Oliver Angus Garden, BSc BVetMed PhD
Philadelphia, PA 19104
BS (Pharmacology with Basic Medical Sciences )
King's College London, UK, 1990.
BVetMed (Veterinary Medicine (distinction in Medicine))
Royal Veterinary College, UK, 1993.
PhD (Gastrointestinal Immunology)
Royal Veterinary College, UK, 1998.
Description of Clinical Expertise
Oliver A. Garden, BVetMed, PhD, joined Penn Vet in 2016 as chair of the Department of Clinical Sciences and Advanced Medicine. He was named the Henry and Corinne R. Bower Professor of Medicine. Oliver graduated from the Royal Veterinary College (1993) after earning his Bachelor of Science degree from King’s College London (1990). Following a rotating internship in small animal medicine and surgery, he completed a Wellcome Trust Clinical PhD program in small animal gastroenterology and immunology at the Royal Veterinary College (1998), followed by a Wellcome Trust Research training fellowship at the School of Medicine at the University of South Carolina. He completed a residency in small animal internal medicine at Cornell University.His particular clinical interests include gastrointestinal and immune-mediated disease, on which he has contributed chapters to two widely read textbooks in the field.
Oliver is the Principal Investigator of the Garden & Luo Immune Regulation Laboratory . He is also involved in the teaching and supervision of both interns and residents in the Matthew J. Ryan Veterinary Hospital , having contributed to the training of 43 interns and 58 residents over the years at his previous academic home, the Royal Veterinary College. He has lectured to veterinarians and veterinary nurses in the UK, USA and Asia – both general practitioners and specialists. Oliver has also been an invited speaker at the Penn Vet Annual Conference, the 2018 American College of Veterinary Pathologists Conference in Washington DC, and numerous American College of Veterinary Internal Medicine Forums and European College of Veterinary Internal Medicine Congresses ─ and other veterinary and immunological conferences ─ over the past 25 years. Oliver is the recipient of the 2017 Kennel Club International Canine Health Award for excellence in clinical research.
Current research in the Garden & Luo Immune Regulation Laboratory focuses on the role of regulatory cells of lymphoid and myeloid origin in the pathogenesis of cancer and autoimmune disease, particularly myasthenia gravis and other antibody-mediated diseases. The laboratory is also interested in the role that regulatory T cells and myeloid-derived suppressor cells play in the development and progression of lymphoma in dogs. Dogs make excellent large animal models of various human cancers, recapitulating the human disease in a spontaneous manner that cannot be captured in genetically modified murine models.
Description of Research ExpertiseGARDEN & LUO IMMUNE REGULATION LAB
Professor Oliver Garden oversees the Garden & Luo Immune Regulation Laboratory at the School of Veterinary Medicine at the University of Pennsylvania, Philadelphia, and specializes in cellular immunology, with a specific expertise in regulatory T cell (Treg) and myeloid-derived suppressor cell (MDSC) biology. Oliver started his laboratory with the aid of a Wellcome Trust Advanced Fellowship in 2001 within the Department of Immunology, Imperial College London, Hammersmith Campus, following post-doctoral training at the University of South Carolina School of Medicine and a Residency in Small Animal Internal Medicine at Cornell University College of Veterinary Medicine.
Oliver Garden's team comprises clinical and research staff, including veterinarians, doctoral candidates, post-doctoral fellows, research assistants, interns, residents, and students. Current Staff includes Dr. Jie Luo, Dr. Julia Ying Wu, Mr. Brandon Lawson, Ms. Sabina Hlavaty, as well as several undergraduate student workers. Alumni include Dr. Michelle Goulart, Mr. Michael Denyer, Dr. Dammy Pinheiro, Dr. James Swann, and Mr. Luca Fortuna. To date, six PhD students, five BSc students and 14 MSc students have successfully graduated following projects carried out within Oliver’s laboratory. Of the MSc students, ten gained Distinctions for their projects and all but two have completed – or are currently completing – successful PhD projects. Of the PhD students, all completed their theses within three or four years (depending on the program) and have carved out successful careers in research, medical practice or (in one case) patent law. Most recently, Sabina Hlavaty was awarded the Howard Hughes Medical Institute-Burroughs Wellcome Fund Medical Research Fellowship for 2018/2019.
Key expertise and funding
Key techniques for which Oliver’s laboratory has specific expertise include T cell culture, including sophisticated Treg assays in vitro; multi-colour analytical flow cytometry; ELISAs and enhanced electrochemiluminescent assays of a number of Th1 and Th2 cytokines; and molecular biological techniques, including PCR, cloning and transduction of constructs into mammalian cells.
Total extra-mural grant income since 2003 has been ≈ $2.2m, including industrial sources, the Medical Research Council, Mizutani Foundation for Glycoscience, Commonwealth Scholarship Commission, Biotechnology and Biological Research Council (BBSRC), European College of Veterinary Internal Medicine (ECVIM), Italian Ministry of Health, American College of Veterinary Emergency and Critical Care (ACVECC), Wellcome Trust, and Petplan Charitable Trust (PPCT). Current funding includes grants from the PPCT and various commercial sponsors.
Delivering for industry
Oliver’s laboratory has successfully worked with seven major industrial partners over the past ten years, consistently delivering on-time and within budget – for both product-orientated projects and blue-sky research. The laboratory has a dynamic, forward-looking, innovative and committed work ethic – with an unquestionable dedication to its team members, to its academic funders and to its industrial partners.
The biennial Treg/Th Cell Symposium
Oliver has been the coordinator for a biennial series of one-day symposia "Treg: Regulatory T Cells and T Helper Cells", the first one of which (March 2012) focused on ontogeny, plasticity and clinical applications. These meetings have been organized with the help of the RVC Continuing Professional Development Unit. Six world-class speakers came to the RVC to share their research findings in March of 2012, supported by three short oral communications and a number of poster presentations by PhD students and post-doctoral scientists.
The second of these exciting symposia was held at the RVC on 25th April 2014. Speakers included Professors Joachim Schultze, Awen Gallimore, Lucy Walker and Anne Cooke, and Drs Jeff Davies and Megan MacLeod.
Two of Oliver's publications have been recognised by prestigious international awards:
(1) His review of systemic inflammatory response syndrome and sepsis, for which the first-named author is Dan Lewis, won an award for being one of the top five most downloaded publications in the Journal of Veterinary Internal Medicine in 2013, being downloaded a total of 6,372 times in this time period.
(2) His study of duodenal lesions in diet-responsive chronic enteropathy, for which the first-named author is David Walker, won a European Emesis Council / European Society of Comparative Gastroenterology award for the best gastrointestinal publication from a European research group in 2013.
Selected PublicationsWu Y, Chang, YM, Polton G, Stell AJ, Szladovits B, Macfarlane M, Peters LM, Priestnall SL, Bacon NJ, Kow K, Stewart S, Sharma E, Goulart MR, Gribben J, Xia D, Garden OA: Gene expression profiling of B cell lymphoma in dogs reveals dichotomous metabolic signatures distinguished by oxidative phosphorylation. Frontiers in oncology 10: 307. doi: 10.3389/fonc.2020.00307, 2020.
Stark AK, Davenport ECM, Patton DT, Scudamore CL, Vanhaesebroeck B, Veldhoen M, Garden OA, Okkenhaug K: Loss of phosphatidylinositol 3-kinase activity in regulatory T cells leads to neuronal inflammation. Journal of immunology Page: doi: 10.4049/jimmunol.2000043, 2020.
Swann James W, Szladovits Balazs, Threlfall Anna J, Garden Oliver A, Chang Yu-Mei, Church David B, Glanemann Barbara: Randomised controlled trial of fractionated and unfractionated prednisolone regimens for dogs with immune-mediated haemolytic anaemia. The Veterinary record 184(25): 771, Jun 2019.
Wu Y, Chang YM, Stell AJ, Priestnall SL, Sharma E, Goulart MR, Gribben J, Xia D, Garden OA: Phenotypic characterisation of regulatory T cells in dogs reveals signature transcripts conserved in humans and mice. Scientific reports 9(1): 13478. doi: 10.1038/s41598-019-50065-8, 2019.
Hlavaty SI, Chang YM, Orth RP, Goulian M, Planet PJ, Thamm DH, Punt JA, Garden OA: Bacterial killing activity of polymorphonuclear myeloid-derived suppressor cells isolated from tumor-bearing dogs. Frontiers in immunology 10: 2371. doi: 10.3389/fimmu.2019.02371, 2019.
Garden Oliver A, Kidd Linda, Mexas Angela M, Chang Yu-Mei, Jeffery Unity, Blois Shauna L, Fogle Jonathan E, MacNeill Amy L, Lubas George, Birkenheuer Adam, Buoncompagni Simona, Dandrieux Julien R S, Di Loria Antonio, Fellman Claire L, Glanemann Barbara, Goggs Robert, Granick Jennifer L, LeVine Dana N, Sharp Claire R, Smith-Carr Saralyn, Swann James W, Szladovits Balazs: ACVIM consensus statement on the diagnosis of immune-mediated hemolytic anemia in dogs and cats. Journal of veterinary internal medicine 33(2): 313-334, Mar 2019.
Goulart Michelle R, Hlavaty Sabina I, Chang Yu-Mei, Polton Gerry, Stell Anneliese, Perry James, Wu Ying, Sharma Eshita, Broxholme John, Lee Avery C, Szladovits Balazs, Turmaine Mark, Gribben John, Xia Dong, Garden Oliver A: Phenotypic and transcriptomic characterization of canine myeloid-derived suppressor cells. Scientific reports 9(1): 3574, Mar 2019.
Swann James W, Garden Oliver A, Fellman Claire L, Glanemann Barbara, Goggs Robert, LeVine Dana N, Mackin Andrew J, Whitley Nathaniel T: ACVIM consensus statement on the treatment of immune-mediated hemolytic anemia in dogs. Journal of veterinary internal medicine 33(3): 1141-1172, May 2019.
Pittaway Rachel, Wu Ying, Szladovits Balazs, Suárez-Bonnet Alejandro, Scurrell Emma J, Garden Oliver A, Polton Gerry, Priestnall Simon L: Diagnosis of anaplastic large-cell lymphoma in a dog using CD30 immunohistochemistry. Journal of veterinary diagnostic investigation : official publication of the American Association of Veterinary Laboratory Diagnosticians, Inc 30(3): 455-458, May 2018.
Davies O, Szladovits B, Polton G, Garden O A, Leo C, Lara-Garcia A: Prognostic significance of clinical presentation, induction and rescue treatment in 42 cases of canine centroblastic diffuse large B-cell multicentric lymphoma in the United Kingdom. Veterinary and comparative oncology 16(2): 276-287, Jun 2018.
Lowrie M, Garden O A, Hadjivassiliou M, Sanders D S, Powell R, Garosi L: Characterization of Paroxysmal Gluten-Sensitive Dyskinesia in Border Terriers Using Serological Markers. Journal of veterinary internal medicine 32(2): 775-781, Mar 2018.
Marconato, L, Polton, G, Sabattini, S, Dacasto, M, Garden, OA, Grant, I, Henrickx, T, Henriques, J, Lubas, G, Morello, E, Stefanello, D, Comazzi, S; European Lymphoma Network: Conformity and controversies in the diagnosis, staging and follow-up evaluation of canine nodal lymphoma: a systematic review of the last 15 years of published literature. Veterinary and Comparative Oncology 15(3): i-i 667-1118. doi: 10.1111/vco.12244 September 2017 Notes: Version of Record online: 14 JUL 2016 | DOI: 10.1111/vco.12244.
Gibbons N, Goulart MR, Chang Y, Efstathiou K, Purcell R, Wu Y, Peters L M, Turmaine M, Szladovits B, Garden OA: Phenotypic heterogeneity of peripheral monocytes in healthy dogs. Veterinary Immunology and Immunopathology 190: 26-30. doi: 10.1016/j.vetimm.2017.06.007, Aug 2017.
Heaps LA, Scudder CJ, Lipscomb VJ, Steinbach SMl, Priestnall SL, Martineau H, Szladovits B, Fowkes RC, Garden OA: Serum anti-Müllerian hormone concentrations before and after treatment of an ovarian granulosa cell tumour in a cat. Journal of Feline Medicine and Surgery Open Reports 3(2): 2055116917722701. doi: 10.1177/2055116917722701, Aug 2017.
Comazzi, S, Avery, PR, Garden, OA, Riondato, F, Rütgen, B, Vernau, W; European Lymphoma Network: European canine lymphoma network consensus recommendations for reporting flow cytometry in canine hematopoietic neoplasms. Cytometry B Clinical Cytometry 92(5): 411-419. doi: 10.1002/cyto.b.21382 September 2017.
Lowrie M, Hadjivassiliou M, Sanders DS, Garden OA.: A presumptive case of gluten sensitivity in a border terrier: a multisystem disorder? Veterinary Record 179(22): 573. doi: 10.1136/vr.103910, December 2016
Carney K, Chang YR, Wilson S, Calnan C, Reddy PS, Chan WY, Gilmartin T, Hernandez G, Schaffer L, Head SR, Morley J, de Mestre A, Affleck K, Garden OA: Regulatory T-cell-intrinsic amphiregulin is dispensable for suppressive function. The Journal of Allergy and Clinical Immunology 137(6): 1907-1909.doi: 10.1016/j.jaci.2016.01.030, Jun 2016.
Giuliano A, Swift R, Arthurs C, Marote G, Abramo F, McKay J, Thomson C, Beltran M, Millar M, Priestnall S, Dobson J, Costantino-Casas F, Petrou T, McGonnell IM, Davies AJ, Weetman M, Garden OA, Masters JR, Thrasivoulou C, Ahmed A: Quantitative Expression and Co-Localization of Wnt Signalling Related Proteins in Feline Squamous Cell Carcinoma. PLOS ONE 11(8): e0161103. doi: 10.1371/journal.pone.0161103, Aug 2016.
Singh Y, Garden OA, Lang F, Cobb BS: MicroRNAs regulate T-cell production of interleukin-9 and identify hypoxia-inducible factor-2α as an important regulator of T helper 9 and regulatory T-cell differentiation. Immunology 149(1): 74-86. doi: 10.1111/imm.12631. Sep 2016.
Peters LM, Glanemann B, Garden OA, Szladovits B.: Cytological findings of 140 bile samples from dogs and cats and associated clinical pathological data. Journal of Veterinary Internal Medicine 30(1): 123-131. doi: 10.1111/jvim.13645, Jan-Feb 2016.
Swann, JW, Woods, K, Wu, Y, Glanemann, B and Garden, OA: Characterisation of the immunophenotype of dogs with primary immune-mediated haemolytic anaemia. PLOS ONE 11(12)(12): e0168296, 2016.
Denyer MP, Pinheiro DY, Shepherd AJ* and Garden OA*: Missed, not missing: Phylogenomic evidence for the existence of avian FoxP3. PLOS ONE 11(3): e0150988 [*Dual last and corresponding authorship] March 2016.
Chang, YM, Hadox, E, Szladovits, B and Garden, OA: Serum biochemical phenotypes in the domestic dog. PLOS ONE 11(2): e0149650, February 2016.
Singh, Y, Garden, OA, Florian, L and Cobb, BS: Retroviral transduction of helper T cells as a genetic approach to study mechanisms controlling their differentiation and function. Journal of Visualized Experiments (117): doi: 10.3791/54698, Nov 4 2016.
Aguiar J, Chang YM, Garden OA: Complications of percutaneous endoscopic gastrostomy in dogs and cats receiving corticosteroid treatment. Journal of Veterinary Internal Medicine 30(4): 1008-13. doi: 10.1111/jvim.13969, July 2016.
Fortuna, L, Relf, J, Chang, YM, Hibbert, A, Martineau, HM* and Garden, OA*: Prevalence of FoxP3+ cells in canine tumours and lymph nodes correlates positively with glucose transporter 1 expression. Journal of Comparative Pathology 155(2-3): 171-180 [*Dual last authorship] 2016.
Schmitz S, Glaneman B, Garden OA,Brooks H, Chang YM, Werling D and Allenspach K: A prospective, randomized, blinded, placebo-controlled pilot study on the effect of Enterococcus faecium on clinical activity and intestinal gene expression in canine food-responsive chronic enteropathy. Journal of Veterinary Internal Medicine 29(2): 533-43, Mar-Apr 2015
Swann JW, Priestnall SL, Dawson C, Chang YM, Garden OA: Histologic and clinical features of primary and secondary vasculitis: a retrospective study of 42 dogs (2004-2011). Journal of Veterinary Diagnostic Investigation 27(4): 489-96, Jul 2015.
Singh Y, Garden OA, Lang F, Cobb BS: MicroRNA-15b/16 Enhances the Induction of Regulatory T Cells by Regulating the Expression of Rictor and mTOR. Journal of Immunology 195(12): 5667-77, Dec 2015.
Lowrie, M, Garden, OA., Hadjivassiliou, M, Harvey, RJ, Sanders, DS, Powell, R, Garosi, L: The clinical and serological effect of a gluten-free diet in border terriers with epileptoid cramping syndrome. Journal of Veterinary Internal Medicine 29(6): 1564-8, 2015.
Anfinsen, KP, Piercy, RJ, Massey, C, Smith, KC, Kenny, PJ, Garden, OA: Severe systemic calciphylaxis in a young cat. Journal of Veterinary Internal Medicine 28(4): 1325-30, 2014.
Ferreira C, Palmer D, Blake K, Garden OA, Dyson J: Reduced regulatory T cell diversity in NOD mice is linked to early events in the thymus. Journal of Immunology 192(9): 4145-52, May 2014.
Pinheiro D, Chang YM, Bryant H, Szladovits B, Dalessandri T, Davison LJ, Yallop E, Mills E, Leo C, Lara A, Stell A, Polton G, Garden OA: Dissecting the regulatory microenvironment of a large animal model of non-Hodgkin lymphoma: evidence of a negative prognostic impact of FOXP3+ T cells in canine B cell lymphoma. PLOS ONE 9(8): e105027, 2014.
Hardy JI, Hendricks A, Loeffler A, Chang YM, Verheyen KL, Garden OA, Bond R: Food-specific serum IgE and IgG reactivity in dogs with and without skin disease: lack of correlation between laboratories. Veterinary Dermatology 25(5): 447-e70, Oct 2014.
Walker, D, Knuchel-Takano, A, McCutchan, A, Chang, YM, Downes, C, Miller, S, Stevens, K, Verheyen, K, Phillips, AD, Miah, S, Turmaine, M, Hibbert, A, Steiner, JM, Suchodolski, JS, Mohan, K, Eastwood, J, Allenspach, K, Smith, K, Garden, OA: A comprehensive pathological survey of duodenal biopsies from dogs with diet-responsive chronic enteropathy. Journal of Veterinary Internal Medicine 27(4): 862-74, 2013.
Kidder Dana, Richards Hannah E, Ziltener Hermann J, Garden Oliver A, Crocker Paul R: Sialoadhesin ligand expression identifies a subset of CD4+Foxp3- T cells with a distinct activation and glycosylation profile. Journal of Immunology 190(6): 2593-602, Mar 2013.
Lawrence Jennifer, Chang Yu-Mei Ruby, Szladovits Balazs, Davison Lucy J, Garden Oliver A: Breed-specific hematological phenotypes in the dog: a natural resource for the genetic dissection of hematological parameters in a mammalian species. PLOS ONE 8(11): e81288, 2013.
Soond, D. R., Garcon, F., Patton, D. T., Rolf, J., Turner, M., Scudamore, C., Garden, O. A., Okkenhaug, K.: Pten loss in CD4 T cells enhances their helper function but does not lead to autoimmunity or lymphoma. Journal of Immunology 188(12): 5935-43, June 2012.
Schmitz, S, Garden, OA, Werling, D, Allenspach, K: Gene expression of selected signature cytokines of T cell subsets in duodenal tissues of dogs with and without inflammatory bowel disease. Veterinary Immunology and Immunopathology 146(1): 87-91, 2012.
Singh, Y, Dyson, J, Garden, OA: Use of SNARF-1 to measure murine T cell proliferation in vitro and its application in a novel regulatory T cell suppression assay. Immunology Letters 140(1-2): 21-9, 2011.
Kathrani, A, Schmitz, S, Priestnall, SL, Smith, KC, Werling, D, Garden, OA, Allenspach, K: CD11c+ cells are significantly decreased in the duodenum, ileum and colon of dogs with inflammatory bowel disease. Journal of Comparative Pathology 145(4): 359-66, 2011.
Bailey, S, Benigni, L, Eastwood, J, Garden, OA, McMahon, L, Smith, K, Steiner, JM, Suchodolski, JS, Allenspach, K: Comparisons between cats with normal and increased fPLI concentrations in cats diagnosed with inflammatory bowel disease. Journal of Small Animal Practice 51(9): 484-9, Sept 2010.
Pinheiro, D, Singh, Y, Grant, CR, Appleton, RC, Sacchini, F, Walker, KR, Chadbourne, AH, Palmer, CA, Armitage-Chan, E, Thompson, I, Williamson, L, Cunningham, F, Garden, OA: Phenotypic and functional characterization of a CD4(+) CD25(high) FOXP3(high) regulatory T-cell population in the dog. Immunology 132(1): 111-22, Jan 2011.
Gajanayake, I, Priestnall, SL, Benigni, L, English, K, Summers, BA, Garden, OA: Paraneoplastic hypercalcemia in a dog with benign renal angiomyxoma. Journal Veterinary Diagnostic Investigation 22(5): 775-80, 2010.
Singh, Y, Ferreira, C, Chan, AC, Dyson, J, Garden, OA: Restricted TCR-alpha CDR3 diversity disadvantages natural regulatory T cell development in the B6.2.16 beta-chain transgenic mouse. Journal of Immunology 185(6): 3408-16, 2010.
Allenspach, K, House, A, Smith, K, McNeill, FM, Hendricks, A, Elson-Riggins, J, Riddle, A, Steiner, JM, Werling, D, Garden, OA, Catchpole, B, Suchodolski, JS: Evaluation of mucosal bacteria and histopathology, clinical disease activity and expression of Toll-like receptors in German shepherd dogs with chronic enteropathies. Veterinary Microbiology 146(3-4): 326-35, Dec 2010.
Carlucci, F, Fossati-Jimack, L, Dumitriu, IE, Heidari, Y, Walport, MJ, Szajna, M, Baruah, P, Garden, OA, Cook, HT, Botto, M: Identification and characterization of a lupus suppressor 129 locus on chromosome 3. Journal of Immunology 184(11): 6256-65, June 2010.