Figure 2

Figure 2. 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, 2013A) Flowchart for telephone...

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]) (Figure 2, panel A). The selection of 1,227 participants in 4 rural sites is illustrated in Figure 2, panel B. The surveys were conducted from May 23 through August 24. During this period, the influenza A(H7N9) epidemic had passed its peak, and few cases occurred. Guangdong Province notified its first human influenza A(H7N9) case on August 9, after the completion of the survey in Guangzhou on June 26.

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 (Table 1). However, because the surveys were conducted in different forms in urban versus rural areas and the general characteristics of participants were different, including the risk for becoming infected with influenza A(H7N9) virus and the types of potential exposure to avian influenza viruses, we did not make any further direct quantitative comparisons between urban and rural respondents. For comparisons among urban areas, respondents were generally similar, but reported incomes were higher for Shanghai and Guangzhou than for the other 3 cities (data not shown).

Figure 3

Figure 3. Age- and sex-specific patterns in exposures to live poultry markets in 5 urban areas of China, 2013A) Chengdu; B) Guangzhou; C) Shanghai; D) Shenyang; E) Wuhan.

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 (Table 2). By imputing midpoints of reported purchasing rates, we estimated that the mean number of live poultry purchased per year varied between cities: 6.8 for Shenyang, 19 for Shanghai, 20 for Wuhan, 28 for Chengdu, and 47 for Guangzhou. Age-specific patterns in exposure to live poultry were generally similar for men and women within each city, with some exceptions. In Guangzhou, women 35–54 years of age purchased poultry in LPMs much more frequently than did men of the same age, but the reverse was true for those >65 years of age (Figure 3). We found no evidence of a substantial difference in poultry exposures by sex in Shanghai (Figure 3).

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 >1 time in the preceding year. Overall, 69% of these respondents reported that they always visited the nearest LPM; median distance from home to the nearest LPM was 1 km. Most respondents reported that they “usually” or “always” picked up poultry for examination before deciding to buy, with the highest proportion in Chengdu and lowest in Shenyang; 87% of respondents always arranged for slaughter of purchased poultry in the LPM, with no notable differences between cities.

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 (Table 3). Perceived risk for influenza A(H7N9) in the following month (absolute susceptibility) and relative to others (relative susceptibility) were generally low in all cities, but highest in Shanghai. Respondents in Shanghai and Guangzhou were more likely to respond that they would be more worried than usual if they experienced an influenza-like illness (ILI). Twelve percent of respondents reported that they had worried about becoming ill with influenza A(H7N9) during the previous week; levels varied among cities, with a greater frequency of worry in Shanghai and Guangzhou (Table 3). Respondents in Shenyang reported the highest perceived severity of influenza A(H7N9) compared with seasonal influenza and avian influenza A(H5N1); respondents in Guangzhou reported the highest perceived severity of influenza A(H7N9) compared with that of SARS (Table 3).

In rural areas, as in urban areas, the mean State Trait Anxiety Inventory was low to moderate (Table 4). A total of 48% of respondents reported that they raised >1 type of poultry at home. Overall, 47% reported raising chickens, 15% raised ducks, and 8% raised geese; these proportions varied between counties (Table 4). In rural areas, levels of perceived absolute and relative susceptibility and concern about ILI or confirmed influenza A(H7N9) infection were generally low; some differences were seen between the 4 rural areas. Respondents in Nanzhang and Zijin were more likely to respond that they would be more worried than usual if they had an ILI; 24% of respondents in Zijin reported that they had worried about becoming ill with influenza A(H7N9) in the previous week, and the average level of worry in Zijin was higher than that for other counties (Table 4). Most respondents in each area perceived influenza A(H7N9) to be more severe than seasonal influenza but less severe than influenza A(H5N1) and SARS.

Among respondents in urban areas who visited LPMs >1 time in the preceding year, 77% reported that they had stopped buying or bought lower amounts of live poultry since March 2013; this proportion was highest (91%) for Shanghai (Table 2). We examined factors affecting the likelihood of changing habits of buying live poultry and found greater changes among women, those with higher educational attainment, and those residing in Shanghai and Wuhan rather than in Chengdu. We found no statistically significant differences by age group (Table 5).

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%) (Table 2). We examined factors affecting the likelihood of supporting the closure of LPMs and found greater support among persons 55–64 years of age (odds ratio [OR] 3.28, 95% CI 1.71–6.29) and >65 years of age (OR 2.36, 95% CI 1.04–5.32). We also found greater support for closure of LPMs in Shanghai (OR 1.77, 95% CI 1.05–2.99) than in Chengdu but no significant differences by sex or educational attainment (Table 5). However, 32% of respondents in Shanghai reported that the closure of LPMs had caused them inconvenience.

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 >1 visit to an LPM in the preceding year (Table 2). Most respondents who purchased poultry in LPMs reported close contact with live poultry before slaughter. It is likely that the number of laboratory-confirmed cases of influenza A(H7N9) virus infection is lower than the actual number of human infections to date (8), and our results show that a broad cross-section of urban residents could be exposed to influenza A(H7N9) virus if it were prevalent among poultry in LPMs. In the spring 2013 outbreak, some evidence pointed to high prevalence of influenza A(H7N9) virus in certain LPMs (6), whereas official surveillance data from the Ministry of Agriculture identified the virus in only a small proportion of samples collected from across the country (of 4,488 samples tested, 0.9% were positive for the virus) (11). The absolute risk for human infection after close contact with poultry infected with the influenza A(H7N9) virus remains unclear.

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 (Figure 3). We had previously hypothesized that exposure to poultry in LPMs might be higher for older men than for older women (3). Our findings suggest that the higher risk for laboratory-confirmed influenza A(H7N9) virus infection among men during the spring 2013 outbreak in the Yangtze River Delta might not be explained by sex differences in exposure but rather by increased susceptibility to serious disease after infection among men (e.g., because of greater prevalence of co-existing conditions) or by increased access to health care and laboratory testing for men. However, our sample size was relatively small, particularly for respondents >65 years of age. As in a previous report of live poultry exposures in the southern China cities of Guangzhou in 2006 and Shenzhen in 2007 (9), we did not identify major differences in exposures among middle-aged adults compared with exposures among the elderly. However, most laboratory-confirmed influenza A(H7N9) cases have been in persons >60 years of age (3), consistent with our hypothesis that exposures in middle-aged adults may have led to milder disease that was less likely to result in laboratory testing (3,9).

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 (20,21) and have been proposed in some areas of China (8).

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 (3). Influenza A(H7N9) virus does not appear to have spread to backyard flocks at this time, however. Most confirmed human cases have occurred in urban areas among persons who have reported recent exposure to live poultry in LPMs, although a smaller number of cases occurred in persons who have reported recent exposure to backyard poultry (3). However, if the circulation of influenza A(H7N9) virus in backyard poultry were to increase, the number of potential exposures could be substantial because almost half of rural residents report raising backyard poultry. The risk for influenza A(H5N1) virus infection among rural residents has been reduced through better education about the danger of close contact with, or consumption of, sick or dead backyard poultry (22,23). Unfortunately, this approach would not be effective for controlling spread of influenza A(H7N9) virus because infected chickens do not show signs of illness.

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 (Table 2), particularly in cities that had not been affected by influenza A(H7N9). Respondents in Guangzhou and Shanghai reported higher likelihood than residents of other cities that they would be worried if they showed signs and symptoms of ILI. This finding is unsurprising for Shanghai, but there had been no confirmed influenza A(H7N9) cases in Guangzhou at the time of our survey.

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 (8,24).