UTMB Department of Pathology

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Arthropod-Borne Viruses

Viruses that are transmitted by arthropods such as mosquitoes, sandflies, blackflies and ticks cause many diseases in both human and other animal hosts. Many of these diseases are emerging in new areas or resurging in areas from which they were previously eradicated. Many factors contribute to this expansion, for example reduced efforts in mosquito control and more rapid and widespread travel. The introduction of West Nile virus into the US demonstrates how a virus in a new area can quickly establish a life cycle involving locally abundant mosquitoes and vertebrates. Such an event demonstrates the importance of arthropod-borne viruses. Dengue viruses, for example, may infect over 100 million people annually, causing disease and economic losses throughout much of the tropics. Ironically, although these diseases have been studied for many years, many aspects of the diseases and the transmission cycles remain unknown.

My group's research encompasses many aspects of mosquito-borne viruses, with my particular interests focusing on mosquito-virus-vertebrate interactions. Using wild type and genetically engineered chikungunya, Sindbis, o'nyong nyong, West Nile and yellow fever viruses we have been examining fundamental aspects of virus-vector interactions.

Some of our work has been directed towards the identification of molecular mechanisms that could be used to reduce the efficiency of pathogen transmission. This research is a critical component in the development of novel strategies to reduce the impact of vector-borne diseases. With colleagues at CSU during the 1990s, sequences were identified that prevented transmission of several viruses. A scorpion neurotoxin that might be used for biological control was evaluated and we pioneered the expression of green fluorescent protein in mosquitoes, that has since become a standard marker of mosquito transgenesis and may be used for identification and tracking of genetically engineered arthropods. We collaborate with colleagues at Notre Dame, and other universities with support form the Bill and Melinda Gates Foundation to evaluate the use of transgenic mosquitoes for the control of dengue.

A recent interest has developed from the realization that during biting, an arthropod secretes substances that not only influence pathogen transmission, but also determine the severity of the disease. In collaboration with Dr. Lynn Soong we are identifying the molecules and mechanisms that are involved in this fascinating phenomenon.

In 2005 we demonstrated direct transmission of West Nile virus from infected to uninfected mosquitoes whilst feeding on an uninfected host. This discovery accelerates the transmission cycle and means that many more vertebrates may be involved in transmission than originally thought.
Our research on chikungunya virus (CHIKV) preceded the ongoing epidemic that has recently infected over 1.25M people. Our development of patented infectious clones of this CHIKV has placed us at the forefront of research on this virus. UTMB encourages collaborative research and we have distributed these research tools to other groups in an effort to better understand the epidemic.

Research facilities at UTMB are second to none, and are continuously being added to. New fully equipped BSL-3 insectaries have just been completed and the Galveston National Laboratory, due for completion in 2008, has additional BSL-3 insectary space and will have the capability for BSL-4 research. UTMB has assembled a unique team of faculty that is comprised of the finest researchers anywhere. The opportunity to work with this team has provided an extraordinary academic environment that I believe will allow us to make a difference in the field of arthropod-borne diseases. The award of a CDC Fellowship Training Grant in Vector-borne Diseases to our group and the success of our graduates support this belief. Recent graduates from my laboratory are employed at CDC Puerto Rico, the Institute Pasteur, Paris and at UC Berkeley.

1. Girard, Y., Schneider, B.S., McGee, C., Wen, J., Han, V., Popov, V., Mason, P., Higgs, S. Salivary gland morphology and virus transmission during long-term cytopathological West Nile virus infection in Culex mosquitoes. Am. J. Trop. Med. Hyg. 76. 118-128. 2007
2. McGee, C.E., Schneider, B.S., Girard, Y.A., Vanlandingham, D.L., & Higgs, S. Nonviremic transmission of West Nile virus: evaluation of the effects of space, time and mosquito species. Am. J. Trop. Med. Hyg. 76: 424-430. 2007
3. Vanlandingham, D.L., Tsetsarkin, K., Klingler, K.A., Hong, C., McElroy, K.L., Lehane, M.J., Higgs, S. Determinants of vector specificity of o’nyong nyong and chikungunya viruses in Anopheles and Aedes mosquitoes. Am. J. Trop. Med. Hyg. 74: 663-669. 2006
4. Wicker, J.A., Whiteman, M.C., Beasley, D.W., Davis, C.T., Zhang, S., Schneider, B.S., Higgs, S., Kinney, R.M. & Barrett, A.D. A single amino acid substitution in the central portion of the West Nile virus NS4B protein confers a highly attenuated phenotype in mice. Virology. 349; 245-53. 2006
5. Schneider, B.S., Soong, Girard, Y.A., Campbell, G., Mason, P. and Higgs, S. Potentiation of West Nile Encephalitis by mosquito feeding. Viral Immunology. 19: 74-82. 2006
6. Higgs, S. A novel method of West Nile virus transmission. Contagion. 3: 95-97
7. Gould, E.A., Higgs, S., Buckley, A. & Gritsun, T. The risk of arbovirus emergence in the UK. Emerg. Infect. Dis. 12: 549-555. 2006
8. Tsetsarkin, T., Higgs, S., McGee, C.E., de Lamballerie, X., Charrel, R.N. & Vanlandingham, D.L. Infectious Clones of Chikungunya Virus (La Réunion Isolate) for Vector Competence Studies Vector-Borne and Zoonotic Diseases 6: 325-337 2006
9. McElroy, K.L., Tsetsarkin, K., Vanlandingham, D.L. and Higgs, S. Manipulation of the yellow fever virus non-structural genes 2A and 4B and the 3'non-coding region to evaluate genetic determinants of viral dissemination from the Aedes aegypti midgut. Am. J. Trop. Med. Hyg. 75, 1158-1164. 2006
10. McElroy, K.L., Tsetsarkin, K., Vanlandingham, D.L. and Higgs, S. Role of the Yellow Fever Virus Structural Protein Genes in Viral Dissemination from the Aedes aegypti Mosquito Midgut J.Gen.Virol. 87: 2993-3001 2006
11. Higgs, S., Vanlandingham, D.L., Klingler, K.A., McElroy, K.L., McGee, C.E., Harrington, L., Lang, J., Monath, T.P. and Guirakhoo, F. Growth characteristics of ChimeriVax-DEN vaccine viruses in Aedes aegypti and Aedes albopictus from Thailand. Am. J. Trop. Med. Hyg. 75: 1158-1164 2006
12. Bryant, J.E., Vasconcelos, P.F.C., Rijnbrand, R.C.A., Mutebi, J.P., Higgs, S. & Barrett, A.D.T. Size heterogeneity in the 3’ noncoding region of south American isolates of yellow fever virus. J. Virol. 79: 3807-3821. 2005
13. Vanlandingham, D.L., Hong, C., Tsetsarkin, K., McElroy, K.L., Powers, A.M., Lehane, M. & Higgs, S. Differential infectivities of o’nyong-nyong and chikungunya viruses in Anopheles gambiae and Aedes aegypti mosquitoes. Am. J. Trop. Med. Hyg. 72: 616-621. 2005
14. McElroy, K.L., Tsetsarkin, K.A., Vanlandingham, D.L. & Higgs, S. Characterization of yellow fever virus-mosquito interactions using an infectious clone of the wild-type Asibi virus. J. Gen. Virol. 86: 1747-1751. 2005
15. Sbrana, E., Tonry, J.H., Xiao, S-Y., Travassos da Rosa, A.P.A., Higgs, S. and Tesh, R.B. Oral transmission of West Nile virus in a hamster model. Am. J. Trop. Med. Hyg. 72: 325-329. 2005
16. Girard, Y.A., Popov, V., Wen, J., Ham, V. and Higgs, S. Ultrastructural study of West Nile virus pathogenesis in Culex pipiens quinquefasciatus (Diptera: Culicidae). J. Med. Entomol. 42: 429-444
17. Higgs, S., Schneider, B.S., Vanlandingham, D.L., Klingler, K. & Gould, E.A. Non-viremic transmission of West Nile virus. PNAS 102: 8871-8874. 2005
18. Eappen, G.A., Pinto, S.B., Ghosh, A., Vanlandingham, D.L., Budd, A., Higgs, S., Kafatos, F.C., Jacobs-Lorena, M. & Michel, K. An immune-responsive serpin, SRPN6, mediates mosquito defense against malaria parasites. PNAS. 102: 16327-16332. 2005
19. Alto, B.W., Lounibos, L.P., Higgs, S. & Juliano, S.A. Larval competition differentially affects arbovirus infection and dissemination in mosquitoes Aedes albopictus and Aedes aegypti. Ecology. 86: 3279-3288. 2005
20. Sim, C., Hong, Y.S., Vanlandingham, D.L., Christophides, G.K., Kafatos, F.C., Higgs, S. & Collins, F.H. Modulation of Anopheles gambiae gene expression in response to o’nyong nyong virus infection. Ins. Mol. Biol. 14: 475-481. 2005
21. Vanlandingham, D.L., Tsetsarkin, T., Hong, C., Klingler, K., Lehane, M.J. and Higgs, S. Development and characterization of a double subgenomic chikungunya virus infectious clone to express heterologous genes in Aedes aegypti mosquitoes. Ins. Biochem. Mol. Biol. 35: 1162-1170. 2005
22. Beasley, D.W.C., Whiteman, M.C., Zhang, S., Huang, C-Y.H.,Schneider, B.S.,Smith, D.R., Gromowski, G.D., Higgs,S., Kinney, R.M. and ADT Barrett. Envelope protein glycosylation status influences mouse neuroinvasion phenotype of genetic lineage 1 West Nile virus strains. J. Virol. 79: 8339-8347. 2005
23. Girard, Y.A., Klingler, K.A. & Higgs, S. West Nile virus dissemination and tissue tropisms in orally-infected Culex pipiens quinquefasciatus. Vector-borne & Zoonotic Diseases. 4: 109-122. 2004
24. Wanasen, N., Nussenzveig, R.H., Champagne, D.E., Soong, L. & Higgs, S. Differential modulation of murine host immune response by salivary gland extracts from the mosquitoes Aedes aegypti and Culex quinquefasciatus J. Med. Vet Entomol. 2004. 18: 191-199. 2004
25. Scholle, F., Girard, Y.A., Zhao, Q., Higgs, S., & Mason, P.W. trans-packaged West Nile virus-like particles: infectious properties in vitro and in orally infected mosquito hosts. J. Virology. 78: 11605-11614. 2004
26. Vanlandingham, D.L., Schneider, B.S., Klingler, K., Fair, J., Beasley, D., Huang, J,m Hamilton, P., & Higgs, S. Real-time RT-PCR quantification of West Nile virus transmitted by Culex pipiens quinquefasciatus. Am. J. Trop. Med. Hyg. 71: 120-123. 2004
27. Higgs, S., Snow, K. & Gould, E.A. The potential for West Nile virus to establish outside of its natural range: a consideration of potential mosquito vectors in the United Kingdom. Trans. Roy. Soc. Trop. Med. Hyg. 98: 82-87. 2004
28. Tüzün, E., Scott, B.G. Yang, H., Wu, B., Goluszko, E., Guigneaux, M., Higgs, S., & Christadoss, P. Circulating Immune Complexes Augment Severity of Antibody Mediated Myasthenia Gravis in Hypogammaglobulinemic RIIIS/J Mice1 J.Immunology 172: 5743 – 5752, 2004
29. Lillibridge, K.M., Parsons, R., Randle, Y., Travassos da Rosa, E., Guzman, H., Siirin, M., Wuithiranyagool, T., Hailey, C., Beasley, D.W., Higgs, S., Pascual, R., Meyer, T., Barrett, A.D.T. & Tesh, R.B. The 2002 introduction of West Nile virus into Harris County, Texas, an area historically endemic for St. Louis encephalitis. Am. J. Trop. Med. Hyg. 70: 676-681. 2004
30. Granwehr, B.P., Lillibridge, K.M., Higgs, S., Mason, P.W., Aronson, J.F., Campbell, G.A., & Barrett, A.D.T. West Nile Virus: Where are we now? Lancet Infectious Diseases. 4: 547-556. 2004
31. Tamang, D., Tseng, S.M., Huang, C.Y., Tsao, I.Y., Chou, S.Z., Higgs, S., Christensen, B.M., & Chen, C.C. The use of a double subgenomic Sindbis virus expression system to study mosquito gene function: effects of antisense nucleotide number and duration of viral infection on gene silencing efficiency. Ins. Mol. Biol. 13: 595-602. 2004
32. Brault, A.C., Foy, B.D., Myles, K.M., Kelly, C.L.H., Higgs, S., Weaver, S.C., Olson, K.E., Miller, B.R., Powers, A.M. Infection patterns of O’nyong nyong virus in the malaria-transmitting mosquito, Anopheles gambiae. Insect. Mol. Biol. 13: 625-635. 2004
33. Schneider, BS, L Soong, NS Zeidner, Higgs, S.. Aedes aegypti Salivary Gland Extracts Modulate Anti-Viral and TH1/TH2 Cytokine Responses to Sindbis Virus Infection. Vir. Immunol. 17: 565-573. 2004
34. Infanger, L-C., Rocheleau,T.A., Bartholomay, L.C., Johnson, J.K., Fuchs, J., Higgs, S., Chen, C-C., & Christensen, B.M. The role of phenylalanine hydroxylase in melanotic encapsulation of filarial worms in two species of mosquito. IBMB 34: 1329-1338. 2004
35. Mutebi, J-P, Gianella, A., Travassos, A., Tesh, R.B., Barrett, A.D.T. & Higgs, S. Infectivity of yellow fever virus for Bolivian Aedes aegypti mosquitoes. Emerging Infectious Diseases. 10: 1657-1660. 2004
36. Tesh, R.B.Parsons, R. Randle, Y., Sargent, C.,Siirin, M., Wuithiranyagool, T., Guzman, H., Higgs, S., Vanlandingham, D.L., Bala, A.A., Haas, K., & Zerinque, B. Evidence of Year-Round West Nile Virus Activity in the Gulf Coast Region of Texas and Louisiana. Emerging Infectious Diseases. 10: 1649-1652. 2004
37. Siirin, M., Sargent, C., Langer, R.C., Parsons, R.,Vanlandingham, D.L., Higgs, S., & Tesh, R.B. Comparative Sensitivity of a Wicking Antigen Assay, Reverse Transcriptase-PCR and Direct Culture in Vero Cells for Detection of West Nile Virus in Dead Birds. Vector-borne and Zoonotic Diseases. 4: 204-209. 2004
38. Tüzün, E., Scott, B.G., Goluszko, E., Higgs, S. & Christadoss, P. Genetic evidence for involvement of classical complement pathway in induction of experimental autoimmune myasthenia gravis. J. Immunol. 171: 3847-1854, 2003
39. Limesand, K.H., Higgs, S., Pearson, L.D. & Beaty, B.J. The effect of mosquito salivary gland treatment on vesicular stomatitis New Jersey virus replication and interferon α/β expression in vitro. J. Med. Entomol. 40: 199-205, 2003
40. Beasley, D.W.C., Davis, T.C., Guzman, H., Vanlandingham, D.L., Travassos da Rosa, A.P.A., Parsons, R.E., Higgs, S., Tesh, R.B. & Barrett, A.D.T. Limited evolution of West Nile virus during its southwesterly spread in the United States. J. Virol. 309: 190-195. 2003
41. Benedict, M.Q., Tabachnick, W.J. & Higgs, S. Arthropod containment guidelines. Vector-Borne and Zoonotic Diseases. 3. 61–98. 2003
42. Diamond, M.S., Sitati, E.M., Friend, L.D., Higgs, S., Shrestha, B. & Engle, M. A critical role for induced IgM in the protection against West Nile virus infection. J. Exp. Med. 12: 1-11. 2003
43. Attardo, G., Higgs, S., Klingler, K.A., Vanlandingham, D.L. & Raikhel. A.S. RNAi-mediated knockdown of a GATA factor reveals a molecular mechanism of anautogeny in the yellow fever mosquito, Aedes aegypti. Proceedings of the National Academy of Science. 100: 13374-13370. 2003
44. Bennett, K.E., Olson, K.E., Munoz, M.L., Fernandez-Sala, I., Farfan, J.A., Higgs, S., Black, W.C. & Beaty, B.J. Variation in vector competence for dengue 2 virus among 24 populations of Aedes aegypti from Mexico and the United States. Am. J. Trop. Med. Hyg. 2002. 67: 85-92. 2002
45. Vanlandingham, D.L., Davis, B.S., Lvov, D., Higgs, S., Calisher, C.H., Black, W.C. & Beaty, B.J. Molecular characterization of California serogroup viruses isolated in Russia. Am J. Trop. Med. Hyg. 67: 306 – 309. 2002
46. Peloquin, J.J., Miller, T.A. & Higgs, S. Pink Bollworm Larvae Infection with a Double Subgenomic Sindbis (dsSIN) Virus to Express Genes of Interest. J. Cotton Sci. 5:114-120. 2001
47. Shiao, S.H., Higgs, S., Adelman, Z., Christensen, B.M., Liu, S.H. & Chen, C.C. Effect of prophenoloxidase expression knockout on the melanization of filarial worms in the mosquito, Armigeres subalbatus. Insect Mol. Biol. 10:315-321. 2001
48. Cheng, L.L., Bartholomay, L.C., Olson, K.E., Lowenberger, C., Viziol, J., Higgs, S., Beaty, B.J. & Christensen, B.M. Characterization of an endogenous gene expressed in Aedes aegypti using an orally infectious recombinant Sindbis virus. J. Insect Sci. (Online journal) 1.10. 14pp. 2001
49. Higgs, S. & Nowell, F. Population biology of Eimeria (Protozoa: Apicomplexa) in the wood mouse Apodemus sylvaticus: a capture/recapture study. Parasitology. 120: 355-363; 2000
50. Wendell, M.D., Wilson, T.G., Higgs, S. & Black, W.C. IV. Chemical and gamma-ray mutagenesis of the white gene in Aedes aegypti. Insect Mol. Biol. 9:119-125; 2000
51. Olson, K.E., Myles, K., Seabaugh, R.C., Higgs, S., Carlson, J.O. & Beaty, B.J. Development of a Sindbis virus expression system that efficiently expresses green fluorescent protein in midguts of Aedes aegypti following per os infection. Insect Mol. Biol. 9:57–65; 2000
52. Limesand, K.H., Higgs, S., Pearson, L.D., & Beaty, B.J. Potentiation of vesicular stomatitis New Jersey virus infection in mice by mosquito saliva. Parasite Immunol. 22:461-467; 2000
53. Higgs, S., Oray,C.T., Myles, K. Olson, K.E.& Beaty, B.J. Infecting Larval Arthropods With a Chimeric Double Subgenomic Sindbis Virus Vector to Express Genes of Interest. BioTechniques. 27:908-911; 1999
54. Johnson, B.W., Olson, K.E., Allen-Muira, T, Rayms-Keller, A., Carlson, J.O., Coates, C.J., Jasinskiene, N.J., James, A.A., Beaty, B.J. & Higgs, S. Inhibition of luciferase expression in transgenic Aedes aegypti mosquitoes by Sindbis virus expression of antisense luciferase RNA. PNAS. 96:13399–13403; 1999
55. Graham, D.H., Holmes, J.L., Higgs, S., Beaty, B.J. & Black, W.C. IV. Selection of refractory and permissive strains of Aedes triseriatus (Diptera: Culicidae) for transovarial transmission of La Crosse virus. J. Med. Entomol. 36:671–678; 1999
56. Lewis, D.L., DeCamillis, M.A., Brunetti, C.R., Halder, G., Kassner, V.A., Selegue, J.E., Higgs, S. & Carroll, S.N. Ectopic gene expression in developing butterflies, beetles and other arthropods using recombinant Sindbis virus. Current Biol. 22:1279–1287; 1999
57. Jordan, T.V., Shike, H., Boulo, V., Cedeno, V., Fang, Q., Davis, B.S., Jacobs-Lorena, M., Higgs, S., Fryxell, K. & Burns, J.C. Pantropic retroviral vectors mediate somatic cell transformation and expression of foreign genes in Dipteran insects. Insect Mol. Biol. 7:215-222; 1998
58. Higgs, S., Rayner, J., Olson, K., Davis, B.S., Beaty, B.J. & Blair, C.D. Engineered resistance in Aedes aegypti to a West African and a South American strain of yellow fever virus. Am. J. Trop. Med. Hyg. 58:663-670; 1998.
59. Edwards, J.F., Higgs, S. & Beaty, B.J. Mosquito feeding-induced potentiation of Cache Valley Virus (Bunyaviridae) in mice. J. Med. Entomol. 35:261-265; 1998
60. Zeidner, N.S., Higgs, S., Happ, C.M., Beaty, B.J. & Miller, B.R. Mosquito feeding modulates Th1 and Th2 cytokines in flavivirus susceptible mice: an effect mimicked by injection of sialokinins, but not demonstrated in flavivirus resistant mice. Parasite Immunol. 21:35-44; 1998
61. Kamrud, K.I., Olson, K.E., Higgs, S., Carlson, J.O. & Beaty, B.J. Use of the Sindbis replicon system for expression of LaCrosse virus envelope proteins in mosquito cells. Arch. Virol. 143:1365-1377; 1998
62. Seabaugh, R.C., Olson, K.E., Higgs, S., Carlson, J.O. & Beaty, B.J. Development of a chimeric Sindbis virus with enhanced Per Os infection of Aedes aegypti. Virology. 243:99-112; 1998.
63. Matsubara, T., Beeman, R.W., Besansky, N., Mukabayire, O., Higgs, S. James, A.A. & Burns, J.C. Pantropic retroviral vectors integrate and express in cells of the malaria mosquito, Anopheles gambiae. PNAS. 93:6181-6185; 1996
64. Powers, A.M., Kamrud, K.I., Olson, K.E., Higgs, S., Carlson, J.O. & Beaty, B.J. Molecularly engineered resistance to California serogroup virus replication in mosquito cells and mosquitoes. PNAS. 93:4187-4191; 1996
65. Higgs, S., Traul, D., Davis, B.S., Kamrud, K.I., Wilcox, C. & Beaty, B.J. Green fluorescent protein expressed in living mosquitoes, without the requirement of transformation. BioTechniques. 21:660-664; 1996
66. Olson, K.E., Higgs, S., Gaines, P.J., Powers, A.M., Davis, B.S., Kamrud, K.I., Carlson, J.O., Blair, C.D. & Beaty, B.J. Genetically engineered resistance in mosquitoes to dengue virus transmission. Science. 272:884-886; 1996
67. Gaines, P.J., Olson, K.E., Higgs, S., Powers, A.M., Beaty, B.J. & Blair, C.D. Pathogen-derived resistance to dengue type 2 virus in mosquito cells by expression of the premembrane coding region of the viral genome. J. Virol.. 70:2132–2137; 1996
68. Carlson, J,. Olson, K., Higgs, S. and Beaty, B. Molecular genetic manipulation of mosquito vectors. Ann. Rev. Entomol. 40:359-88; 1995
69. Higgs, S., Olson, K.E., Klimowski, L., Powers, A.M., Carlson, J.O., Possee, R.D. & Beaty, B.J. Mosquito sensitivity to a scorpion neurotoxin expressed using an infectious Sindbis virus vector. Insect Mol. Biol. 4:97-103; 1995
70. Kamrud, K.I., Powers, A.M., Higgs, S., Olson, K.E., Blair, C.D., Carlson, J.O. & Beaty, B.J. The expression of chloramphenicol acetyl transferase in mosquitoes and mosquito cells using a packaged Sindbis replicon system. Exp. Parasitol. 81:394-403; 1995
71. Rayms-Keller, A., Powers, A.M., Higgs, S., Olson, K.E., Kamrud, K.I., Carlson, J.O. & Beaty, B.J. Replication and expression of a recombinant Sindbis virus in mosquitoes. Insect Mol. Biol. 4:245-251; 1995
72. Olson, K., Higgs, S., Hahn, C.S., Rice, C.M., Carlson, J.O., & Beaty, B.J. Expression of chloramphenicol acetyltransferase in Aedes albopictus (C6/36) cells and Aedes triseriatus mosquitoes using double subgenomic recombinant Sindbis virus vectors. Insect Biochem. Mol. Biol. 24:39-48; 1994
73. Powers, A.M., Higgs, S., Olson, K.E., Carlson, J.O., & Beaty, B.J. Interference to La Crosse virus superinfection by an antisense RNA generated from an infectious Sindbis virus vector. Virus Res. 32: 57-67; 1994
74. Higgs, S., Powers, A.M., and Olson, K.E. Alphavirus expression systems: applications to mosquito vector studies. Parasit. Today. 9:444-452; 1993
75. Jiang, W.R., Lowe, A., Higgs, S., Reid, H. and Gould, E.A. Single amino acid codon changes detected in louping ill virus antibody-resistant mutants with reduced neurovirulence. J. Gen. Virol. 74:931-935; 1993
76. Jones, L.D., Hodgson, E., Williams, T., Higgs, S. & Nuttall, P.A. Saliva activated transmission (SAT) of Thogoto virus: relationship with vector potential of different haematophagous arthropods. Med. Vet. Entomol. 6:261-265; 1992
77. Higgs, S. & Nowell, F. A review of the species of Eimeria infecting hosts in the genus Apodemus. Syst. Parasitol. 20: 203-209; 1991
78. Higgs, S. & Gould, E.A. Differences in fusogenicity and mouse neurovirulence of Japanese encephalitis viruses. Arch. Virol. 119:119-133; 1991
79. Shiu, S.W., Morikawa, S., Buckley, A., Higgs, S., Karunakarannair, V., Blachere, C. & Gould, E.A. 17D yellow fever vaccine virus envelope protein expressed by recombinant baculovirus is antigenically indistinguishable from authentic viral protein. J. Gen. Virol. 72:1451-1454; 1991
80. Gould, E.A., Buckley, A., Higgs, S. & Gaidamovich, S. Antigenicity of flaviviruses. Arch. Virol., Supplementum I:137-152; 1990
81. Marriott, A.C., Ward, V.K., Higgs, S. and Nuttall, P.A. RNA probes detect nucleotide sequence homology between members of two different nairovirus subgroups. Virus Res. 16:77-82; 1990
82. Buckley, A., Higgs, S. & Gould, E.A. Dugbe virus susceptibility to neutralization by monoclonal antibodies as a marker of virulence in mice. Arch. Virol., Supplementum I:197-205; 1990
83. El-Ghorr, A.A., Marriott, A.C., Ward, V.K., Booth, T.F., Higgs, S., Gould, E.A., & Nuttall, P.A. Characterization of Dugbe virus by biochemical and immunochemical procedures using monoclonal antibodies. Arch. Virol., Supplementum I:169-179; 1990
84. Gould, E.A., Buckley, A., Cane, P.A., Higgs, S. and Cammack, N. Use of a monoclonal antibody specific for wild-type yellow fever virus to identify a wild-type antigenic variant in 17D vaccine pools. J. Gen. Virol. 70:1889-1894; 1989
85. Higgs, S. and Nowell, F. Laboratory studies with clones of Eimeria hungaryensis, a parasite of the wood mouse Apodemus sylvaticus. Parasitology. 97:213-220; 1988
86. Nowell, F. and Higgs, S. Eimeria species infecting wood mice (genus Apodemus) and the transfer of two species to Mus musculus. Parasitology. 98:329-336; 1988
87. Higgs, S., Nowell, F. and Ibrahim, S.A.M. The initiation and maintenance of a colony of coccidia-free wood mice (Apodemus sylvaticus). Lab. Animals. 22:54-60; 1987

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