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«Turkey arthritis reovirus: pathogenesis and immune response A DISSERTATION SUBMITTED TO THE FACULTY OF UNIVERSITY OF MINNESOTA BY Tamer Sharaf Eldin ...»

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Turkey arthritis reovirus: pathogenesis and immune response

A DISSERTATION

SUBMITTED TO THE FACULTY OF

UNIVERSITY OF MINNESOTA

BY

Tamer Sharaf Eldin

IN PARTIAL FULFILLMENT OF THE REQUIREMENTS

FOR THE DEGREE OF

DOCTOR OF PHILOSOPHY

Advisors: Drs. Robert E. Porter and Sagar M. Goyal January 2015 ©Tamer Sharaf Eldin 2015 Acknowledgements First, I would like to thank “God”, the creator for his blessings and for granting me the capability to achieve success in my life.

Second, I would like to express my deepest gratitude to my mentors (Dr. Robert Porter and Dr. Sagar Goyal) for their endless sincere support, care and encouragement. Their support started in 2009 when I came to Minnesota on a research training grant (ParOwn).

They helped me with my application to the graduate school and subsequently to get the required funds for my PhD study and research. They gave me all the facilitites to conduct my research and to publish it. They supported me with the healthy environment of work and regular fruitful discussions. They enabled me to present my research in five national and international conferences. I learned many things from them not only in science but also by their wise actions and sincere advice. I can say that they helped me to be more skillful in communication, self organization and positive thinking.

I am also very grateful to my thesis advisory committee (Dr. Kent Reed, Dr. Sally Noll and Dr. Zheng Xing) for their supportive effort that was crucial in the successful completion of this thesis work. They had open doors for me all the time and they provided the valuable guidance that smotthed all the bumpy roads. I never had any struggle to meet with any of them or to hold a committee meeting because of their sincere cooperation.

I owe too much to my colleagues in Dr. Goyal’s laboratory namely Sunil Kumar, Harsha Verma, Aschalew Bekele, Mostafa Youssif, Liliya Ismagilova, Johnathan Erber, Hamada Aboubakr and Nader Yacoob. Their help was priceless and enabled me to finish the huge amount of my reseasch work that included five experiments, 900 birds and thousands of samples that needed much time and effort to process them and analyze their results.

I am very thankful to Dr. Jack Rosenberger for his help and cooperation. I thank also the virology and serology laboratories at the Minnesota Veterinary Diagnostic Laboratory (Dr. Devi Patnayak) for giving me the space to process and preserve my samples. I also thank histopathology laboratory for the huge amount of work that they did for me. I am i very grateful to Dr. James Collins, the director of the Minnesota Veterinary Diagnostic Laboratory.

I express my appreciation and gradtitude to my master advisor Prof. Dr. Abd -Almoneam A. Ali. His sincere guiding supported me with the solid base of science that enabled me to face challenges in my PhD research work.

I appreciate the funding provided by the Rapid Agriculture Response Fund (RARF), University of Minnesota which to conduct my research.

I express my love to my sincere wife “Hadia Mohammad” for her endless love and care which inspired me to face hardships in this life. I would like to thank her for her gifts to me (Mohammad and Hadi). I also thank my father (Ahmed Sharafeldin) for raising me and taking care of me after my mother passed away in 1991. Without his support and kindness, I would not have reached this success.

Finally, I would like to thank the Egyptian people whose money supported the expenses of my PhD. The money that was paid to cover my study would have changed the lives of many of them. I owe them too much and I hope I will be able to pay you back in the future.

–  –  –

In 2011, turkey reoviruses were isolated from tendons and synovial fluids of 15-weekold lame turkeys displaying swollen joints and occasionally ruptured leg tendons in Midwest, USA. These reoviruses were tentatively called turkey arthritis reoviruses (TARV) to differentiate them from reoviruses isolated from intestinal contents and feces of turkeys namely turkey enteric reoviruses (TERV). TARV were found to be genetically distinct from chicken arthritis reoviruses (CARV). Five experiments were conducted to test the pathogenicity of TARV in turkeys and in chickens and to compare it with that of TERV and CARV. Additionally, this work investigated the virus pathogenesis and cytokine immune responses. TARV showed unique capability to induce significantly higher tenosynovitis scores in turkeys as compared with TERV and CARV which induced minimal scores. Clinical lameness was first displayed at 8 weeks of age in TARV-inoculated turkeys at 1 week of age. Lameness in infected group reached approximately 50% at 16 weeks of age. TARV did not induce any lesions in chickens via intratracheal or oral route. TARV inoculation via footpad route induced tenosynovitis in chickens at 2 and 3 weeks PI with no clinical lameness. In pathogenesis study, TARV displayed the greatest replication in intestines and bursa of Fabricius than in leg tendons of turkeys. Viral infection mediated effective antiviral cytokines immune response that limited virus replication in the intestines. Furthermore, viral infection mediated a significantly elevated T helper-1(Th1) cytokine response in intestines and tendons and minimal Th2 and Th17 cytokine response during the early stage (2 weeks) of infection.





This work established an experimental model to study TARV which provides early end points that are indicative of disease pathogenicity. Additionally this work developed a new grading system for histologic tenosynovitis which can be used in a wide variety of experimental models. For lameness evaluation in turkeys, this work developed a grading system for gait scores. In summary, this work showed unique pathogenicity of the newly isolated TARV and added significant knowledge to TARV pathogenesis and immune response using the newly established reproducible experimental model and the newly developed grading systems for evaluation of tenosynovitis and clinical lameness.

iv

Table of Contents Page

Acknowledgements……………………………………………………………….............i Dedication………………………………………………………………………...............iii Abstract………………………………………………………………………………...…iv Table of contents………………………………………………………………………….v List of Tables…………………………………………………..…………………………vi List of Figures…………………………………………………...…………...…………..vii Chapter 1: Introduction, objectives and literature review……………………………......1 Chapter 2: The role of avian reoviruses in turkey tenosynovitis/arthritis...……………..35 Chapter 3: Experimentally induced lameness in turkeys inoculated with a newly emergent turkey reovirus…………….………………………………………………….….60 Chapter 4: Biomechanical properties of gastrocnemius tendons of TARV-infected turkeys…………………………………………………………..……….………80 Chapter 5: Immunopathogenesis of a newly emergent turkey arthritis reovirus in turkeys…………………………………………………………………………...96 Chapter 6: Pathogenicity of turkey arthritis reoviruses in chickens…………………....116 Chapter 7: General Discussion and Conclusions…………………..……………...……131 References…………………………………………………………….…..………….....138

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Table 1.2.

Structure and biology of mammalian and avian orthoreoviruses………..…...19 Table 2.1. Presence of lameness and swollen joints in turkey poults (Experiment 1…....57 Table 2.2. Detection of reovirus by RT-PCR in tissues of turkey poults (Experiment 1).58 Table 2.3. Detection of reovirus by RT-PCR in tissues of turkey poults (Experiment 2).59 Table 3.1. Newly developed six-point (0-5) gait scoring system for turkeys……..…....79 Table 4.1: Tensile strength and elasticity of gastrocnemius tendon at different time points after infection..………………….………………………………………..95 Table 5.1. List of cytokine genes and their primers.…….……………………………..115 Table 6.1.

Virus detection by turkey reovirus specific rRT-PCR….…….……….……130

–  –  –

Figure 2.1.

Gastrocnemius tendon histologic inflammation scoring…………………...50 Figure 2.2.

Gastrocnemius tendon histologic scoring scale for synovium……………..51 Figure 2.3.

Gastrocnemius tendon histologic scoring scale for subsynovium………….52 Figure 2.4.

Additional histologic features in gastrocnemius tendon subsynovium…….53 Figure 2.5. Turkeys with swollen hock joints at 3 weeks PI (Experiment 1)…………..54 Figure 2.6. Gastrocnemius tendon histologic inflammation scores at 4 weeks PI in different groups regardless of route of inoculation……..……………………...55 Figure 2.7. Gastrocnemius tendon histologic inflammation scores for all routes of inoculation at 4 weeks PI….…………………………………………………..56 Figure 3.1.

Average gait scoring system at different time points……..………….…....72 Figure 3.2. Percentage of lame birds in infected and non-infected control groups…...73 Figure 3.3.

Hemorrhage at the site of ruptured tendon. ……………..………….…….74 Figure 3.4.

Average of histologic inflammation scores in gastrocnemius tendon sheath

Figure 3.5.

Lesion progression in infected birds from 4 to 16 weeks of age…...…....76 Figure 3.6.

Correlation coefficient between gastrocnemius tendon histologic inflammation score and gait score. …..…………………………………........77 Figure 3.7.

Average body weights at different time points…...………….……….…..78 Figure 4.1.

The midsection of the gastrocnemius tendon was cut as shown to create a predetermined region for measuring tendon failure..………………………...90

–  –  –

apparatus……………………………………………………………….…….91 Figure 4.3.

A) Stress/strain curve in 16-week-old turkeys. B) Stress/strain curves of infected versus non infected control (16 weeks of age)…………………..….92 Figure 4.4.

Development of histologic lesions from 4 to 16 week-old with special Mason Trichrome stainig……………………………..……………………………...93 Figure5.1. Histologic inflammation in gastrocnemius tendon at 14 dpi……………109 Figure5.2. The virus gene copy number in different tissues at different time points post inoculation….……………………………………………………………….110 Figure 5.3. Fold change in antiviral cytokines (IFN-α and IFN-β) and antiinflammatory IL-10………………………………………………………………………...111 Figure 5.4.

Fold change in proinflammatory cytokines (IL-6 and TNFα) and IL-2..113 Figure 5.5.

The fold changes in Th1, Th2 and Th17 cytokines…………………….114 Figure 6.1.

Calculation of histologic inflammation score for each bird……………127 Figure 6.2. TARV-O’Neil gastrocnemius tendinitis (T) and tenosynovitis (TS) in chickens (2 weeks PI, footpad route).………………………………………128 Figure 6.3.

Histologic inflammation scores of gastrocnemius tendon and sheath..…129

–  –  –

Avian reovirus was first isolated from the respiratory tract of chickens displaying chronic respiratory disease (Fahey and Crawley, 1954). Fahey-Crawley strain of reovirus induced respiratory disease, liver necrosis, and tenosynovitis in experimentally inoculated chickens (Petek et al., 1967). The first clinical case of viral tenosynovitis/arthritis in Mycoplasma synoviae-negative chickens in USA was reported in 1968 (Olson and Solmon, 1968). Since then, several studies have described reovirus as the causative agent of tenosynovitis/arthritis in chickens (Rosenberger, 2003; Jones, 2000; van der Heidi, 1977).

Experimental inoculation of avian reovirus in specific-pathogen-free (SPF) chickens through different inoculation routes resulted in viremia with systemic distribution of the virus to respiratory, enteric, and reproductive organs in addition to hock joints and tendons (Menendez et al., 1975). The incubation period of avian reovirus varies based on age and breed of the infected bird and with the strain of virus (Robertson and Wilcox, 1986; Sterner et al., 1989).

Mucosal IgA induced by vaccination or maternally derived IgG can protect ‘in contact’ birds from acquiring infection from reovirus-challenged birds (Juerissen et al., 2000).

Additionally, avian reoviruses that had higher multiplication rates induced significantly higher production of IL-6, IL-10 and INF-γ compared with reoviruses exhibiting a lower rate of multiplication (Shen et al., 2014).

In turkeys, association of turkey reoviruses with poult enteritis has been the subject of several reports (Lojkic et al., 2010; Mor et al., 2013a; Clavert, 2012; Jindal et al., 2009;

Jindal et al., 2010; Woolcock and Shivaprasad, 2007). Reovirus has also been isolated from joints and ruptured tendons of turkeys displaying tenosynovitis/arthritis (Levisohn et al., 1980; Page et al., 1982). However, experimental infection with turkey reoviruses failed to reproduce tenosynovitis/arthritis in turkeys (Al-Afaleq & Jones, 1989).



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