염증성 질환이 있는 야생 조류에서 혈청 아밀로이드 A의 진단 지표로써의 평가 = Evaluation of Serum Amyloid A as a Diagnostic Marker in Wild Birds with Inflammatory Disease

다국어 초록 (Multilingual Abstract)

Wild birds are exposed to direct killing by human activities, as well as indirect threats from humans, ranging from environmental pollution, habitat destruction, and climate change. This study aimed to identify the most damaging problems for free-ranging birds and the trends in their injuries and diseases, by analyzing the records of birds rescued from the Jeonbuk Wildlife Center in South Korea. Medical data, including species, date and region of rescue, cause of admission, diagnoses, husbandry and treatment records, and outcomes, were collected from January 2019 to February 2021. A total of 1,464 birds belonging to 106 species were included.
The two most frequent causes of admission were healthy orphans and window collisions. The number of admissions due to anthropogenic causes was 43.6%; however, it reached 80% when the considering factors were estimated to be caused by humans. A total of 71% of the diagnoses were associated with trauma, which was much higher than 51% of the causes expected to be traumatic. Inflammatory diseases were found in 82% of the examined birds, regardless of the cause of admission. A total of 82% of the diagnoses were inflammatory diseases, which was also much higher than the 57% expected rescue due to inflammation. This was because the nature of wild animals that hide illness and the inflammatory state was difficult to detect sensitively by general physical examination.
To assess the exact condition of the patient, serum amyloid A (SAA), the main acute-phase protein in birds, was evaluated. Due to the lack of reports on the stability of evaluation of avian SAA samples, changes according to the storage period and repeated freezing-thawing cycles were observed. Seven plasma samples from two species, and six plasma samples from three species stored at -20°C were used for storage period and freezing cycles, respectively. An anti-chicken SAA ELISA kit (Eaglebio, Amherst, NH, USA) was used for measurement. For statistical analysis, the Kruskal-Wallis test and Spearman’s correlation coefficient were applied using SPSS V27 (IBM SPSS, Armonk, NY, USA). Statistical significance was set at P < 0.05.
The daily SAA concentrations measured for 30 days did not show a statistically significant difference. Freezing and thawing were repeated five times in total, and a significant negative relationship was confirmed as the number of times increased (r = -0.8857, p <0.05). Although no specific number of cycles showed a statistically significant decrease, a decrease greater than 10%, the CV value of the ELISA kit, was observed in 4 samples out of 6 at the 4th cycle. One to three freeze-thaw cycles were not expected to result in any critical reduction; however, it was recommended to avoid repeating as much as possible.
The application of serum amyloid A (SAA) to diagnose inflammation in birds has been studied; however, information on the extent of disease-related increase in the large number of wild birds is not yet available. In this study, the value of SAA as a diagnostic marker was evaluated based on disease severity.
A total of 291 samples from 139 birds of six avian species were analyzed. All samples were divided into four groups (severe inflammation, moderate inflammation, mild problem, clinically healthy) based on clinical and/or histopathological examinations and evaluated by group. SAA was measured using an anti-chicken SAA ELISA kit, and leukocyte counts, albumin concentrations, and albumin/globulin ratios were compared. The difference among groups was evaluated using the Kruskal-Wallis test followed by a post-hoc test using the Dunn’s multiple comparisons with SPSS V27. Statistical significance was set at P < 0.05.
The mean concentration and standard deviation (ng/ml) of SAA in each group were 94.66 ± 75.16, 39.05 ± 33.78, 12.76 ± 10.56, and 5.96 ± 8.07 respectively. There was a significant difference in mean levels between groups (H (3)=193.713, p <0.001), and the results were the same when analyzed by each species. The more severe the classification level according to disease, the higher SAA level and WBC counts, and the lower albumin and A/G ratio. All four indices showed significant difference of mean between groups (p < 0.001).
The SAA showed drastic changes reflecting the treatment response or preceding the onset of clinical symptoms when it was measured periodically, confirming that SAA in wild birds can be used to detect asymptomatic disease or to evaluate positive responses to treatment. Along with white blood cells, albumin, and the A/G ratio, SAA is thought to be helpful in accurately identifying current health status. Since the study was conducted on clinical patients who were rescued from the wildlife center, the frequency of inflammation due to trauma was high, and a long-term evaluation in many birds was difficult to perform. We hope that this will be carried out in future studies.

국문 초록 (Abstract)

야생 조류는 환경오염, 서식지 파괴, 기후변화 등 인간의 간접적인 위협 외에도 인간 활동에 의한 직접적인 죽음에 노출되어 있다. 본 연구는 한국의 전북야생동물센터에서 구조된 조류의 기록을 분석하여, 자유롭게 서식하는 야생 조류에게 가장 피해를 주는 문제와 부상 및 질병의 경향을 파악하기 위해 수행되었다. 2019년 1월부터 2021년 2월까지 종, 구조 날짜와 위치, 입원 원인, 진단, 사육 및 치료 기록, 그리고 치료 결과를 포함하는 의료 기록을 수집하였다. 이 분석에는 106종 1,464마리의 새가 포함되었다.
가장 빈도 높은 두 개의 구조 원인은 건강한 미아와 유리창 충돌이었다. 인간에 의한 구조 원인은 43.6%로 집계되었으나, 인간에 의한 부상이나 구조로 추정되는 경우까지 고려하면 80%에 달했다. 진단의 71%는 외상과 관련이 있었고, 이는 외상으로 간주되는 구조 원인의 비율인 51%보다 매우 높은 것이었다. 구조 원인에 관계없이, 염증성 질환은 검사를 수행한 조류의 82%에서 발견되었으며, 이는 또한 염증으로 인한 구조 원인에 해당한 57%보다 훨씬 높았다. 이 것은 질병과 염증 상태를 숨기는 야생동물의 특성과, 기본적인 신체검사로는 민감하게 건강 상태를 감지하기 어려웠기 때문이다.
환자의 정확한 상태를 파악하기 위해 조류의 주요 급성기 단백질인 혈청 아밀로이드 A(SAA)를 평가하였다. 그에 앞서 조류 SAA 시료의 안정성을 평가한 보고가 부족하여, 보관 기간 및 반복되는 동결-해동 횟수에 따른 변화를 관찰하였다. 보관 기간 및 해동 횟수 평가에는 -20 °C에서 보관된 2종의 혈장 샘플 7개와, 3종의 혈장 샘플 6개가 각각 사용되었다. 측정에는 닭 전용 SAA ELISA 키트 (Eaglebio, Amherst, 뉴햄프셔 주, 미국)을 사용하였다. 통계적 분석은 SPSS V27(IBM SPSS, Armonk, 뉴욕 주, 미국)을 이용하여 수행하였고, Kruskal-Wallis 검정과 Spearman의 상관계수를 적용하였다. 0.05 미만의 p-값은 통계적으로 유의한 것으로 설정하였다.
30일 동안 매일 측정한 SAA 농도는 통계적으로 유의한 차이를 보이지 않았다. 동결-해동은 총 5회 반복하였으며, 횟수가 증가할수록 유의한 음의 관계가 확인되었다(r = -0.8857, p <0.05). 통계적으로 유의하게 농도가 감소하는 횟수는 없었으나, 6개의 시료 중 4개에서 네 번째부터 ELISA 키트의 CV값인 10% 이상 농도가 감소하는 것이 관찰되었다. 1~3회의 동결-해동 주기는 심각한 감소를 초래할 것으로 예상되지 않지만, 가능한 한 반복하지 않는 것이 추천된다.
조류에서 염증을 진단하기 위한 혈청 아밀로이드 A(SAA)의 적용은 연구되어왔지만, 아직 다수의 야생 조류에서 질병과 관련되어 증가하는 정도에 대한 정보는 없다. 본 연구에서는 염증성 질병의 중증도에 따라 진단 마커로서 SAA의 가치를 평가하였다. 조류 여섯 종(황조롱이, 집비둘기, 솔부엉이, 수리부엉이, 말똥가리, 참매)에 해당하는 139마리로부터 채집된 총 291개의 시료가 분석되었다. 모든 시료를 임상적인 검사 및/또는 조직병리학적 검사를 기반으로 4개 그룹(중증 염증, 중등도 염증, 경증 문제, 임상적 건강)으로 나누고 그룹별로 평가하였다. SAA는 닭 전용 SAA ELISA 키트로 측정하였고, 백혈구 수, 알부민 농도, 알부민/글로불린 비율과도 비교되었다. 그룹 간의 통계적 차이는 SPSS V27를 이용하여 Kruskal-Wallis 검정으로 평가하였고, 두 그룹 간의 사후 검정에는 Dunn’s 검정이 적용되었다. 0.05 미만의 p-값은 통계적으로 유의한 것으로 설정하였다.
각 그룹에서 SAA의 평균 농도와 표준편차(ng/ml)는 각각 94.66 ± 75.16, 39.05 ± 33.78, 12.76 ± 10.56, 5.96 ± 8.07이었다. 전 그룹간에 통계적으로 유의한 평균의 차이가 있었고(H (3) = 193.713, p <0.001), 각 종 별로 분석한 결과도 동일하였다. 염증성 질병과 심각도에 따른 분류 수준이 높을수록 SAA 농도와 WBC 수치가 증가하였고, 알부민과 A/G 비율이 감소하였다. 네 가지 염증 지표 모두 그룹 간에 유의한 평균 차이를 보였다(p < 0.001).
한 개체에서 주기적으로 SAA를 측정했을 때, 치료에 대한 반응을 반영하거나 임상 증상보다 앞서는 급격한 변화가 관찰되었다. 이 것으로 야생 조류에서 SAA가 무증상 상태의 질병을 진단하거나 치료에 대한 반응을 민감하게 평가하는데 사용할 수 있음을 확인하였다. 백혈구, 알부민 및 A/G 비율과 함께 SAA는 현재 건강 상태를 정확하게 식별하는 데 도움이 될 것으로 여겨진다.
이번 연구를 통해 야생동물 치료 분야의 전문가들이 미래의 조류 환자에게 더 정확한 진단과 효과적인 치료를 제공하는 데에 도움이 되길 희망한다.

목차 (Table of Contents)

• CONTENTS i
• LIST OF FIGURES v
• LIST OF TABLES vii
• ABSTRACT viii
• Part Ⅰ. Retrospective Analysis of Inflammatory Diseases and Admission Causes in Rescued Wild Birds 1
• Introduction 2
• Materials and Methods 4
• 1. Data collection 4
• 2. Admission cause 4
• 3. Diagnosis 7
• Results 9
• 1. Demographic data 9
• A. Species 9
• B. Time 16
• C. Age 22
• D. Location 22
• 2. Admission cause 23
• A. Orphaned 26
• B. Malnutrition 27
• C. Infection 28
• D. Attacked 29
• E. Collision 29
• F. Trapped indoors 31
• G. Injured by man-made structures 31
• H. Traffic accident 33
• I. Poaching 34
• J. Toxicosis 34
• K. Unknown 35
• L. Other 36
• 3. Diagnosis 42
• Discussion 54
• 1. Demographic data 54
• 2. Admission cause 55
• A. Trauma/inflammation 55
• B. Admission causes 55
• 3. Diagnosis 71
• 4. Medical data recording and utilization 84
• Conclusion 86
• Part Ⅱ. Impacts of Storage Time and Repeated Freezing-Thawing on Stability of Avian Serum Amyloid A 87
• Introduction 88
• Materials and Methods 92
• 1. Animals and sample collection 92
• 2. Effect of storage time on concentration of avian SAA 92
• 3. Effect of repeated freezing and thawing on concentration of avian SAA 93
• 4. Statistical analysis 93
• Results 94
• 1. Effect of storage time on concentration of avian SAA 94
• 2. Effect of repeated freezing-thawing on concentration of avian SAA 94
• Discussion 100
• Conclusion 102
• Part Ⅲ. Diagnostic Value of Serum Amyloid A in Differentiating the Inflammatory Disorders in Birds 103
• Introduction 104
• Materials and Methods 107
• 1. Animals 107
• 2. Sample collection 107
• 3. Clinical groups 108
• 4. SAA by diseases 109
• 5. Follow-up evaluation 109
• 6. ELISA 109
• 7. Statistical analysis 110
• Results 111
• 1. Avian SAA concentrations by groups 111
• 2. SAA by disease 121
• 3. Follow-up evaluations 124
• 4. WBC, albumin, and A/G levels by groups 128
• 5. Comparison of SAA with WBC, albumin, and A/G 132
• Discussion 135
• Conclusion 141
• GENERAL CONCLUSION 142
• REFERENCES 144
• 감사의 글 158
• 국문 초록 160

참고문헌 (Reference)

1 Landman WJ , Gruys E , Gielkens AL, "Avian Amyloidosis", 27 ( 5 ) :437-49 ., 1998

2 Karl TR , Trenberth KE ., "Modern Global Climate Change", 302 ( 5651 ) :1719-1723 ., 2003

3 Jones MP, "Vascular Diseases in Birds of Prey .", 22 ( 4 ) :348-357 ., 2013

4 Cray C , Zaias J , Altman NH ., "Acute Phase Response in Animals : A Review .", 59 ( 6 ) :517-26 ., 2009

5 Blomqvist M , Christerson L , Waldenstrom J , et al ., "Chlamydia Psittaci in Birds of Prey , Sweden", 2, 2012

6 Cray C , Rodriguez M , Zaias J ., "Protein Electrophoresis of Psittacine Plasma", 36 ( 1 ) :64-72 ., 2007

7 Doherty TS , Glen AS , Nimmo DG , Ritchie EG , Dickman CR, "Invasive Predators and Global Biodiversity Loss", 113 ( 40 ) :11261- 11265, 2016

8 Eckersall PD, "The Time Is Right for Acute Phase Protein Assays", 168 ( 1 ) :3-5 ., 2004

9 Zorn SMT, "Highway Mortality of Barn Owls in Northeastern France", 32:229-232, 1998

10 Schwartz AL , Williams HF , Chadwick E , Thomas RJ , Perkins SE, "Roadkill Scavenging Behaviour in an Urban Environment", 4 ( 1 ) : juy006 ., 2018

11 Eo K-Y , Kim Y-H , Cho K-H , et al, "Infection of Avian Pox Virus in Oriental Turtle- Doves", 31 ( 4 ) :354-356 ., 2011

12 Eckersall PD, "Acute Phase Proteins as Markers of Inflammatory Lesions", 5 ( 2 ) :93-97 ., 1995

13 Kim T , Kwon Y, "Bone Fractures in Raptors in the Daegu-Gyeongbuk Region", 33 ( 5 ), 2016

14 Siembieda J , Kock R , McCracken T , Newman S., "The Role of Wildlife in Transboundary Animal Diseases .", 12 ( 1 ) :95-111 ., 2011

15 Harden J ., "An Overview of Anthropogenic Causes of Avian Mortality .", 25 ( 1 ) :4-11 ., 2002

16 Suffredini AF , Fantuzzi G , Badolato R , Oppenheim JJ , O'Grady NP, "New Insights into the Biology of the Acute Phase Response", 19 ( 4 ) :203-214 ., 1999

17 Cray C , Zielzienski-Roberts K , Bonda M , et al ., "Antemortem Diagnosis of Sarcocytosis in Psittacine Birds .", 19 ( 3 ) :208-215 ., 2005

18 Millar DJ , Hutchinson WL , Pepys MB, "Immunoradiometric Assay for Human Serum Amyloid P Component", 371 ( 1-2 ) :18-24, 2011

19 Pimm SL , Jenkins CN , Abell R , et al ., "The Biodiversity of Species and Their Rates of Extinction ,", 344 ( 6187 ) :1246752 ., 2014

20 Sleeman JM , Clark EE, "Clinical Wildlife Medicine : A New Paradigm for a New Century", 17 ( 1 ) :33-37 ., 2003

21 Nakamura M , Takahashi M , Ohno K , et al, "C-Reactive Protein Concentration in Dogs with Various Diseases", 70 ( 2 ) :127-131 ., 2008

22 Loss SR , Will T, "Marra PP . Direct Mortality of Birds from Anthropogenic Causes", 46 ( 1 ) :99-120, 2015

23 Rosenthal KL , Johnston MS , Shofer FS, "Assessment of the Reliability of Plasma Electrophoresis in Birds", 66 ( 3 ) :375-378 ., 2005

24 Choi K-S , Jeon W-J , Kye S-J , et al ., "Seroprevalance of Newcastle Disease Virus in Wild Birds in Korea", 39 ( 2 ) :97-104 ., 2012

25 Ratton P , Secco H , Da Rosa CA ., "Carcass Permanency Time and Its Implications to the Roadkill Data", 60 ( 3 ) :543-546 ., 2014

26 Nam DH , Lee DP, "Mortality Factors and Lead Contamination of Wild Birds from Korea", 178 ( 1-4 ) :161-9 ., 2011

27 Stalder S , Marti H , Borel N , Sachse K , Albini S , Vogler BR ., "Occurrence of Chlamydiaceae in Raptors and Crows in Switzerland .", ; 9 ( 9 ), 2020

28 Stone WB , Okoniewski JC , Stedelin JR ., "Poisoning of Wildlife with Anticoagulant Rodenticides in New York .", 35 ( 2 ) :187-193 ., 1999

29 Boyanton Jr BL , Blick KE, "Stability Studies of Twenty-Four Analytes in Human Plasma and Serum", 48 ( 12 ) :2242-2247 ., 2002

30 Franson JC , Hansen SP , Creekmore TE , et al, "Lead Fishing Weights and Other Fishing Tackle in Selected Waterbirds", 26 ( 3 ) :345-352 ., 2003

31 Carroll D , Wang J , Fanning S , McMahon BJ, "Antimicrobial Resistance in Wildlife : Implications for Public Health", 62 ( 7 ) :534-542 ., 2015

32 Kim S , Park M-Y , Kim H-J , et al ., "Analysis of Insecticides in Dead Wild Birds in Korea from 2010 to 2013", 96 ( 1 ) :25-30 ., 2016

33 Burton SA , Honor D , Mackenzie A , Eckersall P , Markham R , Horney BS, "C-Reactive Protein Concentration in Dogs with Inflammatory Leukograms .", 55 ( 5 ) :613-618 ., 1994

34 Allen HK , Donato J , Wang HH , Cloud-Hansen KA , Davies J , Handelsman J ., "Call of the Wild : Antibiotic Resistance Genes in Natural Environments .", 8 ( 4 ) :251-259 ., 2010

35 Lee G , Tak J-H , Pak S-I ., "Spatial and Temporal Patterns on Wildlife Road-Kills on Highway in Korea", 31 ( 4 ) :282-287 ., 2014

36 Fix AS , Barrows SZ ., "Raptors Rehabilitated in Iowa During 1986 and 1987 : A Retrospective Study", 26 ( 1 ) :18-21 ., 1990

37 Wood KA , Brown MJ , Cromie RL , et al ., "Regulation of Lead Fishing Weights Results in Mute Swan Population Recovery", 230:67-74, 2019

38 McDonald TL , Weber A , Smith JW, "A Monoclonal Antibody Sandwich Immunoassay for Serum Amyloid a ( Saa ) Protein", 144 ( 2 ) :149-155 ., 1991

39 Tatum LM , Zaias J , Mealey BK , Cray C , Bossart GD, "Protein Electrophoresis as a Diagnostic and Prognostic Tool in Raptor Medicine", 31 ( 4 ) :497-502 ., 2000

40 Medina FM , Bonnaud E , Vidal E , et al ., "A Global Review of the Impacts of Invasive Cats on Island Endangered Vertebrates", 17 ( 11 ) :3503-3510 ., 2011

41 Krogh AK , Lundsgaard JF , Bakker J , et al, "Acute-Phase Responses in Healthy and Diseased Rhesus Macaques ( Macaca Mulatta )", 45 ( 2 ) :306-14 ., 2014

42 Petersen HH , Nielsen JP , Heegaard PMH, "Application of Acute Phase Protein Measurements in Veterinary Clinical Chemistry", 35 ( 2 ) :163-187 ., 2004

43 Neese MR , Seitz J , Nuzzo J , Horn DJ, "Cause of Admittance in Raptors Treated at the Illinois Raptor Center , 1995-2006", 30 ( 2 ), 2010

44 Jensen LE , Whitehead AS, "Regulation of Serum Amyloid a Protein Expression During the Acute-Phase Response", 334 ( 3 ) :489-503 ., 1998

45 Loss SR , Will T, "Marra PP . The Impact of Free-Ranging Domestic Cats on Wildlife of the United States", 4:1396, 2013

46 Jeong J , An I , Oem JK , et al, "Molecular Prevalence and Genotyping of Chlamydia Spp . In Wild Birds from South Korea", 79 ( 7 ) :1204-1209 ., 2017

47 Horadagoda N , Knox K , Gibbs H , et al, "Acute Phase Proteins in Cattle : Discrimination between Acute and Chronic Inflammation", 144 ( 16 ) :437-441 ., 1999

48 Gatt ME , Urieli-Shoval S , Preciado-Patt L , et al, "Effect of Serum Amyloid a on Selected in Vitro Functions of Isolated Human Neutrophils", 132 ( 5 ) :414-420 ., 1998

49 Kim H-J , Chae H-Y , Park S-J , Sung H-W , Kim J-T, "The Survey on Avian Pox Infections in Migratory Birds at a Stopover Site , South Korea", 40 ( 2 ) :149-153 ., 2017

50 Gopee NV , Adesiyun AA , Caesar K., "Retrospective and Longitudinal Study of Salmonellosis in Captive Wildlife in Trinidad .", 36 ( 2 ) :284-293 ., 2000

51 Park I-C , Kim J-W , Kim J-T, "Analysis of the Wildlife Distress and Rescue of Wild Avian Animals in Gangwon Province .", 35 ( 1 ) :39-45 ., 2012

52 Rhim H , Park J-Y , Lee D-J , Han J-I ., "Epicoccum Nigrum-Induced Respiratory Infection in a Wild Eurasian Scops Owl ( Otus Scops )", 81 ( 9 ) :1348-1350 ., 2019

53 Cray C , Rodriguez M , Zaias J , Altman NH ., "Effects of Storage Temperature and Time on Clinical Biochemical Parameters from Rat Serum .", 48 ( 2 ) :202-204 ., 2009

54 Sawicka A , Durkalec M , Tomczyk G , Kursa O ., "Occurrence of Mycoplasma Gallisepticum in Wild Birds : A Systematic Review and Meta-Analysis", 15 ( 4 ) : e0231545-e0231545 ., 2020

55 Vandenplas ML , Moore JN , Barton MH , Roussel AJ , Cohen ND, "Concentrations of Serum Amyloid a and Lipopolysaccharide-Binding Protein in Horses with Colic", 66 ( 9 ) :1509-1516 ., 2005

56 Rhim H , Kim H-C , Na K-J , Han J-I, "Multidrug Resistance of Coagulase-Negative Staphylococci Isolated from Rescued Wild Animals .", 42 ( 4 ) :251-255 ., 2019

57 Cutler SJ , Fooks AR , Van der Poel WH, "Public Health Threat of New , Reemerging , and Neglected Zoonoses in the Industrialized World", 16 ( 1 ) :1 ., 2010

58 Jang J-H , Bong Y-H , Kim D-G , Kim M , Chung G-S , Son S-W, "Analysis of Residual Pesticides in Dead Wild Birds and Other Animals During 2008-2009 in Korea", 50 ( 3 ) :197-203 ., 2010

59 Ivey ES ., "Serologic and Plasma Protein Electrophoretic Findings in 7 Psittacine Birds with Aspergillosis .", 14 ( 2 ) :103-106 ., 2000

60 Jayson S , Guzman DS-M , Petritz O , Freeman K , Maggs DJ, "Medical Management of Acute Ocular Hypertension in a Western Screech Owl ( Megascops Kennicottii )", 28 ( 1 ) :38-44 ., 2014

61 Rhim H , Bae J , Kim H , Han J-I, "Prevalence and Phylogenetic Analysis of Avian Haemosporidia in Wild Birds in the Republic of Korea", 54 ( 4 ) :772-781 ., 2018

62 Hart BL , Hart LA ., "How Mammals Stay Healthy in Nature : The Evolution of Behaviours to Avoid Parasites and Pathogens .", 373 ( 1751 ) :20170205 ., 2018

63 Soler L , Gutierrez A , Martinez-Subiela S , Ceron JJ, "Development and Validation of a Novel Competitive Elisa for the Detection of Serum Amyloid a in Pigs", 190 ( 2 ) : e7-e11 ., 2011

64 Krone O , Altenkamp R , Kenntner N., "Prevalence of Trichomonas Gallinae in Northern Goshawks from the Berlin Area of Northeastern Germany", 41 ( 2 ) :304-309 ., 2005

65 Jakubowski J , Aebischer V , Luetzelschwab J , Vogel B , Donatsch P , Cordier A ., "Stability of Clinical Chemistry Parameter Values in Minipig Serum under Different Storage Conditions", 25:197-204, 1998

66 Wellehan JF , Zens MS , Calsamiglia M , Fusco PJ , Amonsin A , Kapur V., "Diagnosis and Treatment of Conjunctivitis in House Finches Associated with Mycoplasmosis in Minnesota", 37 ( 2 ) :245-51 ., 2001

67 Kurył J , Gasparska J ., "The Differences in Plasma Protein Pattern between Laying and Non-Laying Chickens , Quails and Geese .", 80 ( 2 ) :309-313 ., 1985

68 Kneeland M , Berman E , Grade T , et al ., "Plasma Biochemistry and Protein Electrophoresis Reference Intervals of the Common Loon ( Gavia Immer )", 51 ( 3 ) :561-570 ., 2020

69 Hager SB , Cosentino BJ , McKay KJ ., "Scavenging Affects Persistence of Avian Carcasses Resulting from Window Collisions in an Urban Landscape", 83 ( 2 ) :203-211 ., 2012

70 Jacobsen S , Niewold TA , Halling-Thomsen M , et al ., "Serum Amyloid a Isoforms in Serum and Synovial Fluid in Horses with Lipopolysaccharide-Induced Arthritis", 110 ( 3-4 ) :325-330 ., 2006

71 Lumeij J , De Bruijne J ., "Evaluation of the Refractometric Method for the Determination of Total Protein in Avian Plasma or Serum .", 14 ( 3 ) :441-444 ., 1985

72 Eckersall PD, "Recent Advances and Future Prospects for the Use of Acute Phase Proteins as Markers of Disease in Animals", 151:577-584, 2000

73 Jansson DS , Brojer C , Neimanis A , et al ., "Post Mortem Findings and Their Relation to Aa Amyloidosis in Free-Ranging Herring Gulls ( Larus Argentatus )", 13 ( 3 ) : e0193265 ., 2018

74 Smith WA , Mazet JAK , Hirsh DC, "Salmonella in California Wildlife Species : Prevalence in Rehabilitation Centers and Characterization of Isolates", 33 ( 3 ) :228-235 , 8 ., 2002

75 Cray C , Arheart KL , Hunt M , et al, "Acute Phase Protein Quantitation in Serum Samples from Healthy Atlantic Bottlenose Dolphins ( Tursiops Truncatus )", 25 ( 1 ) :107-111 ., 2013

76 Seo C , Thorne JH , Choi T , Kwon H , Park C-h., "Disentangling Roadkill : The Influence of Landscape and Season on Cumulative Vertebrate Mortality in South Korea .", 11 ( 1 ) :87-99 ., 2015

77 Lee S , Hwang J , Kim J , et al ., "Biofilm Production of Coagulase-Negative Staphylococci Isolated from Rescued Wild Animals in the Republic of Korea .", 61 ( 1 ) :50 ., 2019

78 MacGuire JG , Christe KL , Yee JL , Kalman-Bowlus AL , Lerche NW ., "Serologic Evaluation of Clinical and Subclinical Secondary Hepatic Amyloidosis in Rhesus Macaques ( Macaca Mulatta )", 59 ( 2 ) :168-173 ., 2009

79 Fischer D , Van Waeyenberghe L , Cray C , et al, "Comparison of Diagnostic Tools for the Detection of Aspergillosis in Blood Samples of Experimentally Infected Falcons", 58 ( 4 ) :587-598 ., 2014

80 Jang H-J , Na K-J , Rhim H , Han J-I, "High Prevalence of Avian Hematozoan Parasite Infection in Wild Owls in Chungbuk Province of Korea ( Mid-South Korea )", 40 ( 2 ) :95-99 ., 2017

81 Cray C , Watson T , Rodriguez M , Arheart KL ., "Application of Galactomannan Analysis and Protein Electrophoresis in the Diagnosis of Aspergillosis in Avian Species .", 40 ( 1 ) :64-70 ., 2009

82 Gillmore JD , Lovat LB , Persey MR , Pepys MB , Hawkins PN ., "Amyloid Load and Clinical Outcome in Aa Amyloidosis in Relation to Circulating Concentration of Serum Amyloid a Protein", 358 ( 9275 ) :24-29 ., 2001

83 Moller AP , Erritzoe H , Erritzoe J ., "A Behavioral Ecology Approach to Traffic Accidents : Interspecific Variation in Causes of Traffic Casualties among Birds", 32 ( 2 ) :115-27 ., 2011

84 Smith KA , Campbell GD , Pearl DL , Jardine CM , Salgado-Bierman F , Nemeth NM ., "A Retrospective Summary of Raptor Mortality in Ontario , Canada ( 1991-2014 ) , Including the Effects of West Nile Virus", 54 ( 2 ) :261-271 ., 2018

85 Hampel MR , Kinne J , Wernery U , Pospischil A , Kellermann J , Linke RP ., "Increasing Fatal Aa Amyloidosis in Hunting Falcons and How to Identify the Risk : A Report from the United Arab Emirates", 16 ( 3 ) :122-132 ., 2009

86 Evans M , Otter A ., "Fatal Combined Infection with Haemoproteus Noctuae and Leucocytozoon Ziemanni in Juvenile Snowy Owls ( Nyctea Scandiaca )", 143 ( 3 ) :72-76 ., 1998

87 Thoresen SI , Tverdal A , Havre G , Morberg H., "Effects of Storage Time and Freezing Temperature on Clinical Chemical Parameters from Canine Serum and Heparinized Plasma .", 24 ( 4 ) :129-133 ., 1995

88 Amery-Gale J , Legione AR , Marenda MS , et al, "Surveillance for Chlamydia Spp . With Multilocus Sequence Typing Analysis in Wild and Captive Birds in Victoria , Australia", ; 56 ( 1 ) :16-26 ., 2020

89 Cray C , Dickey M , Brewer LB , Arheart KL ., "Assessement of Serum Amyloid a Levels in the Rehabilitation Setting in the Florida Manatee ( Trichechus Manatus Latirostris )", 44 ( 4 ) :911-7 ., 2013

90 Thoresen SI , Havre GN , Morberg H , Mowinckel P., "Effects of Storage Time on Chemistry Results from Canine Whole Blood , Heparinized Whole Blood , Serum and Heparinized Plasma", 21 ( 3 ) :88-94 ., 1992

91 Loss SR , Will T, "Marra PP . Direct Human-Caused Mortality of Birds : Improving Quantification of Magnitude and Assessment of Population Impact", 10 ( 7 ) :357-364 ., 2012

92 Tsai IT , Chi CH , Yu PH . Hematologic, "Plasma Biochemical , Protein Electrophoretic , and Total Solid Values of Captive Oriental Turtle Doves ( Streptopelia Orientalis )", 57 : e11 ., 2018

93 Randall NJ , Blitvich BJ , Blanchong JA ., "Efficacy of Wildlife Rehabilitation Centers in Surveillance and Monitoring of Pathogen Activity : A Case Study with West Nile Virus", 48 ( 3 ) :646-653 ., 2012

94 Steele CM , Brown RN , Botzler RG, "Prevalences of Zoonotic Bacteria among Seabirds in Rehabilitation Centers Along the Pacific Coast of California and Washington , USA", 41 ( 4 ) :735-744 ., 2005

95 Depauw S , Delanghe J , Whitehouse-Tedd K , et al ., "Serum Protein Capillary Electrophoresis and Measurement of Acute Phase Proteins in a Captive Cheetah ( Acinonyx Jubatus ) Population", 45 ( 3 ) :497-506 ., 2014

96 Ramey AM , Ahlstrom CA ., "Antibiotic Resistant Bacteria in Wildlife : Perspectives on Trends , Acquisition and Dissemination , Data Gaps , and Future Directions", 56 ( 1 ) :1-15 ., 2020

97 Flower JE , Langan JN , Wells RS , et al, "Serum Acute-Phase Proteins in Bottlenose Dolphins ( Tursiops Truncatus ) and Correlation with Commonly Utilized Inflammatory Indices .", 51 ( 3 ) :657-662 ., 2020

98 Azmanis PN, "The Additional Diagnostic Value of Optical Coherence Tomography ( Oct ) and Its Application Procedure in a Wide Variety of Avian Species", 06 ( 03 ), 2015

99 Jacobsen S , Kjelgaard-Hansen M , Hagbard Petersen H , Jensen AL ., "Evaluation of a Commercially Available Human Serum Amyloid a ( Saa ) Turbidometric Immunoassay for Determination of Equine Saa Concentrations", 172 ( 2 ) :315-9 ., 2006

100 Yang M , Liu Y , Dai J , et al ., "Apolipoprotein a-Ii Induces Acute-Phase Response Associated Aa Amyloidosis in Mice through Conformational Changes of Plasma Lipoprotein Structure", 8 ( 1 ) :5620 ., 2018

101 Levin M , Pras M , Franklin EC, "Immunologic Studies of the Major Nonimmunoglobulin Protein of Amyloid : I . Identification and Partial Characterization of a Related Serum Component", 138 ( 2 ) :373-380 ., 1973

102 Niedringhaus KD , Fenton HMA , Cleveland CA , et al . Case Series, "Virulent Hemosporidiosis Infections in Juvenile Great Horned Owls ( Bubo Virginianus ) from Louisiana and California , USA . Veterinary Parasitology", 12:49-54, 2018

103 Molina-Lopez RA , Casal J , Darwich L., "Causes of Morbidity in Wild Raptor Populations Admitted at a Wildlife Rehabilitation Centre in Spain from 1995-2007 : A Long Term Retrospective Study", 6 ( 9 ) : e24603 ., 2011

104 Christensen M , Jacobsen S , Ichiyanagi T , Kjelgaard-Hansen M., "Evaluation of an Automated Assay Based on Monoclonal Anti-Human Serum Amyloid a ( Saa ) Antibodies for Measurement of Canine , Feline , and Equine Saa .", 194 ( 3 ) :332-7 ., 2012

105 Lee HR , Koo BS , Kim JT , et al, "Molecular Epidemiology of Avian Poxvirus in the Oriental Turtle Dove ( Streptopelia Orientalis ) and the Biting Midge ( Culicoides Arakawae ) in the Republic of Korea", 53 ( 4 ) :749-760 ., 2017

106 Anderson NL , Johnson CK , Fender S , et al, "Clinical Signs and Histopathologic Findings Associated with a Newly Recognized Protozoal Disease ( Trichomonas Gallinae ) in Free- Ranging House Finches ( Carpodacus Mexicanus )", 41 ( 2 ) :249-254 ., 2010

107 Harr KE , Rember R , Ginn PE , et al ., "Serum Amyloid a ( Saa ) as a Biomarker of Chronic Infection Due to Boat Strike Trauma in a Free-Ranging Florida Manatee ( Trichechus Manatus Latirostris ) with Incidental Polycystic Kidneys", 47 ( 4 ) :1026- 1031 ., 2011