**3. The Nigerian scenario**

## **3.1 Index outbreak**

Nigeria experienced an outbreak of HPAI H5N1 virus in both commercial and local poultry populations during January 2006 as an extension of the global outbreaks [7]. The index HPAI-H5N1 was confirmed in Nigeria at a commercial poultry farm in Kaduna State, and by the end of the initial outbreak, over 46,000 poultry

*Viruses and Viral Infections in Developing Countries*

strain [1]. The artificial increased density of individual host pathogens increases spread to other hosts, and the short life cycles of the virus prevent the host from developing immunity against the organism [2]. With high density and short life span, contagiousness is not under selective pressure, and a selection criteria on strains allow strains to be selected mainly on virulence, i.e., harm to the host [2]. In addition, inadequate disinfection measures between batches allow the virus to survive in the environment [2]. Three potential clinical outcomes have been observed with AI infection in birds; these are (a) no clinical signs, (b) mild disease, and (c) severe disease with death [3]. The H5 and H7 subtypes of avian influenza (AI) virus associated with HPAI, which is extremely virulent, cause up to 100% mortality in domestic poultry. The virulence and ability to cause systemic infection have been attributed to the multibasic cleavage motif (minimal consensus sequence of -R-X-K/RR-) in their hemagglutinin molecule, which are recognized by subtilisin-like endoproteases that are virtually present in every tissue of their host and preferentially expressed at the surface of respiratory and gastrointestinal epithelia [4], making them capable of replicating in multiple tissue [5, 6]; hence, lesions are multisystemic (i.e., nervous, circulatory, respiratory, integumentary, musculoskeletal, hemopoietic, gastrointestinal, reproductive systems [7]). This chapter considers avian influenza virus infection with a special X-ray on the Nigerian outbreak scenario, general clinicopathologic features in domestic poultry and factors that support the persistence of the virus in the environment, and, when not adequately

controlled, how these can lead to an endemic and/or a pandemic state.

from LPAI progenitors of the H5 and H7 subtypes [16–18].

Influenza viruses are segmented negative-sense single-stranded RNA, belonging to the family *Orthomyxoviridae* [8]. This family is classified into influenza viruses' types A, B, and C, *Thogotovirus*, and *Isavirus* [9]. Only influenza type A viruses infect poultry [8], and avian influenza viruses are known to be a diverse group of viruses in the *Orthomyxoviridae* family, genus *Influenza A virus*, and have been categorized into subtypes based on the two surface glycoproteins, the hemagglutinin (H) and neuraminidase (N) [10]. There are now 18 H and 11 N surface glycoproteins [11]. Previously, HA1-16 and NA1-9 have been identified to occur naturally in avian host, mostly waterfowls where they exist in benign form (low pathogenic) [12]. Subtypes HA 17 and 18 and NA 10 and 11 were identified in bats [13] recently. Avian influenza viruses have also been further classified into two different pathotypes (low pathogenicity [LP] and high pathogenicity [HP]), based on the ability to produce disease and death in the major domestic poultry species, the chicken (*Gallus gallus domesticus*) [14]. HPAI has been shown to be caused in susceptible host species by only the avian influenza viruses of H5 and H7 subtypes, which contain multiple basic amino acids at the cleavage site of the hemagglutinin molecule, [15]. However, not all H5 and H7 avian influenza viruses are highly pathogenic. It has been shown that HPAI viruses emerge in domestic poultry

A typical flow of avian influenza virus in poultry mostly begins with the introduction of the virus to a region or country where the virus has not been known to be present. This introduction has been known to occur by way of contact of resident water fowls and/or backyard poultry with an infected migratory wild bird

**2. Avian influenza transmission**

**2.1 The virus**

**62**

**2.2 Transmission**

[25, 26] had been destroyed. This outbreak brought the Asian strain of highly pathogenic avian influenza (HPAI) H5N1 into Africa for the first time in the beginning of January 2006 [7, 27–29] in Nigeria. During this first incursion of the virus into Nigeria, the country lost excess of 1 million birds of various species [30, 31]. Since its emergence in Africa in 2006, avian influenza viruses of the H5N1 subtype have spread rapidly to poultry farms in several African countries.

This acute, generalized, fatal disease [32] affected free-ranged domestic poultry, backyard poultry, and commercial poultry comprising of chickens, ducks, geese, turkeys, guinea fowls, other gallinaceous birds, and ostriches in the poultry industry of the country. Although elsewhere in the world quails, ratites, passerine bird, flamingos, herons, raptors [32], and mammals have also been found to be susceptible to HPAI, this was not so in Nigeria. HPAI which is known to be caused by avian influenza viruses (AIVs) that are extremely virulent, resulting in up to 100% mortality in domestic chickens [33], was isolated in several outbreaks that occurred in Nigeria.

#### **3.2 Source of the virus**

Several sources have been found to be responsible for the introduction and reintroduction of the virus; these include wild bird sources, trade in poultry [29], and direct source introduction. Following the waves of outbreaks during the 2006–2007 periods, phylogeographic analysis [22] identified the north-central (Katsina, Jigawa, Yobe, Kano, Kaduna, Bauchi, and Gombe) and southwest (Lagos, Ogun, Oyo, Ekiti, and Kwara) regions as the two major sources for the HPAIV in Nigeria [22]. This supports the hypothesis that the introduction of the virus into Nigeria may be by wild birds and trade in poultry [29] and its products. Wild birds are strongly believed to be a major source of the virus to the northeastern states of Jigawa and Yobe, which are home to the Hadejia-Nguru wetlands and are said to be characterized by permanent and seasonal lakes and numerous population of migratory and residential waterfowl [22]. It is also known that this area sustains a large backyard poultry population and the highest concentration of domestic ducks, reared under free-range conditions, providing opportunities for contact between wild birds and backyard poultry [24].

#### **3.3 The poultry structure**

The poultry structure in Nigeria is comprised of two major systems, rural poultry production and commercial poultry production [34], as classified by the Food and Agricultural Organization (FAO) of the United Nation (UN). In the rural poultry production, it is a common practice to keep poultry in free-range, multispecies, multiage holdings with low biosecurity levels, thus exposing them to many at-risk contacts, and they could act as the epidemiologic link between the wild reservoir of AI viruses [22, 35] and industrial poultry. The commercial poultry production can be fully intensive or semi-intensive, depending on the level of automation and husbandry. **Figure 2A**–**D**, gives an insight to the poultry structure practiced in Nigeria.

#### **3.4 Surveillance and outbreaks investigation**

As far back as early February 2004, the veterinarians have been saddled with the responsibility of gearing efforts toward managing HPAIV outbreaks [37] if Nigeria was at risk or eventually experience an outbreak. Prevention strategy document for the emergency preparedness and response plan (EPP) [37] was ready as early as 2005. This included a risk analysis of the 24 wetlands in Nigeria and the two major

**65**

*Features of Highly Pathogenic Avian Influenza (HPAI) H5N1 in Domestic Poultry*

migratory routes of wild birds, evaluation and upgrading of veterinary services, ban on importation of poultry and poultry products, and increased surveillance for the virus [37]. Surveillance and disease reporting included passive and active surveillance and regular disease reporting. The active surveillance component involved epidemiological surveillance of network of 170 points within the country and targeted surveillance of wetlands and farms [37]. Surveillance was carried out between September and November 2005 at the Nguru-Hadejia wetlands [37]. Similarly, active surveillance was carried out in the same period in the high-risk agroecological farming areas and among live bird (poultry) markets, but all these surveillance activities failed to detect H5 or H7 avian influenza virus [37]. Several investigations have been carried out and are available to the public about the HPAI H5N1 outbreaks in Nigeria, including the virological identification and confirmation [26, 28, 37, 38], epidemiology and pathology of early [7] and resurgent outbreaks [39], and molecular characterization [29], including regional mortality and

*(A) Intensive poultry production system in the tropics [36]. (B) A semi-intensive poultry production system in the tropics [36]. (C) A mixed species backyard poultry production system comprising of ostriches, geese, Muscovy, mallard, and Pekin ducks before the introduction of HPAI [36]. (D) An extensively (free-ranging)* 

Reintroduction of the virus to Nigeria was first detected in January 2015, when the National Veterinary Research Institute (NVRI), Vom, Nigeria, received some chicken carcasses from the Kano State Ministry of Agriculture [39]. The carcasses were gotten from a backyard-commercial poultry farm and also from a live bird market (LBM) in Kauna and Sabon Gari, Kano State, northwestern Nigeria, respectively. The farm husbandry was mixed poultry species system where different types of chickens of various ages and stages were kept and were experiencing high mortality of 350 birds daily with eventual 100% mortality observed in the older birds (54 weeks) [39]. Also, in a concurrent incidence, unusual high mortality of birds brought from the northern part of Nigeria to two LBMs in Onipanu and Mushin, Lagos State, Southwestern Nigeria, was reported [39]. The specimens were analyzed by RT-PCR and virus isolation in embryonating chicken eggs, and all samples were found to be positive for HPAI (H5N1) subtype [39]. This ended the 9-year silence of the activity of the virus in Nigerian poultry [39]. Again, a strong genetic link between viruses isolated in Nigerian poultry and wild bird from Europe has been established [21, 22, 41, 42], thereby suggesting that wild birds are the major

*DOI: http://dx.doi.org/10.5772/intechopen.86098*

morbidity characteristics [40].

*reared Muscovy/mallard duck flock [36].*

**Figure 2.**

**3.5 Reintroduction of the virus into domestic poultry**

*Features of Highly Pathogenic Avian Influenza (HPAI) H5N1 in Domestic Poultry DOI: http://dx.doi.org/10.5772/intechopen.86098*

#### **Figure 2.**

*Viruses and Viral Infections in Developing Countries*

**3.2 Source of the virus**

wild birds and backyard poultry [24].

**3.4 Surveillance and outbreaks investigation**

**3.3 The poultry structure**

practiced in Nigeria.

[25, 26] had been destroyed. This outbreak brought the Asian strain of highly pathogenic avian influenza (HPAI) H5N1 into Africa for the first time in the beginning of January 2006 [7, 27–29] in Nigeria. During this first incursion of the virus into Nigeria, the country lost excess of 1 million birds of various species [30, 31]. Since its emergence in Africa in 2006, avian influenza viruses of the H5N1 subtype

This acute, generalized, fatal disease [32] affected free-ranged domestic poultry, backyard poultry, and commercial poultry comprising of chickens, ducks, geese, turkeys, guinea fowls, other gallinaceous birds, and ostriches in the poultry industry of the country. Although elsewhere in the world quails, ratites, passerine bird, flamingos, herons, raptors [32], and mammals have also been found to be susceptible to HPAI, this was not so in Nigeria. HPAI which is known to be caused by avian influenza viruses (AIVs) that are extremely virulent, resulting in up to 100% mortality in domestic chickens [33], was isolated in several outbreaks that occurred in Nigeria.

Several sources have been found to be responsible for the introduction and reintroduction of the virus; these include wild bird sources, trade in poultry [29], and direct source introduction. Following the waves of outbreaks during the 2006–2007 periods, phylogeographic analysis [22] identified the north-central (Katsina, Jigawa, Yobe, Kano, Kaduna, Bauchi, and Gombe) and southwest (Lagos, Ogun, Oyo, Ekiti, and Kwara) regions as the two major sources for the HPAIV in Nigeria [22]. This supports the hypothesis that the introduction of the virus into Nigeria may be by wild birds and trade in poultry [29] and its products. Wild birds are strongly believed to be a major source of the virus to the northeastern states of Jigawa and Yobe, which are home to the Hadejia-Nguru wetlands and are said to be characterized by permanent and seasonal lakes and numerous population of migratory and residential waterfowl [22]. It is also known that this area sustains a large backyard poultry population and the highest concentration of domestic ducks, reared under free-range conditions, providing opportunities for contact between

The poultry structure in Nigeria is comprised of two major systems, rural poultry production and commercial poultry production [34], as classified by the Food and Agricultural Organization (FAO) of the United Nation (UN). In the rural poultry production, it is a common practice to keep poultry in free-range, multispecies, multiage holdings with low biosecurity levels, thus exposing them to many at-risk contacts, and they could act as the epidemiologic link between the wild reservoir of AI viruses [22, 35] and industrial poultry. The commercial poultry production can be fully intensive or semi-intensive, depending on the level of automation and husbandry. **Figure 2A**–**D**, gives an insight to the poultry structure

As far back as early February 2004, the veterinarians have been saddled with the responsibility of gearing efforts toward managing HPAIV outbreaks [37] if Nigeria was at risk or eventually experience an outbreak. Prevention strategy document for the emergency preparedness and response plan (EPP) [37] was ready as early as 2005. This included a risk analysis of the 24 wetlands in Nigeria and the two major

have spread rapidly to poultry farms in several African countries.

**64**

*(A) Intensive poultry production system in the tropics [36]. (B) A semi-intensive poultry production system in the tropics [36]. (C) A mixed species backyard poultry production system comprising of ostriches, geese, Muscovy, mallard, and Pekin ducks before the introduction of HPAI [36]. (D) An extensively (free-ranging) reared Muscovy/mallard duck flock [36].*

migratory routes of wild birds, evaluation and upgrading of veterinary services, ban on importation of poultry and poultry products, and increased surveillance for the virus [37]. Surveillance and disease reporting included passive and active surveillance and regular disease reporting. The active surveillance component involved epidemiological surveillance of network of 170 points within the country and targeted surveillance of wetlands and farms [37]. Surveillance was carried out between September and November 2005 at the Nguru-Hadejia wetlands [37]. Similarly, active surveillance was carried out in the same period in the high-risk agroecological farming areas and among live bird (poultry) markets, but all these surveillance activities failed to detect H5 or H7 avian influenza virus [37]. Several investigations have been carried out and are available to the public about the HPAI H5N1 outbreaks in Nigeria, including the virological identification and confirmation [26, 28, 37, 38], epidemiology and pathology of early [7] and resurgent outbreaks [39], and molecular characterization [29], including regional mortality and morbidity characteristics [40].

#### **3.5 Reintroduction of the virus into domestic poultry**

Reintroduction of the virus to Nigeria was first detected in January 2015, when the National Veterinary Research Institute (NVRI), Vom, Nigeria, received some chicken carcasses from the Kano State Ministry of Agriculture [39]. The carcasses were gotten from a backyard-commercial poultry farm and also from a live bird market (LBM) in Kauna and Sabon Gari, Kano State, northwestern Nigeria, respectively. The farm husbandry was mixed poultry species system where different types of chickens of various ages and stages were kept and were experiencing high mortality of 350 birds daily with eventual 100% mortality observed in the older birds (54 weeks) [39]. Also, in a concurrent incidence, unusual high mortality of birds brought from the northern part of Nigeria to two LBMs in Onipanu and Mushin, Lagos State, Southwestern Nigeria, was reported [39]. The specimens were analyzed by RT-PCR and virus isolation in embryonating chicken eggs, and all samples were found to be positive for HPAI (H5N1) subtype [39]. This ended the 9-year silence of the activity of the virus in Nigerian poultry [39]. Again, a strong genetic link between viruses isolated in Nigerian poultry and wild bird from Europe has been established [21, 22, 41, 42], thereby suggesting that wild birds are the major

possible source of introduction and reintroduction of HPAI viruses into Nigeria's poultry. On the other hand, rural poultry mainly kept in free-range, multispecies, multiage holdings with low biosecurity levels are exposed to many at-risk contacts and therefore act as the epidemiologic link between the wild reservoir of AI viruses and industrial poultry [22, 35]. The predominant species in the rural poultry sector of Africa is the scavenging indigenous domestic fowl (*Gallus gallus domesticus*) [43], which in most African countries has no regular health control program, may or may not have shelter, and scavenges for most of their nutritional needs [43]. In fact, village chickens have been reported to act as potential reservoirs and carriers of infections to themselves and to the more susceptible exotic breeds in commercial poultry farms [44].
