Knowledge, attitudes, and practices of avian influenza, poultry workers, Italy.

We asked Italian poultry workers about knowledge, attitudes, and practices regarding avian influenza. It was perceived to be a low occupational hazard, and wearing protective equipment and handwashing were not routine practices. Knowledge of transmission and preventive measures should be improved. Employers and health professionals should provide more effective information.

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Infection of poultry with influenza A (subtype H5N1) virus is responsible for outbreaks in birds and a human case-fatality rate of 58% (1). The most likely means of transmission is from infected birds to humans and from the environment to humans, but evidence for human-to-human transmission is limited (2). This virus can be transmitted if a person has direct contact with infected poultry or surfaces and objects contaminated by poultry droppings. Two epidemics caused by avian influenza virus H5 and H7 subtypes occurred in poultry in Italy from 1997 through 2001. A plan was recently developed for adequate response to influenza pandemics, and farmers, veterinarians, and healthcare workers have been educated about diagnosing, detecting, and preventing the spread of avian influenza (3).

Workers in the poultry industry, who commonly have contact with live, sick, or dying poultry, are at high risk for avian influenza. These workers are at increased risk because of food handling and preparation of raw poultry meat and products. Concern exists that avian influenza could be transmitted from uncooked birds or bird products to humans (4,5). This study evaluated knowledge, attitudes, and infection control practices of poultry workers in Italy regarding avian influenza.

The Study

A total of 284 poultry workers at 110 poultry farms throughout the Campania region of Italy were recruited into the study from December 2005 through March 2006. The workers were interviewed confidentially in their workplace regarding demographics, work activity, knowledge of transmission and prevention of avian influenza, attitudes toward this disease, compliance with precautions at work, and sources of information (online Appendix Figure, available in English and Italian from http://www.cdc.gov/ncidod/EID/vol 12no 11/06-0671_ appG.htm). Multiple logistic regression analysis with adjusted odds ratios and 95% confidence intervals and multiple linear regression analysis with adjusted 13 coefficients were performed with Stata software (6).

A total of 257 poultry workers were interviewed (response rate 90.5%.). Average age was 43 years (range 19-75 years), average duration of work activity was 18 years, and median number of daily exposures to breeder animals was 18,500. One third of the workers had a high school or college education.

Of the 257 workers, 63.8% correctly defined avian influenza as a contagious infection caused by a virus that can affect all species of birds (Table 1), and 21.8%-81.7% knew that avian influenza can be transmitted by touching uncooked eggs or infected animals. Nearly all workers identified poultry and wild birds as common vectors. Most knew that poultry workers had a high risk of being infected and that butchers and veterinarians had a lower risk. Only 22.6% provided a correct definition of this disease and knew routes and vectors of transmission.

Knowledge was greater in persons with more education, those who worked a longer time, those who believed they were at high risk of contracting avian influenza, and those who needed information (Table 2). With respect to identifying measures that protect poultry workers from exposure to avian influenza, correct responses ranged from 34.2% for all protective measures to 43.2% for eye protection and 68.5% for face masks. Greater knowledge was observed in those who received information from health professionals and employers, those who believed they were at high risk, and those who worked only with poultry (Table 2).

Most poultry workers believed that avian influenza was a serious (69.7%) but preventable (70.8%) disease. Mean-total scores (scale of 1 to 10) for perceived risk of contracting avian influenza during work activity and for co-workers and family members were 3.2 and 3.1, respectively, which indicated low-risk perception. Only 4.3% showed great concern about risk. Respondents who were more likely to believe that they were at high risk worked fewer hours, knew protective measures for exposure to avian influenza, had received information from the mass media, and needed information. Workers who were exposed only to poultry were less likely to perceive risk (Table 2).

A total of 23.7% reported that in the past 3 months they had modified their work habits because of fear of contracting avian influenza. Those more likely to modify their behavior were younger, married, had more knowledge of avian influenza, believed that it was a serious but preventable disease, and received information from sources other than health professionals and employers (Table 2).

Regarding compliance with precautions to avoid spreading virus through food while working, 59.9% routinely washed their hands and disinfected surfaces and utensils that had been in contact with raw meat. Wearing personal protective equipment was not a routine practice because 82.9% always wore outer garments, 82.9% wore boots or protective boot covers, 59.9% wore gloves, 59.9% wore face masks, 24.5% wore eye protection, and 87.9% washed their hands. A total of 24.1% always wore protective clothing and washed their hands; these practices were more common in poultry workers who knew that these measures were protective and less common by workers who handled only eggs (Table 2).

All poultry workers had received information regarding avian influenza. The most common sources were mass media (91.8%), health professionals (47.5%), and employers (6.2%); 62.3% wanted more information.

Conclusions

Knowledge of avian influenza can be improved, as shown in a study of consumers (G. Di Giuseppe et al., unpub, data). We expected to find more knowledge in educated poultry workers, especially in how to identify potential animal cases and minimize risk for transmission. However, our observations indicate that information is not correctly disseminated because those who receive information from the mass media and who need information were more likely to have a perception of high risk. Therefore, tailored educational programs, including booklets and seminars, could be beneficial in improving self-risk assessment of poultry workers.

Two thirds of poultry workers believed that avian influenza is a serious and preventable disease, but the study showed a perception of low risk of contracting this disease at work because only 4.3% indicated strong con ecru, although the largest percentage correctly recognized that they are a risk group. Workers who handled only poultry were less likely to perceive a risk than those who handled other products.

Studies have identified direct exposure to infected poultry as the primary risk factor in transmission of avian influenza virus to humans. A cohort study of poultry workers in Hong Kong showed that greater exposure to poultry was associated with antibody to H5 hemagglutinin (4). In Thailand, a case-control study showed that activities involving exposure to poultry were associated with influenza caused by H5N1 virus (7). In Vietnam, a population study in a rural area with outbreaks of highly pathogenic avian influenza showed a dose-response relationship between poultry exposure and illness (8).

Low adherence to the recommendations of the World Health Organization to avoid spread of avian influenza through food while working has been reported; use of protective clothing and handwashing is inadequate (9). In our study, there was a subset of workers who routinely followed guidelines because lower compliance was observed in those working only with eggs. Moreover, those who did not know precautions had a 6-fold greater risk for inconsistent adherence to preventive guidelines compared with those who identify them.

Improving knowledge of transmission and application of preventive measures is a useful public health strategy for reducing the effects of avian influenza in poultry workers. Employers and health professionals should work together to provide effective and coordinated information to these workers.

Acknowledgments

We thank the poultry workers for their participation in the study and the veterinarians of the local health units for their contributions.

Dr Abbate is a doctoral student at the Medical School of the Second University in Naples, Italy. Her primary research interests are epidemiology and prevention of infectious diseases, health policy and management, and epidemiology and prevention of chronic diseases.

References

(1.) World Health Organization. Cumulative number of confirmed human cases of avian influenza A/(H5N1) reported to WHO. 2006 [cited 2006 Aug 2]. Available from http://www.who.int/csr/disease/avian influenza/country/cases_table_2006_07_26/en/index.html

(2.) The Writing Committee of the World Health Organization (WHO) Consultation on Human Influenza A/H5. Avian influenza A (H5N1) infection in humans. N Engl J Med. 2005;353:1374-85.

(3.) Piano nazionale di preparazione e risposta a una pandemia influenzale. Roma: Centro Nazionale per la Prevenzione e il Controllo delle Malattie; 2006.

(4.) Bridges CB, Lim W, Hu-Primmer J, Sims L, Fukuda K, Mak KH, et al. Risk of influenza A (H5N1) infection among poultry workers, Hong Kong, 1997-1998. J Infect Dis. 2002;185:1005-10.

(5.) Swayne DE. Occupational and consumer risks from avian influenza viruses. Dev Biol (Basel). 2006;124:85-90.

(6.) Stata Reference Manual Release 8.1. College Station (TX): Stata Corporation; 2003.

(7.) Areechokchai D, Jiraphongsa C, Laosiritaworn Y, Hanshaoworakul W, O'Reilly M; Centers for Disease Control and Prevention (CDC). Investigation of avian influenza (H5N1) outbreak in humans--Thailand, 2004. MMWR Morb Mortal Wkly Rep. 2006;55 (Suppl 1):3-6.

(8.) Thorson A, Petzold M, Chuc NT, Ekdahl K. Is exposure to sick or dead poultry associated with flulike illness? A population-based study from a rural area in Vietnam with outbreaks of highly pathogenic avian influenza. Arch Intern Med. 2006; 166:119-23.

(9.) World Health Organization. Public health interventions for prevention and control of avian influenza. A manual for improving biosecurity in the food supply chain: focusing on live animal markets. New Delhi: Regional Office for South-East Asia. 2006

Address for correspondence: Italo F. Angelillo, Department of Public, Clinical and Preventive Medicine, Second University of Naples, Via Luciano Armanni, 5-80138, Naples, Italy; email: italof.angelillo@ unina2.it

Rossella Abbate,* Gabriella Di Giuseppe, [dagger] Paolo Marinelli,* and Italo F. Angelillo*

* Second University of Naples, Naples, Italy; and [dagger] University of Catanzaro Magna Graecia Medical School, Catanzaro, Italy

Table 1. Knowledge of avian influenza among 257 poultry workers,
Italy

                                                 Correctly answered,
Variable                                               no. (%)

Definition (contagious infection caused by           164 (63.8)
virus that can affect all species of birds)
Modes of transmission
 Animal to human                                     210 (81.7)
 Animal to animal                                    206 (80.2)
 Environment to human                                153 (59.5)
 Eating uncooked poultry                             149 (58)
 Eating uncooked eggs                                102 (39.7)
 Touching uncooked poultry                            88 (34.2)
 Touching uncooked eggs                               56 (21.8)
 Touching wild birds                                 246 (95.7)
 Touching poultry                                    232 (90.3)
 Touching saliva, nasal secretions,                  167 (65)
 feces, and fomites of infected birds
Risk groups
 Poultry workers                                     194 (75.5)
 Butchers                                            134 (52.1)
 Veterinarians                                       108 (42)
Use of preventive measures
 Face mask                                           176 (68.5)
 Gloves                                              158 (61.5)
 Outer garments                                      157 (61.1)
 Boots or boot covers                                144 (56)
 Eye protection                                      111 (43.2)
 Handwashing with soap and water                     161 (62.7)

Table 2. Logistic and linear regression models results of knowledge,
attitudes, and practices of avian influenza among 257 poultry
workers, Italy *

                                                                   p
Variable                                   OR          95% CI    value

Model 1: General knowledge about avian influenza; log likelihood
-124.45, [chi square] 25.58, df 6, p = 0.0003
  Years of working activity          1.03            1.01-1.06    0.015
  Need of additional information     2.59            1.17-5.72    0.019
  Perception of risk for avian
    influenza                        1.13            1.01-1.26    0.037
  Education level                    1.63            1.02-2.61    0.042
  Avian influenza is a serious and
    preventable disease              1.44            0.72-2.88    0.31
  No. breeder animals exposed to
    per day                          0.87            0.65-1.16    0.33
Model 2: Knowledge of all measures that protect poultry workers
from exposure to avian influenza; log likelihood -142.95, [chi square]
44.40, df 7, p < 0.0001
  Health professionals and
    employers as sources of
    information                      3.62            1.99-6.59   -0.001
  Perception of risk for avian
    influenza                        1.19            1.07-1.34    0.002
  Working with poultry and eggs      1.0 ([dagger])  --            --
  Working with only poultry          2.11            1.17-3.81    0.013
  Education level                    1.37            0.90-2.08    0.14
  General knowledge of avian
    influenza                        1.44            0.74-2.8     0.28
  No. breeder animals exposed to
    per day                          0.88            0.68-1.14    0.33
  Hours worked per day               1.05            0.95-1.14    0.35
Model 3: Modification of working habits in the past 3 mo; log
likelihood -119.48, [chi square] 42.72, df 10, p < 0.0001
  Health professionals and
    employers as sources of
    information                      0.34            0.17-0.69    0.003
  Marital status                     0.31            0.13-0.76    0.01
  Age                                0.96            0.92-0.99    0.018
  Avian influenza is a serious
    and preventable disease          2.29            1.09-4.76    0.028
  General knowledge of avian
    influenza                        2.11            1.03-4.31    0.041
  Poultry workers are a risk group   2.30            0.94-5.65    0.07
  Perception of risk for avian
    influenza                        1.09            0.97-1.22    0.15
  Working with poultry and eggs      1.0 ([dagger])  --            --
  Working with only poultry          0.64            0.03-1.34    0.24
  Sex                                1.45            0.73-2.86    0.29
  Education level                    1.32            0.78-2.22    0.3
Model 4: Preventive measures behavior; log likelihood -119.36,
[chi square] 45.26, df 4, p < 0.0001
  Knowledge of preventive measures   5.95            3.06-11.56  <0.001
  Working with poultry and eggs      1.0 ([dagger])  --            --
  Working with only eggs             0.28            0.11-0.73    0.009
  General knowledge of avian
    influenza                        1.48            0.72-3.02    0.28
  Health professionals and
    employers as sources of
    information                      1.37            0.70-2.69    0.37

                                         [beta]                    p
Variable                              coefficient        t       value

Model 5: Perception of risk for avian influenza; F(7,249) = 8.25,
p < 0.0001, [R.sup.2] 18.8%, adjusted [R.sup.2] 16.6%
  Working with poultry and eggs      -- ([dagger])       --        --
  Working with only poultry              -1.72         -5.0      -0.001
  Hours worked per day                   -0.19         -3.74     -0.001
  Need additional information             1.16          3.56     -0.001
  Media and television as sources
    of information                        2.02          3.36      0.001
  Knowledge of preventive measures        0.77          2.36      0.019
  No. children                           -0.21         -1.56      0.12
  Sex                                    -0.32         -0.9       0.37
  Constant                                3.42

* OR, odds ratio; CI, confidence interval; df, degrees of freedom.

([dagger]) Reference category.