Avian influenza outbreak in Turkey through health personnel's views: a qualitative study

Background Avian influenza threatens public health worldwide because it is usually associated with severe illness and, consequently, a higher risk of death. During the first months of 2006, Turkey experienced its first human avian influenza epidemic. A total of 21 human cases were identified, 12 of which were confirmed by the National Institute for Medical Research. Nine of the cases, including the four fatal ones, were from the Dogubeyazit-Van region. This study aims to evaluate the efforts at the avian influenza outbreak control in the Van-Dogubeyazit region in 2006 through the experiences of health personnel. Methods We conducted in-depth interviews with seventeen key informants who took active roles during the avian influenza outbreak in East Turkey during the first months of 2006. We gathered information about the initial responses, the progress and management of the outbreak control, and the reactions of the health professionals and the public. The findings of the study are reported according to the topics that appeared through thematic analysis of the interview transcripts. Results Following the first suspected avian influenza cases, a Van Crisis Coordination Committee was formed as the coordinating and decision-making body and played an important role in the appropriate timing of decisions. The health and agriculture services could not be well coordinated owing to the lack of integrated planning in preparation for outbreak and of integrated surveillance programs. Traditional poultry practice together with the low socio-economic status of the people and the lack of health care access in the region seemed to be a major risk for animal to animal and animal to human transmission. The strengths and weaknesses of the present health system – primary health care services, national surveillance and notification systems, human resource and management – affected the inter organizational coordination during the outbreak. Open communication between the government and the public played an important part in overcoming difficulties. Conclusion Although there were problems during the avian influenza outbreak in Turkey, the rapid responses of the central and regional health authorities and the performance of the health workers were the key points in controlling the epidemic. The lessons from this outbreak should provide an opportunity for integrating the preparation plans of the health and agricultural organizations, and for revising the surveillance system and enhancing the role of the primary health care services in controlling epidemic disease. Developing successful strategies based on knowledge and experience may play a valuable role in delaying an avian influenza pandemic.


Background
The highly pathogenic Avian Influenza A (H5N1) virus has caused more than ten outbreaks worldwide and many related human fatalities have occurred since 1997. A total of 258 laboratory-confirmed cases have been reported in South East Asia, North Africa and Europe by the World Health Organization (WHO) and 154 people with confirmed avian influenza died between 2003 and 2006 [1,2]. Most patients have similar features; they are children, they have a history of close contact with poultry or wild birds, and they live in some of the poorest areas of the world. The human cases in Turkey and Azerbaijan were the first confirmed reports of human avian influenza infection outside Asia and Africa. This was alarming not only for Turkey but also for the European Union and other countries. After considering the epidemiological and laboratory evidence, WHO has maintained its pandemic alert at Phase 3 (of 6), indicating that the new influenza strain causes human infections with no or very limited human to human transmission [3].
Effective surveillance, early warning systems and containment measures based upon a general capacity for health care have been recognized by WHO as the essential action strategies [4,5]. In May 2002, "The Global Agenda for Influenza", which was issued by WHO, stressed the necessity of expanding animal influenza surveillance, and noted that studies at the domestic-wild bird and humandomestic bird interfaces are part of this activity [6].
The H5N1 type of avian influenza virus outbreak was lived in Turkey on January 2006; a total of 21 human cases were identified [3], 12 of which were confirmed by the National Institute for Medical Research [3,7]. Nine of the cases, including the 4 fatal ones, were from the Dogubeyazit-Van region. The confirmed cases were people aged 3-16 years who had close contact with ill poultry in the rural area in Dogubeyazit or in migrant wards in Van [3,7,8]. The timeline of events was summarized in Table 1.
In this period, more than one hundred suspected human cases (21% of total suspected patient in YYU Hospital) underwent prophylactic therapy in the outpatient clinic and twenty five percent of patients who had a history of contact and/or clinical findings were hospitalized in YYU Hospital [7]. Tens of thousands of chickens were culled [8].
Avian influenza infections in Turkey provide an example of concurrent animal and human avian influenza epidemics. These were the first occurrences of human cases in the country, and the impact of the epidemic was quite strong. It was the main agenda for the local and national institutions of health, agriculture and other sectors, the community and the media during the first months of 2006.
This study aims to understand the course of the avian influenza outbreak control in Turkey through the views of health care providers. It will also highlight what local health personnel in various positions experienced during that period.

Methods
This qualitative study was carried out in Dogubeyazit and Van in May 2006. We interviewed seventeen key informants who took active roles during the outbreak of avian influenza in East Turkey during the first months of 2006. The twelve of interviewees were medical doctors (directors, specialists and general practitioners), three were allied health personnel (one director and two health officers), and two were midwife and nurse (primary health care provider and director). Most of the informants were senior staff and had primary responsibilities for the management of the outbreak control.
Five informants were from the Van Provincial Health Directorate (PHD). These informants were the Director and the Deputy Director of the PHD, who were the main coordinators of the avian influenza outbreak intervention, two department chiefs who were involved in implementing the intervention and one health officer who is responsible for transportation of the samples and record keeping.
Four informants were health personnel in primary health care centers; three general practitioners and one midwife, who have active roles in surveillance in Van and Dogubeyazit. One of the general practitioners made the initial diagnosis of the avian case at a primary health care center in Van. Two general practitioners were staff of the primary health care center in Dogubeyazit. One of the doctors were the chief of the primary health care center and worked as a coordinator of avian influenza outbreak intervention and the other one was assigned to the avian influenza surveillance.
Three informants were staff of the State Hospitals in Van and Dogubeyazit. The first was an infectious disease specialist working in Van State Hospital. The second was the Director of Dogubeyazit State Hospital during the outbreak. The third was a pediatrician working in Dogubeyazit State Hospital who pre-diagnosed the avian cases in Dogubeyazit. They worked as if gate-keepers between the primary health care center and the YYU Hospital during the outbreak.
Five informants were Van YYU hospital staff. They were the Director of the University Hospital, the chief of nursing staff, two specialists and one health officer. The infectious disease specialist is on duty in the infectious disease control committee of YYU Hospital, who was a counselor in the Van Crisis Coordination Committee (CCC) and communicated with WHO representatives for the outbreak control. One internal medicine specialist who was also a native of Dogubeyazit helped the Provincial Health Directorates and WHO representatives to communicate with families from Dogubeyazit. The health officer was assigned to the emergency services during the outbreak and he was also the representative of the Health Workers Union in Van.
We used a semi structured guide consisting of open ended questions during in-depth interviews. All interviews were audio-taped and field notes were taken afterwards from each interview for data-gathering. The appointments with the informants were arranged by the second author of this study, who worked in Van Yuzuncu Yil University, and the interviews were conducted by the first author, who worked outside the region. The authors clarified the purposes of the study and the interviews were conducted with the informants' consent for audio-taping and for the use of their words in the report. In the institutions where the authors were affiliated, interview studies are not subject to permissions from ethical committees. Thus, the authors did not apply for approval of these institutions.
Following the interview guide, we asked the participants to inform us about the events chronologically: the first responses of the organizations, the management of outbreak control, the reactions of the health personnel and the resident population, the inter-organizational coordination, and interviewees' roles during the avian influenza outbreak in Turkey. We also asked them to evaluate the strength and weakness of the outbreak control, and the lessons from the avian influenza outbreak.
Records were transcribed verbatim. The authors read and identified codes for major themes according to their interest for the study. These codes were then marked to lines of text and the relevant codes were collected one under the other for preliminary analysis. The second analysis  [7] involved recovering the relevant codes from the text. The results of the study are reported according to the topics revealed by the analysis.

Results
In the avian influenza outbreak, the studies by health organizations were defined by two features as suggested by the interviewees: it was perceived as a new and unknown disease; and it was encountered as a regional, national and international crisis by the health authorities. The preparedness of animal and human health organizations for outbreak-human resource, management, surveillance approach and notification systems-affected inter organizational coordination during the outbreak. The comments related to follow up show us that there is an inconsistency between the pandemic influenza action plan and avian influenza surveillance approach. Although a circular of Turkish MoH was announced on October 2005 including a flow chart to evaluate the suspected cases, the exclusion of primary health care centers and hospitals in the sentinel surveillance and the lack of regional preparedness might have caused health care workers to miss some cases in the referral and reporting procedures. The cost of the culling animals was partially paid to the owners to compensate their economic loss. But in practice the official records couldn't be made exactly, therefore most of poultry owners could not receive the compensations and they had been subject to high rates of financial loss. The situation was expressed by the general practitioner from the primary health care center in Dogubeyazit:"Now about 90-100 thousand chickens were slaughtered. Five Turkish liras were to be paid for each but only 30% of this price was paid because 70% of them were taken without any official record so people couldn't claim their rights."

First reactions of the health care providers and problems
After the declaration of avian influenza outbreak by the Turkish MoH, people's reactions to the disaster and patient applications increased to health care centers. The fear and panic were experienced among health care providers. This situation was explained by a health officer from YYU hospital: "When cases arrived in Van  According to the health care providers' experiences, to deal with an outbreak, the health system must be strengthened, health services should be coordinated, surveillance system and the notification for communicable diseases must be operated efficiently, human and animal health care should be integrated.
Health personnel suggested that the preparedness of the health organizations is very important for an outbreak in terms of equipment, human resources and information gathering The preparation studies should not only be on the management level, but also throughout the health organization and the experience of public health workers must be taken into account: "My opinion is that continuing education of health care providers should be provided, so the practitioner who notices a suspected case can take the details of the patient's history. If it is done like this, the system will work better, a recording system is formed".
According to the experiences of health personnel, sectors and institutions related to the outbreak control must work in collaboration and be coordinated: "(...) avian influenza control absolutely a multi-sector activity. No one should try to be a hero. Every health organization continues with its task; if the organizations of agriculture, municipality, gendarme, police, mufti, education are not included, your success will be overshadowed, and your aim is not achieved." The subjects that most stressed by the health personnel were the prevention of transmission from animal to animal and from animal to human. The health personnel agreed that besides culling animals, studies on preserving animal health must be developed and sustained. In place of traditional poultry farming, alternatives suggested included changes to modern poultry farming at nearby settlements: "At this time our advice to the Van PAD was that since all of them were culling, new projects must be developed and information should be gathered on poultry farming. Of course, this should be done with government support." "The origin oriented control should be. Firstly, a surveillance system at our borders must work well, especially in terms of animal surveillance, but also mainly before disaster happens, not only when a pandemic or epidemic occurs (...)." As the health personnel, communication and information gathering is very important for the outbreak control. The public's psychology and needs must be taken into account to enable them to cooperate with the health teams. The general practitioner who has a close relationship with the local people emphasized the importance of people's psychology and environmental factors. "I mean, why wasn't 'a child playing with chicken heads like puppets' put on the agenda? When she was discharged from the hospital, she came to visit me and I bought her a doll and advised her not to play with chickens, which are microbial things. She slept with the doll for many nights. Why didn't anyone underline this occasion? Why was the people's psychological status not taken into account? Why wasn't attention paid to the problems related to the housing infrastructure or the lack of clean water? I still can't accept this; it still affects me."

Discussion
The Turkish Avian Influenza outbreak is an example for other countries in respect of the experiences and lessons achieved by the health organization managers and health care providers who actively worked in the process.
The health care providers who participated in our study think that the avian outbreak reached national and regional crisis level because they faced an unknown emerging infectious disease and the threat to health that it was not predicted.
According to the health care providers, the most critical issue was the coordination between the agriculture and health organizations during crisis control. The main reason for this problem was the lack of organizational preparation compatible with central or regional plans. To be prepared for an outbreak, it is vital to define the central, regional and local organizational framework, to maintain close cooperation and collaboration between the health and agriculture sectors and to share information on surveillance, evaluating the risk to humans and planning interventions at the time when a case occurs [9][10][11][12]. WHO indicated that Turkey's preparedness plan provided a framework for action, even if not yet fully developed [3].
Indeed the Turkish MoH published the country's first national pandemic influenza action plan in October 2005 and a circular was sent to health organizations about possible avian influenza case descriptions and precautions [3,8]. On the other hand, the results of this study indicates that, the circulation of the avian influenza action plan was insufficient, and regional and national activities related the outbreak control only started after following the verification of H5N1 virus in poultry. As preventive human and animal health care, organizational preparations were incomplete. WHO states that there was no active surveillance in neighbouring provinces after a domestic animal outbreak was confirmed in Igdir in December 2005 [3].
According to the health care providers who participated in our study, a reference laboratory could not meet the demand for the animal samples and after the human cases arose, the Turkish MoA decided to cull all the poultry without searching for possible or confirmed cases. Because there were not enough agriculture personnel for the culling at Van, the Turkish MoA purchased support from private veterinary clinics. This shows us the size of crisis and the lack of preparedness such as reviewing organizational facilities and operational plans in pre-outbreak phase. As a result, the work of outer-organizational teams, which proceeded in their own region, was not integrated with that of other regional health teams that continued surveillance. The evaluation of animal health services at that period is limited in this study because we did not interview agriculture personnel. Future research should focus on the experiences of the animal health service personnel.
Evidently, chaos is unavoidable in primary health care services that do not include central and organizational level intervention plans for emerging avian influenza-like infectious diseases, as in the Turkey example. The health care providers think that the strengths and weaknesses of the health organizational structure before the outbreak affected the success of the intervention and problems were encountered in coordination between health institutions. While a failure is expected even in the health services of developed countries following a possible avian influenza pandemic [13,14], the chaos can be bigger in developing countries due to the weaknesses of health organization. Therefore, strengthening the healthsystem in developing countries shouldbe considered as a factor in delaying the worldwide spread of avian influenza. National and international network and partnerships have to maintain current public health and animal health infrastructures and resources for construction, modernization, enhancement and recruitment for unprecedented emerging and reemerging disease [15].
The most critical issue related to the health system is the surveillance system. The notification of communicable diseases in Turkey was changed in recent years. In the new system, influenza group diseases are subject to sentinel surveillance. According to the sentinel surveillance, primary health care centers have no obligation to notify influenza group diseases including the possible avian influenza cases. Only the training and research hospitals in some selected provinces have the duty for notification of confirmed influenza cases. During the Turkish avian influenza outbreak, Van and Dogubeyazit (Agri) were not included among the selected provinces.
The health care providers who participated in our study emphasized that the widespread of the outbreak requires follow-up and assessment of all influenza cases who applied to health care centers. As the interviewees stated, trace-back investigations were not performed because of the current surveillance system mentioned above. The need for an active surveillance system is clear for an epidemic disease such as avian influenza, which is seasonal, regional and closely related to epidemic diseases related to agricultural practice. In the WHO Report dealing with lessons from the avian influenza outbreak in Turkey, the need for active surveillance of animal and human avian influenza outbreaks was underlined [3]. A well integrated effort such as lining up a network between animal and public health laboratory system is needed to define an epidemic earlier, ensure more effective control measures [7,15]. This will possibly make us gain valuable time by delaying a pandemic.
Practitioners, midwives and nurses, who are responsible for population-based health care services in the primary health care system, became the most important human resource for surveillance during the avian influenza outbreak in Turkey. This experience clearly shows that primary health care centers should be included in the surveillance system. For a efficient surveillance system, upgrading the sentinel physician network by enlisting and retraining more participants and [16] the coordination among public health workers, clinicians and managers is most necessary. It is accepted that public health workers will play an integral role in an influenza pandemic [17]. The health managers and providers whom we interviewed believe that their experiences must be reflected in national avian influenza preparedness plans.
Another problem encountered during the avian influenza outbreak in Turkey was the fear of contamination risk among the health care providers who have no protective equipment against H5N1 when the outbreak started. It is as important to train the health personnel to be prepared for an outbreak as it is to stock protective equipment for them at the sites of preparation studies [14,15,18]. Interviewees believe that the delay in supplying protective equipment and the lack of orderly planning in the distribution of it caused concerns among health care providers about contamination risk, which affected their work output. Health personnel must be accepted as the primary group in prevention, and mortality and morbidity among them must be minimized to allow for efficient intervention by the maximum number of personnel during an avian influenza pandemic. Even if epidemiological evidence about the spread of the H5N1 virus from patients to health personnel is limited [19], studies indicate that nurses who work in hospitals and public health workers touching the suspected avian influenza cases may experience fear and anxiety for their own and their families' health and can face ethical dilemmas when deciding between continuing their work and maintaining their families' health [20,21].
Several problems were experienced during intervention in the outbreak by health care providers who participated in the study. They may be classified as problems related to the socio-economic conditions of people living in the region, and those related to the health care system, including the management and surveillance systems: The health care providers emphasized that people who lived in the rural part of Dogubeyazit and the suburban areas of Van that gather migrants lacked basic needs such as health, education and infrastructure. According to the interviewees, the outbreak in Turkey was influenced by factors closely related to traditional poultry farming and poverty-line economics, as was the case in Asian countries [22]. According to the health personnel who participated in our study, the infection spread rapidly because domestic birds belonging to neighbourhood backyards were able to walk around freely. It is possible that wild migrant birds may be in contact with poultry in the area for food or water. Family-based small-scale poultry farming is a major source of income and nutrition for the region.
All our interviewees thought that the most important factor in the transmission of the H5N1 virus from animal to human was the sharing of shelter according to the low socioeconomic status of the family. Especially during fall and winter, family members share their one sleeping and dining room with poultry. From the year 2004, the contact histories of children and young adults who are described as a risk group for avian influenza cases throughout the world resemble the ones in Turkey [23]. Health care providers who worked in Van and Dogubeyazit stated that people had eaten ill chickens before death and young adults had taken part in the cleaning, cooking and slaughtering of the chickens. Children had played with sick animals and corpses.
The low socio-economic status of the people was accompanied by insufficient primary health care services in the region. The first avian influenza cases were diagnosed after lower respiratory tract infection symptoms appeared. All the fatalities were among those who had recently applied to a health center and been diagnosed as avian influenza. Informants have differing explanations for the late diagnosis of the patients. According to some, the first admission of the families was late. Others claim that the family of the first cases was sent back home during the first admission, and avian flu was diagnosed only after their second admission.
The community was affected psychologically and economically from the disaster. Avian influenza created the fear of a mysterious disease on the people. Most of the people were subject to a financial loss because of the slaughtering of their poultries and were impoverished relative to previous status. In this study we found that the communication between community and health personnel is important for establishing public support for outbreak control and to overcome obstacles such as lack of confidence in governmental organizations. After the avian cases were verified in Turkey, the declaration by the Turkish MoH was evaluated affirmative by the health care providers. It is very important that managers be clear about the known and unknown issues by the first stage of the avian influenza crisis, inform the people about health risks and precautions as early as possible, and be sensitive the worries of people [24,25].
According to the health personnel interviewed, the reason why poultry were kept as a supply of food and living in Van and Dogubeyazit at the time the culling started was the lack of public education about preventable health problems in the region, as much as economic security. The experiences of health personnel indicate that the people participated more after the crisis centers were established by the health and agriculture boards, phone counselling services were made available, good communication was established between health personnel and the people during surveillance, and information studies were applied by media channels.

Conclusion
Turkey experience in avian influenza outbreak shows that preparation planning and surveillance systems should be rational and sustainable. The lack of organizational emergency disease plans delineating the tasks and responsibilities of health care providers in the event of a possible avian influenza outbreak, and the lack of training about preventive care, caused health personnel to be caught unprepared by the outbreak. The problems in supplying and distributing protective equipment, reflecting another dimension of the lack of organizational preparedness, influenced the efficiency of the health care providers' work because they were anxious about their own and their families' health. During the preparation and updating of national epidemic and pandemic plans, and during outbreak management, public health workers should participate effectively in decision-making and risk communication. A well designed communication strategy people's participation in control and may relieve from the psychological effects of the outbreak.
Animal and human health care services could not be well coordinated owing to the lack of integrated preparation and planning. Because the sentinel surveillance of influenza infections in Turkey was based on the confirmation of the cases diagnosed at the training and research hospitals in selected provinces, detection of possible human avian influenza cases at the primary health care level was hindered and trace-back investigation was precluded. To evaluate the spread of the avian influenza outbreak accurately, evaluation and follow-up of influenza cases needs to be done in all health care centers. Such evaluation also necessitates integrated human and animal surveillance and control measures.
The causes of transmission of the H5N1 virus from wild to domestic animals in Turkey are closely related to socioeconomic conditions and traditional poultry farming. Poverty in the region played a predisposing role in the outbreak and the outbreak also increased poverty. Limited access to education, shelter, water supply and waste removal formed the basis for virus transmission from animals to animals and animals to humans. To reduce the risks rising from these predisposing conditions, infrastructure needs to be built specially at the village level.
Although the limited access to health care services and the high contact rate with ill chickens were among the characteristics of the vulnerable group, the rapid organization of the health authorities during intervention studies prevented an increase in the mortality rate. Despite the above-mentioned problems in preparedness about coordination during the avian influenza outbreak control, the rapid response and performance of the health workers played an important role in controlling epidemic.
the manuscript. TE arranged appointments with the informants during the course of data gathering and contributed to analyzing the data. Both authors read drafts of the manuscript, made comments and approved the final version.