Discussion

The highly pathogenic avian influenza (HPAI) virus generally causes severe outbreaks in poultry population. However, occasionally HPAI infect humans exposed to infected poultry. The HPAI-H5N1 outbreak confirmed in this study have been implicated in previous outbreaks in many African countries including Nigeria, Egypt, Côte d’Ivoire, Burkina Faso, Niger and Cameroun [10,17]. In Cameroun, two strains of HPAI; H5N1 and H5N8 were isolated in outbreaks that occurred on commercial farms in 2016 affecting birds with mortality rates ranging between 8% and 96%. In Ghana, previous outbreaks of HPAI (H5N1 and H9N2) have been reported in many regions since the first outbreak in 2007 [10,11]. The circulating H5N1 and H9N2 strains in Ghana have been reported to be homologous to that observed in Nigeria, Burkina Faso and other West African countries, suggesting a potential cross-border contamination of bird species [10,11]. The low mortality rate; 9% and 13%, observed on Case farms 2 and 1 respectively in the current study, are similar to those previously reported in the West Africa region [18]. This may be explained by the similarity in the strains identified in the region.
Our study revealed concerning findings of how birds were moved between farms without inspection by regulatory bodies at the entry points of the district. Even more concerning was how one of the affected farmers moved dead and sick birds back to the farm (source) in the neighboring region for replacement without detection. These lapses contributed to the importation and subsequent spread of the HPAI outbreak in the affected farms. Similar links with poor regulation, were shown in previous HPAI outbreaks [9,10,17,19]. The key sources of the transmissions of HPAI previously reported includes unregulated movements of poultry and eggs dealers from one farm, market, or town to another without appropriate preventive care as well as poor biosecurity measures on farms and live poultry markets [17]. In Nigeria, similar biosecurity non-compliances have been implicated in H5N1 and H5N8 outbreaks occurring between 2014 and 2017 [7]. Similar lapses in biosecurity measures were implicated in HPAI outbreaks globally especially in Europe and Asia [20–23]. The poor regulation of movement of animals have a potential to affect trade negatively in the future.
Owing to the difficulties in restricting the movement of poultry in many settings, some control strategies implemented in previous HPAI outbreaks in Egypt include mass vaccination, surveillance and preemptive culling of infected birds [9]. In Ghana, control measures utilized in previous HPAI outbreaks involved depopulation of all birds on affected farms, disinfection of affected farms, and restricted movement of poultry and poultry products after which, active influenza surveillance is initiated among birds, domestic poultry, and the human population [10]. These measures were equally effective in the current outbreak response. The depopulation of all birds on affected farms, disinfection of farms and live bird market, and ban on sale and movement of live birds during the current outbreak response, contributed to a successful control of the outbreak. Similar control measures have been used in other settings with success [9,21]. The collaborative efforts of both human and animal health personnel through a One Health approach as well as the legislation and enforcement by the municipal assembly through the municipal coordinating council also contributed largely to containment and prevention of further spread of the infection in the present outbreak.
Although human cases of HPAI have been reported in 15 different countries following outbreaks in birds including in Hong Kong [21], Thailand [24], Turkey [25], Egypt [26] and Cameroon [17], none of the human contacts in our study developed flu-like symptoms after two maximum incubation periods follow-up. Almost all of the human cases reported in previous avian influenza outbreaks were caused by zoonotic transmission from poultry and disproportionately affects women and their children. This is because women and children were observed to be more exposed when nursing birds raised in backyard farms compared to adult males who are less involved on the backyard farms [9]. Transmission generally depends on every country’s own dynamics associated with raising poultry and other intrinsic immunologic susceptibility to the infection. Nevertheless, transmission of HPAI from poultry to humans continues to be rare, despite frequent and widespread close contact between humans and affected poultry [27]. However, our study could not assess how and why the human contacts were asymptomatic after follow-up.
The effects of avian influenza outbreaks are often devastating for farmers. Generally, the economic consequences of these outbreaks are severe, since it results in culling of all affected birds and their eggs [28]. To alleviate the impact of losses suffered on farmers and encourage farmers to report bird deaths, payment of financial compensation to farmers is common in some settings including in Egypt [9] and the United States of America [29]. Although compensation was not paid to the affected farmers in the present outbreak, the farmers were educated and counselled to prevent future outbreaks.

Public Health Actions

The affected farmers were informed of laboratory confirmation of HPAI-H5 on Saturday June, 23 2018. The farmers were educated on the essential biosecurity measures to adopt to mitigate future occurrences. They were sensitized on the need for regular hand washing with soap and running water after attending to the poultry. The health facilities within the municipality were also placed on high alert for influenza-like illnesses and any unusual events.
The Municipal Assembly initiated a ban on the sale and movement of birds from affected farms. Similarly, a ban on the sale of live birds at the Nkawkaw market was also instituted. A depopulation exercise was conducted on June 26, 2018. A pit of about 3 meters high was dug with an excavator and the birds transported in a container to the pit together with all the eggs found on the farms. Carbon dioxide foam concentrate was sprayed on the birds in the pit before they were covered with a soil layer of about 2 meters. Disinfection of the live bird market was conducted on June 27, while the infected farms were disinfected on June 30, 2018. The farms were cleared of remaining litters and beddings and the decontamination of the pens done using Izal solution.