Advances in Virology

Advances in Virology / 2018 / Article

Review Article | Open Access

Volume 2018 |Article ID 6097291 |

Muhammad Bashir Bello, Khatijah Mohd Yusoff, Aini Ideris, Mohd Hair-Bejo, Ben P. H. Peeters, Abdurrahman Hassan Jibril, Farouk Muhammad Tambuwal, Abdul Rahman Omar, "Genotype Diversity of Newcastle Disease Virus in Nigeria: Disease Control Challenges and Future Outlook", Advances in Virology, vol. 2018, Article ID 6097291, 17 pages, 2018.

Genotype Diversity of Newcastle Disease Virus in Nigeria: Disease Control Challenges and Future Outlook

Academic Editor: Binod Kumar
Received21 Jun 2018
Accepted28 Aug 2018
Published02 Dec 2018


Newcastle disease (ND) is one of the most important avian diseases with considerable threat to the productivity of poultry all over the world. The disease is associated with severe respiratory, gastrointestinal, and neurological lesions in chicken leading to high mortality and several other production related losses. The aetiology of the disease is an avian paramyxovirus type-1 or Newcastle disease virus (NDV), whose isolates are serologically grouped into a single serotype but genetically classified into a total of 19 genotypes, owing to the continuous emergence and evolution of the virus. In Nigeria, molecular characterization of NDV is generally very scanty and majorly focuses on the amplification of the partial F gene for genotype assignment. However, with the introduction of the most objective NDV genotyping criteria which utilize complete fusion protein coding sequences in phylogenetic taxonomy, the enormous genetic diversity of the virus in Nigeria became very conspicuous. In this review, we examine the current ecological distribution of various NDV genotypes in Nigeria based on the available complete fusion protein nucleotide sequences (1662 bp) in the NCBI database. We then discuss the challenges of ND control as a result of the wide genetic distance between the currently circulating NDV isolates and the commonest vaccines used to combat the disease in the country. Finally, we suggest future directions in the war against the economically devastating ND in Nigeria.

1. Introduction

Poultry production is globally threatened by a highly devastating disease of birds called Newcastle disease (ND). The disease was named after a place known as Newcastle Upon Tyne, in England where it was reported for the first time in 1926 [1]. The disease was also reported around the same time in Java, Indonesia [2]. Amazingly, its geographic distribution slowly expanded, leading to a well-established pandemic of the disease barely two decades after its novel emergence [3]. Subsequently in the late 1960s, the second pandemic of the disease occurred with an incredibly high speed, taking only four years to spread throughout the world, probably due to extensive commercialization of poultry production and the improvement of air transport systems which facilitated the exchange of exotic birds into new areas [4]. Although this pandemic was quickly placed under control with the then available ND vaccines, the third pandemic still occurred around the early 1980s among the racing pigeons [5, 6]. This particular pandemic proved to be difficult to control because of the nature of racing pigeon husbandry system. Eventually, the pandemic virus spilt over to the domesticated chicken and caused serious economic losses in the poultry subsector [7]. The fourth pandemic, which started around the mid-1980s in the South-Eastern Asia, is currently believed to be on-going and has so far spread extensively to the Middle East, Europe, America, and Africa [811]. In Nigeria, the first official documentation of ND was in 1952 (Hill et al. 1953) and at present, the disease has been reported in all the ago-ecological zones of the country [1215].

The aetiology of ND is an avian paramyxovirus type-1, which is a member of the genus Avulavirus in the family Paramyxoviridae [16]. The genetic material of the virus is a negative sense RNA made up of six genes encoding six structural proteins in the order 3′NP-P-M-F-HN-L5′ [17, 18]. Pathogenicity indices such as the mean death time (MDT) in 9-10-day-old embryonated chicken eggs and the intracerebral pathogenicity index (ICPI) in 1-day-old chicks are often used to classify the virus isolates into velogenic, mesogenic, and lentogenic strains [19]. The velogenic strains (neurotrophic or viscerotropic) are highly fatal and therefore demonstrate the severest clinical form of the disease, causing haemorrhagic gastroenteritis, pneumonia, and/or encephalitis [20, 21]. The mesogenic strains which are moderately pathogenic cause respiratory and neurological symptoms but with significantly low mortality [22, 23]. On the other hand, the lentogenic pathotypes are of extremely low virulence, causing only mild respiratory or asymptomatic enteric disease in the affected chicken [23, 24]. Interestingly, the major determinant of NDV virulence has been traced to be the amino acid composition of its fusion protein cleavage site [25]. All virulent strains have multiple basic amino acid residues at positions 112-116 and a phenyl alanine at position 117, making them cleavable by most of the ubiquitously distributed intracellular furin-like proteases in various chicken tissues [26]. In contrast, the F cleavage site of the avirulent strains is normally composed of monobasic amino acid residues at positions 112-116 and a leucine residue at position 117 [27]. Thus the chemistry of Fo cleavage site can be used as a good index for rapid pathotyping of NDV using molecular based assays.

In Nigeria, molecular characterization of ND outbreaks was until recently very scanty and largely focused on the partial F gene sequences for phylogenetic grouping of isolates [29, 30]. With the introduction of more objective criteria that utilizes the complete F gene coding sequences for assigning new genotypes [31], the genetic diversity of NDV in Nigeria has become more apparent [3234]. Unfortunately to date, the consequences of this genetic diversity on disease control using the available vaccines in the country remain poorly addressed. Therefore in this review, we analyze the current ecological distribution of NDV genotypes in various parts of Nigeria and discuss the implication of the genotype mismatch between the circulating field strains and the vaccine strains to ND control in the country.

2. Taxonomy and Global Distribution of Newcastle Disease Virus Isolates

Although all NDV strains are classified under one serotype [35], their genetic diversity is enormous [3639]. In the past, various schemes have been concurrently used to classify NDV based on their genetic information. The first classification system proposed by the Aldous group divides all the isolates into six lineages and 13 sublineages [40]. An additional lineage and seven more sublineages were later proposed [41, 42]. The other scheme of NDV taxonomy proposed by Ballagi-Pordány et al. [3] and later substantiated by Czeglédi et al. [43] groups the NDV isolates into various genotypes and subgenotypes. Conflicts and confusion generated by these schemes of classification necessitated the need to develop unified criteria for NDV taxonomy. After analyzing the two systems extensively, Diel et al. [31] proposed the adoption of the genotype based classification not only because it is the most widely used, but also because it gives a stronger correlation between the intergenetic groups evolutionary distances and their phylogenetic relationships. Therefore, a unified nomenclature system was proposed for the then existing isolates and more comprehensive criteria for the assignment of newly emerged genotypes were proposed [31]. According to the criteria, classification of a new genotype will be based on the phylogenetic topology using the complete, not partial F gene coding sequences. Furthermore, at least four isolates obtained from epidemiologically distinct events must form a phylogenetic cluster with a bootstrap value of nothing less than 60%. In addition, the isolates should have an average interpopulation evolutionary distance of ≥ 10. However, a mean evolutionary distance of 3-10% shall be used to designate a new subgenotype within a group [31].

Using these objective criteria, NDV isolates have been broadly classified into class I and class II [4446]. The class I isolates are all grouped into a single genotype and three subgenotypes because of their high genetic relatedness which is nearly 96% [47]. They are mostly isolated from wild and domesticated birds found in Africa, Asia, Europe, and America [36, 48, 49]. With the exception of one isolate that caused serious disease outbreak in the Northern Ireland around the early 1990s [50], all members of this class are considered of low virulence in chicken. On the contrary, the class II isolates are a mixture of viruses with diverse virulence potentials ranging from the most popular vaccine strains used for disease control to the highly virulent strains that cause outbreaks in different parts of the world (Table 1). According to the recent literatures, class II isolates are classified into genotypes I-XVIII, with majority of the genotypes being further subdivided into various subgenotypes [5153]. For instance, genotype I isolates which are globally distributed are composed of three subgenotypes: 1a, 1b, and 1c most of which are considered lentogenic. Indeed, the widely reported Queensland V4 and Ulster/chicken/Ireland/1967 vaccine strains are all grouped under this genotype [52, 53]. However, Gould et al. [54] reported the occurrence of virulent genotype I isolates in Australia. Similarly, the genotype II isolates are a mixture of velogenic [37, 38] and lentogenic viruses such as LaSota and B1 strains used globally for disease control [55]. Isolates in this genotype have been majorly recovered from domestic fowl, chicken, and wild birds found in North and South America, Africa, Asia, and Europe [44, 45].

GenotypesSubgenotypesGeographic distributionRemarks

IIa, Ib, IcAustralia, Africa, Europe, US, AsiaLow virulence, Ulster, V4
II-North and South America, Africa, Asia and EuropeAvirulent, lentogenic, Lasota, B1
III-Japan and Australia, Taiwan, ZimbabweAncient strains but still emerging, mesogenic Mukteshwar
IV-Europe, Africa, AsiaVirulent, Herts/33 (UK)
VVa, Vb, Vc, VdSouth America, Europe and AfricaVirulent, Anhinga (US)
VIVIa, VIb, VIc, VId, VIe, VIf, VIg, VIh, VIi, VIj, VIkEurope, Asia, Africa, South AmericaPigeon paramyxoviruses
VIIVIIa, VIIb, VIIc,, VIId, VIIe, VIIf, VIIg, VIIh, VIIiEmerged in Far East in 1990, spread to Europe and Asia, Africa.Virulent, 4th ND panzootic virus, 5th panzootic virus
VIII-South Africa, AsiaHighly virulent, AF22440
IX-First isolated in China in 1948Highly virulent
X-Taiwan, Argentina, USAVirulent
XI-MadagascarVirulent, restricted distribution
XII-South America and ChinaVirulent
XIIIXIIIa, XIIIb, XIIIcAsia, Europe and AfricaVirulent, continuously emerging
XIVXIVa, XIVbWest AfricaHighly virulent, recovered from domestic birds only
XV-ChinaOriginated from mixed virulent and vaccine viruses
XVI-Europe in 1940s, Africa and Asia in 1980sHighly related to genotype IV
XVIIXVIIa, XVIIbWest and Central AfricaHighly virulent, continuously emerging evolving
XVIIIXVIIIa, XVIIIbWest AfricaHighly virulent

Isolates belonging to genotypes III, IV, V, and VI are all predicted or pathotyped to be virulent in chicken. The genotype III isolates which include the popular mesogenic Mukteshwar strain used as a vaccine strain were recovered from birds in Japan as early as 1930s and also in Pakistan around the mid 1970s before they subsequently resurge in China less than two decades ago [56, 57]. Likewise, the genotype IV isolates occurred among the European poultry before the 1940s and include the extensively characterized Herts/33 strain [3, 58]. However, isolates in this genotype are currently thought to be extinct [44, 45] due to the absence of their recent genetic information in the GenBank database. As for the genotype V isolates that emerged for the first time around the 1970s in America and spread to the European continent in 1980s [43, 59], their recovery from poultry has recently been reported in East Africa, suggesting the expansion of their geographic distribution [60] and their continuous evolution. So far, isolates in this genotype are divided into four distinct subgenotypes (Va, Vb, Vc, and Vd) because of their within-the-group heterogeneity. However, the genotype VI isolates which are cosmopolitan in distribution are much more heterogeneous genetically. They are currently divided into subgenotypes VIa-k [37, 38, 51] because of their enormous genetic diversity. In addition, they are mainly found in wild birds, chicken, and more frequently in domestic pigeons, hence the name pigeon paramyxoviruses [6, 52, 61].

Genotype VII isolates are arguably the most important group of NDV reported in the 21st century. From the year 2000 to date, these viruses have been incriminated in several economically important disease outbreaks in Asia, the Middle East, and some parts of America and South Africa [6265]. Because of their extensive genetic diversity and continuous emergence, they are currently grouped into twelve subgenotypes (VIIa-l) [66] and are believed to be associated with the ongoing fourth pandemic of the disease. As a matter of fact, some of these subgenotypes are predicted to be the potential fifth ND pandemic viruses because of the recent expansion of their host range and geographic distribution as well as their increased virulence among the vaccinated birds [6770]. In particular, subgenotype VIIi isolates have recently replaced the predominant VIIa isolates in countries such as Pakistan since 2011 [71]. Similarly, subgenotype VIIj isolates believed to have emerged from viruses circulating in China and Ukraine are increasingly isolated in several countries including Iran [72]. This complex genetic diversity of genotype VII NDV highlights the need to monitor the epidemiological dynamics of the emerging viruses so that effective vaccination program can be designed. Unlike the genotype VII isolates, members of genotype VIII taxon are less diverse both genetically and in terms of spatial distribution. Apart from the report on their occurrence in Malaysia, Singapore, China, Turkey, Argentina, and South Africa between the 1960s and 1990s [8, 17], no report exists on their emergence in other parts of the world in the recent times. Hence they are thought to currently cease circulation in domestic birds. In contrast, the genotype IX isolates are still evolving in wild birds and domesticated poultry since survey of NDV between 2008 and 2011 revealed their presence in China [73, 74]. Nevertheless, they are still considered to be among the early genotypes, having been isolated as early as 1940s [3]. However, unlike members of this genotype (genotype IX) which are mostly virulent in chicken, genotype X isolates are all predicted to be in the lentogenic class. Despite their restricted geographic distribution, they are still maintained between the turkeys and wild birds in Argentina and the United States of America [75, 76]. They are however among the less genetically diverse groups of NDV.

Perhaps the most geographically restricted group of NDV are the genotype XI isolates. They have only been reported from Madagascar, where they are believed to circulate between the wild birds and domestic chicken [35, 58]. Although they are all predicted to be virulent based on the chemistry of their F cleavage site, there are reports of their isolation from apparently normal unvaccinated birds in Madagascar [35]. Meanwhile the genotype XII isolates, which are all predicted to be virulent, have been reported from both China and America in geese and chicken, respectively [44, 45, 77]. The epidemiological connection between the isolates in America and those in China is however still not clear, since migratory birds have not so far been incriminated in carrying these viruses [31, 44, 45]. Genotype XIII isolates which have been recovered from birds in Europe, Asia, and Africa are all predicted to be virulent based on the amino acid composition of their F cleavage site [78]. They are thought to be continuously evolving especially in Asia and the Middle East. Currently, they are divided into subgenotypes XIIIa, XIIIb, and XIIIc [79, 80].

The rest of the NDV genotypes are all predicted to be virulent in chicken. Isolates belonging to genotypes XIV, XVII, and XVIII have been recovered mainly from domesticated birds such as chicken, turkeys, and guinea fowls. Each of these genotypes is currently divided into two subgenotypes, a and b [53]. Because their geographic distribution is restricted to the west and central Africa, they are often referred to as regional NDV genotypes. On the other hand, members of the genotype XV group are considered to be recombinant isolates that might have emerged from the suboptimally vaccinated poultry in China some two decades ago [44, 45]. However, it is doubtful if they are still maintained in the poultry due to the absence of report on their occurrence in the last 15 years. Finally, genotype XVI isolates which were isolated from the Mexican chicken as early the 1940s [81] are believed to have been maintained in either the vaccinated or wild birds unnoticed for quite several years. They were also isolated in the Caribbean islands between 1986 and 2008 [43].

3. Ecology of NDV Genotypes in Nigeria

Analysis of the complete F gene coding sequences (1662bp) for Nigerian strains of NDV available in the NCBI database reveals the occurrence of genetically distinct strains in various species of birds across the lengths and breadths of Nigeria (Table 2). Based on phylogenetic relationships and evolutionary distances, those isolates were grouped into class II genotypes I, VI, XIV, XVII, and XVIII. Except the genotype I isolates with GRQGRL amino acid motifs at positions 112-117 of the F gene, all other isolates considered in this study are predicted to be virulent in chicken based on the presence of multiple basic amino acid residues in their F cleavage sites (Table 1). Notably, among those virulent cleavage sites, the “RRQKRF” is the most diverse, being possessed by all the analyzed sequences except those from genotypes I and VIh. Furthermore, some strains from subgenotypes XVIIa, XIVb, and VIh display “RRRKRF” at their cleavage sites whereas only one isolate from subgenotype VIg, another one from subgenotype XVIIb, and four isolates from subgenotype VIh possess “KRQKRF”, “RRQRRF”, and “RRKKRF” cleavage sites, respectively. Interestingly, recent studies on amino acid composition of NDV F cleavage site revealed that strains with Q at the third position in the cleavage site are predicted to have an enhanced cell-cell spreading ability [27]. Thus, in future development of vaccines based on indigenous NDV isolates in Nigeria, special consideration should be given to those isolates with Q at the third position of their F cleavage site.

SubgenotypeStrain IdentityYear of isolationCleavage siteLocation

VIgJQ039385.1 dove/Nigeria/VRD07-163/20072007RRQKRFKano
JQ039389.1 pigeon/Nigeria/VRD07-369/20072007KRQKRFJigawa

VIhHG326601.1 pigeon/Nigeria/NIE07-061/20072007RRKKRFOyo
HG326602.1 pigeon/Nigeria/NIE07-062/20072007RRKKRFOyo
HG326603.1 pigeon/Nigeria/NIE07-063/20072007RRKKRFOyo
HG326604.1 pigeon/Nigeria/NIE09-1898/20092009RRKKRFLagos
HG424627.1 pigeon/Nigeria/NIE13-092/20132013RRRKRFOyo
HG424628.1 pigeon/Nigeria/NIE13-093/20132013RRRKRFOyo
JQ039387.1 Nigeria/VRD08-37BRpe(7-9)/20082008RRRKRFJigawa
JQ039388.1 Nigeria/VRD08-37(10-11-13)/20082007RRRKRFJigawa
JQ039391.1 Nigeria/VRD07-231/20072007RRRKRFJigawa

VIiHG424625.1 pigeon/Nigeria/NIE13-005/20132013RRQKRFOyo
HG424626.1 pigeon/Nigeria/NIE13-008/20132013RRQKRFOyo

XIVaHF969131.1 chicken/Nigeria/NIE08-2117/20092009RRQKRFSokoto
HF969136.1 chicken/Nigeria/NIE08-2194/20092009RRQKRFSokoto
HF969139.1 chicken/Nigeria/NIE08-2280/20092009RRQKRFSokoto
HF969144.1 chicken/Nigeria/NIE09-2009/20092009RRQKRFYobe
HF969150.1 chicken/Nigeria/NIE09-2044/20092009RRQKRFYobe
HF969153.1 chicken/Nigeria/NIE09-2079/20092009RRQKRFYobe
HF969155.1 chicken/Nigeria/NIE09-2087/20092009RRQKRFYobe
HF969167.1 turkey/Nigeria/NIE10-082/20112011RRQKRFSokoto
HF969186.1 chicken/Nigeria/NIE07-125/20072007RRQKRFLagos
HF969193.1 chicken/Nigeria/NIE08-2150/20092009RRQKRFSokoto
HF969200.1 chicken/Nigeria/NIE08-2362/20092009RRQKRFSokoto
HF969205.1 turkey/Nigeria/NIE09-2071/20092009RRQKRFYobe
HF969206.1 chicken/Nigeria/NIE09-2101/20092009RRQKRFYobe
JQ039386.1 VRD08-36/20082008RRQKRFTaraba
HF969158.1 avian/Nigeria/NIE09-2168/20092009RRQKRFYobe

XIVbHF969133.1 chicken/Nigeria/NIE08-2159/20092009RRRKRFSokoto
HF969141.1 chicken/Nigeria/NIE08-2359/20092009RRRKRFSokoto
HF969142.1 chicken/Nigeria/NIE09-1596/20092009RRQKRFBenue
HF969143.1 chicken/Nigeria/NIE09-1597/20092009RRQKRFBenue
HF969145.1 chicken/Nigeria/NIE09-2014/20092009RRRKRFYobe
HF969146.1 chicken/Nigeria/NIE09-2017/20092009RRRKRFYobe
HF969149.1 chicken/Nigeria/NIE09-2041/20092009RRRKRFYobe
HF969151.1 chicken/Nigeria/NIE09-2053/20092009RRRKRFYobe
HF969157.1 chicken/Nigeria/NIE09-2166/20092009RRRKRFYobe
HF969161.1 chicken/Nigeria/NIE10-024/20112011RRRKRFSokoto
HF969162.1 chicken/Nigeria/NIE10-032/20112011RRRKRFSokoto
HF969163.1 chicken/Nigeria/NIE10-034/20112011RRQKRFSokoto
HF969164.1 chicken/Nigeria/NIE10-041/20112011RRRKRFSokoto
HF969165.1 chicken/Nigeria/NIE10-043/20112011RRRKRFSokoto
HF969166.1 chicken/Nigeria/NIE10-076/20112011RRRKRFSokoto
HF969169.1 chicken/Nigeria/NIE10-150/20112011RRRKRFSokoto
HF969170.1 chicken/Nigeria/NIE10-160/20112011RRRKRFSokoto
HF969172.1 chicken/Nigeria/NIE10-258/20112011RRQKRFSokoto
HF969173.1 chicken/Nigeria/NIE10-302/20112011RRRKRFSokoto
HF969177.1 chicken/Nigeria/NIE10-409/20112011RRRKRFSokoto
HF969178.1 chicken/Nigeria/NIE08-2270/20092009RRRKRFSokoto
HF969187.1 chicken/Nigeria/NIE08-0453/20082008RRRKRFYobe
HF969190.1 chicken/Nigeria/NIE08-2032/20092009RRRKRFSokoto
HF969198.1 chicken/Nigeria/NIE08-2279/20092009RRRKRFYobe
HF969201.1 chicken/Nigeria/NIE09-1599/20092009RRQKRFBenue
HF969202.1 chicken/Nigeria/NIE09-2013/20092009RRRKRFYobe
HF969203.1 turkey/Nigeria/NIE09-2021/20092009RRRKRFYobe
HF969208.1 chicken/Nigeria/NIE10-122/20112011RRRKRFSokoto
HF969210.1 chicken/Nigeria/NIE10-139/20112011RRQKRFSokoto
HF969211.1 chicken/Nigeria/NIE10-263/20112011RRRKRFSokoto
HF969212.1 chicken/Nigeria/NIE10-318/20112011RRRKRFSokoto
HF969213.1 chicken/Nigeria/NIE10-325/20112011RRQKRFSokoto
HF969214.1 chicken/Nigeria/NIE10-333/20112011RRRKRFSokoto
JQ039390.1 chicken/Nigeria/VRD07-233/20072007RRRKRF-
KC568205.1 NG-705/KD.TW.7C2009RRQKRFKaduna
KC568206.1 NG-706/JG.KZ.14T2009RRRKRFJigawa
KC568209.1 NG-720/KD.TW.03T2009RRQKRFKaduna
KT948996.1 duck/Nigeria/NG-695/KG.LOM.11-16/20092009RRRKRFKogi
KY171989.1 chicken/Nigeria/VRD10/143/N68/913/20102010RRRKRF-
KY171990.1 chicken/Nigeria/KD/TW/03T/N45/720/20092009RRQKRFKaduna
KY171993.1 chicken/Nigeria/VRD09/031/N23/715/20092009RRRKRF-
KY171994.1 chicken/Nigeria/VRD09/001/N19/714/20092009RRRKRF-

UnassignedKC568207.1 NG-707/GM.GMM.17-18T2009RRRKRFGombe
KU058680.1 duck/Nigeria/903/KUDU-113/19921992RRQKRF-

XVIIaFJ772449.1 avian-913-33-Nigeria-20062006RRQKRF-
FJ772486.1 avian-3724-6-Nigeria-20082008RRQKRF-
HF969129.1 chicken/Nigeria/NIE08-1363/20082008RRQKRFPlateau
HF969130.1 guinea fowl/Nigeria/NIE08-2004/20092009RRQKRFSokoto
HF969132.1 chicken/Nigeria/NIE08-2149/20092009RRQKRFSokoto
HF969134.1 chicken/Nigeria/NIE08-2168/20092009RRQKRFSokoto
HF969135.1 chicken/Nigeria/NIE08-2187/20092009RRQKRFSokoto
HF969137.1 chicken/Nigeria/NIE08-2208/20092009RRQKRFSokoto
HF969138.1 chicken/Nigeria/NIE08-2224/20092009RRQKRFSokoto
HF969140.1 chicken/Nigeria/NIE08-2340/20092009RRQKRFSokoto
HF969147.1 chicken/Nigeria/NIE09-2031/20092009RRQKRFYobe
HF969148.1 chicken/Nigeria/NIE09-2034/20092009RRQKRFYobe
HF969152.1 chicken/Nigeria/NIE09-2072/20092009RRQKRFYobe
HF969154.1 chicken/Nigeria/NIE09-2083/20092009RRQKRFYobe
HF969156.1 chicken/Nigeria/NIE09-2128/20092009RRQKRFYobe
HF969168.1 chicken/Nigeria/NIE10-124/20112011RRRKRFSokoto
HF969174.1 chicken/Nigeria/NIE10-304/20112011RRRKRFSokoto
HF969175.1 chicken/Nigeria/NIE10-306/20112011RRRKRFSokoto
HF969176.1 chicken/Nigeria/NIE10-310/20112011RRRKRFSokoto
HF969188.1 chicken/Nigeria/NIE08-1365/20082008RRQKRFPlateau
HF969189.1 chicken/Nigeria/NIE08-1366/20082008RRQKRFPlateau
HF969191.1 chicken/Nigeria/NIE08-2042/20092009RRQKRFSokoto
HF969192.1 chicken/Nigeria/NIE08-2119/20092009RRQKRFSokoto
HF969195.1 chicken/Nigeria/NIE08-2247/20092009RRQKRFSokoto
HF969197.1 chicken/Nigeria/NIE08-2267/20092009RRQKRFSokoto
HF969199.1 chicken/Nigeria/NIE08-2349/20092009RRQKRFSokoto
HF969204.1 chicken/Nigeria/NIE09-2028/20092009RRQKRFYobe
HF969207.1 avian/Nigeria/NIE09-2167/20092009RRQKRFYobe
HF969209.1 chicken/Nigeria/NIE10-123/20112011RRRKRFSokoto
HF969215.1 chicken/Nigeria/NIE10-335/20112011RRRKRFSokoto
JQ039392.1 avian/Nigeria/VRD07-733/20072007RRQKRF-
JQ039393.1 chicken/Nigeria/VRD07-141/20072007RRQKRFSokoto
JQ039394.1 chicken/Nigeria/VRD07-410/20072007RRQKRFJigawa
KC568204.1 pigeon/Nigeria/ZM/KN/PG01/N1/688/20092009RRQKRFZamfara
KC568208.1 NG-710/GM.PLBM.10-12T2009RRQKRFGombe
KY171991.1 Nigeria/VRD17/04/N2/861/20042004RRQKRF-
KY171992.1 chicken/Nigeria/JN/469/N44/892/20092009RRQKRFPlateau
KY171995.1 chicken/Nigeria/VRD124/06/N11/867/20062006RRQKRF-

XVIIbFJ772446.1 avian-913-1-Nigeria-20062006RRQKRF-
HF969128.1 avian/Nigeria/NIE07-216/20072007RRQKRF-
HF969171.1 chicken/Nigeria/NIE10-182/20112011RRQKRFSokoto
HF969194.1 chicken/Nigeria/NIE08-2199/20092009RRQKRFSokoto
HF969196.1 chicken/Nigeria/NIE08-2261/20092009RRQKRFSokoto
KF442614.1 Nigeria/228-7/20062006RRQRRF-

XVIIIbHF969216.1 chicken/Nigeria/NIE11-1286/20112011RRQKRFOyo
HF969217.1 chicken/Nigeria/NIE10-171/20112011RRQKRFSokoto

Class IHG326605.1 Spur-winged goose/Nigeria/ NIE-08-0121/20082008GKQGRLYobe
HG326606.1 Spur-winged goose/Nigeria/ NIE-08-0121/20082008GKQGRLYobe
HG326607.1 Spur-winged goose/Nigeria/ NIE-08-0121/20082008GKQGRLYobe
HG326608.1 Spur-winged goose/Nigeria/ NIE-08-0121/20082008GKQGRLYobe

Isolates of NDV belonging to the genotype VI group have been recovered from pigeons, doves, and chicken in the Northern (Kano and Jigawa) as well as the Southern (Oyo and Lagos) parts of Nigeria (Table 2). They are classified into subgenotypes VIg, VIh, and VIi with the overall average evolutionary divergence among the three subgenotypes being 7.3%. The highest genetic distance among these groups occurs between the subgenotypes VIh and VIi (Table 2). Surprisingly, the Nigerian genotype VIg isolates share a high degree of phylogenetic relationship with the Russian, Egyptian, and Ukrainian isolates whereas the genotype VIh isolates are more related to the pigeon paramyxovirus isolated from wild birds in Kenya (Figure 1(a)). On the other hand, the isolates grouped under subgenotypes VIi form the same phylogenetic cluster with the Italian strains. These close genetic relationships among the isolates could be of epidemiological significance and certainly suggest a recent common ancestry during their evolution [52, 53]. Given that these viruses can easily be transmitted from pigeons and doves to domesticated chicken especially at ecological contact surfaces [8284] and that some of them have been shown to dramatically gain virulence upon a few passages in chicken [85, 86], their occurrence in Nigerian pigeon population economically threatens the poultry subsector in the country. Thus, there is a need to intensify disease surveillance in live birds markets, households, and commercial poultry farms, so that disease epidemics due to these isolates can be quickly detected and contained.

Isolates belonging to genotype XIV are the most predominantly isolated strains of NDV in Nigeria. Both subgenotypes, XIVa and XIVb, have been recovered from domestic birds found in the North-West (Sokoto, Kaduna, Jigawa), North-Central (Benue, Kogi), North-East (Taraba and Yobe), and South-Western parts of the country (Lagos) (Table 1). The intergroup genetic distance between the two subgenotypes averages at 6.7% (Table 3). Meanwhile, subgenotype XIVa isolates appear to be more genetically diverse, having an average intragenotype evolutionary divergence of 2.6%. On the other hand, isolates in the subgenotype XIVb are less divergent with about 98.6% overall mean similarity among themselves (data not shown). Phylogenetically, the genotype XIVa isolates form a cluster with some strains in Niger Republic while the Nigerian genotype XIVb isolates tend to be more closely related to the 2009 isolates from Benin Republic (Figure 1(b)). Interestingly, the isolates in genotype XIVa that share the highest nucleotide similarity with those from Niger Republic were all obtained from Sokoto State which shares a direct international border with Niger Republic. Their intimate phylogenetic relationship could therefore be partially explained by the cross border movements between the two countries which may facilitate the spread of the virus from one place to another. Notably, all genotype XIV isolates are so far restricted in distribution to only the West African subregion where they cause havoc in the regional poultry industry [11]. However, their emergence in other parts of the continent within the next few years would not be unexpected given the poor transboundary biosecurity measures in most of the African countries.


VIg (0.005)(0.006)(0.007)(0.008)(0.007)(0.007)(0.008)

The table shows number of base differences per site from averaging over all sequence pairs between groups. Standard error estimate(s) are shown above the diagonal and were obtained by a bootstrap procedure (500 replicates). The analysis involved 120 nucleotide sequences. Codon positions included were 1st+2nd+3rd+Noncoding. All positions containing gaps and missing data were eliminated. Evolutionary analyses were conducted in MEGA6 [28].

Several strains of NDV isolated in Nigeria from 2006-2011 belong to either subgenotype XVIIa or XVIIb, with the mean evolutionary divergence between the two subgenotypes being 4.1% (Table 3). Members of the subgenotypes XVIIa are highly similar, with an average nucleotide sequence similarity of 98.1% at the level of F protein gene. Surprisingly, despite their extensive spatial distribution in the northern states (Sokoto, Zamfara, Plateau, Gombe, and Yobe states), none of these isolates was recovered from the southern parts of the country. It is however not clear whether this is due to sampling bias or they truly do not exist in those areas. On the basis of phylogenetic analysis, genotype XVIIa isolates from Nigeria are closely related to those from Niger Republic, Cameroun, Burkina Faso, and Mali whereas the genotype XVIIb isolates, whose mean intrasubgenotype distance was estimated to be 1.5%, are so far exclusively composed of Nigerian strains (Figure 1(c)). Importantly, the ecological distribution of genotype XVII isolates is to date restricted to the West and Central Africa [32, 53] where they are believed to considerably militate against poultry production. Indeed, representatives of these isolates have recently been shown to cause a typical velogenic viscerotropic ND [87] characterized by end stage morbidity and high mortality in chicken. There is therefore need to intensify the ongoing passive and active surveillance for ND in various parts of the country in order to avert the potential economic losses due to outbreaks with these strains.

Two highly similar sequences (99%) obtained from Nigerian NDV strains in the NCBI database were categorised under the subgenotype XVIIIb. They were obtained from Sokoto State in the North and Oyo State from the South. Based on the phylogenetic tree analysis, the two strains are quite related to the isolates from Togo and Ivory-Coast (Figure 1(c)) as earlier reported by Shittu et al. [32]. On the contrary, subgenotype XVIIIa isolates are yet to be encountered in Nigeria. Surprisingly, the interpopulation evolutionary distance between the two isolates in the subgenotype XVIIIb and those in either subgenotype XVIIa or XVIIb is slightly lower than the 10% cut-off for differentiating new genotypes (Table 2). This discrepancy was earlier observed by [88] who wondered if genotype XVIII isolates could be another subgroup of genotype XVII. However, Snoeck and Muller (2016) maintained that the two genotypes (XVII and XVIII) still stand and that the parameter used by Desingu et al. to challenge the existence of genotype XVIII was incorrect. Therefore, it is possible that the slightly lower than the threshold interpopulation distance observed in this study was due to the small number of genotype XVIII sequences from Nigeria (n=2) used in the analysis. As all the known genotype XVIII isolates are predicted to be virulent in chicken, their emergence in other parts of the country should be carefully monitored as part of the usual disease surveillance programme in the country.

4. Challenges for Newcastle Disease Control in Nigeria

Vaccination remains the most practical method of disease control in poultry and therefore plays a major role in strengthening the modern poultry industry [89, 90]. The ultimate goal of any vaccination program is the induction of sterilising immunity in the vaccinated host [91]. However, this is hardly achievable in poultry [89], owing to numerous factors that may adversely affect the efficacy of vaccination. The fact that all NDV strains are grouped into one serotype [92] suggests that immunity developed against one strain should offer cross protection against challenge with any other strains. Unfortunately to date, outbreaks of ND are frequently reported among farms that have vaccinated using the available vaccines [32, 52, 53]. The cause of these disease outbreaks among the vaccinated birds is still controversial in the literature. While some researchers hold the view that the poor vaccine induced immunity is due to the suboptimal vaccine intake following its mass administration in poultry [93], others believe that the genetic variation between the vaccine and the circulating field strains might be the major factor responsible for the incomplete protective efficacy of the current vaccines [94, 95]. Although the currently used vaccines, when correctly administered, are known to fully protect birds against clinical disease and mortality [95, 96], they cannot block the replication of the virulent virus post challenge [44, 45]. Thus, the vaccinated birds may look apparently healthy but still excrete a large amount of the virulent virus, which can in turn cause disease among unprotected birds. Since it is an established fact that ND vaccines are more effective in reducing virus shedding when the vaccine strains are genetically closer to the challenge strain [57, 97], the evolutionary distance between the vaccine strains and the circulating field strain represents an important factor in effective disease control, since it explains the continuous occurrence of ND outbreaks despite the extensive poultry vaccination programs in the country.

Based on the evolutionary analysis of the complete F coding sequences performed in this study, all the virulent NDV genotypes circulating in Nigeria are shown to be distantly related to the currently available vaccine strains in the country (Table 4). LaSota which is the most widely used live attenuated ND vaccine in Nigeria and indeed many parts of the world has an average nucleotide sequence divergence of 15.7-18.6% when compared with all the existing virulent class II subgenotypes in Nigeria (Table 4). Similarly, the very popular Komarov inactivated NDV vaccine differs from the circulating NDV subgenotypes in the country with an average evolutionary distance of 15.5-18% (Table 4). Recently in Indonesia, sequence divergence between the field and the vaccine strains has been implicated in a severe disease outbreak that led to 70% mortality among the vaccinated birds [95]. Furthermore, in Malaysia where the prevalent isolates are genotype VII strains that considerably diverge from the LaSota strain, the frequency of ND outbreaks among the vaccinated farms has steadily increased from 2009 to date [62, 98]. Therefore, the wide genetic divergence between the Nigerian NDV strains and vaccine strains used in the country should be a source of a serious concern to the national poultry industry and requires urgent attention. These problems collectively highlight the possible limitations of the current vaccines in offering a complete protection against the circulating strains of NDV in Nigeria. The need to improve the current disease control strategies is therefore imperative.

VaccinePrevalent subgenotype


The table shows number of base substitutions per site of the complete F gene sequence pairs between vaccine strains and NDV subgenotypes in Nigeria. The analysis involved 126 nucleotide sequences. Codon positions included were 1st+2nd+3rd+Noncoding. All positions containing gaps and missing data were eliminated. Evolutionary analyses were conducted in MEGA6 [28].

5. Way Forward

The panacea for all these ND control challenges in Nigeria is the maintenance of strict biosecurity and the development of rationally designed vaccines based on the currently circulating isolates in the country. With the advent of reverse genetics technology that allows the recovery of recombinant NDV from their cloned cDNA [99], genotype-matched live attenuated vaccines can be easily generated. Since the complete genome sequence of some biologically well-characterized viruses in the country has already been obtained [33, 34], efforts should be intensified towards rescuing their attenuated counterparts by simply engineering their F cleavage site to encode monobasic amino acid residues instead of the poly basic motifs [100]. By developing a reverse genetics system for one prevalent strain in the country, vaccine candidates against all the circulating strains can easily be obtained by F gene swapping in the full length infectious clone followed by the recovery of the chimeric viruses by reverse genetics techniques. Alternatively, recombinant viral vectors such as herpesvirus of turkey [101] (HVT) expressing surface glycoproteins (F and/or HN) of the circulating NDV can be developed as an effective genotype-matched vaccine against the prevailing genotypes in the country.

6. Conclusion

In summary, a comprehensive distribution of NDV genotypes in various regions of Nigeria has been provided. Apparently, multiple genetically distinct strains of NDV are cocirculating in some states of the federation, an important factor that may favour the emergence of novel virulent isolates in the country. In particular, apart from genotype VI isolates, all the virulent NDV genotypes prevalent in Nigeria have been isolated in Sokoto State between 2007 and 2011, making the State a potential hotspot of different NDV genotypes in Nigeria. It is interesting to know that genotype VII isolates responsible for the on-going fourth and the imminent fifth ND panzootic [102, 103] have not been reported in Nigeria despite their recent emergence in some African countries [104, 105]. Since these panzootic viruses have a high potential for international spread, there is a need to intensify disease surveillance activities and strengthen biosecurity barriers so as to avoid their introduction into the country. Finally, given the wide evolutionary divergence between the commonly used vaccines and the circulating NDV strains in the country, there is a need to revise the current ND control strategies in Nigeria. Genotype-matched vaccines with improved protective efficacy and virus shedding blocking ability should be designed to specifically target the currently circulating NDV genotypes in the country.

Conflicts of Interest

The authors declare that they have no conflicts of interest.


This is a review article and does not require any substantial funding. However, the cost of open access publication will be covered by the Transdisciplinary Research Grant Scheme (TRGS) of the Ministry of Higher Education Malaysia with the grant number 5535402.


  1. D. J. Alexander, “Newcastle disease,” British Poultry Science, vol. 42, no. 1, pp. 5–22, 2001. View at: Publisher Site | Google Scholar
  2. D. J. Alexander, “Ecology and Epidemiology of Newcastle Disease,” Avian Influenza and Newcastle Disease: A Field and Laboratory Manual, pp. 19–26, 2009. View at: Google Scholar
  3. A. Ballagi-Pordány, E. Wehmann, J. Herczeg, S. Belák, and B. Lomniczi, “Identification and grouping of Newcastle disease virus strains by restriction site analysis of a region from the F gene,” Archives of Virology, vol. 141, pp. 243–261, 1996. View at: Google Scholar
  4. D. J. Alexander, E. W. Aldous, and C. M. Fuller, “The long view: a selective review of 40 years of Newcastle disease research,” Avian Pathology, vol. 41, no. 4, pp. 329–335, 2012. View at: Google Scholar
  5. D. J. Alexander, G. Parsons, and R. Marshall, “Avian paramyxovirus type 1 infections of racing pigeons: 4 laboratory assessment of vaccination.,” Veterinary Record, vol. 118, no. 10, pp. 262–266, 1986. View at: Publisher Site | Google Scholar
  6. J. T. Lumeij and J. W. E. Stam, “Paramyxovirus disease in racing pigeons,” Veterinary Quarterly, vol. 7, no. 1, Article ID 9693954, pp. 60–65, 1985. View at: Publisher Site | Google Scholar
  7. G. Cross, “Paramyxovirus-1 infection (Newcastle disease) of pigeons,” Seminars in Avian and Exotic Pet Medicine, vol. 4, no. 2, pp. 92–95, 1995. View at: Publisher Site | Google Scholar
  8. J. Herczeg, E. Wehmann, R. R. Bragg et al., “Two novel genetic groups (VIIb and VIII) responsible for recent Newcastle disease outbreaks in Southern Africa, one (VIIb) of which reached Southern Europe,” Archives of Virology, vol. 144, no. 11, pp. 2087–2099, 1999. View at: Publisher Site | Google Scholar
  9. E. K. Lee, W. J. Jeon, J. H. Kwon, C. B. Yang, and K. S. Choi, “Molecular epidemiological investigation of Newcastle disease virus from domestic ducks in Korea,” Veterinary Microbiology, vol. 134, no. 3, pp. 241–248, 2009. View at: Google Scholar
  10. H. Liu, Z. Wang, Y. Wang, C. Sun, D. Zheng, and Y. Wu, “Characterization of Newcastle disease virus isolated from waterfowl in China,” Avian Diseases, vol. 52, no. 1, pp. 150–155, 2008. View at: Google Scholar
  11. A. Samuel, B. Nayak, A. Paldurai et al., “Phylogenetic and pathotypic characterization of newcastle disease viruses circulating in west africa and efficacy of a current vaccine,” Journal of Clinical Microbiology, vol. 51, no. 3, pp. 771–781, 2013. View at: Publisher Site | Google Scholar
  12. O. J. Ibu, J. O. A. Okoye, E. P. Adulugba et al., “Prevalence of newcastle disease viruses in wild and captive birds in central Nigeria,” International Journal of Poultry Science, vol. 8, no. 6, pp. 574–578, 2009. View at: Publisher Site | Google Scholar
  13. A. H. Jibril, J. U. Umoh, J. Kabir et al., “Newcastle Disease in Local Chickens of Live Bird Markets and Households in Zamfara State, Nigeria,” ISRN Epidemiology, vol. 2014, Article ID 513961, 4 pages, 2014. View at: Google Scholar
  14. A. H. Jibril, J. U. Umoh, J. Kabir, M. M. Gashua, and M. B. Bello, “Application of participatory epidemiology techniques to investigate Newcastle disease among rural farmers in Zamfara state, Nigeria,” Journal of Applied Poultry Research, vol. 24, no. 2, pp. 233–239, 2015. View at: Publisher Site | Google Scholar
  15. L. Sa’idu, L. B. Tekdek, and P. A. Abdu, “Prevalence of Newcastle disease antibodies in domestic and semi-domestic birds in Zaria, Nigeria,” Veterinarski Arhiv, vol. 74, no. 4, pp. 309–317, 2004. View at: Google Scholar
  16. P. Gogoi, K. Ganar, and S. Kumar, “Avian paramyxovirus: a brief review,” Transboundary and Emerging Diseases, vol. 64, no. 1, pp. 53–67, 2017. View at: Google Scholar
  17. K. Murulitharan, K. Yusoff, A. R. Omar, and A. Molouki, “Characterization of Malaysian velogenic NDV strain AF2240-I genomic sequence: A comparative study,” Virus Genes, vol. 46, no. 3, pp. 431–440, 2013. View at: Publisher Site | Google Scholar
  18. D. A. Satharasinghe, K. Murulitharan, S. W. Tan et al., “Detection of inter-lineage natural recombination in avian paramyxovirus serotype 1 using simplified deep sequencing platform,” Frontiers in Microbiology, vol. 7, pp. 1–14, 2016. View at: Google Scholar
  19. OIE, “Newcastle Disease (Infection with Newcastle Disease Virus),” in Manual of Diagnostic Tests and Vaccines for Terrestrial Animals: (Mammals, Birds and Bees), vol. 1, pp. 555–574, 2012. View at: Google Scholar
  20. M. Banerjee, W. M. Reed, S. D. Fitzgerald, and B. Panigraphy, “Neurotropic velogenic Newcastle disease in cormorants in Michigan: pathology and virus characterization,” Avian Diseases, vol. 38, no. 4, pp. 873–878, 1994. View at: Google Scholar
  21. A. M. Piacenti, D. J. King, B. S. Seal, J. Zhang, and C. C. Brown, “Pathogenesis of Newcastle disease in commercial and specific pathogen-free turkeys experimentally infected with isolates of different virulence,” Veterinary Pathology, vol. 43, no. 2, pp. 168–178, 2006. View at: Google Scholar
  22. W. Fan, Y. Wang, S. Wang et al., “Virulence in Newcastle disease virus: A genotyping and molecular evolution spectrum perspective,” Research in Veterinary Science, vol. 111, pp. 49–54, 2017. View at: Publisher Site | Google Scholar
  23. V. M. B. D. Moura, L. Susta, S. Cardenas-Garcia et al., “Neuropathogenic capacity of lentogenic, mesogenic, and velogenic newcastle disease virus strains in day-old chickens,” Veterinary Pathology, vol. 53, no. 1, pp. 53–64, 2016. View at: Google Scholar
  24. H. Hamid, R. S. F. Campbell, and C. Lamichhane, “The Pathology of infection of chickens with the lentogenic V4 strain of newcastle disease virus,” Avian Pathology, vol. 19, no. 4, pp. 687–696, 1990. View at: Google Scholar
  25. O. S. de Leeuw, L. Hartog, G. Koch, and B. P. H. Peeters, “Effect of fusion protein cleavage site mutations on virulence of Newcastle disease virus: Non-virulent cleavage site mutants revert to virulence after one passage in chicken brain,” Journal of General Virology, vol. 84, pp. 475–484, 2003. View at: Google Scholar
  26. A. Panda, Z. Huang, S. Elankumaran, D. D. Rockemann, and S. K. Samal, “Role of fusion protein cleavage site in the virulence of Newcastle disease virus,” Microbial Pathogenesis, vol. 36, no. 1, pp. 1–10, 2004. View at: Google Scholar
  27. Y. Wang, W. Yu, N. Huo et al., “Comprehensive analysis of amino acid sequence diversity at the F protein cleavage site of Newcastle disease virus in fusogenic activity,” PLoS ONE, vol. 12, no. 9, Article ID e0183923, 2017. View at: Publisher Site | Google Scholar
  28. K. Tamura, G. Stecher, D. Peterson, A. Filipski, and S. Kumar, “MEGA6: molecular evolutionary genetics analysis version 6.0,” Molecular Biology and Evolution, vol. 30, no. 12, pp. 2725–2729, 2013. View at: Publisher Site | Google Scholar
  29. T. Hamisu, H. Kazeem, K. Majiyagbe et al., “Molecular screening and isolation of Newcastle disease virus from live poultry markets and chickens from commercial poultry farms in Zaria, Kaduna state, Nigeria,” Sokoto Journal of Veterinary Sciences, vol. 14, no. 3, pp. 18–25, 2017. View at: Publisher Site | Google Scholar
  30. P. Solomon, C. Abolnik, T. M. Joannis, and S. Bisschop, “Virulent Newcastle disease virus in Nigeria: Identification of a new clade of sub-lineage 5f from livebird markets,” Virus Genes, vol. 44, no. 1, pp. 98–103, 2012. View at: Google Scholar
  31. D. G. Diel, L. H. A. da Silva, H. Liu, Z. Wang, P. J. Miller, and C. L. Afonso, “Genetic diversity of avian paramyxovirus type 1: Proposal for a unified nomenclature and classification system of Newcastle disease virus genotypes,” Infection, Genetics and Evolution, vol. 12, no. 8, pp. 1770–1779, 2012. View at: Google Scholar
  32. I. Shittu, T. M. Joannis, G. N. Odaibo, and O. D. Olaleye, “Newcastle disease in Nigeria: epizootiology and current knowledge of circulating genotypes,” VirusDisease, vol. 27, no. 4, pp. 329–339, 2016. View at: Google Scholar
  33. I. Shittu, P. Sharma, T. M. Joannis et al., “Complete genome sequence of a genotype XVII newcastle disease virus, isolated from an apparently healthy domestic duck in nigeria,” Genome Announcements, vol. 4, no. 1, Article ID e01716-15, 2016. View at: Publisher Site | Google Scholar
  34. I. Shittu, P. Sharma, J. D. Volkening et al., “Identification and complete genome sequence analysis of a genotype XIV newcastle disease virus from Nigeria,” Genome Announcements, vol. 4, no. 1, Article ID e01581-15, 2016. View at: Publisher Site | Google Scholar
  35. R. S. de Almeida, S. Hammoumi, P. Gil et al., “New avian paramyxoviruses type I strains identified in Africa provide new outcomes for phylogeny reconstruction and genotype classification,” PLoS ONE, vol. 8, no. 10, Article ID e76413, 2013. View at: Publisher Site | Google Scholar
  36. L. M. Kim, D. J. King, P. E. Curry et al., “Phylogenetic diversity among low-virulence newcastle disease viruses from waterfowl and shorebirds and comparison of genotype distributions to those of poultry-origin isolates,” Journal of Virology, vol. 81, no. 22, pp. 12641–12653, 2007. View at: Publisher Site | Google Scholar
  37. L. M. Kim, D. J. King, H. Guzman et al., “Biological and phylogenetic characterization of pigeon paramyxovirus serotype 1 circulating in wild North American pigeons and doves,” Journal of Clinical Microbiology, vol. 46, no. 10, pp. 3303–3310, 2008. View at: Publisher Site | Google Scholar
  38. L. M. Kim, D. L. Suarez, and C. L. Afonso, “Detection of a broad range of class I and II Newcastle disease viruses using multiplex real-time reverse transcription polymerase chain reaction assay,” Journal of Veterinary Diagnostic Investigation, vol. 20, no. 4, pp. 414–425, 2008. View at: Google Scholar
  39. H. Liu, P. Zhang, P. Wu et al., “Phylogenetic characterization and virulence of two Newcastle disease viruses isolated from wild birds in China,” Infection, Genetics and Evolution, vol. 20, pp. 215–224, 2013. View at: Publisher Site | Google Scholar
  40. E. W. Aldous, J. K. Mynn, J. Banks, and D. J. Alexander, “A molecular epidemiological study of avian paramyxovirus type 1 (Newcastle disease virus) isolates by phylogenetic analysis of a partial nucleotide sequence of the fusion protein gene,” Avian Pathology, vol. 32, pp. 237–255, 2003. View at: Google Scholar
  41. G. Cattoli, A. Fusaro, I. Monne et al., “Emergence of a new genetic lineage of Newcastle disease virus in West and Central Africa-Implications for diagnosis and control,” Veterinary Microbiology, vol. 142, no. 3-4, pp. 168–176, 2010. View at: Publisher Site | Google Scholar
  42. C. J. Snoeck, M. F. Ducatez, A. A. Owoade et al., “Newcastle disease virus in West Africa: New virulent strains identified in non-commercial farms,” Archives of Virology, vol. 154, no. 1, pp. 47–54, 2009. View at: Publisher Site | Google Scholar
  43. A. Czeglédi, D. Ujvári, E. Somogyi, E. Wehmann, O. Werner, and B. Lomniczi, “Third genome size category of avian paramyxovirus serotype 1 (Newcastle disease virus) and evolutionary implications,” Virus Research, vol. 120, no. 1-2, pp. 36–48, 2006. View at: Publisher Site | Google Scholar
  44. K. M. Dimitrov, C. L. Afonso, Q. Yu, and P. J. Miller, “Newcastle disease vaccines—A solved problem or a continuous challenge?” Veterinary Microbiology, vol. 206, pp. 126–136, 2016. View at: Google Scholar
  45. K. M. Dimitrov, A. M. Ramey, X. Qiu, J. Bahl, and C. L. Afonso, “Infection, Genetics and Evolution Temporal, geographic, and host distribution of avian paramyxovirus 1 (Newcastle disease virus),” Infection, Genetics and Evolution, vol. 39, pp. 22–34, 2016. View at: Google Scholar
  46. Y. Kang, Y. Li, R. Yuan et al., “Phylogenetic relationships and pathogenicity variation of two Newcastle disease viruses isolated from domestic ducks in Southern China,” Virology Journal, vol. 11, no. 1, article 147, 2014. View at: Publisher Site | Google Scholar
  47. S. Ren, X. Xie, Y. Wang et al., “Molecular characterization of a Class I Newcastle disease virus strain isolated from a pigeon in China,” Avian Pathology, vol. 45, no. 4, pp. 408–417, 2016. View at: Publisher Site | Google Scholar
  48. M. A. Hoque, G. W. Burgess, D. Karo-Karo, A. L. Cheam, and L. F. Skerratt, “Monitoring of wild birds for Newcastle disease virus in north Queensland, Australia,” Preventive Veterinary Medicine, vol. 103, no. 1, pp. 49–62, 2012. View at: Publisher Site | Google Scholar
  49. H. Liu, F. Chen, Y. Zhao et al., “Genomic characterization of the first class I Newcastle disease virus isolated from the mainland of China,” Virus Genes, vol. 40, no. 3, pp. 365–371, 2010. View at: Google Scholar
  50. D. J. Alexander, G. Campbell, R. J. Manvell, M. S. Collins, G. Parsons, and M. S. McNulty, “Characterisation of an antigenically unusual virus responsible for two outbreaks of Newcastle disease in the Republic of Ireland in 1990,” Veterinary Record, vol. 130, no. 4, pp. 65–68, 1992. View at: Google Scholar
  51. Y. He, T. L. Taylor, K. M. Dimitrov et al., “Whole-genome sequencing of genotype VI Newcastle disease viruses from formalin-fixed paraffin-embedded tissues from wild pigeons reveals continuous evolution and previously unrecognized genetic diversity in the U.S.,” Virology Journal, vol. 15, no. 1, 2018. View at: Publisher Site | Google Scholar
  52. C. J. Snoeck, A. T. Adeyanju, A. a. Owoade et al., “Genetic diversity of newcastle disease virus in wild birds and pigeons in West Africa,” Applied and Environmental Microbiology, vol. 79, no. 24, pp. 7867–7874, 2013. View at: Google Scholar
  53. C. J. Snoeck, A. A. Owoade, E. Couacy-Hymann et al., “High genetic diversity of newcastle disease virus in poultry in west and central Africa: Cocirculation of genotype XIV and newly defined genotypes XVII and XVIII,” Journal of Clinical Microbiology, vol. 51, no. 7, pp. 2250–2260, 2013. View at: Publisher Site | Google Scholar
  54. A. R. Gould, J. A. Kattenbelt, P. Selleck, E. Hansson, A. Della-Porta, and H. A. Westbury, “Virulent Newcastle disease in Australia: Molecular epidemiological analysis of viruses isolated prior to and during the outbreaks of 1998-2000,” Virus Research, vol. 77, no. 1, pp. 51–60, 2001. View at: Publisher Site | Google Scholar
  55. B. S. Seal, M. G. Wise, J. C. Pedersen et al., “Genomic sequences of low-virulence avian paramyxovirus-1 (Newcastle disease virus) isolates obtained from live-bird markets in North America not related to commonly utilized commercial vaccine strains,” Veterinary Microbiology, vol. 106, no. 1-2, pp. 7–16, 2005. View at: Publisher Site | Google Scholar
  56. A. Czeglédi, E. Wehmann, and B. Lomniczi, “On the origins and relationships of Newcastle disease virus vaccine strains Hertfordshire and Mukteswar, and virulent strain Herts'33,” Avian Pathology, vol. 32, no. 3, pp. 271–276, 2003. View at: Publisher Site | Google Scholar
  57. P. J. Miller, E. L. Decanini, and C. L. Afonso, “Newcastle disease: evolution of genotypes and the related diagnostic challenges,” Infection, Genetics and Evolution: Journal of Molecular Epidemiology and Evolutionary Genetics in Infectious Diseases, vol. 10, no. 1, pp. 26–35, 2010. View at: Google Scholar
  58. O. F. Maminiaina, P. Gil, F. Briand et al., “Newcastle Disease Virus in Madagascar: Identification of an Original Genotype Possibly Deriving from a Died Out Ancestor of Genotype IV,” PLoS ONE, vol. 5, no. 11, Article ID e13987, 2010. View at: Publisher Site | Google Scholar
  59. L. Susta, K. R. Hamal, P. J. Miller et al., “Separate evolution of virulent Newcastle disease viruses from Mexico and Central America,” Journal of Clinical Microbiology, vol. 52, no. 5, pp. 1382–1390, 2014. View at: Publisher Site | Google Scholar
  60. M. Sabra, K. M. Dimitrov, I. V. Goraichuk et al., “Phylogenetic assessment reveals continuous evolution and circulation of pigeon-derived virulent avian avulaviruses 1 in Eastern Europe, Asia, and Africa,” BMC Veterinary Research, vol. 13, no. 1, 2017. View at: Publisher Site | Google Scholar
  61. C. Terregino, G. Cattoli, B. Grossele, E. Bertoli, E. Tisato, and I. Capua, “Characterization of Newcastle disease virus isolates obtained from Eurasian collared doves (Streptopelia decaocto) in Italy,” Avian Pathology, vol. 32, no. 1, pp. 63–68, 2003. View at: Publisher Site | Google Scholar
  62. O. A. Aljumaili, S. K. Yeap, A. R. Omar, and I. Aini, “Isolation and characterization of genotype VII newcastle disease virus from NDV vaccinated farms in Malaysia,” Pertanika Journal of Tropical Agricultural Science, vol. 40, no. 4, pp. 677–690, 2017. View at: Google Scholar
  63. S. A. Shohaimi, R. A. Raus, O. G. Huai, B. M. Asmayatim, N. Nayan, and A. M. Yusuf, “Sequence and phylogenetic analysis of newcastle disease virus genotype VII isolated in Malaysia during 1999-2012,” Jurnal Teknologi, vol. 77, no. 25, pp. 159–164, 2015. View at: Google Scholar
  64. J. Wang, Y. Cong, R. Yin et al., “Generation and evaluation of a recombinant genotype VII Newcastle disease virus expressing VP3 protein of Goose parvovirus as a bivalent vaccine in goslings,” Virus Research, vol. 203, pp. 77–83, 2015. View at: Publisher Site | Google Scholar
  65. Y. Zhang, yuan. Shao, M. yu, X. Yu, J. Zhao, and G. Zhang, “Molecular characterization of chicken-derived genotype VIId Newcastle disease virus isolates in China during 2005-2012 reveals a new length in hemagglutinin-neuraminidase,” Infection, Genetics and Evolution, vol. 21, pp. 359–366, 2014. View at: Google Scholar
  66. F. Sabouri, M. Vasfi Marandi, and M. Bashashati, “Characterization of a novel VIIl sub-genotype of Newcastle disease virus circulating in Iran,” Avian Pathology, vol. 47, no. 1, 2017. View at: Google Scholar
  67. M. M. Ebrahimi, S. Shahsavandi, G. Moazenijula, and M. Shamsara, “Phylogeny and evolution of Newcastle disease virus genotypes isolated in Asia during 2008-2011,” Virus Genes, vol. 45, no. 1, pp. 63–68, 2012. View at: Google Scholar
  68. M. Esmaelizad, V. Mayahi, M. Pashaei, and H. Goudarzi, “Identification of novel Newcastle disease virus sub-genotype VII-(j) based on the fusion protein,” Archives of Virology, vol. 162, no. 4, pp. 971–978, 2017. View at: Google Scholar
  69. N. Siddique, K. Naeem, M. A. Abbas et al., “Sequence and phylogenetic analysis of virulent Newcastle disease virus isolates from Pakistan during 2009-2013 reveals circulation of new sub genotype,” Virology, vol. 444, no. 1-2, pp. 37–40, 2013. View at: Publisher Site | Google Scholar
  70. S. W. Tan, A. Ideris, A. R. Omar, K. Yusoff, and M. Hair-Bejo, “Sequence and phylogenetic analysis of Newcastle disease virus genotypes isolated in Malaysia between,” Archives of Virology, vol. 155, no. 1, pp. 63–70, 2010. View at: Google Scholar
  71. S. Umar, “Emergence of new sub-genotypes of Newcastle disease virus in Pakistan,” World's Poultry Science Journal, vol. 73, no. 3, pp. 567–580, 2017. View at: Publisher Site | Google Scholar
  72. C. Xue, Y. Cong, R. Yin et al., “Genetic diversity of the genotype VII Newcastle disease virus: identification of a novel VIIj sub-genotype,” Virus Genes, vol. 53, no. 1, pp. 63–70, 2017. View at: Publisher Site | Google Scholar
  73. X. Duan, P. Zhang, M. Jing et al., “Characterization of genotype IX Newcastle disease virus strains isolated from wild birds in the northern Qinling Mountains, China,” Virus Genes, vol. 48, no. 1, pp. 48–55, 2014. View at: Publisher Site | Google Scholar
  74. X. Qiu, Q. Sun, S. Wu et al., “Entire genome sequence analysis of genotype IX Newcastle disease viruses reveals their early-genotype phylogenetic position and recent-genotype genome size,” Virology Journal, vol. 8, article no. 117, 2011. View at: Publisher Site | Google Scholar
  75. N. L. Hines, M. L. Killian, J. C. Pedersen et al., “An rRT-PCR Assay to Detect the Matrix Gene of a Broad Range of Avian Paramyxovirus Serotype-1 Strains,” Avian Diseases, vol. 56, no. 2, pp. 387–395, 2012. View at: Google Scholar
  76. R. Maqbool, S. A. Wani, A. Wali et al., “Avian paramyxovirus serotype-1 detection from chicken reared in Kashmir valley,” Journal of Pure and Applied Microbiology, vol. 11, no. 1, pp. 355–357, 2017. View at: Publisher Site | Google Scholar
  77. A. Chumbe, R. Izquierdo-Lara, L. Tataje-Lavanda et al., “Characterization and sequencing of a genotype XII Newcastle disease virus isolated from a peacock (Pavo cristatus) in Peru,” Genome Announcements, vol. 3, no. 4, pp. 3-4, 2015. View at: Google Scholar
  78. V. Gowthaman, S. D. Singh, K. Dhama et al., “Isolation and characterization of genotype XIII Newcastle disease virus from Emu in India,” VirusDisease, vol. 27, no. 3, pp. 315–318, 2016. View at: Google Scholar
  79. M. Das and S. Kumar, “Evidence of independent evolution of genotype XIII Newcastle disease viruses in India,” Archives of Virology, vol. 162, no. 4, pp. 997–1007, 2017. View at: Publisher Site | Google Scholar
  80. B. Nath and S. Kumar, “Emerging variant of genotype XIII Newcastle disease virus from Northeast India,” Acta Tropica, vol. 172, pp. 64–69, 2017. View at: Publisher Site | Google Scholar
  81. S. C. Courtney, L. Susta, D. Gomez et al., “Highly divergent virulent isolates of newcastle disease virus from the dominican republic are members of a new genotype that may have evolved unnoticed for over 2 decades,” Journal of Clinical Microbiology, vol. 51, no. 2, pp. 508–517, 2013. View at: Publisher Site | Google Scholar
  82. S. Akhtar, M. A. Muneer, K. Muhammad et al., “Genetic characterization and phylogeny of pigeon paramyxovirus isolate (PPMV-1) from Pakistan,” SpringerPlus, vol. 5, no. 1, article 1295, 2016. View at: Google Scholar
  83. T. Munir, A. Aslam, B. Zahid, I. Ahmed, M. S. Imran, and M. Ijaz, “Potential of commonly resident wild birds towards newcastle disease virus transmission,” Pakistan Veterinary Journal, vol. 35, no. 1, pp. 106-107, 2015. View at: Google Scholar
  84. P. Zhang, G. Xie, X. Liu et al., “High genetic diversity of Newcastle disease virus in wild and domestic birds in northeastern China from 2013 to 2015 reveals potential epidemic trends,” Applied and Environmental Microbiology, vol. 82, no. 5, pp. 1530–1536, 2016. View at: Publisher Site | Google Scholar
  85. J. C. F. M. Dortmans, P. J. M. Rottier, G. Koch, and B. P. H. Peeters, “Passaging of a newcastle disease virus pigeon variant in chickens results in selection of viruses with mutations in the polymerase complex enhancing virus replication and virulence,” Journal of General Virology, vol. 92, no. 2, pp. 336–345, 2011. View at: Google Scholar
  86. C. Meng, X. Qiu, S. Yu et al., “Evolution of newcastle disease virus quasispecies diversity and enhanced virulence after passage through chicken air sacs,” Journal of Virology, vol. 90, no. 4, pp. 2052–2063, 2016. View at: Publisher Site | Google Scholar
  87. L. Susta, M. E. B. Jones, G. Cattoli et al., “Pathologic Characterization of Genotypes XIV and XVII Newcastle Disease Viruses and Efficacy of Classical Vaccination on Specific Pathogen-Free Birds,” Veterinary Pathology, vol. 52, no. 1, pp. 120–131, 2015. View at: Google Scholar
  88. P. A. Desingu, K. Dhama, Y. S. Malik, and R. K. Singh, “May newly defined genotypes XVII and XVIII of newcastle disease virus in poultry from west and central Africa be considered a single genotype (XVII)?” Journal of Clinical Microbiology, vol. 54, no. 9, article 2399, 2016. View at: Publisher Site | Google Scholar
  89. S. Marangon and L. Busani, “The use of vaccination in poultry production,” Revue Scientifique et Technique, vol. 26, no. 1, pp. 265–274, 2006. View at: Google Scholar
  90. W. I. Muir, W. L. Bryden, and A. J. Husband, “Immunity, vaccination and the avian intestinal tract,” Developmental and Comparative Immunology, vol. 24, no. 2-3, pp. 325–342, 2000. View at: Google Scholar
  91. H. W. Doerr and A. Berger, “Vaccination against infectious diseases: What is promising?” Medical Microbiology and Immunology, vol. 203, no. 6, pp. 365–371, 2014. View at: Google Scholar
  92. D. R. Kapczynski, C. L. Afonso, and P. J. Miller, “Immune responses of poultry to Newcastle disease virus,” Developmental and Comparative Immunology, vol. 41, no. 3, pp. 447–453, 2013. View at: Google Scholar
  93. J. C. F. M. Dortmans, B. P. H. Peeters, and G. Koch, “Newcastle disease virus outbreaks: Vaccine mismatch or inadequate application?” Veterinary Microbiology, vol. 160, no. 1-2, pp. 17–22, 2012. View at: Google Scholar
  94. Z. Hu, S. Hu, C. Meng, X. Wang, J. Zhu, and X. Liu, “Generation of a genotype VII Newcastle disease virus vaccine candidate with high yield in embryonated chicken eggs,” Avian Diseases, vol. 55, no. 3, pp. 391–397, 2011. View at: Google Scholar
  95. S. Xiao, B. Nayak, A. Samuel et al., “Generation by Reverse Genetics of an Effective, Stable, Live-Attenuated Newcastle Disease Virus Vaccine Based on a Currently Circulating, Highly Virulent Indonesian Strain,” PLoS ONE, vol. 7, no. 12, Article ID e52751, 2012. View at: Publisher Site | Google Scholar
  96. M. B. Bello, K. Yusoff, A. Ideris, M. Hair-bejo, B. P. H. Peeters, and A. R. Omar, “Diagnostic and vaccination approaches for newcastle disease virus in poultry: the current and emerging perspectives,” Biomed Research International, vol. 2018, Article ID 7278459, 18 pages, 2018. View at: Google Scholar
  97. P. J. Miller, C. L. Afonso, J. El Attrache et al., “Effects of Newcastle disease virus vaccine antibodies on the shedding and transmission of challenge viruses,” Developmental and Comparative Immunology, vol. 41, no. 4, pp. 505–513, 2013. View at: Google Scholar
  98. K. Roohani, S. W. Tan, S. K. Yeap, A. Ideris, M. H. Bejo, and A. R. Omar, “Characterisation of genotype VII Newcastle disease virus (NDV) isolated from NDV vaccinated chickens, and the efficacy of LaSota and recombinant genotype VII vaccines against challenge with velogenic NDV,” Journal of Veterinary Science, vol. 16, no. 4, pp. 447–457, 2015. View at: Publisher Site | Google Scholar
  99. B. P. H. Peeters, O. S. De Leeuw, G. Koch, and A. L. J. Gielkens, “Rescue of Newcastle disease virus from cloned cDNA: Evidence that cleavability of the fusion protein is a major determinant for virulence,” Journal of Virology, vol. 73, no. 6, pp. 5001–5009, 1999. View at: Google Scholar
  100. O. S. de Leeuw, G. Koch, L. Hartog, N. Ravenshorst, and B. P. H. Peeters, “Virulence of Newcastle disease virus is determined by the cleavage site of the fusion protein and by both the stem region and globular head of the haemagglutinin-neuraminidase protein,” Journal of General Virology, vol. 86, no. 6, pp. 1759–1769, 2005. View at: Publisher Site | Google Scholar
  101. V. Palya, I. Kiss, T. Tatár-Kis, T. Mató, B. Felföldi, and Y. Gardin, “Advancement in vaccination against newcastle disease: Recombinant HVT NDV provides high clinical protection and reduces challenge virus shedding with the absence of vaccine reactions,” Avian Diseases, vol. 56, no. 2, pp. 282–287, 2012. View at: Publisher Site | Google Scholar
  102. P. J. Miller, R. Haddas, L. Simanov et al., “Identification of new sub-genotypes of virulent Newcastle disease virus with potential panzootic features,” Infection, Genetics and Evolution, vol. 29, pp. 216–229, 2015. View at: Publisher Site | Google Scholar
  103. F. Perozo, R. Marcano, and C. L. Afonso, “Biological and phylogenetic characterization of a genotype VII Newcastle disease virus from Venezuela: Efficacy of field vaccination,” Journal of Clinical Microbiology, vol. 50, no. 4, pp. 1204–1208, 2012. View at: Google Scholar
  104. S. S. Ewies, A. Ali, S. M. Tamam, and H. M. Madbouly, “Molecular characterization of Newcastle disease virus (genotype VII) from broiler chickens in Egypt,” Beni-Suef University Journal of Basic and Applied Sciences, vol. 6, no. 3, pp. 232–237, 2017. View at: Google Scholar
  105. S.-H. Kim, S. Nayak, A. Paldurai et al., “Complete genome sequence of a novel newcastle disease virus: Strain isolated from a chicken in West Africa,” Journal of Virology, vol. 86, no. 20, pp. 11394-11395, 2012. View at: Publisher Site | Google Scholar

Copyright © 2018 Muhammad Bashir Bello et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

More related articles

 PDF Download Citation Citation
 Download other formatsMore
 Order printed copiesOrder

Related articles

Article of the Year Award: Outstanding research contributions of 2020, as selected by our Chief Editors. Read the winning articles.