Hemoflagellates, host-parasite relationships, and strategies against salmonid cryptobiosis
"To strive, to seek, to find, and not to yield" - Alfred Tennyson
Patrick TK Woo MSc, PhD (profile)
University Professor Emeritus
Department of Integrative Biology
University of Guelph
Guelph, Ontario, Canada N1G 2W1

Email: pwoo@uoguelph.ca
Phone: 519-824-4120 ext. 53581
Office: Room 2443, Science Complex
Laboratory: Room 2401, Science Complex

I. Parasites and their Pathobiology: (a) blood flagellates (b) diseases

II. Publications: (a) CABI books (b) reviews (c) journal papers

III. Current/Recent Research: programs and sponsors

IV. Six Selected Research Contributions

V. Presentations: (a) invited (b) contributed (c) seminars

VI. Research Collaborators: (a) associates (b) MSc and PhD students

VII. Major Editorial Activities: (a) editor, CABI books (b) editor-in-chief, The Open Parasitology Journal (c) topic editor, Diseases: Impacts on Aquaculture

I (a). Trypanosoma, Cryptobia and Spironucleus:

Patrick Woo has always focused his research on the blood flagellates (Figs. 1 - 3 & 7) including those that are of medical (Fig. 2) and economic importance (Figs. 3 & 7). His early research was mainly on trypanosomes (Figs. 1 & 2), and on mammalian trypanosomiases which involved field studies in Africa (e.g. Figs. 4 - 6).

Fig. 1: Trypanosoma rotatorium in the blood of Rana pipiens Fig. 2: Trypanosoma b. rhodesiense in the blood of Homo sapiens Fig. 3: Spironucleus sp. in the blood of Oncorhynchus tschawytscha

He and his students have also concentrated their efforts on Cryptobia (Trypanoplasma) salmositica (Fig. 7) and cryptobiosis (Figs. 8 - 10). The parasite has been recorded from all species of Pacific salmon (Oncorhynchus spp.) on the west coast of North America, and it is normally transmitted by the freshwater leech (Piscicola salmositica) in streams and rivers. Some of his major research contributions have been on mammalian trypanosomiasis and on salmonid cryptobiosis.
Another of his project is on systemic spironucleosis, and outbreaks of the disease have been reported in salmonids in sea cages in Canada and Norway. Spironucleus (Fig. 3) is morphologically similar to the intestinal Hexamita. The pathogen is transmitted directly between fish, and it is in the blood, in internal organs, and in ulcers on the body surface (Figs. 3 & 11 - 13).

I (b). Diseases: Trypanosomiasis, Cryptobiosis and Spironucleosis

Human Trypanosomiasis

Fig. 4: Human trypanosomiasis, EATRO (Trypanosoma b. gambiense) Fig. 5: Hematocrit Centrifuge Technique, human trypanosomiasis survey, SRI Fig. 6: Bovine trypanosomiasis, EATRO (Trypanosoma congolense)
One of his contributions on human trypanosomiasis was the description of the Hematocrit Centrifuge Technique (HCT; Woo, 1969), and its use in hospitals to detect trypanosomes (Fig. 2) in the blood and cerebral spinal fluid of patients with African trypanosomiasis (Woo, 1970). The HCT was later adapted for use under field conditions (Woo, 1971), and this rapid and simple-to-use technique " . . . is still in use in many HAT [Human African Trypanosomiasis] control programs" (Chappuis et al., 2005). Since it is a sensitive technique (Woo & Rogers, 1974) it is also " . . . widely used for the diagnosis of animal trypanosomiasis" (Schlater & Van Den Bossche, 2004).
The HCT is sometimes called the "Woo test" (Chappuis et al., 2005) , or "Woo technique" (Quispe et al., 2003) , or "Woo method" ( Uilenberg, 1998; Schlater & Van Den Bossche, 2004).

Salmonid Cryptobiosis
Fig. 7: Cryptobia (T.) salmositica with a red blood cell from an anemic fish Fig. 8: Bilateral exophthalmia in salmonid cryptobiosis (acute phase)
Fig. 9: Splenomegaly (6 - 8 times by volume) Fig. 10: General edema and abdominal distension with ascites
Cryptobiosis is caused by the hemoflagellate, Cryptobia (T.) salmositica (Fig. 7; Woo, 2003). The parasite is normally transmitted indirectly by leeches (Piscicola salmositica) in streams and rivers on the Pacific coast of N. America; however, direct transmission can also occur when infected and uninfected fish are held for prolonged periods in the same tank or under certain hatchery conditions. Clinical signs include anorexia, exophthalmia (Fig. 8), splenomegaly (Fig. 9), hepatomegaly, general edema and abdominal distention with ascites (Fig. 10), a microcytic and hypochromic anemia, and red cells give a positive antiglobulin reaction. Infected fish are susceptible to environmental hypoxia, and their metabolism and swimming performance are reduced. Also, serum hemolytic complement activity of infected fish and their ability to mount a protective response against a secondary pathogen are significantly depressed. The anemia and the anorexia contribute to the immunodepression. Cysteine protease is a metabolic enzyme while the metalloprotease is the main disease-causing factor.

His program on "salmonid cryptobiosis" is a multidisciplinary 'proof-of-concept' study. It is on the biology and transmission of the pathogen, diagnosis of infection, pathobiology in cryptobiosis including elucidation of the disease mechanism, host immune responses, and the development of control strategies against cryptobiosis (Woo, 2003). Control strategies include exploiting innate and adaptive immunity, chemotherapy and immunochemotherapy (Woo, 2010).

Salmonid Spironucleosis
Systemic spironucleosis is caused by Spironucleus (Fig. 3) - the parasite is in the blood and internal organs of fish. It is morphologically similar to the intestinal flagellate (Hexamita) in fish, and both parasites are closely related to the Giardia in mammals. The parasite causes morbidity and mortality in fishes and there have been outbreaks of the disease in salmon cultured in sea cages - in chinook salmon on the west coast of Canada and in Atlantic salmon in Norway. Fish mortality was high and some infected chinook salmon had abdominal distensions and were anaemic while infected Atlantic salmon were significantly smaller than healthy fish and they behaved 'abnormally' prior to death. Little is known about the biology of the pathogen nor factors that precipitated the outbreaks, consequently there are no preventive nor control strategies against the parasite. (Woo, 2006. Chapter 3. In: Fish Diseases and Disorders, Vol. 1: Protozoan and Metazoan Infections, 2nd edition, pp. 46-114).

Fig. 11: Unilateral exophthalmia Fig. 12: Ulceration on body surface Fig. 13: Globulated and enlarged spleen
 Spironucleus barkhanus has a blood and a tissue phase in experimentally infected Atlantic salmon. It first appears in the blood about a week after infection in some fish and the parasitaemia peaks at about 6 weeks. The parasite is not detectable in the blood at about 8 weeks after infection but it occurs in high numbers in the spleen, liver, eye socket, and muscles. Thirty eight out of 40 infected fish died in one experiment, and mortality was equally high (29 out of 30 infected fish) in another experiment with Atlantic salmon from 3 families of fish. Clinical signs of spironucleosis include unilateral exophthalmia (Fig. 11), skin blisters and ulcerations (Fig. 12), enlarged and globulated spleens (Fig. 13), livers with whitish to yellowish nodules, and hemorrhaging in organs. The parasite can be transmitted directly from infected to uninfected fish through co-habitation (Guo & Woo, 2004. Dis. Aquat. Org. 61: 59-66).

II (a). Books:

Woo P.T.K. & Buchmann K. (eds.), 2011. Fish Parasites: Pathobiology and Protection (brief description), CABI Publishing, Wallingford, Oxfordshire, U.K. ("in preparation").

Woo P.T.K. & Bruno D.W. (eds.) 2010. Fish Diseases and Disorders, Volume 3: Viral, Bacterial and Fungal Infections, 2nd edition (Table of Contents), CABI Publishing, Wallingford, Oxfordshire, U.K., ~1000 pages [CABI Special Offer: Fish Diseases and Disorders, Volumes 1-3].

Leatherland J.F. & Woo P.T.K. (eds.) 2010. Fish Diseases and Disorders, Volume 2: Non-infectious Disorders, 2nd edition (Table of Contents), CABI Publishing, Wallingford, Oxfordshire, U.K., ~400 pages [CABI Special Offer: Fish Diseases and Disorders, Volumes 1-3].

Woo P.T.K. (ed.) 2006. Fish Diseases and Disorders, Volume 1: Protozoan and Metazoan Infections, 2nd edition (Table of Contents), CABI Publishing, Wallingford, Oxfordshire, U.K., 800 pages [CABI Special Offer: Fish Diseases and Disorders, Volumes 1-3].

Woo P.T.K., Bruno D.W. & Lim L.H.S. (eds.) 2002. Diseases and Disorders of Finfish in Cage Culture (Table of Contents), CABI Publishing, Wallingford, Oxfordshire, U.K., 384 pages.

Woo P.T.K. & Bruno D.W. (eds.) 1999. Fish Diseases and Disorders, Volume 3: Viral, Bacterial and Fungal Infections (Table of Contents), CABI Publishing, Wallingford, Oxfordshire, U.K., 874 pages.

Leatherland J.F. & Woo P.T.K. (eds.) 1998. Fish Diseases and Disorders, Volume 2: Non-infectious Disorders (Table of Contents), CABI Publishing, Wallingford, Oxfordshire, U.K., 386 pages.

Woo P.T.K. (ed.) 1995. Fish Diseases and Disorders, Volume 1: Protozoan and Metazoan Infections (Table of Contents), CABI Publishing, Wallingford, Oxfordshire, U.K., 808 pages.

II (b). Selected Book Chapters and Refereed Conference Proceedings:
[complete list - book chapters and conference proceedings]

Guo, F.C. & Woo, P.T.K. 2009. Selected parasitosis in cultured and wild fish. In: 22nd World Association for the Advancement of Veterinary Parasitology, Calgary, Canada (conference held in 2009); Vet. Parasitol. 163: 207-216.

Woo, P.T.K. 2007. Protective immunity in fish against protozoan diseases. In: 7th International Symposium on Fish Parasites, Viterbo, Italy (conference held in 2007); Parassitologia 49: 185-191.

Woo, P.T.K. 2006. Strategies against piscine parasitosis: the Cryptobia model*. In: Innovations and Technologies in Oceanography for Sustainable Development (eds. S.M. Phang, Siti Aisyah, V.C. Chong, M. George, Siti Aisyah & S.C. Ho), Kuala Lumpur, Malaysia (conference held in 2005); Maritime Research Centre, University of Malaya, Kuala Lumpur, Malaysia, pp. 17-28 .

Woo, P.T.K. 2006. Diplomonadida (Phylum Parabasalia) and Kinetoplastea (Phylum Euglenozoa). In: Fish Diseases and Disorders, Volume 1: Protozoan and Metazoan Infections, 2nd edition (ed. P.T.K. Woo), CABI Publishing, Oxfordshire, U.K. pp. 46-114.

Ardelli, B.F. & Woo, P.T.K. 2006. Immunocompetent cells and their mediators in finfish. In: Fish Diseases and Disorders, Volume 1: Protozoan and Metazoan Infections, 2nd edition (ed. P.T.K. Woo), CABI Publishing, Oxfordshire, U.K. pp. 699-721.

Woo, P.T.K. 2005. Salmonid cryptobiosis and strategies against the disease. In: 19th International Congress of Zoology, Beijing, China (conference held in 2004); Acta Zool. Sinica 51: 546-549.

Woo, P.T.K. 2004. The pathophysiology of salmonid cryptobiosis and Glossina-transmitted mammalian trypanosomiasis in livestock. In: Host-Parasite Interactions (eds. G.F. Wiegerties & G. Flik), BIOS Scientific Publishers, New York, U.S.A. pp. 91-105.

Bruno, D.W. & Woo, P.T.K. 2002. Sporadic, emerging diseases and disorders. In: Diseases and Disorders of Finfish in Cage Culture (eds. P.T.K. Woo, D.W. Bruno & S.L.H. Lim), CABI Publishing, Oxfordshire, U.K., pp. 305-343.

Woo, P.T.K. 2001. Cryptobiosis and its control in North American fishes. In: 3rd. Internet Conference on Salivarian Trypanosomes. (conference held in 2000); Internat'l. J. Parasitol. 31: 565-573 .

II (d). Selected Publications in Refereed Journals:
[complete list]

Woo, P.T.K. 2010. Immunological and therapeutic strategies against salmonid cryptobiosis (Special issue: Immunology and Cell Biology of Parasitic Diseases), J. Biomed. Biotechnol. Article ID341783, 9 pages [doi:10.1155/2010/341783]. .

Guo, F.C. & Woo, P.T.K. 2009. Selected parasitosis in cultured and wild fish. Vet. Parasitol. 163: 207-216.

Nourollahi-Fard, S.R. & Woo P.T.K. 2008. Contribution of food deprivation to the immune response in rainbow trout (Oncorhynchus mykiss) vaccinated against Cryptobia salmositica and Aeromonas salmonicida. Acta Vet. Hung. 56: 197-206.

Tan, C.W., Jesudhasan, R.R.R. & Woo, P.T.K. 2008. Towards a metalloprotease-DNA vaccine against piscine cryptobiosis caused by Cryptobia salmositica. Parasitol. Res. 102: 265-275.

Currie, J.L.M. & Woo, P.T.K. 2007. Susceptibility of sexually mature rainbow trout, Oncorhynchus mykiss to experimental cryptobiosis caused by Cryptobia salmositica. Parasitol. Res. 101: 1057-1067.

Jesudhasan, P.R.R., Tan, C.W. & Woo, P.T.K. 2007. A metalloproteinase gene from the pathogenic piscine hemoflagellate, Cryptobia salmositica. Parasitol. Res. 100: 899-904.
[Jesudhasan, P.R.R. & P.T.K. Woo (2004) Major surface glycoprotein metalloproteinase gene - key gene involved in pathogensis. GENBANK No. AY632692.]

Chin, A. & Woo, P.T.K. 2005. Innate cell-mediated immune response and peripheral leukocyte populations in Atlantic salmon, Salmo salar L., to a live Cryptobia salmositica vaccine. Parasitol. Res. 95: 299-304.

Woo, P.T.K. 2005. Salmonid cryptobiosis and strategies against the disease. Acta Zool. Sinica 51: 546-549.

Guo, F.C. & Woo, P.T.K. 2004. Experimental infections of Atlantic salmon, Salmo salar L. (Salmonidae) with Spironucleus barkhanus (Diplomonidida: Hexamitidae). Dis. Aquat. Org. 61: 59-66.

Chin, A., Guo, F.C., Bernier, N. & Woo, P.T.K. 2004. Cryptobia salmositica-induced anorexia and its effects on gastric evacuation, feeding hierarchy, and immune response against a live vaccine in juvenile rainbow trout, Oncorhynchus mykis. Dis. Aquat. Org. 58: 17-26.

Torgerson, D.G., Lampo, M., Velazquez, Y. & Woo, P.T.K. 2003. Genetic relationships among some species groups within the genus Lutzomyia (Diptera: Psychodidae). Amer. J. Trop. Med. & Hyg. 69: 484-493.

Woo, P.T.K. 2003. Cryptobia (Trypanoplasma) salmositica and salmonid cryptobiosis. J. Fish Dis. 26: 627-646.

Ardelli, B.F. & Woo, P.T.K. 2002. Experimental Cryptobia salmositica (Kinetoplastida) infections in Atlantic salmon (Salmo salar): Cell-mediated and humoral response against the pathogenic and vaccine strains of the parasite. J. Fish Dis. 25: 265-274.

Mehta, M. & Woo, P.T.K. 2002. Acquired cell-mediated protection in rainbow trout, Oncorhynchus mykiss, against the haemoflagellate, Cryptobia salmositica. Parasitol. Res. 88: 956-962.

Bahmanrokh, M. & Woo, P.T.K. 2001. Relationships between histopathology and parasitaemias in Oncorhynchus mykiss infected with Cryptobia salmositica, a pathogenic haemoflagellate. Dis. Aquat. Org. 46: 41-45

Feng, S. & Woo, P.T.K. 2001. Cell membrane glycoconjugates on virulent and avirulent strains of the pathogenic haemoflagellate Cryptobia salmositica Katz. J. Fish Dis. 24: 23-32.

Ardelli, B.F., Witt, J.D.S. & Woo, P.T.K. 2000. The identification of glycosomes and metabloic end products in pathogenic and nonpathogenic strains of Cryptobia salmositica (Kinetoplastida: Bodonidae). Dis. Aquat. Org. 42: 41-51.

Zuo, X. & Woo, P.T.K. 2000. In vitro haemolysis of piscine erythrocytes by purified metallo-protease from the pathogenic haemoflagellate, Cryptobia salmositica Katz. J. Fish Dis. 23: 227-230.

III (a). Research Program:
Hemoflagellates, host-parasite relationships including disease mechanism(s), and strategies against salmonid cryptobiosis

III (b). Current and Recent Research Sponsors:
(1) Natural Sciences and Engineering Research Council (continuous NRC/NSERC support: 1975-present)
Cryptobia and Cryptobiosis in Fish (2009-12).
Piscine Flagellates and the Diseases they Cause (2004-09).
Cryptobia and Cryptobiosis in Fish (2000-04).

(2) AquaNet, Networks of Centres of Excellence (2000-05)
Production of Atlantic Salmon with an Efficient Immune System, and the Identification of Molecular Markers Associated with this Trait (2003-05).
Production of Disease Resistant Transgenic Salmonids Expressing Major Histocompatibility Complex Genes at all Temperatures (2000-03).
Immunological Response in Atlantic Salmon, and the Identification of Molecular Markers Associated with an Efficient Immune System (2001-03).

V (a). Recent Invited Presentations:
[complete list of lectures and seminars]

2009. "Relacion entre parasitos protozoarios patogenos y estrategias de defensa del sistema immune: perspectiva para el desarrollo de una vacuna" (Plenary), Seminario Internacional de Parasitologia Applicada a la Acuicultura, Puerto Montt, Chile.

2009. "Selected parasitosis in cultured and wild fish' (Plenary; presenter - F.C. Guo), 22nd World Association for the Advancement of Veterinary Parasitology, Calgary, Canada.

2008. "Aquaculture and parasitosis: strategies against protozoan diseases in finfish" (Special), College of Fisheries and Ocean Sciences, Chonnam National University, Republic of Korea.

2007. "Protective immunity in fish against protozoan diseases" (Plenary), 7th International Symposium on Fish Parasites, Viterbo, Italy.

2006. "Development of an integrated strategy against parasitic diseases in finfish under aquaculture conditions" (Special), College of Fisheries and Ocean Sciences, Chonnam National University, Republic of Korea.

2005. "Strategies against piscine parasitosis: the Cryptobia model" (Symposium – Marine Biotechnology: New Uses of Marine Resources), International Conference on Innovations and Technologies in Oceanography for Sustainable Development, Kuala Lumpur, Malaysia

2005. "Strategies against piscine parasitosis: the Cryptobia model"
(a) University of Malaya, Kuala Lumpur, Malaysia
(b) Burapha University, Bangsaen, Thailand

2004. "Salmonid cryptobiosis and strategies against the disease" (Symposium - Parasitic Diseases of Finfish and Their Control), 19th International Congress of Zoology, Beijing, China.

2004. "Control measures against Cryptobia and cryptobiosis" (Special), Kolej Universiti Sains dan Technologi Malaysia, Kuala Terengganu, Malaysia.

2003. "Strategies against salmonid diseases" (Plenary), Sustainable Control of Fish Diseases in Aquaculture, Danish Network for Fisheries and Aquaculture Research, Copenhagen, Denmark.

2003. "Cryptobia and cryptobiosis: some recent studies" (Special), The Royal Veterinary and Agriculture University, Copenhagen, Denmark.

2003. "Current and future trends in Biological Sciences" (Special), Kolej Universiti Sains dan Technologi Malaysia, Kuala Terengganu, Malaysia.

2002. "Salmonid cryptobiosis and its control" (Workshop - Haemoflagellate Diseases), Wageningen University, Wageningen, The Netherlands.

2002. "The pathophysiology in piscine and mammalian haemoflagellate diseases" (Symposium - Host Parasite Interactions: A Comparative Approach), American Physiological Society, San Diego, U.S.A.

2002. "Towards an integrated strategy against salmonid cryptobiosis" (Special), The Royal Veterinary and Agricultural University, Copenhagen, Denmark.

2002. "Cryptobia and cryptobiosis in economically important fishes" (Plenary - Impact and Control of Diseases in Fish), Danish Network for Fisheries and Aquaculture Research, Denmark.

2002. "Immunological response in Atlantic salmon, and the identification of molecular markers associated with an efficient immune system", Animal Production Theme, AquaNet Meeting, Moncton, Canada.

2001. "Fish as an important animal protein and the development of an integrated strategy against piscine parasitosis" (Plenary), International Congress of Parasitology and Tropical Medicine, Kuala Lumpur, Malaysia.

2001. "The pathobiology in salmonid cryptobiosis" (Symposium - Infectious Organisms in the Aquatic System: From Molecules to Organisms), International Congress of Parasitology and Tropical Medicine, Kuala Lumpur, Malaysia.

VI (a). Current and Recent Research Collaborators/Postdoctoral Fellows:
[complete list]

S.J. Jung, Department of Aqualife Medicine, Chonnam National University, Yosu, Chonnam, Republic of Korea (2007-present)
N. Bernier, Department of Integrative Biology, University of Guelph, Guelph, Canada (2003; 2005-present).
B.D. Glebe, Huntsman Marine Science Centre, St. Andrews, Canada (2001-03)
R. Danzmann, Department of Zoology, University of Guelph, Guelph, Canada (2001-03).
M.M. Ferguson, Department of Zoology, University of Guelph, Guelph, Canada (1994-95; 2001-03).
P.R.R. Jesudhasan, Department of Zoology, University of Madras, Chennai, India (2002-03)
S.R. Nourollahi-Fard, Department of Pathobiology, Shiraz University, Shiraz, Iran (2002-03)
M. Mehta, Gurudas College, University of Calcutta, Calcutta, India (2001)
B. Dixon, Department of Biology, University of Waterloo, Waterloo, Canada (2000-02)
B.F. Ardelli, Department of Zoology, University of Guelph, Guelph, Canada (2000)
M. Lampo, Centro de Ecologia, Instituto Venezolano de Investigaciones Cientificas, Caracas, Venezuela (1998-00)

VI (b). Recent Graduate Students:
[complete list]

Ph.D. Students (year of completion)*:
Guo, F.C. (2006)* Spironucleus spp. and experimental spironucleosis in salmonids.
Ardelli, B.F. (2000)* A chemotherapeutic strategy against salmonid cryptobiosis.

M.Sc. Students (year of completion)*:
MacDonald, L.E. (2007)* Exploring potential mechanisms mediating Cryptobia-induced anorexia in rainbow trout (Oncorhynchus mykiss)
Tan, C.W. (2005)* Towards a DNA vaccine against salmonid cryptobiosis.
Currie, J.L.M. (2004)* The effects of cryptobiosis on reproduction in Oncorhynchus mykiss.
Chin, A. (2004)* Susceptibility and immune response of Salmo salar against the hemoflagellate, Cryptobia salmositica.
Torgerson, D.G. (2000)* Genetic relationships between phlebotomine sandflies (Diptera: Psychodidae) from Venezuela.

9th International Congress of Parasitology, Chiba
Fish Parasitologists with the Official ICOPA Flag
(Photograph: Courtesy of the late Shunya Kamegai
 Meguro Parasitology Museum, Tokyo, Japan)


University of Guelph
The Weather at Guelph
Updated: 03/01/09