Poultry Production and Sustainability in Developing Countries under the COVID-19 Crisis: Lessons Learned

Simple Summary Globally, poultry production provides high-quality, affordable animal protein, a high chance for investment, job opportunities, and a source of income for smallholders worldwide. However, the recent COVID-19 affected the sustainability of various animal production sectors worldwide, and these influences are more severe in developing countries. The unprecedented negative influences are attributed to the lockdown, movement restriction, and close of some markets. The present review focuses on the impacts of the COVID-19 crisis on poultry production in developing countries in terms of causes and possible solutions to decrease and improve profits. Work must be coordinated between the public and private sectors to facilitate the restoration of the poultry industry to its economic and social position to remedy these problems. Abstract Poultry farming is a significant source of revenue generation for small farmers in developing countries. It plays a vital role in fulfilling the daily protein requirements of humans through meat and eggs consumption. The recently emerged pandemic Coronavirus Disease-19 (COVID-19) impacts the poultry production sector. Although the whole world is affected, these impacts may be more severe in developing countries due to their dependency on exporting necessary supplies such as feed, vaccines, drugs, and utensils. In this review, we have discussed poultry production in developing countries under the COVID-19 crisis and measures to regain the loss in the poultry industries. Generally, due to the lockdown, trade limitations have negatively impacted poultry industries, which might exacerbate global poverty. Coordinated activities have to be taken at the private and government levels to arrange soft loans so that these farms can restore their production and marketing to normal levels. In addition, here, we have focused on the supply of farm input, feed, other raw materials, management system, improved breeding efficiency, veterinary services, and marketing of egg and meat, which have to be ensured to secure a sustainable poultry production chain.


Introduction
In November 2019, the Coronavirus Disease 2019 , caused by Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2), which is a highly infectious disease, originated from Wuhan, China, resulting in severe health implications. To date, a total of 5,824,622 deaths and 410,022,236 COVID-19 cases have been reported. Due to the implementation of lockdowns and trade limitations as control strategies, considerable collateral health damage [1] and unprecedented economic crisis have been reported [1][2][3], including the agricultural value chain, such as the livestock production sector, especially in developing countries. Thus, the negative impacts might have more devastating consequences on the most vulnerable people and poorest nations. In this review, we have discussed the effects of the COVID-19 pandemic on poultry production, along with measures that need to be implemented to ensure sustainability in developing countries.

Introduction
In November 2019, the Coronavirus Disease 2019 , caused by Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2), which is a highly infectious disease, originated from Wuhan, China, resulting in severe health implications. To date, a total of 5,824,622 deaths and 410,022,236 COVID-19 cases have been reported. Due to the implementation of lockdowns and trade limitations as control strategies, considerable collateral health damage [1] and unprecedented economic crisis have been reported [1][2][3], including the agricultural value chain, such as the livestock production sector, especially in developing countries. Thus, the negative impacts might have more devastating consequences on the most vulnerable people and poorest nations. In this review, we have discussed the effects of the COVID-19 pandemic on poultry production, along with measures that need to be implemented to ensure sustainability in developing countries.

Impacts of COVID-19 on Food Security and Poultry Production
The COVID-19 pandemic, unlike previous pandemics such as SARA-CoV and Ebola, severely impacted the food supply chain indirectly through disruptions of the downstream stages such as transport and logistics [4][5][6][7][8]. It affected all dimensions of food security, including availability, access, utilization, stability, and sustainability, depending on the industry, the locality, and the financial status of the affected region [9,10]. Figure 1 illustrates the impacts of the COVID-19 pandemic on poultry production. Generally, animal production sectors in several countries, such as China, the US, the UK, Germany, Spain, Italy, France, and India, were significantly influenced by COVID-19 [4,11,12]; both food availability and demand were also affected [13]. In Canada, the COVID-19 pandemic has damaged the poultry and dairy sectors [14]. This damage even affected the main factors in the industry and animal husbandry, including disruptions in supply chains, scarcity of human resources, the malfunctioning of livestock markets, price volatility, and changes in consumer shopping behavior [15]. No evidence was found indicating that SARS-CoV-2 can be transmitted to humans via poultry products; thus, poultry Generally, animal production sectors in several countries, such as China, the US, the UK, Germany, Spain, Italy, France, and India, were significantly influenced by COVID-19 [4,11,12]; both food availability and demand were also affected [13]. In Canada, the COVID-19 pandemic has damaged the poultry and dairy sectors [14]. This damage even affected the main factors in the industry and animal husbandry, including disruptions in supply chains, scarcity of human resources, the malfunctioning of livestock markets, price volatility, and changes in consumer shopping behavior [15]. No evidence was found indicating that SARS-CoV-2 can be transmitted to humans via poultry products; thus, poultry are resistant to SARS-CoV-2 [16]. However, the poultry industry is negatively impacted globally. It is estimated that the losses might be greater than those due to the avian influenza pandemic of 2006 [17], as 400 million birds were culled globally in 2006. The negative impacts of COVID-19 on the poultry industry are attributed to the indirect effects on necessary supplies such as feed, chicks, medicine and vaccines, and poultry products due to the restriction of movement (Figure 1). Additionally, the strict restrictions during this pandemic disrupted the marketing of poultry products. Due to the closure of markets, farmers were unable to sell eggs at local markets or restaurants, which resulted in substantial financial losses [4]. In developing countries, the negative impacts of COVID-19 on poultry were found to be much higher than those in developed countries because poultry production serves to fight poverty and food scarcity [18]. Table 1 summarizes the negative impacts of SARS-CoV-2 on poultry production observed in some developing countries.

Concern about the Spread of SARS-CoV-2 from Animals and Social Rumors
At the beginning of this pandemic, the unknown nature of COVID-19 transmission was a major concern, particularly how it spread from animals to humans and vice versa [30,31]. However, poultry are not susceptible to SARS-CoV-2, although they are susceptible to other CoVs such as infectious bronchitis (IBV) that causes respiratory, intestinal, and urogenital problems in chickens [32,33]. IBV has also been reported in pheasants and peafowl [34]. The turkey coronavirus (TCoV) also causes enteric lesions [35,36] and might be involved in the poult enteritis and mortality syndrome (PEMS) [36]. There were also social rumors in some developing countries such as Bangladesh that SARS-CoV-2 can be transmitted via eggs and chickens, leading to price fluctuations for poultry meat and eggs and reducing consumption [31]. It has also been proposed that SARS-CoV-2 can spread through processed foods because it can survive for hours to several days on inanimate surfaces [37]; however, there is no evidence that the virus can be transmitted directly through food, milk, milk products, or eggs [38].

Lockdown and Restrictions of Trades
The lockdown of the food distributors, such as food courts, adversely influenced the retail demand. The transport restrictions negatively impacted the products, thus cumulatively affecting the animals in the farms, showing increased animal numbers and high husbandry costs [39,40]. The dynamics of the impacts of lockdown on food security are shown in Figure 2. social rumors in some developing countries such as Bangladesh that SARS-CoV-2 can be transmitted via eggs and chickens, leading to price fluctuations for poultry meat and eggs and reducing consumption [31]. It has also been proposed that SARS-CoV-2 can spread through processed foods because it can survive for hours to several days on inanimate surfaces [37]; however, there is no evidence that the virus can be transmitted directly through food, milk, milk products, or eggs [38].

Lockdown and Restrictions of Trades
The lockdown of the food distributors, such as food courts, adversely influenced the retail demand. The transport restrictions negatively impacted the products, thus cumulatively affecting the animals in the farms, showing increased animal numbers and high husbandry costs [39,40]. The dynamics of the impacts of lockdown on food security are shown in Figure 2. The dynamics of the impacts of lockdown on food security production adapted after HLPE [10]. Several overlapping and reinforcing dynamics affect the food system, such as disruption of the food supply chain and social protection programs, loss of income, shifted food environments, and uneven food prices.
The negative impact of the COVID-19 pandemic on the food supply chain can be attributed to the global policies of lockdown according to the One Health world approach, the global economic recession, food price fluctuation, production changes, disrupted social protection, and changes in food environments. This complex relationship between different factors and the disruptions of the food supply chain indicated the slow recovery of the food supply chain in the future and the need for economic reform for faster recovery [20]. The production, imports, and exports of poultry meat in some African countries are shown in Table 2. The dynamics of the impacts of lockdown on food security production adapted after HLPE [10]. Several overlapping and reinforcing dynamics affect the food system, such as disruption of the food supply chain and social protection programs, loss of income, shifted food environments, and uneven food prices.
The negative impact of the COVID-19 pandemic on the food supply chain can be attributed to the global policies of lockdown according to the One Health world approach, the global economic recession, food price fluctuation, production changes, disrupted social protection, and changes in food environments. This complex relationship between different factors and the disruptions of the food supply chain indicated the slow recovery of the food supply chain in the future and the need for economic reform for faster recovery [20]. The production, imports, and exports of poultry meat in some African countries are shown in Table 2. Table 2. Production, imports, exports, and utilization of poultry meat (thousand tonnes-carcass weight equivalent) in the world continents from 2019 to 2020 (before and during the COVID-19 pandemic). Although the poultry production in 2020 was higher than in 2019, there is a significant global decline in import and export supplies, leading to disruptions in the food supply chain [42]. Therefore, there is a trend towards increasing world production, imports, and utilization of poultry meat after COVID-19; however, the exports have declined. For example, Africa showed an increased poultry production and consumption accompanied by decreased imports and exports. In South Africa, poultry production, import, and utilization have decreased, but their exports were not affected. The activities related to poultry production in Africa followed a similar trend to that of the least developed countries. Meanwhile, the least developed countries showed different trends in the production and utilization of poultry products. Moreover, the decrease in exports in Asia may be attributed to the lockdown of borders and ports and/or the trend of the governorates to increase food security and self-sufficiency. The same trend was observed in Africa; however, the values of production, imports, exports, and utilization are significantly different between the two continents, favoring Asia. In North America, all values related to poultry activity have increased; however, in Europe, only the imports have decreased. This indicates that the changes in production, imports, and exports are affected by the stages of development for the world continents.

Continents of the World
The negative impacts of lockdown on poultry productions are as follows: (i) The animal feed supply was disrupted as due to lockdown, several countries such as Argentina and Brazil had to reduce their exports of raw materials of feed such as soybean and corn, which led to a shortage of dry feed in several developing countries [7,8,43]. In several African countries, the cost of chicken feed has increased [44]. (ii) Poultry services were reduced, such as equipment, day-old chicks for stock replacements, feed, vaccines, drugs, diagnostics, and feed additives (vitamins and minerals) [8]. Exporters in several countries also faced a considerable drop in demand for livestock-based foods in major importing markets.
(iii) Market closures and transportation restrictions hampered access to markets and customers, affecting both animals and animal products, such as eggs and meat. (iv) The shortage of laborers severely impacted the poultry industry in developing countries, since poultry farmers rely on human resources rather than machines [19][20][21].

Small-Scale Poultry Farms
Several small-scale poultry farms are widely distributed in developing countries. Rahman and coworkers summarized the problems that make small farmers more susceptible to any crisis, such as a lack of training on poultry farming, inadequate education and farming expertise, a lack of biosecurity awareness, a lack of infrastructure and marketing system, demand and supply imbalance, information disparity on market stability and estimation, a tendency to respond more to rumors about commercial poultry and poultry products, and a lack of access to veterinary services [19]. The general problems for small-scale poultry farming in developing countries are summarized in Figure 3.

Small-Scale Poultry Farms
Several small-scale poultry farms are widely distributed in developing countries. Rahman and coworkers summarized the problems that make small farmers more susceptible to any crisis, such as a lack of training on poultry farming, inadequate education and farming expertise, a lack of biosecurity awareness, a lack of infrastructure and marketing system, demand and supply imbalance, information disparity on market stability and estimation, a tendency to respond more to rumors about commercial poultry and poultry products, and a lack of access to veterinary services [19]. The general problems for smallscale poultry farming in developing countries are summarized in Figure 3. Small-scale poultry production in developing countries is operated informally and represents a high portion of poultry production. In Egypt, for example, small-scale poultry production represents 70% of all poultry production in Egypt [45]. Small-scale production has been found to be severely damaged due to the COVID-19 pandemic since it affected farm management, production systems, and resource endowment. All these effects were, directly and indirectly, related to movement restriction, resulting in less availability of supply of farm raw materials, like feed, essential veterinary services, and manpower, and ultimately production fall. It was reported that most small-scale farmers are on the edge of collapse, facing capital challenges, and are worried that they would be unable to continue their business owing to livestock supply chain disruptions. The severe negative impact on small-scale production in developing countries can be attributed to the following factors [21]: Lockdown harmed small-scale production severely because small-scale producers in developing countries rely more on labor than machinery. ii) Most small-scale-producing farms, including poultry farms, operate informally and, therefore, are excluded from the stimulus plans offered by governments to private businesses. Smallholder poultry producers mostly live in rural areas (sell eggs and live birds and purchase day-old chicks, feed, drugs, and disinfectants) [46]. However, Small-scale poultry production in developing countries is operated informally and represents a high portion of poultry production. In Egypt, for example, small-scale poultry production represents 70% of all poultry production in Egypt [45]. Small-scale production has been found to be severely damaged due to the COVID-19 pandemic since it affected farm management, production systems, and resource endowment. All these effects were, directly and indirectly, related to movement restriction, resulting in less availability of supply of farm raw materials, like feed, essential veterinary services, and manpower, and ultimately production fall. It was reported that most small-scale farmers are on the edge of collapse, facing capital challenges, and are worried that they would be unable to continue their business owing to livestock supply chain disruptions. The severe negative impact on small-scale production in developing countries can be attributed to the following factors [21]: (i) Lockdown harmed small-scale production severely because small-scale producers in developing countries rely more on labor than machinery. (ii) Most small-scale-producing farms, including poultry farms, operate informally and, therefore, are excluded from the stimulus plans offered by governments to private businesses. Smallholder poultry producers mostly live in rural areas (sell eggs and live birds and purchase day-old chicks, feed, drugs, and disinfectants) [46]. However, the animal husbandry services were severely interrupted due to lockdown and movement restrictions. Because most small-scale poultry farms are unregistered, they are not eligible for government stimulus programs [47]. (iii) Compared with large-scale production, small farmers earn fewer benefits due to increased production expenses [30,48], and they are reliant on the local dealers for feeds, medications, and operating capital [48][49][50]. (iv) The implementation of sanitary measures in small-scale farms is difficult due to the lack of logistical and financial resources [31], making them more vulnerable to other infections.
Therefore, it is recommended to enhance the preparedness and resilience of small-scale poultry production systems in developing countries to tackle future pandemics.

Prospective to Improve Poultry Husbandry under COVID-19 Pandemic
Challenges facing poultry sustainability in developing countries, problems, causes, and suggestions are summarized in Table 3.
Creating techniques that will help boost nutrition and food security is essential while simultaneously containing COVID-19 in African countries and handling significant socioeconomic problems [30]. Moreover, these techniques could also be applied to many Asian countries. The global spread of COVID-19 forced the imposition of self-isolation and physical distance to reduce the transmission risk and ensure human safety. The medical facilities and positive human responses were of particular concern; however, there are growing concerns about the effects of the COVID-19 pandemic on the food chain due to the lockdown of borders, seaports, and airports, its consequences on food security, and its influences on the poultry sector [18,51]. In the post-COVID-19 period, the policy of adapting backyard poultry as an alternative source of income not only increases poultry production but also ensures the availability of animal protein to the poorer sections of society, improves their purchasing power, and protects against labor "reverse migration" [17]. Small-scale poultry farmers may play a key role in supplying the demand for animal products in emerging markets. Several initiatives to give marginal farmers chicks, feed, and medicine were launched by the government and private organizations in India, Bangladesh, and Cambodia during the lockdown to reduce the catastrophic effect of COVID-19 on the agricultural economy [31].
The One Health concept integrates human, environmental, and animal health to regulate and prevent disease outbreaks [52][53][54]. The proliferation of the novel coronavirus created great health hazards to both humans and animals at various times, resulting in significant economic losses and environmental damage [4,8,31,51,55]. Chickens, ducks, and pigs are resistant to the SARS-CoV-2 virus or have a low vulnerability to this unique virus. However, many COVID-19 outbreaks have been reported in several countries in association with meat and poultry processing plants [56]. Due to the transmission of infectious agents outside workplaces to family and contacts of workers, the detection of hazard variables particular to meat-packing plants may aid in developing customized control programs in this business, which exemplifies the personal connection between workplace safety and public health.
According to the Centers for Disease Control and Prevention (CDC), 4913 cases with 20 deaths have been reported in different meat and poultry processing units [57]. It is recommended that all employees and supervisors should get regular training on infection control, workplace safety, and health tailored to their reading levels and chosen languages. The training should cover the following points: what employees should do if they feel sick before or at work; COVID-19 symptoms; sick leave regulations; social distance guidelines; proper use of PPE and face shield; sanitation facilities; application for screening when it becomes more readily accessible; possible transmission routes at work and elsewhere. Culturally competent trainers should deliver training in a context social distance is maintained and in the dialects used by employees and pay attention to the different levels of education [58]. Table 3. Sustainability of poultry production in developing countries, problems, causes, and suggestions.

Disruption of oultry supply chain
Persistence of the pandemic, rumors, panic, blockage of transportation restrictions, delivery delays, sales losses, operational disruptions, price fluctuation, lockdown, blockage of distribution channel, imbalance between supply and demand, and consumer's dilemma due to COVID-19 transmission When workers in poultry processing plants tested positive for COVID-19, public health officials suspended the plant for ten days. Those who have been identified as cases or close contacts have been told to self-isolate. According to the Canadian Food Inspection Agency (CFIA), there is no evidence that food is a common cause or route of viral transmission. No reports have yet linked the spread of COVID-19 to food or packaged food. As a result, there is no need to recall chicken products distributed by this plant [12]. Meat-packing facilities, abattoirs, and processing plants are at high risk of transmission of COVID-19. They are depicted as major sources of regional epidemics and, on rare occasions, as a critical source of a nationwide epidemic when the disease was otherwise under control. The identified danger to meat and poultry facility operations, part of the national reaction to COVID-19, necessitates immediate action to reduce worker risks and protect facility performance and the food chain. Cooperative management is necessary to minimize workplace hazards, enhance cleanliness and sanitation, and apply operating procedures and source control in poultry processing plants, which may help reduce the incidence of COVID-19 among employees. The following items are recommended during food processing: (1) applying soap and water on both hands for at least 20 s; (2) cleaning and sanitizing surfaces regularly; (3) thoroughly cooking the meat; (4) minimizing the risk of cross-contamination between cooked and raw foods.

Lessons Learned from the COVID-19 Pandemic
The COVID-19 pandemic has shown us how vulnerable we are as human beings to the invisible enemy, the SARS-CoV-2. The devastating impact of the virus is not limited to human civilization, as animals, the environment, and the ecosystem are all affected. In addition to the loss of human life, the actual impact of the pandemic on the global economy is beyond our estimation. These impacts are more severe in developing countries than those in developed countries. SARS-CoV-2 is zoonotic in nature. The pandemic has taught us to implement more basic research and surveillance on animal pathogens in the wild using the One Health-based approach. Findings of research, such as One Health-based research, will help in adopting intervention strategies for reducing contact or spread of infectious by creating a buffer zone. The factors that trigger the virus to cross the species barrier need to be revealed to better control future pandemic outbreaks. Besides, to overcome the impacts on the animal sector, such as poultry production and supply chain, attention has to be paid to smart farm management, including feed supply, biosecurity, veterinary service, human resources, and product sales. Moreover, it is now time to change relevant government policies so that farmers and farm owners who suspended their work due to lack of the necessary supplies and/labor receive compensations smoothly as soon as possible. Other measures are also recommended to implement the One Health concept (Table 3). Collectively, the following measures are described by several authors [16,59,60]: Moreover, the One Health strategy focuses not only on the pathogens and their host but also on the ecology and environment where the pathogens are maintained.
Thus, anthropogenic activities, such as urbanization, agricultural expansion, deforestation, and globalization, that destroy the ecosystem may cause the emergence of pathogens. Findings of the One Health-based research will help adopt intervention strategies for reducing contact or spread of infectious by creating a buffer zone.

Conclusions
The COVID-19 pandemic has significantly reduced poultry production and supply chain at the local and international levels, resulting in severe economic loss. In this pandemic situation, we have to take measures to ensure sustainable poultry production for regaining the loss in poultry industries. Such loss can be overcome if sustainable poultry production is ensured at local and industry levels. Compensating the farmers is an important step to retaining their production system. Continuous supply of raw materials in terms of day-old chicks, feed, vaccines, and human resources and a better farm management system are necessary to maintain sustainable poultry production during the COVID-19 era.