, and all authors contributed to review and revision of the report.
Dr Wang is a director of the Branch of General Affairs on Infectious Disease, Division of Infectious Disease, Key Laboratory of Surveillance and Early-warning on Infectious Disease, Chinese Center for Disease Control and Prevention. Her research interests include notifiable infectious diseases surveillance and related policy research.