Influence of COVID-19 on the poultry production and environment

Although chickens are not susceptible to SARS-CoV-2, several coronavirus disease outbreaks have been described concerning poultry processing facilities in different countries. The COVID-19 pandemic and the developed strain caused 2nd, 3rd, and recent Indian strain waves of epidemics that have led to unexpected consequences, such as forced reductions in demands for some industries, transportation systems, employment, and businesses due to public confinement. Besides, poultry processing plants' conditions exacerbate the risks due to the proximity on the line, cold, and humidity. Most workers do not have access to paid sick time or adequate health care, and because of the low wages, they have limited reserves to enable them to leave steady employment. In addition, workers in meat and poultry slaughterhouses may be infected through respiratory droplets in the air and/or from touching dirty surfaces or objects such as workstations, break room tables, or tools. Egg prices have increased dramatically during the lockdown as consumers have started to change their behaviors and habits. The COVID pandemic might also substantially impact the international poultry trade over the next several months. This review will focus on the effect of COVID-19 on poultry production, environmental sustainability, and earth systems from different process points of view.


Introduction
Coronavirus infections have been associated with many diseases, such as the Middle East respiratory syndrome (MERS) (WHO 2019) and severe acute respiratory syndrome (SARS) (Law et al. 2020) in humans. Recently, a new coronavirus (SARS-CoV-2 or COVID-19) has been isolated; it is responsible for the recent COVID-19 pandemic, and new strains developed that spread in European Union (EU), causing the 2nd lockdown (Alagawany et al. 2021;Saghir et al. 2021   infection causes a systemic disease that is spread via airborne/droplets/aerosol. COVID-19 has indirectly affected humans, animal production, the environment, earth systems, social and economic conditions worldwide (Sharun et al. 2021). There have been rumors about the potential involvement of eggs and chicken meat in the spread f COVID-19, which resulted in a dramatic drop in demand for poultry goods beginning in February 2020, just before the declaration of the lockout and culminating in the deterioration of poultry economics due to working capital erosion. From local farmers to large integrators, all aspects of poultry processing were severely impacted, much worse than the Avian influenza outbreak of 2006 (Das and Samanta 2021).
There is great attention on the adverse impact of the environment inside poultry house and increase the harmful dust and gaseous and the incidences of asthma, allergy diseases and repository and pulmonary disorders diseased among poultry workers and keepers. In addition, a high prevalence of nasal (51.1%) and asthmatic (42.5%) symptoms were observed in poultry keepers mainly, which may increase the susceptibility of works to Covid-19 (Viegas et al. 2013;Arcangeli et al. 2020;Clarke et al. 2021). Recent evidence indicates high incidences of COVID-19 among patients with chronic diseases and respiratory diseases (Hafez and Attia 2020). The contents of nitrogen (N) and phosphorus (P) in poultry litter and its negative impact on soil surface and groundwater because of continuous poultry litter application raises the risk of depletion of surface and the quality of the groundwater supplies (Bolan et al. 2010). The use of poultry litter has been shown to raise the edge-of-field losses of N and P in surface and subsurface runoff. Nitrate-N losses in groundwater will accumulate to amounts that surpass reasonable human intake limits (10 mg/L) (Colt 2006). Therefore, it is logical to expect the direct and indirect relationship between the economic and environmental influence of COVID-19 with concern to the poultry production sector through a health issue. This review shed light on the impact of COVID-19 on poultry production and the environment.
The Betacoronavirus genus contains COVID-19, SARS-CoV, and MERS-CoV (Shereen et al. 2020). COVID-19 is an enveloped virus that is highly infectious, even though it is easily destroyed by soap and common disinfectants. COVID-19 infection causes a systemic disease in which fever, dry cough, and fatigue have been most commonly reported; in some cases, diarrhea and vomiting can also be observed. Although chickens are not susceptible to SARS-CoV-2 (Schlottau et al. 2020), several coronavirus disease outbreaks have been described concerning poultry processing facilities in different countries as Brazil, Canada, and Spain (Durand-Moreau et al. 2020). Studies have linked livestock plants to a high potential for a community spread in the surrounding areas (Middleton et al. 2020;Taylor et al. 2020). Work routines in livestock processing make plants susceptible to local outbreaks of respiratory viruses. The long work shifts near coworkers, difficulty maintaining proper face-covering due to physical demands, and shared transportation among workers (Taylor et al. 2020). Besides, the virus thrives in lower temperatures and very high or very low relative humidity, and metallic surfaces retain live viruses for longer than other environments (Middleton et al. 2020).
The virus is thought to spread principally via respiratory droplets from an infected person to a healthy one through close contact. Strategies to prevent the spread and the strengthening of COVID-19 include increasing public awareness about transmission and decreasing trade activities. The possibility of the viruses spread among people is related to the biological properties of each virus. Still, it is also affected by external factors such as temperature, humidity, population density, and thus lack of hospital beds ). In addition, the symptoms of the infection have multiple facets.
The public services and facilities must provide decontaminating reagents for cleaning hands daily. In addition, physical contact with wet and contaminated objects should be considered in dealing with the virus, avoiding contact with confirmed or suspected patients, and using face protective devices (Rothan and Byrareddy 2020;Islam et al. 2020).
Another way to contrast the SARS-CoV-2 spread is to know the virus's mechanisms and develop appropriate therapeutic strategies. Essential acquired knowledge is that the virus comes in the human cells through its high binding affinity with angiotensin-converting enzyme 2 (ACE2) (Benseñor and Lotufo 2020;Chen et al. 2020). So, Chen et al. (2020) proposed that specific antibodies and small molecules can prevent the binding between ACE2 and the receptors (RBD) of the virus, and this way could represent a potential strategy against COVID-19 disease prevention and control.
To control a further outbreak, strategies should be developed and applied around the world. A myriad of lessons has been learned from the COVID-19 pandemic, which pays great attention to the relationship among humans, wild animals, and livestock. Where there is a high human population density, the government in each country must be ready with specific pandemic plans to avoid the suffering of the health systems (Benseñor and Lotufo 2020). Other lessons will be learned  because it will take time to develop an effective and successful vaccine and/or specific antiviral therapy for COVID-19 Rahman et al. 2020). Therefore, it is essential to determine whether a neutralizing antibody and/or SARS-CoV-2-specific T cell response is sufficient to prevent clinical disease transmission, determine the magnitude of the reactions required to provide protection and the longevity of these protective responses (Sariol and Perlman 2020).
In 2019, the weakness of health systems worldwide came into focus due to insufficient hospital beds, lack of adequate diagnostic kits, inadequately trained physicians, and high numbers of deaths, including health professionals, physicians, nurses, and health care workers. Therefore, it is fundamental to pay more attention to the development of medical education, health care programs, fighting poverty, and addressing hunger rather than developing instruments of war, namely bombs, missiles, and nuclear weapons. Furthermore, with limited knowledge about the COVID-19 pandemic and our increasingly interlinked and multifaceted world, what is ultimately and necessarily required are robustness, flexibility, and pliability to deal with unforeseen future situations and dialogs (Luo 2020).
In general, the average worldwide lethality of SARS-COV-2 is approximately 2.21% (total deaths divided by the total confirmed cases), which is quite a bit lower than SARS (9.6%), and far below MERS-CoV (34%) and Ebola (65.7%). The overall numbers of infections worldwide, specifically in several leading coronavirus countries and authors' countries (Brazil, Germany, Italy, Saudi Arabia; Egypt) are reported in Table 2. The cases are continuing to growth with the release of the 2nd and 3rd waves of the disease and the new Indian strains. USA, India, Brazil, Russia, and France are the leading countries in the incidences and death in Covid-19 cases. The USA is the dominant country in confirmed cases and death, followed by India and Brazil, which showed a high incidence of confirmed cases. From the death cases per million-population point of view, the countries can be ranked as Italy>USA>Brazil> France>Russia>Germany>Saudi Arabia> India> Egypt. In Saudi Arabia, prevention and control programs for COVID-19 have so far achieved considerable success. As of February 28, 2021, the confirmed number of cases infected with COVID-19, as reported by (19 and 20) in Saudi Arabia, was 362,601 (1.04% of the total population), and recovered patients was 356,387, which represents 98.3 of the confirmed cases. Thus, there have been 6,214 deaths or 179 cases per million of the population (WHO 2020a). In Egypt, India, and Saudi Arabia, the cases are much lower than the global cases, showing 104, 108, and 179 cases per million people, respectively, compared to the average global cases with 230 per million people. Details about total cases and deaths due to COVID-19 around the globe are shown in Table 3.
These discrepancies may be due to several factors, such as early lockdown, decreased trade activities that block transmission pathways, and increasing public awareness of disease control and prevention, which was initiated with early confirmed cases in March 2020. In addition to the use of active and random surveys, other programs, such as working from home, may be implemented as a part of the control and prevention programs when necessary.
In Italy, the situation has been quite different, with 2,067,487 confirmed cases and 73,029 death cases. Several hypotheses have been considered to explain the high mortality rate, as a relatively older average age of the Italian people, more intensive social contacts among children and older people, and underestimating the total number of COVID-19 cases in Italy (Worldmeters 2020  per million, showing the lowest number as of February 28, 2020 (WHO 2020a; Worldmeters 2020). COVID-19 was first detected in Brazil on February 25, 2020, making it the first Latin American country to report a case of the novel coronavirus (WHO 2020a). Since then, the number of infections has risen drastically; today, Brazil is the Latin American country with the highest number of confirmed COVID-19 cases (COVID-19 situation update worldwide 2020; Montanez 2020a), with over 7,561,550 (Onder et al. 2020). The first death due to this disease was registered on March 17, 2020 (COVID-19 situation update worldwide 2020), and approximately 3 months later, the number of fatalities surpassed 50,617, with 594,108 recoveries (Montanez 2020b; Scalzaretto 2020). As of December 31, 2020, the number of deaths reached 192,681 cases (Onder et al. 2020, show-ing cumulative increase over time. The number of cases and deaths has probably been underestimated. An experiment by the Imperial College (London, UK) about the spread rate of COVID-19 in 48 countries showed Brazil at the top. Large cities such as São Paulo and Rio de Janeiro are currently the top hotspots. Still, there are signs that infections are spreading into minor cities with insufficient numbers of ventilators and intensive care beds (Montanez 2020b;Scalzaretto 2020). While the World Health Organization (WHO) has suspended chloroquine trials in Brazil, the Health Ministry has issued a reference for the public health system to use the medicine in COVID-19 patients from the very early phases of the disease onward. This directive is contrary to recommendations from medical associations (Ficetola and Rubolini 2020;Montanez 2020b;Scalzaretto 2020).

The influence of the COVID-19 pandemic on the environment
The environmental effects of the COVID-19 pandemic have received relatively little attention. Still, this growing interest after the outbreak of 2nd and 3rd waves of COVID-19 and One of the other effects of the COVID-19 pandemic has been a drop in coal and oil consumption worldwide, a phenomenon that has contributed to a large-scale decline in air pollution (IEA 2020; Saadat et al. 2020). While this reduction is essential for environmental health in general, it also benefits individuals who contract COVID-19. Indeed, areas with higher air pollution have presented markedly higher mortality rates from COVID-19 (BBC News 2020).
The repeal of single-use plastic bans, a phenomenon that has translated into a heightened demand for bottled water, personal protective equipment (e.g., masks for individuals who must venture into public), plastic bags, and packaging (Tenenbaum 2020). Medical waste and the trash from personal protective equipment, such as gloves and masks, are also on the rise (Zambrano-Monserrate et al. 2020). Some fast food and retail chains have banned the use of reusable cups and food containers (Peszkô 2020). Thus, the oil industries have produced more plastics to mitigate financial losses (Van der Made 2020). The generation of inorganic and organic waste has been increased due to the consumer's demand for online shopping and home delivery, and trash recycling has been reduced in many countries because of the concerns about the hazard of SARS-COV-2 spreading in recycling centers (Zambrano-Monserrate et al. 2020).
It is possible that a virus can persist in drinking water, but COVID-19 has not been observed in drinking water supplies; based on present data, the hazard to water supplies is low. However, according to the WHO (2020b), studies of surrogate coronaviruses have indicated that the virus could remain infectious in water contaminated with feces for days to weeks. The influence of the COVID-19 pandemic on the environment is illustrated in Fig. 2. The impact of the COVID-19 pandemic on the poultry economy Poultry producers have been affected by the COVID-19 pandemic, but the influences vary substantially from one area to another. Indeed, each country differs concerning how the disease progresses. In a study performed in England and Spain (Clements 2020a), producers indicated a recent increase in product demands, with 17.4% mentioning that the rise had been marked. Nevertheless, this situation has not been universal because 37% stated that requests had dropped, with 28% indicating that the reduction had been considerable. In addition, there has been increased acceptance to perform work over the Internet in favor of live production; 17% of respondents stated that farms had used fewer laborers. Over 14% of respondents revealed that the pandemic had rejuvenated a switch to fully automatic slaughtering plants. According to 8% of respondents, the issues caused by the COVID-19 pandemic have encouraged them to hasten their plans for automatization (Clements 2020b).
In poultry, significant efforts have been made to restrict the avian infectious bronchitis virus (IBV) with is part of the genus Gammacoronavirus; it is not transmitted to humans. In addition, SARS-CoV and COVID-19 are from the same group and use the same ACE2 host cell receptor, and thus SARS-CoV does not infect or cause disease in poultry. This finding suggests that poultry are unlikely to serve as a reservoir for SARS coronaviruses (Hafez 2010).
The immune system of human and avian species varies greatly and thus vaccination protocols, the appropriate vaccine virus serotype, and applications are different (Hafez 2005;Torremorell and Bender 2020). The production of human vaccines is essential to safety and wellbeing. Poultry production has not been at risk to the global spread of SARS-CoV (Hafez 2010). Recent data have indicated that it is not associated with poultry or poultry products, and chickens are not susceptible to intranasal infection by the virus (Friedrich-Loefler-Institut 2020a, 2020b; Schlottau et al. 2020). All swabs and organ samples, and contact birds remained negative for COVID-19 RNA, while infected fruit bats and ferrets were susceptible to the infection; the symptoms were stronger in ferrets than fruit bats (Friedrich-Loefler-Institut 2020a). Additionally, Shi et al. (2020) stated that cats and ferrets are highly susceptible to COVID-19, dogs have a low risk, and livestock, including chickens, pigs, and ducks, are not vulnerable to the virus. Improved poultry resistance to COVID-19 based on enhanced hygiene, biosecurity, and immunity would provide additional benefits for producers (Hafez 2010). It is recognized that vitamins C, B6, and E and minerals such as zinc and magnesium have played and will continue to play vital roles in sustaining immune function during the COVID-19 pandemic (CSIS 2020).
The economic pressures induced by the COVID-19 pandemic can be seen from different points of view. For example, the pandemic has increased unemployment. Restaurants chains and retailers are trying to fulfill their obligations to their employees while attempting to keep their businesses solvent ). In addition, the conditions in poultry processing plants exacerbate the risks due to the proximity on the line, cold and humidity. Most of the workers do not have access to paid sick time or adequate health care, and because of the low wages, they have limited reserves to enable them to leave steady employment (CNN 2020).
The COVID-19 pandemic has had a huge impact on farmers and food suppliers in several ways. First, there are not enough people in slaughterhouses to process the poultry, and farmers are being forced to euthanize their stock. Recently, about 2 million chickens in Delaware and Maryland were humanely killed because processing plants are short-staffed (CNN 2020). Nonetheless, poultry is not affected by COVID-19 (Berkhout 2020) and do not transfer it to humans, and the animal feed industry has been influenced by the cessation of slaughterhouses (Brown and Fu 2020), restaurants, and fast-food chains around the world to avoid contamination among workers and consumers. The closure of processing facilities may ultimately cause the depopulation of millions of animals (chickens, pigs, and cattle) (McDougal 2020). Third, biosecurity is the main line of defense that each breeder, hatchery, and poultry owner has against diseases. Improvements in biosecurity practices will help workers remain safe. Personal and facility cleanliness and avoiding transporting contaminated material such as chicken manure are essential (Benjamin 2020; Montanez 2020a).

Meat and eggs
Workers in meat and poultry slaughterhouses have had to keep working during the COVID-19 pandemic. Therefore, their work situations in the slaughterhouses and zones, where they must remain near coworkers and directors, may considerably increase their possible exposure risk to COVID-19. In addition, workers in meat and poultry slaughterhouses may be infected through respiratory droplets in the air and/or from touching dirty surfaces or objects such as workstations, break room tables, or tools (CDC 2019).
Despite the COVID-19 pandemic, global food prices have remained stable. According to the Center for Strategic International Studies (CSIS 2020; Galimberti 2020), global prices only dropped 4.3% from February to March 2020 due to the demand for contractions amid lockdowns and quarantines (Welshans 2020). The need for poultry meat and eggs has increased at the retail level due to confinement. The retail market for poultry meat was amplified by nearly 75% during the panic buying phase, which took place in the first few weeks of the crisis; however, this demand has returned to normal levels. Demand for eggs has increased by 20-35% in England (NFU 2020). Fig. 2 The influence of the COVID-19 pandemic on the environment The European Poultry Producers Association (AVEC) has observed a 10-30% reduction in broiler slaughtering in European Union (EU) member states (AVEC 2020). Furthermore, poultry prices have declined around 20% since the beginning of March 2020, reversing the trend in EU poultry meat prices from December 2019 to the beginning of March 2020 (ANCO 2020). This evolving EU market situation is being compounded by the closure of export markets for poultry producers in EU member states (AVEC 2020). Poland is one of the countries suffering the most. In the United States of America (USA), which exports a lot of chicken meat, the global export estimates for the chicken meat market have been cut due to emerging risks from the COVID-19 spread (USDA 2020). China's agriculture ministry has stated that the supply of chicken and egg losses of US$14.3 million (Clements 2020a(Clements , 2020b. Egg prices have increased dramatically during the lockdown as consumers have started to change their behaviors and habits. Consumers had stockpiled necessary food items, including milk, eggs, and bread, to prepare for potential quarantines. Still, as lockdowns were introduced and people had to stay at home, actual consumption increased. People no longer eat out, so the demand for eggs is shifting from the foodservice sector to the retail channel, as consumers are cooking more meals at home (ANCO 2020). Egg consumption has also increased to replace more expensive protein forms in households that are seeing a decline in their income because of COVID-19-related job losses.

Hatcheries
The impact of the pandemic on poultry hatcheries has also been strong. The lockdown and the consequent limitation to the international poultry market have decreased the request for eggs to be used for incubation. Some governments have banned the import of poultry meat mainly to protect their internal market; this action has reduced general chicken placements by 15-25% (De Lange 2020). In Italy, several hatcheries have been forced to euthanize chickens and then reduce the number of incubated eggs (Tuttoggi 2020). If eggs are regularly sent to a hatchery, one way to reduce the number of incubated eggs is to prolong their storage at low temperatures. However, in the long term, this approach can harm hatchability and chick quality. Consequently, it might be better to reduce the number of eggs that enter hatchery, an action that is possible by culling old flocks and inducing forced molting in young flocks (De Lange 2020). Nevertheless, this approach reduces the cost of 1-day-old chickens: in Italy, the price has dropped by 35%.

Feed and food security
The availability of raw materials to prepare poultry feed has been strongly reduced by the COVID-19 pandemic in almost all countries, although the reasons are variable. The main ingredients in poultry feeds are corn and soybeans. The primary producers of corn are the USA, China, Brazil, and Argentina; the same countries also produce the most soy, albeit in a different order: the USA, Brazil, Argentina, and China. Thus, many countries around the world, dependent on imports for these raw materials, have had substantial problems in procuring the ingredients to prepare poultry feeds. In addition, about 65% of the net annual production of wheat, corn, and soybeans is used in the feed industry for farm animals, while the remaining 35% is used to meet human needs (All About Feed 2020a, 2020b). Thus, even though there has been an increase in grain consumption for human use, it has been unable to compensate for the losses tied to lowering animal feed production use (All About Feed 2020b; Berkhout 2020).
Furthermore, some agricultural sector activities are connected to migrant workers, who are stuck in their home countries due to lockdowns. Hence, the feed industries have lost a significant portion of their workforce (All About Feed 2020a). These factors have significantly impacted the global poultry sector (The Poultry Site 2020; Poudel et al. 2020).
Another possible risk in the next future is the concern about food safety and security. Even though it has been well established that poultry does not host COVID-19 and thus cannot transmit it to humans (Shi et al. 2020), most concerns are about intensive animal production that could amplify the threats of disease spread and emergence. The likelihood of outbreaks of high-impact animal diseases is elevated by the quarantine of many animals in limited zones, narrowed genetic diversity, and thus the increasing turnover of animals (CDC 2019; Tomley and Shirley 2009). Currently, there is no evidence that COVID-19 can be transmitted by food; however, the transmission is possible if an infected person touches food and another one, within a short time, touches the same food and then her or his mouth or eyes (CDC 2019; BfR 2020). Furthermore, the persistence of the virus at frozen temperatures has not been well described (CDC 2019), but other coronaviruses (e.g., MERS and SARS-CoV-1) can continue to pose a risk for up to 2 years in a frozen state (Hafez and Attia 2020). Thus, this pandemic must push poultry production to achieve several goals. First, the industry must move toward intensive production sustainability, especially by using modern technologies (precision poultry farming) or increasing extensive meat and egg production techniques. Second, the health and immune status of farmed poultry must be improved to increase their disease resistance. Third, feeding strategies must improve the content of poultry products of bioactive compounds that can stimulate the human immune defense (Parrish et al. 2008). Finally, high hygienic standards should be ensured through the entire food chain, from farm to fork. Impacts of COVID -19 on the global poultry sector is briefed in Fig. 3.

International poultry trade
The COVID pandemic might also substantially impact the international poultry trade over the next several months. For example, in the EU, many poultry meat (around 850,000 tons) is imported from developing countries, mainly Brazil, Thailand, and Ukraine, every year. Those imports are mainly destined for the foodservice market. However, to not lose their rights in the EU Tariff Rate Quota system, these countries continue to export poultry meat, even though the EU market does not demand it at the moment. Thus the meat is stored until the HORECA (hotel, restaurant, café) chains reopen. This action will result in a significant oversupply of poultry meat on the EU market in the weeks and months to come, with dangerous consequences on the price and quality of the products and future trade. On top of that, avian influenza outbreaks in Eastern Europe continue to hit hard in some countries (Poland, Hungary, and Romania). This issue has resulted in the closure of export markets in developing countries, driving this meat intended for exports back on the EU market and adding to the crisis (AVEC 2020; Parrish et al. 2008).
In conclusion, the possibility of poultry being infected by COVID-19 is remote, given that there is only a 60% genetic similarity between humans and chickens (Warren and Sawyer 2019). However, proper handling of animal products and safety measures should be taken during marketing and handling as a general role for all food supplies. Moreover, the possibility of the existence of COVID-19 in feedstuff and feed is not likely due to high temperature and pressure during feed processing. In addition, the impact of the COVID-19 pandemic on the various poultry sectors such as slaughterhouses, broiler industry, table egg industry, hatcheries, and international poultry trade were favorable for the egg industry and adverse for the other sectors. Therefore, biosecurity, hygiene, and immunity have been and will remain the front line of defense during the COVID-19 pandemic. Therefore, developing and enhancing the current biosecurity measurements is essential to face the new emergence of diseases and overcome the unseen enemy after spreading the 2nd and the ongoing 3rd wave of COVID-19.
Author contributions HMH, YAA, FB, MEA, AFK and MCO were equally contributed to all stages of preparing, drafting, writing and revising this review article. All authors listed have made a substantial, direct, and intellectual contribution to the work during different preparation stages. All authors read, revised and approved the final version of this manuscript.
Funding Open Access funding enabled and organized by Projekt DEAL.
Data availability The datasets used in this study are available in text and cited in the reference section.

Decalarations
Ethics statement As a review, this section may not be applicable. Conflict of interest The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
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