Continental J.

Veterinary Sciences 5 (1): 1 - 5, 2011 © Wilolud Journals, 2011 ` Printed in Nigeria

ISSN: 2141 – 4041 http://www.wiloludjournal.com

MOLECULAR EPIDEMIOLOGY OF CONTAGIOUS BOVINE PLEUROPNEUMONIA IN NIGERIA-A REVIEW
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Bamaiyi, P.H1. and Wade, A2. Department of Animal Production, Faculty of Agriculture, Adamawa State University, Nigeria 2 The National Veterinary Laboratory, Bokle (Lanavet), Cameroon

ABSTRACT Contagious Bovine PleuroPneumonia (CBPP) is an old debilitating highly contagious disease of cattle and buffaloes caused by Mycoplasma mycoides subsp. mycoides Small Colony biotype (MmmSC). The disease is responsible for lots of economic losses in Nigeria. To have a good understanding of the trend of the disease epidemiologically many tools have been employed. But in recent times the advent of molecular tools is proving useful for the study of the disease that is threatening the cattle population of Africa and in particular Nigeria. Molecular epidemiology is an indispensable tool now in tracing disease outbreak and ensuring disease control and its potentials must be fully utilized if CBPP is to be eradicated in Nigeria. KEYWORDS: Molecular epidemiology, Contagious Bovine Pleuropneumonia, Nigeria INTRODUCTION Contagious Bovine PleuroPneumonia (CBPP) caused by Mycoplasma mycoides subsp. mycoides Small Colony biotype (MmmSC) is an infectious and highly contagious disease of cattle and water buffaloes (Masiga, et al., 1996). The disease is considered to be amongst the most important infectious diseases in livestock around the world. For many years the greatest threat to cattle in Nigeria had been Rinderpest cattle plague before it was finally brought under control and eradicated. Now the attention of veterinary professionals and regulatory authorities concerned has turned to CBPP which initially had been significantly controlled up to the mid-1980s through vaccination, slaughter programs and control of movement of animals. CBPP experienced a resurgence taking place from the late 1980s to the present largely due to inadequate funding of control programs (Egwu, et al., 1996; Aliyu, et al., 2000). Currently, CBPP is endemic in most parts of East, Central and West Africa and is spreading fast towards the Southern part of Africa especially Zambia and Namibia, where it is responsible for huge economic losses (Musisi, et al., 2011). The major organ affected is the lungs and the major body system affected is the respiratory system. Affected animals have difficulty in breathing due to damage to the lungs, loss of body condition and a proportion die. All ages of cattle are susceptible but young cattle develop joint swellings rather than lung infections. Many cattle show no disease signs despite being infected and others recover quickly after a transient mild disease, yet they can carry infection for as long as two years and may be responsible for passing on infection at a later date (Egwu, et al., 1996; Masiga, et al., 1996; Musisi, et al., 2011). Some animals are called “Lungers” (chronically infected animals with encapsulated lesions in the lungs) which happens due to prolonged antibiotic usage leading to reduced clinical manifestations of the disease in the animals. Species of mycoplasma In recent years, more than 20 species of Mycoplasma, Ureaplasma and Acholeplasma have been isolated from cattle with different diseases. All of the 20 aforementioned species have been referred to as the Mycoplasmas (Nicholas, et al., 2000). It is generally believed that Mycoplasmas play a secondary role in infections, most often exacerbating pre-existing disease. However, it has been shown that Mycoplasma bovis (M. bovis) can play a primary role. M. bovis is considered as one of the more pathogenic species and is the most frequent Mycoplasma pathogen of pneumonia, mastitis, and arthritis in cattle (Nicholas, et al., 2000). Other species of mycoplasma include among others, Mycoplasma wenyonii (Hoelzle, et al., 2011), mycoplasma Candidatus Mycoplasma haemobos (Hoelzle, et al., 2010), Mycoplasma capricolum subsp. Capripneumoniae (Kusiluka, et al., 2001). The members of the M. mycoides cluster which are specially difficult to differentiate due to phenotypic and genotypic features that cross react serologically include the following: (i) contagious agalactiae of sheep and goats (Mycoplasma capricolum subsp. capricolum and (ii)Mycoplasma mycoides subsp. capri, including the recently reclassified serovar Mycoplasma mycoides subsp. mycoides biotype Large Colony) (iii) contagious bovine pleuropneumonia of cattle (Mycoplasma mycoides subsp. mycoides biotype Small Colony), and (iv) contagious caprine pleuropneumonia of goats (Mycoplasma capricolum subsp. capripneumoniae). The

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Bamaiyi, P.H and Wade, A: Continental J. Veterinary Sciences 5 (1): 1 - 5, 2011

fifth, recently reclassified M. mycoides cluster member, Mycoplasma leachii sp. nov. (formerly Mycoplasma sp. bovine group 7 of Leach) has been isolated from calves with pneumonia(Righter, et al., 2011). Among the several species of Mycoplasma found in cattle, only Mycoplasma mycoides mycoides Small Colony is known to cause fatal respiratory disorders (Masiga, et al., 1996; Musisi, et al., 2011). Transmission and economic impact Contagious bovine pleuropneumonia (CBPP), caused by Mycoplasma mycoides subsp. mycoides Small Colony biotype (MmmSC), is a highly infectious cattle disease endemic in many African countries, and the Sub-Saharan region is under constant threat due to the carrier status of its host (Musisi, et al., 2011). In Nigeria the infection is widespread in cattle and years of vaccination have not brought the disease under control (Aliyu, et al., 2000). The pathogen affects the pulmonary tract of adult cattle and buffalos that can lead to severe pulmonary inflammation leaving some animals with hepatised lungs, pulmonary oedema and chronic necrotic sequestra (potential reservoir for disease spread) (Jores, et al., 2009). Transmission is mainly by aerosol through close contact with infected animals and occasionally from latent carriers intermittently shedding Mycoplasma organisms from sequestra. Direct close contact between animals excreting flugge-type droplets by coughing ensures the rapid spread of the infection. CBPP spread alarmingly during the 1990s, infecting several countries previously free from the disease, and was reported by the Office International des Epizooties (OIE) meeting on January 1995 as causing greater losses in cattle than any other disease, including Rinderpest (Masiga, et al., 1996; Masiga, et al, 1999). Because of the great economic losses due to this disease in endemic regions, OIE has declared CBPP to be one of the most serious contagious animal diseases, and has thereby listed it in the group of reportable animal diseases of high socio-economic impact and the Food and Agriculture Organisation (FAO) regards it as one of the major transboundary animal diseases (TADs). Both organizations consider CBPP as a serious constraint to the development of the livestock sector in Africa. Current losses are estimated to be around 2 billion US$ per annum (Masiga, et al., 1999). In Nigeria, the disease is widespread and endemic. Transmission occurs within herds and from herd to herd from direct contact and repeated contact between sick and healthy animals, due to the nomadic way of life of the predominant cattle rearers who migrate for hundreds to thousands of kilometres in search of pasture for their cattle (Adekunle, et al., 2002). Also the borders with neighbouring endemic countries such as Cameroon, Chad republic and Niger republic are highly porous hence control of spread of infection is nearly impossible. Transhumance and nomadism contributes greatly to the spread of CBPP in Nigeria coupled with the failure of “cordons sanitaires” (National Disease Surveillance and Monitoring). This has made the vaccination campaigns ineffective to halt the transmission and spread of the disease (Aliyu, et al., 2000). CBPP causes severe economic losses to farmers in Nigeria and to the livestock industry as a whole in spite of years of attempts at vaccination which have been inconsistent (Aliyu, et al., 2000). The direct economic losses due to CBPP in Nigeria which affects mostly the beef sector of the cattle but does not spare the dairy sector also, is put at US$3.6 Million (Osiyemi, 1981) and in northern Nigeria alone it is put at US$1.5Million (Egwu, et al., 1996). These figures for a largely underdeveloped cattle industry in a country with multiple economic challenges are staggering more so considering that these are conservative estimates and the reality on the ground may be bleaker than this. Eradication and Resurgence of CBPP This disease requires special international regulations for its eradication. The Office International des Epizooties - International Office of Epizootics (OIE) which is the World Organization for Animal Health recommends a test and slaughter policy for the eradication of CBPP. This is not practicable in Nigeria because of the cost and logistics of payment of compensation to farmers. Therefore, nationwide vaccination of cattle and surveillance is practiced. The vaccination coverage is as high as only 14.2% and could be as low as 2% (Aliyu, et al., 2000). With this very low vaccination coverage control of the disease is still far away from being realized and eradication is impossible. CBPP was eradicated from most continents during the 19th century but remained endemic in Africa (Egwu, 1996; Musisi, et al., 2011). In spite of strict sanitary control measures, it re-emerged in Europe in the 1980s and 1990s in countries like Spain and Portugal, thus posing a serious threat to animal health and livestock production around the world (Masiga, et al., 1999; Regalla, 2011).

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Bamaiyi, P.H and Wade, A: Continental J. Veterinary Sciences 5 (1): 1 - 5, 2011

Many factors contributed to the resurgence of CBPP in places where it had disappeared or was thought to be eradicated. Contributing factors to this current resurgence are thought to include the breakdown of Veterinary services, increased and unrestricted cattle movements (due to drought, war, and civil strife), and a lack of vaccine efficacy (known to induce antibodies in only 70% of all correctly vaccinated animals). Inadequate government funding and trained personnel are also major contributors to this trend (Aliyu, et al., 2000; Masiga, et al., 1999). In Nigeria, a study found that the over-all lesion based prevalence of the disease from abattoir surveys was 0.29% and the average vaccination coverage was 9.5% (Aliyu, et al., 2000) Molecular epidemiology M. mycoides subsp. mycoides SC strains were reported to be homogeneous. However, genetic variations are known to occur within MmmSC as evidenced by restriction fragment length polymorphism (Poumarat and Solsona, 1995; Varela, et al., 2010). Furthermore, all MmmSC strains isolated in Europe since 1990 revealed a major chromosomal deletion of 8.84 kb, including genes of the glycerol ABC transporter operon and the lipoprotein gene lppB (Vilei & Frey, 2009). These studies demonstrated that the genome of M. mycoides subsp. mycoides SC has a higher degree of plasticity than expected. The relatively strong genomic variability must also be taken into consideration when assessing the stability and safety of live vaccine strains. The genome of MmmSC has a high degree of repetitive sequences compared to those of other bacteria. In total, the repetitive sequences in MmmSC constitute 29% of the genome. M. mycoides subsp. mycoides SC is known to have the highest density of insertion sequences (IS) among bacterial genomes (Righter, et al., 2011). In addition to genomic variations, Intraclonal antigenic variation in pathogenic mycoplasma species is considered an important feature of host–pathogen interaction which was observed for MmmSc with monoclonal antibodies 3F3 (Gaurivaud, et al., 2004). Latent carriers are not detected by serological test. In addition, the direct and classical diagnosis of MmmSC is always hampered by problems since classical bacteriological detection methods need several days to establish a result and sample transport requires a proper cold chain. There is paucity of literature on molecular epidemiological work on CBPP in Nigeria until recent years. The application of Polymerase Chain Reaction (PCR) adapted to real time technology was developed in 2005 by Gorton, et al. (2005). It is a rapid, sensitive and highly specific detection tool of MmmSC-specific genetic loci using TaqMan-based assay for the detection of MmmSC and is a modern diagnostic assay that is sensitive and specific for biological agents involved in outbreaks of CBPP in Nigeria and other endemic countries. The recent development of a new molecular technique based on Variable-number tandem-repeat (VNTR) analysis for MmmSC genome typing is an epidemiological tool to enable the differentiation of strains (McAuliffe, et al., 2007). Before implementing an effective control plan or eradication process, the epidemiological situation of the disease must first be clearly addressed. It was during such an investigation that a new strain involved in a CBPP outbreak in Botswana and Tanzania was discovered and named Botswanan strain, M375. This new strain displayed numerous and significant phenotypic differences from both contemporary field isolates and older field and vaccine strains which must have originated from a gene deletion along the line (March, et al., 2000). Recently in Nigeria, West Africa, a variable number tandem repeat (VNTR) analysis was conducted on 13 isolates using tandem repeat (TR) 34. The study revealed diversity within MmmSc isolates with 5 different VNTR types indicated (Nwankpa, et al., 2010). This tool is going to be useful in tracing of outbreaks for Mycoplasma mycoides mycoides small colony and in disease control. CONCLUSION Considering the devastating economic implications of CBPP in Nigeria and with the escalating trend of the highly contagious disease it is imperative that more attention be given to molecular epidemiological researches that have the potential to provide the missing link needed to control and eradicate the disease from Nigeria and other endemic countries.

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Bamaiyi, P.H and Wade, A: Continental J. Veterinary Sciences 5 (1): 1 - 5, 2011

REFERENCES Adekunle, O. A., Oladele, O. I., & Olukaiyeja, T. D. (2002). Indigenous control methods for pests and diseases of cattle in Northern Nigeria Livestock Research for Rural Development, 14(2). Aliyu, M. M., Obi, T. U., & Egwu, G. O. (2000). Prevalence of contagious bovine pleuropneumonia (CBPP) in northern Nigeria. Preventive Veterinary Medicine, 47(4), 263-269. Egwu, G. O., Nicholas, R. A. J., Ameh, J. A., & Bashiruddin, J. B. (1996). Contagious bovine pleuropneumonia: an update. Veterinary Bulletin, 66, 875-888. Gaurivaud, P., Persson, A., Grand, D. L., Westberg, J., Solsona, M., Johansson, K.-E., et al. (2004). Variability of a glucose phosphotransferase system permease in Mycoplasma mycoides subsp. mycoides Small Colony. Microbiology, 150(4009-4022). Gorton, T. S., Barnett, M. M., Gull, T., French, R. A., Lu, Z., Kutish, G. F., et al. (2005). Development of realtime diagnostic assays specific for Mycoplasma mycoides subspecies mycoides Small Colony. Vet Microbiol, 111(1-2), 51-58. Hoelzle, K., Hofmann-Lehmann, R., & Hoelzle, L. E. (2010). Candidatus Mycoplasma haemobos', a new bovine haemotrophic Mycoplasma species? Veterinary Microbiology, 144(3-4), 525-526. Hoelzle, K., Winkler, M., Kramer, M. M., Wittenbrink, M. M., Dieckmann, S. M., & Hoelzle, L. E. (2011). Detection of Candidatus Mycoplasma haemobos in cattle with anaemia. The Veterinary Journal, 187(3), 408410. Jores, J., Meens, J., Buettner, F. F. R., Linz, B., Naessens, J., & Gerlach, G. F. (2009). Analysis of the immunoproteome of Mycoplasma mycoides subsp. mycoides small colony type reveals immunogenic homologues to other known virulence traits in related Mycoplasma species. Veterinary Immunology and Immunopathology, 131(3-4), 238-245. Kusiluka, L. J. M., Ojeniyi, B., Friis, N. F., Kokotovic, B., & Ahrens, P. (2001). Molecular analysis of field strains of Mycoplasma capricolum subspecies capripneumoniae and Mycoplasma mycoides subspecies mycoides, small colony type isolated from goats in Tanzania. Veterinary Microbiology, 82(1), 27-37. March, J. B., Clark, J., & Brodlie, M. (2000). Characterization of strains of Mycoplasma mycoides subsp. mycoides small colony type isolated from recent outbreaks of contagious bovine pleuropneumonia in Botswana and Tanzania: evidence for a new biotype. J Clin Microbiol, 38(4), 1419-1425. Masiga, W. N., Domenech, J., & Windsor, R. S. (1996). Manifestation and epidemiology of contagious bovine pleuropneumonia in Africa. Rev. Sci. Tech. Int. Off. Epiz., 15, 1283-1308. Masiga, W. N., Rossitor, P., & Bessin, R. (1999). Contagious bovine pleuropneumonia: Report of the FAO/OIE/OUI-BAR CBPP Consultative Group meeting, Rome, Italy 5-7 October 1998. McAuliffe, L., Ayling, R. D., & Nicholas, R. A. (2007). Identification and characterization of variable-number tandem-repeat markers for the molecular epidemiological analysis of Mycoplasma mycoides subspecies mycoides SC. FEMS Microbiol Lett, 276(2), 181-188. Musisi, F. L., Dungu, B., Thwala, R., Mogajane, M. E., & Mtei, B. J. (2011). The threat of contagious bovine pleuropneumonia and challenges for its control in the SADC region Retrieved 20.06.11, 2011, from http://www.fao.org/docrep/007/y5510e/y5510e0d.htm Nicholas, R., Baker, S., Ayling, R., & Stipkovits, L. (2000). Mycoplasma infections in growing cattle. Cattle practice, 8(2), 115-118.

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Nwankpa, N. D., Manso-silvan, L., Lorenzon, S., Yaya, A., Lombin, L. H., & Thiaucourt, F. (2010). Variable Number Tandem Repeat (VNTR) analysis reveals genetic diversity within Mycoplasma mycoides mycoides Small Colony isolates from Nigeria. Veterinary Microbiology, 146(3-4), 354-355. Osiyemi, T. I. O. (1981). The eradication of CBPP in Nigeria: prospects and problems. Bulletin of Animal Health and Production in Africa, 29, 95-97. Poumarat, F., & Solsona, M. (1995). Molecular epidemiology of Mycoplasma mycoides subsp. mycoides biotype Small Colony, the agent of contagious bovine pleuropneumonia. Veterinary Microbiology, 47(3-4), 305315. Regalla, J. (2011). Specific diagnostic and epidemiological procedures adopted for the contagious bovine pleuropneumonia eradication programme (1995-2002) in Portugal: A working model for the disease control in African countries Retrieved 20.06.11, 2011, from http://www.fao.org/docrep/007/y5510e/y5510e0o.htm Righter, D. J., Rurangirwa, F. R., Call, D. R., & McElwain, T. F. (2011). Development of a bead-based multiplex PCR assay for the simultaneous detection of multiple Mycoplasma species. Veterinary Microbiology, In Press, Accepted Manuscript. Varela, F., Inácio, J., & Botelho, A. (2010). Molecular diversity assessed by VNTR and IS1296 typing of historical Mycoplasma mycoides subsp. mycoides SC strains. Veterinary Microbiology, 146(3-4), 295-302. Vilei, E. M., & Frey, J. (2009). Detection of Mycoplasma mycoides subsp. mycoides SC in bronchoalveolar lavage fluids of cows based on a TaqMan real-time PCR discriminating wild type strains from an lppQ- mutant vaccine strain used for DIVA-strategies. Journal of Microbiological Methods, 81(3), 211-218. Received for Publication: 21/06 /2011 Accepted for Publication: 19/08 /2011 Corresponding Author Bamaiyi, P.H Department of Animal Production, Faculty of Agriculture, Adamawa State University, Nigeria Emaila: phbamaiyi@yahoo.com Present address: Faculty of Veterinary Medicine, Universiti Putra Malaysia

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