ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Yu X-J, Walker DH , 2005. Family I. Rickettsiaceae. Brenner DJ, Kreig NR, Stanley JT, eds. Bergey’s Manual of Systematic Bacteriology. New York, NY: Springer, 96–116.
-
2.
Azad AF , 1990. Epidemiology of murine typhus. Annu Rev Entomol 35: 553–569.
-
3.
Kuo CC, Wardrop N, Chang CT, Wang HC, Atkinson PM , 2017. Significance of major international seaports in the distribution of murine typhus in Taiwan. PLoS Negl Trop Dis 11: e0005430.
-
4.
Traub R, Wisseman CL, Farhang-Azad A , 1978. The ecology of murine typhus-a critical review. Trop Dis Bull 75: 237–317.
-
5.
Azad AF, Radulovic S, Higgins JA, Noden BH, Troyer JM , 1997. Flea-borne rickettsioses: ecologic considerations. Emerg Infect Dis 3: 319–327.
-
6.
Pratt HD , 1958. The changing picture of murine typhus in the United States. Ann N Y Acad Sci 70: 516–527.
-
7.
Davis DE , 1947. The use of DDT to control murine typhus fever in San Antonio, Texas. Public Health Rep 62: 449–463.
-
8.
Hill EL, Morlan HB , 1948. Evaluation of county-wide DDT dusting operations in murine typhus control. Public Health Rep 63: 1635–1653.
-
9.
Adams WH, Emmons RW, Brooks JE , 1970. The changing ecology of murine (endemic) typhus in southern California. Am J Trop Med Hyg 19: 311–318.
-
10.
Older JJ , 1970. The epidemiology of murine typhus in Texas, 1969. JAMA 214: 2011–2017.
-
11.
Adjemian J, Parks S, McElroy K, Campbell J, Eremeeva ME, Nicholson WL, McQuiston J, Taylor J , 2010. Murine typhus in Austin, Texas, USA, 2008. Emerg Infect Dis 16: 412–417.
-
12.
Blanton LS, Idowu BM, Tatsch TN, Henderson JM, Bouyer DH, Walker DH , 2016. Opossums and cat fleas: new insights in the ecology of murine typhus in Galveston, Texas. Am J Trop Med Hyg 95: 457–461.
-
13.
Buttery CM, Magnuson LW, McLerran G, Villarreal T, 1984. Endemic (murine) typhus in Corpus Christi. Tex Med 80: 53–54.
-
14.
Boostrom A, Beier MS, Macaluso JA, Macaluso KR, Sprenger D, Hayes J, Radulovic S, Azad AF , 2002. Geographic association of Rickettsia felis–infected opossums with human murine typhus, Texas. Emerg Infect Dis 8: 549–554.
-
15.
Sorvillo FJ, Gondo B, Emmons R, Ryan P, Waterman SH, Tilzer A, Andersen EM, Murray RA, Barr R , 1993. A suburban focus of endemic typhus in Los Angeles County: association with seropositive domestic cats and opossums. Am J Trop Med Hyg 48: 269–273.
-
16.
VandeBerg JL, Robinson ES , 1997. The laboratory opossum (Monodelphis domestica) in laboratory research. ILAR J 38: 4–12.
-
17.
Fadem BH, Trupin GL, Maliniak E, VandeBerg JL, Hayssen V , 1982. Care and breeding of the gray, short-tailed opossum (Monodelphis domestica). Lab Anim Sci 32: 405–409.
-
18.
Eremeeva ME, Dasch GA, Silverman DJ , 2003. Evaluation of a PCR assay for quantitation of Rickettsia rickettsii and closely related spotted fever group rickettsiae. J Clin Microbiol 41: 5466–5472.
-
19.
Guedes E, Leite RC, Prata MC, Pacheco RC, Walker DH, Labruna MB , 2005. Detection of Rickettsia rickettsii in the tick Amblyomma cajennense in a new Brazilian spotted fever-endemic area in the state of Minas Gerais. Mem Inst Oswaldo Cruz 100: 841–845.
-
20.
Philip RN, Casper EA, Ormsbee RA, Peacock MG, Burgdorfer W , 1976. Microimmunofluorescence test for the serological study of Rocky Mountain spotted fever and typhus. J Clin Microbiol 3: 51–61.
-
21.
Walker DH, Feng HM, Ladner S, Billings AN, Zaki SR, Wear DJ, Hightower B , 1997. Immunohistochemical diagnosis of typhus rickettsioses using an anti-lipopolysaccharide monoclonal antibody. Mod Pathol 10: 1038–1042.
-
22.
Chapman J, Chapman AA , 1935. Typhus-like fever contracted from o’possum fleas. Tex State J Med 31: 36–39.
-
23.
Brigham GD , 1936. Susceptibility of the opossum (Didelphis virginiana) to the virus of endemic typhus fever. Public Health Rep 51: 333–337.
-
24.
Boston RJ , 1940. Public health engineering phases of murine typhus control. Am J Public Health Nations Health 30: 619–626.
-
25.
Boston RJ , 1941. Advances in methods of murine typhus control. Am J Public Health Nations Health 31: 720–727.
-
26.
Strandtmann RW, Eben DJ , 1953. A survey of typhus in rats and rat ectoparasites in Galveston, Texas. Tex Rep Biol Med 11: 144–151.
-
27.
Mohr CO, Morlan HB , 1959. The nature of parasitism of the opossum by fleas in southwestern Georgia. J Parasitol 45: 233–237.
-
28.
Murray KO, Evert N, Mayes B, Fonken E, Erickson T, Garcia MN, Sidwa T , 2017. Typhus group rickettsiosis, Texas, USA, 2003–2013. Emerg Infect Dis 23: 645–648.
-
29.
Blanton LS, Vohra RF, Bouyer DH, Walker DH , 2015. Reemergence of murine typhus in Galveston, Texas, USA, 2013. Emerg Infect Dis 21: 484–486.
-
30.
Erickson T, da Silva J, Nolan MS, Marquez L, Munoz FM, Murray KO , 2017. Newly recognized pediatric cases of typhus group rickettsiosis, Houston, Texas, USA. Emerg Infect Dis 23: 2068–2071.
-
31.
Bezerra-Santos MA, Ramos RAN, Campos AK, Dantas-Torres F, Otranto D , 2021. Didelphis spp. opossums and their parasites in the Americas: a one health perspective. Parasitol Res 120: 4091–4111.
-
32.
Hopkins D , 1980. Ectoparasites of the Virginia opossum (Didelphis virginiana) in an urban environment. Northwest Sci 54: 199–201.
-
33.
Arango-Jaramillo S, Farhang-Azad A, Wisseman CL Jr , 1984. Experimental infection with Rickettsia mooseri and antibody response of adult and newborn laboratory rats. Am J Trop Med Hyg 33: 1017–1025.
-
34.
Farhang-Azad A, Traub R, Sofi M, Wisseman CL Jr , 1984. Experimental murine typhus infection in the cat flea, Ctenocephalides felis (Siphonaptera: Pulicidae). J Med Entomol 21: 675–680.
-
35.
Farhang-Azad A, Traub R, Wisseman CL Jr , 1983. Rickettsia mooseri infection in the fleas Leptopsylla segnis and Xenopsylla cheopis. Am J Trop Med Hyg 32: 1392–1400.
-
36.
Mooser H , 1928. Experiments relating to the pathology and the etiology of Mexican typhus (tabardillo): 2. Diplobacillus from the proliferated tunica vaginalis of guinea-pigs reacting to Mexican typhus. J Infect Dis 43: 261–272.
-
37.
Pinkerton H, Hass GM , 1932. Typhus Fever: V. The Effect of temperature on the multiplication of Rickettsia prowazeki in tissue culture. J Exp Med 56: 145–150.
-
38.
Wike DA, Tallent G, Peacock MG, Ormsbee RA , 1972. Studies of the rickettsial plaque assay technique. Infect Immun 5: 715–722.
-
39.
Kraus DB, Fadem BH , 1987. Reproduction, development and physiology of the gray short-tailed opossum (Monodelphis domestica). Lab Anim Sci 37: 478–482.
-
40.
Haro P, Ruiz-Pina HA, Canche-Pool EB, Medina S, Mercado JA , 2018. Physiological basal parameters of free-ranging opossums (Didelphis virginiana) in the Yucatan Peninsula, Mexico. J Zoo Wildl Med 49: 480–483.
-
41.
Bozeman FM, Shiral A, Humphries JW, Fuller HS , 1967. Ecology of Rocky Mountain spotted fever. II. Natural infection of wild mammals and birds in Virginia and Maryland. Am J Trop Med Hyg 16: 48–59.
-
42.
Horta MC, Moraes-Filho J, Casagrande RA, Saito TB, Rosa SC, Ogrzewalska M, Matushima ER, Labruna MB , 2009. Experimental infection of opossums Didelphis aurita by Rickettsia rickettsii and evaluation of the transmission of the infection to ticks Amblyomma cajennense. Vector Borne Zoonotic Dis 9: 109–118.
-
43.
Horta MC, Sabatini GS, Moraes-Filho J, Ogrzewalska M, Canal RB, Pacheco RC, Martins TF, Matushima ER, Labruna MB , 2010. Experimental infection of the opossum Didelphis aurita by Rickettsia felis, Rickettsia bellii, and Rickettsia parkeri and evaluation of the transmission of the infection to ticks Amblyomma cajennense and Amblyomma dubitatum. Vector Borne Zoonotic Dis 10: 959–967.
-
44.
Dias Cordeiro M, de Azevedo Baeta B, Barizon Cepeda M, da Fonseca AH , 2020. Experimental infection of Monodelphis domestica with Rickettsia parkeri. Ticks Tick Borne Dis 11: 101366.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 1802 | 844 | 106 |
| Full Text Views | 209 | 73 | 2 |
| PDF Downloads | 182 | 28 | 2 |
Experimental Rickettsia typhi Infection in Monodelphis domestica: Implications for Opossums as an Amplifying Host in the Suburban Cycle of Murine Typhus
Lucas S. Blanton
Lucas S. Blanton
Department of Internal Medicine—Division of Infectious Diseases, University of Texas Medical Branch, Galveston, Texas;
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Bethany R. Quade
Bethany R. Quade
Department of Internal Medicine—Division of Infectious Diseases, University of Texas Medical Branch, Galveston, Texas;
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Alejandro Ramírez-Hernández
Alejandro Ramírez-Hernández
Veterinary Parasitology Research Group, National University of Colombia, Bogotá, Colombia;
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Nicole L. Mendell
Nicole L. Mendell
Department of Pathology, University of Texas Medical Branch, Galveston, Texas;
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Alejandro Villasante-Tezanos
Alejandro Villasante-Tezanos
Department of Preventive Medicine and Population Health, University of Texas Medical Branch, Galveston, Texas;
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Donald H. Bouyer
Donald H. Bouyer
Department of Pathology, University of Texas Medical Branch, Galveston, Texas;
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John L. VandeBerg
John L. VandeBerg
Department of Human Genetics, South Texas Diabetes and Obesity Institute, and Center for Vector-Borne Diseases, The University of Texas Rio Grande Valley, Brownsville, Texas
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David H. Walker
David H. Walker
Department of Pathology, University of Texas Medical Branch, Galveston, Texas;
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ABSTRACT.
Murine typhus is an acute undifferentiated febrile illness caused by Rickettsia typhi. In the United States, its reemergence appears to be driven by a shift from the classic rat–rat flea cycle of transmission to one involving opossums (Didelphis virginiana) and cat fleas. Little is known of the ability of opossums to act as a reservoir and amplifying host for R. typhi. Here, we use Monodelphis domestica (the laboratory opossum) as a surrogate for D. virginiana. Opossums were inoculated via the intraperitoneal (IP) or intradermal (ID) route with 1 × 106 viable R. typhi. Blood and tissues were collected on days 6, 13, 20, and 27 or if moribund. Although one ID-infected opossum died, the remainder did not appear ill, whereas half of the IP-inoculated animals succumbed to infection. Rickettsemia was demonstrated in all animals through week 2 of infection and sporadically in weeks 3 and 4. Rickettsia typhi DNA was detected in all tissues, with most animals demonstrating the presence of bacteria into weeks 3 and 4. Histopathology and immunohistochemistry demonstrated typical findings of rickettsial infection. Akin to infection in rats, the demonstration of disseminated infection, typical inflammation, and prolonged rickettsemia with relatively few clinical effects (especially in the more natural route of ID inoculation) supports the potential of opossums to act as a competent mammalian reservoir and component of the zoonotic maintenance cycle of R. typhi. Understanding the dynamics of infection within opossums may have implications for the prevention and control of murine typhus.
Author Notes
Financial support: At the time of this work, Lucas Blanton was supported by the Institute for Translational Sciences at the University of Texas Medical Branch, supported in part by a CTSA Mentored Career Development (KL2) Award (KL2TR001441) from the National Center for Advancing Translational Sciences, National Institutes of Health. This study was funded by a pilot grant provided by the University of Texas Medical Branch Institute for Human Infections and Immunity.
Authors’ addresses: Lucas S. Blanton and Bethany R. Quade, Department of Internal Medicine, Division of Infectious Diseases, University of Texas Medical Branch, Galveston, TX, E-mails: lsblanto@utmb.edu and bequade@utmb.edu. Alejandro Ramírez-Hernández, Veterinary Parasitology Research Group, National University of Colombia, Cra. 30 No. 45-03. Ed. 481. Lab 4. Ciudad Universitaria, Bogotá D.C., Colombia, E-mail: alerrah@yahoo.com. Nicole L. Mendell, Donald H. Bouyer, and David H. Walker, Department of Pathology, University of Texas Medical Branch, Galveston, TX, E-mails: nlmendel@utmb.edu, dobouyer@utmb.edu, and dwalker@utmb.edu. Alejandro Villasante-Tezanos, Department of Preventive Medicine and Population Health, University of Texas Medical Branch, Galveston, TX, E-mail: alvillas@utmb.edu. John L. VandeBerg, Department of Human Genetics, South Texas Diabetes and Obesity Institute, and Center for Vector-Borne Disease, Brownsville, TX, E-mail: john.vandeberg@utrgv.edu.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Yu X-J, Walker DH , 2005. Family I. Rickettsiaceae. Brenner DJ, Kreig NR, Stanley JT, eds. Bergey’s Manual of Systematic Bacteriology. New York, NY: Springer, 96–116.
-
2.
Azad AF , 1990. Epidemiology of murine typhus. Annu Rev Entomol 35: 553–569.
-
3.
Kuo CC, Wardrop N, Chang CT, Wang HC, Atkinson PM , 2017. Significance of major international seaports in the distribution of murine typhus in Taiwan. PLoS Negl Trop Dis 11: e0005430.
-
4.
Traub R, Wisseman CL, Farhang-Azad A , 1978. The ecology of murine typhus-a critical review. Trop Dis Bull 75: 237–317.
-
5.
Azad AF, Radulovic S, Higgins JA, Noden BH, Troyer JM , 1997. Flea-borne rickettsioses: ecologic considerations. Emerg Infect Dis 3: 319–327.
-
6.
Pratt HD , 1958. The changing picture of murine typhus in the United States. Ann N Y Acad Sci 70: 516–527.
-
7.
Davis DE , 1947. The use of DDT to control murine typhus fever in San Antonio, Texas. Public Health Rep 62: 449–463.
-
8.
Hill EL, Morlan HB , 1948. Evaluation of county-wide DDT dusting operations in murine typhus control. Public Health Rep 63: 1635–1653.
-
9.
Adams WH, Emmons RW, Brooks JE , 1970. The changing ecology of murine (endemic) typhus in southern California. Am J Trop Med Hyg 19: 311–318.
-
10.
Older JJ , 1970. The epidemiology of murine typhus in Texas, 1969. JAMA 214: 2011–2017.
-
11.
Adjemian J, Parks S, McElroy K, Campbell J, Eremeeva ME, Nicholson WL, McQuiston J, Taylor J , 2010. Murine typhus in Austin, Texas, USA, 2008. Emerg Infect Dis 16: 412–417.
-
12.
Blanton LS, Idowu BM, Tatsch TN, Henderson JM, Bouyer DH, Walker DH , 2016. Opossums and cat fleas: new insights in the ecology of murine typhus in Galveston, Texas. Am J Trop Med Hyg 95: 457–461.
-
13.
Buttery CM, Magnuson LW, McLerran G, Villarreal T, 1984. Endemic (murine) typhus in Corpus Christi. Tex Med 80: 53–54.
-
14.
Boostrom A, Beier MS, Macaluso JA, Macaluso KR, Sprenger D, Hayes J, Radulovic S, Azad AF , 2002. Geographic association of Rickettsia felis–infected opossums with human murine typhus, Texas. Emerg Infect Dis 8: 549–554.
-
15.
Sorvillo FJ, Gondo B, Emmons R, Ryan P, Waterman SH, Tilzer A, Andersen EM, Murray RA, Barr R , 1993. A suburban focus of endemic typhus in Los Angeles County: association with seropositive domestic cats and opossums. Am J Trop Med Hyg 48: 269–273.
-
16.
VandeBerg JL, Robinson ES , 1997. The laboratory opossum (Monodelphis domestica) in laboratory research. ILAR J 38: 4–12.
-
17.
Fadem BH, Trupin GL, Maliniak E, VandeBerg JL, Hayssen V , 1982. Care and breeding of the gray, short-tailed opossum (Monodelphis domestica). Lab Anim Sci 32: 405–409.
-
18.
Eremeeva ME, Dasch GA, Silverman DJ , 2003. Evaluation of a PCR assay for quantitation of Rickettsia rickettsii and closely related spotted fever group rickettsiae. J Clin Microbiol 41: 5466–5472.
-
19.
Guedes E, Leite RC, Prata MC, Pacheco RC, Walker DH, Labruna MB , 2005. Detection of Rickettsia rickettsii in the tick Amblyomma cajennense in a new Brazilian spotted fever-endemic area in the state of Minas Gerais. Mem Inst Oswaldo Cruz 100: 841–845.
-
20.
Philip RN, Casper EA, Ormsbee RA, Peacock MG, Burgdorfer W , 1976. Microimmunofluorescence test for the serological study of Rocky Mountain spotted fever and typhus. J Clin Microbiol 3: 51–61.
-
21.
Walker DH, Feng HM, Ladner S, Billings AN, Zaki SR, Wear DJ, Hightower B , 1997. Immunohistochemical diagnosis of typhus rickettsioses using an anti-lipopolysaccharide monoclonal antibody. Mod Pathol 10: 1038–1042.
-
22.
Chapman J, Chapman AA , 1935. Typhus-like fever contracted from o’possum fleas. Tex State J Med 31: 36–39.
-
23.
Brigham GD , 1936. Susceptibility of the opossum (Didelphis virginiana) to the virus of endemic typhus fever. Public Health Rep 51: 333–337.
-
24.
Boston RJ , 1940. Public health engineering phases of murine typhus control. Am J Public Health Nations Health 30: 619–626.
-
25.
Boston RJ , 1941. Advances in methods of murine typhus control. Am J Public Health Nations Health 31: 720–727.
-
26.
Strandtmann RW, Eben DJ , 1953. A survey of typhus in rats and rat ectoparasites in Galveston, Texas. Tex Rep Biol Med 11: 144–151.
-
27.
Mohr CO, Morlan HB , 1959. The nature of parasitism of the opossum by fleas in southwestern Georgia. J Parasitol 45: 233–237.
-
28.
Murray KO, Evert N, Mayes B, Fonken E, Erickson T, Garcia MN, Sidwa T , 2017. Typhus group rickettsiosis, Texas, USA, 2003–2013. Emerg Infect Dis 23: 645–648.
-
29.
Blanton LS, Vohra RF, Bouyer DH, Walker DH , 2015. Reemergence of murine typhus in Galveston, Texas, USA, 2013. Emerg Infect Dis 21: 484–486.
-
30.
Erickson T, da Silva J, Nolan MS, Marquez L, Munoz FM, Murray KO , 2017. Newly recognized pediatric cases of typhus group rickettsiosis, Houston, Texas, USA. Emerg Infect Dis 23: 2068–2071.
-
31.
Bezerra-Santos MA, Ramos RAN, Campos AK, Dantas-Torres F, Otranto D , 2021. Didelphis spp. opossums and their parasites in the Americas: a one health perspective. Parasitol Res 120: 4091–4111.
-
32.
Hopkins D , 1980. Ectoparasites of the Virginia opossum (Didelphis virginiana) in an urban environment. Northwest Sci 54: 199–201.
-
33.
Arango-Jaramillo S, Farhang-Azad A, Wisseman CL Jr , 1984. Experimental infection with Rickettsia mooseri and antibody response of adult and newborn laboratory rats. Am J Trop Med Hyg 33: 1017–1025.
-
34.
Farhang-Azad A, Traub R, Sofi M, Wisseman CL Jr , 1984. Experimental murine typhus infection in the cat flea, Ctenocephalides felis (Siphonaptera: Pulicidae). J Med Entomol 21: 675–680.
-
35.
Farhang-Azad A, Traub R, Wisseman CL Jr , 1983. Rickettsia mooseri infection in the fleas Leptopsylla segnis and Xenopsylla cheopis. Am J Trop Med Hyg 32: 1392–1400.
-
36.
Mooser H , 1928. Experiments relating to the pathology and the etiology of Mexican typhus (tabardillo): 2. Diplobacillus from the proliferated tunica vaginalis of guinea-pigs reacting to Mexican typhus. J Infect Dis 43: 261–272.
-
37.
Pinkerton H, Hass GM , 1932. Typhus Fever: V. The Effect of temperature on the multiplication of Rickettsia prowazeki in tissue culture. J Exp Med 56: 145–150.
-
38.
Wike DA, Tallent G, Peacock MG, Ormsbee RA , 1972. Studies of the rickettsial plaque assay technique. Infect Immun 5: 715–722.
-
39.
Kraus DB, Fadem BH , 1987. Reproduction, development and physiology of the gray short-tailed opossum (Monodelphis domestica). Lab Anim Sci 37: 478–482.
-
40.
Haro P, Ruiz-Pina HA, Canche-Pool EB, Medina S, Mercado JA , 2018. Physiological basal parameters of free-ranging opossums (Didelphis virginiana) in the Yucatan Peninsula, Mexico. J Zoo Wildl Med 49: 480–483.
-
41.
Bozeman FM, Shiral A, Humphries JW, Fuller HS , 1967. Ecology of Rocky Mountain spotted fever. II. Natural infection of wild mammals and birds in Virginia and Maryland. Am J Trop Med Hyg 16: 48–59.
-
42.
Horta MC, Moraes-Filho J, Casagrande RA, Saito TB, Rosa SC, Ogrzewalska M, Matushima ER, Labruna MB , 2009. Experimental infection of opossums Didelphis aurita by Rickettsia rickettsii and evaluation of the transmission of the infection to ticks Amblyomma cajennense. Vector Borne Zoonotic Dis 9: 109–118.
-
43.
Horta MC, Sabatini GS, Moraes-Filho J, Ogrzewalska M, Canal RB, Pacheco RC, Martins TF, Matushima ER, Labruna MB , 2010. Experimental infection of the opossum Didelphis aurita by Rickettsia felis, Rickettsia bellii, and Rickettsia parkeri and evaluation of the transmission of the infection to ticks Amblyomma cajennense and Amblyomma dubitatum. Vector Borne Zoonotic Dis 10: 959–967.
-
44.
Dias Cordeiro M, de Azevedo Baeta B, Barizon Cepeda M, da Fonseca AH , 2020. Experimental infection of Monodelphis domestica with Rickettsia parkeri. Ticks Tick Borne Dis 11: 101366.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 1802 | 844 | 106 |
| Full Text Views | 209 | 73 | 2 |
| PDF Downloads | 182 | 28 | 2 |