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Comprehensive Review on Peste Des Petits [PPR] Disease in Ruminants and Camels: with Emphasis on Clinical Signs and Histopathological Finding

Article · January 2016 DOI: 10.4172/2325-9590.1000207

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, the morbillivirus of marine mammals, and Feline Comprehensive Review on morbillivirus [8]. PPR is a small, one strand RNA virus which has 15948 nucleotides and 8 genes [3’-N-P/C/V-M-F-HN-L-5’] Peste Des Petits Ruminants [9]. These genes are responsible to produce 6 structural proteins, N-[nucleocapsid], P-[phosphoprotein], M-[matrix protein] F-[fusion [PPR] Disease in Ruminants protein], HN-[haemagglutininaminidase protein], L-[large/ polymerase] and two nonstructural proteins [protein C and protein and Camels: with Emphasis V] [9-12]. Four PPR virus lineages have been identified. Lineage 1 was isolated from Western Africa, lineage 2 from West African countries, on Clinical Signs and , Guinea and Burkina Faso, lineage 3 originated from Histopathological Finding Eastern Africa, Sudan, Yemen and Oman, lineage 4 was isolated from Arabian Peninsula, and [9,13-15]. Amir Zakian1*, Mohammad Nouri1, Kokab Faramarzian1, Meysam Tehrani-Sharif2, Annahita Rezaie3 and Mohammad- Geographical distribution of disease 4 Reza Mokhber-Dezfouli The disease was first described at 1942 in Côte d’Ivoire, in and [1]. Nowadays PPR is a very well-known disease not only in West Africa but also in the Middle East and south Abstract Asia [16-20]. Peste des petits ruminants [PPR] is a highly acute disease of small ruminants with high morbidity and mortality. The geographic Strain-4 PPRV had been isolated at 2000, 2004, 2008, and 2009 distribution of disease is almost global. The PPRV affecting small from Sudan [21]. Natural of PPRV movement in the domestic and wild ruminants and camels. PPRV is a lymphotropic and flock was shown in Tanzania. Swai et al., showed high seroprevalence epitheliotropic virus which causes and rhinotracheitis, of PPRV among sheep and flocks in Tanzania [22]. The results stomatitis, gastroenteritis and . Histopathologically, of Swai et al., study indicated higher anti PPRV titers in goat flocks pseudomembraneous [necrotic] stomatitis, necrotic tonsillitis, in comparison to sheep [22]. PPRV was isolated 1987 and 1990 in fibrinohemorrhagic enteritis, proliferative interstitial pneumonia suppurative bronchointerstitial pneumonia, multi-nucleated giant [23]. cells [syncytia] and cytoplasmic and/or nuclear eosinophilic PPRV isolated from Iran, Saudi Arabia, Iraq, Israel, Jordan, inclusion bodies are considered as pathognomonic signs. An acute Kuwait, Lybia, Oman, United Emirates and Yemen. Seroepidemiologic form usually is seen in goat and is similar to . The classic feature of PPR is a severe respiratory disease. The subacute form, studies show disease distribution in Turkey and Syria [24]. The usually occurs in sheep, but also possible in goats. Control and PPR seroprevalence was not notable in Saudi Arabia in 2000 [25] prevention program is based on , quarantine, movement but last studies are showing prevalence increased dramatically [26- control and sanitary slaughter and disinfection. 29]. Various seroprevalence was performed in Jordan and Lebanon Keywords [30,31]. PPR; Lymphotropic; Epitheliotropic; Camels; Small ruminants Amjad et al., isolated PPRV by PCR technique in the Panjab region in Pakistan [32]. Ahmad showed that healthy goats were seropositive due to PPRV prevalence [33]. Various Introduction seroprevalence studies have done in Pakistan indicated that PPRV Peste des petits ruminants [PPR] also known as ovine rinderpest, is widely distributed among country [2,34-38]. Iraq has experienced goat plague, plague of small ruminants, pneumoentritis syndrome, a widespread high morbidity and low mortality rate virus at 2000 pneumoentritis complex, contagious postular stomatitis [1] is a [39]. Seroanalysis indicated that the isolated virus had been in a highly contagious animal disease affecting small ruminants, camel circulation [40]. The PPR is widespread in Iran and leads to economic and wild ruminants e.g. Ibex, gazelle [2-6] losses among sheep and goat flocks [41]. An outbreak of PPR in camels in Iran was first reported by Zakian et al [6] and in India was Etiology first reported by Taylor et al. [42]. PPR caused by an RNA coated virus belongs to genus morbillivirus, Sensitive species family Paramyxoviridae and order [7]. The PPRV affecting small domestic and wild ruminants [18,43- Other morbillivirus include Rinderpest virus, virus, 47] and camel [6,16]. Among small ruminants goats are severely Canine distemper virus, Porcine distemper virus, Cetacean affected [30,48,49]. Morbidity rate and seroprevalence increased significantly in mixed [sheep and goat] flocks [16,50-53]. The virus *Corresponding author: Amir Zakian, Department of Clinical Sciences, seroprevalence has been reported in , buffalo [54-57], pig [57] College of Veterinary Medicine, Shahid Chamran University of Ahvaz, Iran, and camel [16,58] but no clinical signs was observed in these animals E-mail: [email protected] except camel. Death and clinical signs have been reported in calves Received: August 09, 2016 Accepted: September 19, 2016 Published: infected with PPRV in an experimental study [59]. The virus of PPR September 22, 2016 has been isolated from domestic buffalo in India [60]. There are

All articles published in Journal of Veterinary Science & Medical Diagnosis are the property of SciTechnol, and is protected by International Publisher of Science, copyright laws. Copyright © 2016, SciTechnol, All Rights Reserved. Technology and Medicine Citation: Zakian A, Nouri M, Faramarzian K, Sharif MT, Rezaie A, et al. (2016) Comprehensive Review on Peste Des Petits Ruminants [PPR] Disease in Ruminants and Camels: with Emphasis on Clinical Signs and Histopathological Finding. J Vet Sci Med Diagn 5:4.

doi: 10.4172/2325-9590.1000207 many reports indicate that camel may be infected with the PPRV. pulp of the spleen and gastrointestinal submucosal lymphoid tissues The virus has been isolated from camels in epizootic outbreaks in that associated with necrosis and apoptosis was found in PPRV [74]. Ethiopia [58,61]. Khalafalla et al., and Kwiatek et al., isolated PPRV Intestinal lymph node necrotic ulcers cause diarrhea [82]. Central from camels in Sudan by PCR method [21,62]. A clinical case of PPR nervous system [CNS] involvement is not seen in PPRV and rinderpest in camels was reported from Iran [6]. Dorcas gazelle, Thomson’s while CNS manifestations are common in measles virus [83]. gazelle, Gemsbok and Ibex are also susceptible species [63,64]. The However brain inoculation of PPRV and rinderpest cause clinical virus was also isolated from wild goat and Bharals from Iran [44,65]. infections. Recent studies showed that PPRV and border disease virus In Pakistan PPRV was isolated by PCR and immuncapture ELISA [IC co-infection facilitates PPRV transmission to the brain [84]. However, ELISA] methods from Sindh Ibex [4]. infectious particles are found in tears and oral secretion during the Transmission incubation period [74,79]. But virus isolates from conjunctiva 7 days after exposure. The recovered goats shed virus from feces for a period PPRV is secreted in tears, nasal discharges, and secretion from of 12 weeks [85]. coughing and in feces of infected animal. The virus is shed from the intestine and is found in feces at the end stage of the disease [66]. Immunosuppression Swine and cattle do not show clinical signs after exposure Immunosuppression is a common finding following morbillivirus to the virus [57,67]. [57]. Cattle don’t show clinical signs infections. There is a direct correlation between white blood cell following experimental inoculation [67]. However, there are infection rate and Immunosuppression. The suppressed immune few reports concerning the cattle PPR occurrence in the calf response might be due to inhibition of interferon production, and immunosuppressed animal [9,66]. Small infectious particles change in cytokine response, inflammatory response suppression, released into the environment after sneezing and coughing of leukocyte destruction, B cell destruction, cell cycle disruption [86]. affected animals [68,69]. Pathogenesis PPRV is a lymphotropic and epitheliotropic virus which causes conjunctivitis and rhinotracheitis, stomatitis, gastroenteritis and pneumonia [70]. After PPRV exposure, the virus will be captured by antigen presenting cells (APCs) in inter epithelial space and respiratory nasopharynx, then transferred to local lymphoid tissue for virus proliferation [70,71]. The virus spreads throughout the body via infected lymphocyte in both blood and lymphoid system [72-74]. Pneumonia occurs in the late stage of disease and following virus high dose exposure [74]. The blood lymphocyte count is reduced in affected animals due to lymphoid tissue necrosis [spleen, payer patch, lung, lymph node] [74-76]. In vitro studies indicated polymorph nuclear cells [PMN] induced apoptosis following PPRV exposure [77]. 3-5 days after the Figure 1: Suppurative bronchointerstitial pneumonia. PPR in goat. Note to incubation period, there is a persistent fever, hyperemia, muco-nasal thickening of alveolar walls (black arrows) and accumulation of inflammatory discharge, anorexia, and diarrhea. There is a negative correlation cells in alveolar spaces (white asterisks) (H&E), (Referral cases to the Veterinary hospital of Shahid Chamran University). between the dose of virus and incubation period [74]. In sensitive species the lung acute congestion and edema is common following PPRV exposure and usually death occurs [78]. Chronic infection is uncommon and should be differentiated with bronchopneumonia. These animals might be alive for as long as a month. Post infection consequences vary among animals and depend on immune response [79,80]. Parasite infestation and nutrition status might have a role in disease severity, morbidity and mortality rate [79,80]. Histopathological findings Histopathologically, pseudomembraneous [necrotic] stomatitis, necrotic tonsillitis, fibrinohemorrhagic enteritis, proliferative interstitial pneumonia and suppurative bronchointerstitial pneumonia (Figures 1, 2 and 3) are seen. Multi-nucleated giant cells [syncytia] and cytoplasmic and/or nuclear eosinophilic inclusion bodies are considered as pathognomonic (Figures 3 and 5). Like the other , PPR virus can also cause lesions in the kidney, brain, and abomasum. The PPRV tropism can be explained Figure 2: Suppurative bronchointerstitial pneumonia. PPR in goat. by the mechanism in which PPRV binds to receptors on the cell Accumulation of inflammatory cells in bronchus and alveolar spaces (black asterisks) is obvious and note to hyperemia in alveolar walls (arrow) (H&E), surface. The PPR in small ruminants often shows co-association with (Referral cases to the Veterinary hospital of Shahid Chamran University). secondary viral, bacterial, and parasitary infections [81]. The white

Volume 5 • Issue 4• 1000207 • Page 2 of 8 • Citation: Zakian A, Nouri M, Faramarzian K, Sharif MT, Rezaie A, et al. (2016) Comprehensive Review on Peste Des Petits Ruminants [PPR] Disease in Ruminants and Camels: with Emphasis on Clinical Signs and Histopathological Finding. J Vet Sci Med Diagn 5:4.

doi: 10.4172/2325-9590.1000207

While only a fraction of peripheral blood cells became infected, but immunosuppression could take weeks [87]. strain may cause transient immunosuppression [82]. The significance of viral proteins [P, N, H] as proliferation inhibitors and lymphoid tissue depletion inducers in measles virus and rinderpest virus has been described [88- 92]. In vitro studies indicated that N protein of morbillivirus attaches to human Fc-γ RII and inhibit production [74]. Marie et al., showed the remarkable role of measles virus N-protein in T cell proliferation inhibitor and reduced immune inflammatory responses [93]. Cellular destruction is a consequence of morbillivirus infections. Cellular leakage products, e.g. nucleic acid and proteins might evoke an autoimmune response [82]. Immune system response While morbillivirus is known as an immunosuppressor but Figure 3: Suppurative bronchointerstitial pneumonia. PPR in goat. Part of animal recovered from an acute form, usually gains long term figure 2 with higher magnification. Between inflammatory cells multinucleated immunity against reinfection [82]. The protective immunity is usually giant cells (syncitia) (black arrow) are obvious and note to intracytoplasmic eosinophilic inclusion bodies in the proliferated cells of bronchial evoked against F, N and H proteins [13,94]. Glycoprotein F and H of (red arrows) (H&E), (Referral cases to the Veterinary hospital of Shahid rinderpest and PPRV induce a humoral response [94-97]. There are Chamran University). evidences that indicate the significance of cellular immune response in PPR protection. Although the N- protein of the virus had the highest frequency, but doesn’t induce neutralizing antibody response [98]. N-protein induces a cellular immune response [99-101]. The PPRV infection in goats leads to a classic inflammatory response that identified with increased expression of cytokines such as IFNβ, IFNγ, IL-4, IL-1β, IL-8, IL-10, IL-6 and IL-12 [102,103]. Clinical findings The clinical signs of PPR are similar to rinderpest, but rinderpest is an occurrence in small is rare [104]. The clinical signs vary from subacute in sheep to fatal in goat. Although non clinical infection can occur in both species, especially in flocks that are migrating in endemic areas [105]. The most remarkable finding in affected camels includes sudden death, yellowish diarrhea [6,21], stomatitis, ulcerative keratitis conjunctivitis, fever, respiratory distress, pneumonia, enlargement of lymph node, dermatitis, obvious Figure 4: Necrotic stomatitis in the tongue of goat with PPR. Note to necrosis dehydration [6], abortion, subcutaneous edema, submandibular of stratified squamous epithelium (asterisks) (H&E), (Referral cases to the Veterinary hospital of Shahid Chamran University). enlargement, chest pain and infrequent coughing [21]. Acute form: An acute form usually is seen in goat and is similar to rinderpest. The classic feature of PPR is a severe respiratory disease. The incubation period is 3-6 days [106]. Young animals are more susceptible to PPR and the prognosis is poor and death occurs [35]. The acute form is identified by sudden fever [40-41.3°C], sneezing, tears and nasal discharges [55]. 1-2 days after necrotic lesions are observed in the nasal cavity and inside the oral cavity. Diphtheria plaque is produced and nasal discharges give a putrid odor to the breath. Affected animals have a dry muzzle and mucopurulent discharges. Dyspnea and were seen at late stage of the disease. Vaginal and prepuce erosions and abortion have been reported. Death occurs 7-10 days of the onset of fever [106]. Subacute form: The subacute form, usually occurs in sheep, but also possible in goats. Necrotic ulcers are not obvious and most of the affected animals are recovered. Death is rare [106]. The disease duration is usually more than two weeks [107]. Figure 5: Necrotic stomatitis in the tongue of goat with PPR. Part of figure 4 with higher magnification. Note to multinucleated giant cells (syncitia) (black Laboratory diagnosis arrows) and necrosis of epithelium (red arrow). (H&E), (Referral cases to the Veterinary hospital of Shahid Chamran University). Clinical features of PPR and rinderpest are similar so differentiation of these diseases by clinical signs is difficult. The antibody produced

Volume 5 • Issue 4• 1000207 • Page 3 of 8 • Citation: Zakian A, Nouri M, Faramarzian K, Sharif MT, Rezaie A, et al. (2016) Comprehensive Review on Peste Des Petits Ruminants [PPR] Disease in Ruminants and Camels: with Emphasis on Clinical Signs and Histopathological Finding. J Vet Sci Med Diagn 5:4.

doi: 10.4172/2325-9590.1000207 against nucleocapsis protein and haemagglutinin protein in PPRV and foci in cranial and cardiac lobes of the lung. The gastrointestinal and rinderpest facilitated diseases diagnosis by serologic tests. Methods lung lymph node are involved so lymphadenopathy may be seen. The of diagnosis are based on virus isolation, antigen and antibody abomasum exhibits regulatory outlined erosions and hemorrhages, identification and molecular methods. The virus isolation is the gold and less frequently erosions are seen in the first portion of the small standard method for PPR diagnosis. The virus has isolated In vitro intestine. The is more severely affected disseminated in sheep and cattle primary cells [108], Vero cells [18] and marmoset hemorrhage along the fold of mucous of the large intestine, which B-lymphoblastoid-B95a cells [109]. This method is time consuming, exhibits a streak of congestion, resulting in the zebra line appearance requires specific facilities and has less sensitivity in comparison to [133]. The cadaver gives a putrid odor [133]. The specimens required RT-PCR [110]. The virus antigen diagnosis methods include: Indirect for antigen detection are from lung, small and large intestine, oral immunofluorescence test [IFAT] and Immunoperoxidase [108]; CIE mucosa and mesentric lymph nodes [105,106]. [111] AGID, AGPT [112]; Haemagglutination Tests [113,114]; MAb- Differential diagnosis based immunocapture ELISA [52,114]; sandwich ELISA [s-ELISA] [115]; and dot-ELISA [114,116]. PPR should be differentiated from other viral infections such as goat pox, blue tongue, contagious pustular stomatitis, foot and mouth However the AGPT is the most common method of PPR and disease [FMD], and contagious caprine pleuropneumonia [CCPP] rinderpest diagnosis, but differentiation of PPR and rinderpest by [106,134]. this method is not applicable [14]. PPRV as morbillivirus shows appropriate hemagglutinin [85,117-119]. HA is more sensitive Control and prevention for virus antigen in comparison to AGPT [14]. HA is the choice The standard disease control measures consisting of quarantine, method for differential diagnosis of PPR from rinderpest [120]. movement control and sanitary slaughter and disinfection. A However the CIE as AGPT is not capable to differentiate PPR from modified live vaccine is used in endemic areas [106]. In the past an rinderpest but it is more sensitive and easier to perform [111]. CIE attenuated heterologous vaccine (Tissue culture rinderpest vaccine), is an appropriate method for PPR and rinderpest antigen isolation which is consist of live rinderpest was used [135,136], but with [111]. The monoclonal antibody based immunocapture ELISA is a current efforts to eradicate rinderpest worldwide, it’s no longer an valid and complex method commonly used in reference laboratories acceptable method, because interfere with the eradication global [115], the sensitivity and specificity of sandwich monoclonal based schedule [54]. Gilbert and Monnier 1962 showed cytopathic effects of ELISA on comparison to IC ELISA were 89% and 93% respectively PPRV in sheep hepatocyte and PPRV adaptation in cell culture [137]. [115]. In another study conveyed by Singh et al., 2004 the efficacy of a sandwich ELISA to detect PPR was evaluated. The result of An attenuated homologous PPR vaccine prepared in Vero cell this study indicated an acceptable sensitivity and specificity [121]. culture is available [114,138,139]. This vaccine affords protection Dot ELISA is monoclonal antibody based agonist protein M or N from natural disease for more than 1 year. The vaccinated animals and commonly used when referred samples are more than usual produce neutralizing against proteins F, H and N similar [114,116]. The sensitivity and specificity of this method are 82.5 and to animals recovered from the disease [95,140]. The first homologous 91%, respectively [114]. Antibody based detection methods include: vaccine against PPRV was 75/1 originated from lineage 1. VNT [47,18]; C-ELISA and b-ELISA [54,122,123]. The virus was isolated from a dead goat had infected with PPRV [67]. In order to minimize the severity, the virus was passaged 63 times VTN is the choice method for differentiation of PPRV and in Vero cell culture. The humoral immune response will start 7 days rinderpest virus [18,47]. ELISA is a rapid, easy to perform and after vaccination and afford 3 years protection [141]. Sungari/96 sensitive serologic method for PPR screening. C-ELISA and vaccine is originated from lineage 4. The virus was isolated from b-ELISA are monoclonal antibody based methods [anti protein a goat at 1994 in India [142]. The isolated virus was adapted in H and antiproton N antibody] with an appropriate sensitivity and Marmoset lymphoblastoid 1395a cell line after 10 times passages. In specificity [54,121,123]. Singh et al., showed that c-ELISA were order to minimize severity, the virus was passaged 54 times in Vero sensitive and specific method 92.2% and 98.4% in comparison to cell line [141]. The other available vaccine includes Arasure 87 and VNT [121]. Molecular based techniques such as PCR, RT-PCR, and Coimbator 97 [143]. It is suggested to not use Nigeria 75/1 vaccine cDNA hybridization are very precise for PPRV diagnosis, but these in Asia region because it may also lead to mutation and increased techniques are time consuming and require specific facilities [124- virulence [144]. It’s recommended to use vaccine Sungri/96 in Asia 127]. The target gene in PPRV PCR methods includes genes P, F, M and vaccine Nigeria 75/1 in Africa [144]. Sungri 96 can be used in and N [15,126,128-131]. Detection of PPRV specific genes such as M, pregnant animals and doesn’t cause immunosuppression [12,141]. N are the base of the RT-PCR method [128,132]. Arasure 87 and Coimbator 97 are used in south India. Saravanan et Necropsy finding al., 2010 showed that all three Sungri/96, Arasure 87 and Coimbator 97 afford acceptable protection against PPR in both sheep The necrotic ulcers are found throughout the gastrointestinal and goat [143]. Although attenuated vaccines provide adequate tract and respiratory system, however, it may be found in other organs immunity, but it’s not recognizable from the natural response, so [35]. The affected animals are usually emaciated are characterized by recombinant vaccine are suggested [145]. dried secretion on the face. Necrotic lesions observed in the lower and on the adjacent gum, hard and soft palate and on the ventral Firstly recombinant rinderpest vaccine has produced by expressing surface of the tongue that extended to the . Stomatitis is protein H and F, however, this vaccine was not produced against characterized by erosions and nodules in the oral cavity and usually PPRV but the immune response occurs post PPRV exposure in goats seen at late stage of disease [133]. The nasal cavity is hyperemic with [97,146]. A recombinant Capri pox virus vaccine with expressing F serous and mucopurulent discharges. Bronchopneumonia is seen at [147] and H protein [148] can produce protection against PPRV in the end stage of disease and characterized by coughing and necrotic goats [148]. Recombinant Capri pox virus vaccine that expressing

Volume 5 • Issue 4• 1000207 • Page 4 of 8 • Citation: Zakian A, Nouri M, Faramarzian K, Sharif MT, Rezaie A, et al. (2016) Comprehensive Review on Peste Des Petits Ruminants [PPR] Disease in Ruminants and Camels: with Emphasis on Clinical Signs and Histopathological Finding. J Vet Sci Med Diagn 5:4.

doi: 10.4172/2325-9590.1000207 both F and H Proteins is used in both sheep and goats [149]. The 14. Osman NA, Rahman MEA, Ali AS, Fadol MA (2008) Rapid detection of Peste vaccinia virus vector [Modified vaccinia Ankara] expressing Peste des des Petits Ruminants (PPR) virus antigen in Sudan by agar gel precipitation (AGPT) and haemagglutination (HA) Tests.Trop Anim Health Prod 40: 363-368. petits ruminants virus F and H proteins was shown to protect goats against the disease after the administration of two doses of the vaccine 15. Shaila MS, David S, Foryth MA, Diallo A, Goatley L, et al. (1996) Geographical distribution and epidemiology of PPR . Virus Res 43: 149-153. [150]. The other produced recombinant vaccines are fowl pox virus [151] and recombinant adenovirus vector [151-154]. 16. Abraham G, Sintayehu A, Libeau G, Albina E, Roger F, et al. (2005) Antibody seroprevalences against peste des petits ruminants (PPR) virus in camels, Whether the cattle should be vaccinated to control PPR? cattle, goats and sheep in Ethiopia. Pre Vet Med 70: 51-57. Rinderpest and PPRV both belong to morbillivirus with cross 17. Felix N (2013) Current scenario and control initiatives for PPR at global, regional and country level according to the risk factors and socioeconomic reactivity and relatively similar immunological response and clinical impact. In Proceedings of the Second Regional Conference on Progressive feature. Rinderpest is a fatal and acute disease in cattle while in Control of Peste Des Petits Ruminants in South Asia. sheep and goat characterized as a subacute and mild disease [79]. 18. Lefevre PC, Diallo A (1990) Peste des petits ruminants. Rev SciTechnol 9: It is assumed that PPRV is the consequence of rinderpest natural 951-65. passage in sheep and goat. Seroprevalence surveys showed 19. Lefevre PCA, Diallo F, Schenkel S, Hussein G (1991) Serological evidence of seropositive case causes a humoral response against PPRV in peste des petits ruminants in Jordan. Vet Rec 128: 110. cattle and buffalo [16]. 20. Taylor WP, Busaidy S, Barrett T (1990) The epidemiology of peste des petits PPR virus in cattle is now a threat. Whether the cattle should be ruminants in the Sultanate of Oman. Vet Microbiol 22: 341-352. vaccinated to control PPR or not? However, the vaccination of cattle 21. Khalafalla AI, Saeed IK, Ali YH, Abdurrahman MB, Kwiatek O, et al. (2010) with goats and sheep is not cost beneficial. An outbreak of peste des petits ruminants (PPR) in camels in the Sudan. Acta Tropica 116: 161-165. References 22. Swai ES, Kapaga A, Tinuga D, Joshua G, Sanka P (2009) Prevalence and 1. Gargadennec L, Lalanne A (1942) La peste des petits ruminants (in French). distribution of Peste des petits ruminants virus antibodies in various districts Bull Serv Zoot Epiz Afr Occ Fr 5: 16-21. of Tanzania. Vet Res Commun 33: 927-36.

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Sarkar J, Sreenivasa BP, Singh RP, Dhar P, Bandyopadhyay SK (2003) Comparative efficacy of various chemical stabilizers on the thermostability of a live-attenuated peste des petits ruminants (PPR) vaccine. Vaccine 21: 4728-4735. 139. Singh RP, De UK, Pandey KD (2010) Virological and antigenic characterization of two peste des petits ruminants (PPR) vaccine viruses of Indian origin. Comp Immunol Microb 33: 343-353. 140. Sinnathamby G, Renukaradhya GJ, Rajasekhar M, Nayak R, Shaila MS (2001) Immune responses in goats to recombinant hemagglutinin- Author Affiliations Top neuraminidase glycoprotein of peste des petits ruminants virus: Identification of a T-cell determinant. Vaccine 19: 4816-4823. 1Department of Clinical Sciences, College of Veterinary Medicine, Shahid Chamran University of Ahvaz, Iran 141. Sreenivasa BP, Dhar P, Singh RP, Bandyopadhyay SK (2002) Development 2Department of Clinical Sciences, College of Veterinary Medicine, of peste des petits ruminants (PPR) challenge virus from a field isolate. XIV Islamic Azad University, Garmsar Branch, Semnan, Iran Annual Conference and National Seminar on Management of Viral Diseases with Emphasis on Global Trade and WTO Regime of Indian Virological 3Department of Pathobiology, College of Veterinary Medicine, Shahid Society. Chamran University of Ahvaz, Iran 4 142. Couacy-Hymann ERF, Bidjeh K, Angba A, Domenech J, Diallo A (1995) Department of Internal Medicine, College of Veterinary Medicine, Protection of goats against rinderpest by vaccination with attenuated peste University of Tehran, Iran des petits ruminants virus. Res Vet Sci 59: 106-109 143. Saravanan P, Sena, A, Balamurugan V, Rajak KK, Bhanuprakash V, et al. (2010) Comparative efficacy of peste des petits ruminants (PPR) vaccines. Submit your next manuscript and get advantages of SciTechnol Biologicals 38: 479-485 submissions 144. Sen A, Saravanan P, Balamurugan V, Rajak KK, Sudhakar SB, et al. (2010) ™™ 50 Journals Vaccines against peste des petits ruminants virus. Expert Rev Vaccines 9: ™™ 21 Day rapid review process 785-796. ™™ 1000 Editorial team ™™ 2 Million readers 145. Balamurugan V, Hemadri D, Gajendragad MR, Singh RK, Rahman H (2014) ™™ Publication immediately after acceptance Diagnosis and control of peste des petits ruminants: a comprehensive ™™ Quality and quick editorial, review processing review. Virus Dis 25: 39-56. 146. Das SC, Baron MD, Barrett T (2000) Recovery and characterization of a chimeric rinderpest virus with the glycoproteins of peste-des-petits- Submit your next manuscript at ● www.scitechnol.com/submission ruminants virus: Homologous F and H proteins are required for virus viability. ‎J Virol 74: 9039-9047.

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