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Intensity and duration of Borrelia burgdorferi and Babesia microti infectivity in rodent hosts
Inrenzarionallournaifor Printed in Great Brimin.
Pamsirology
Vol. 18. No. 5, pp. 687-689,
0020-75
I98M. Q 1988
Ausrmlion
19/88 $3.00 + 0.00 Pergamon Press plc Society for Parasitology.
RESEARCHNOTE
INTENSITY AND DURATION OF BORRELIA BURGDORFERI AND BABESIA hfICRO7’I INFECTIVITY IN RODENT HOSTS JOSEPH PIESMAN Department of Epidemiology, School of public Health, University of Alabama at Birmingham, University Station, Birmingham, AL 35294, U.S.A. (Received 28 January 1988; accepted 8 February 1988) Abstract-PmMm
J. 1988. Intensity and duration of Borreliu burgdorferi and Babesia microti infectivity in rodent hosts. International Journal for Parasitology 18: 687-689. Hamsters were simultaneously infected with Borrelia burgdorferi and Babesia microti and subsequently exposed to xenodiagnostic larval Ixodes dammini at 1,4 and 7 months post-infection. The proportion of ticks acquiring Borreliu infection (1 month = 85%; 4 month = 44%; 7 month = 50%) was significantly greater than the-proportion acquiring Babesia infection (1 month = 73%; 4 month = 3%; 7 month = 16%). Hamsters maintained infectivity for Bo. burgdotferi and Ba. microti for at least 7 months.
INDEX KEY WORDS: Bubesia microti; Borrelia burgdorferi; human babesiosis; Lyme disease; infectivity; transmission; ticks; Ixodes dummini; hamsters.
RODENTS, particularly
the
white-footed
and maintained as previously described (Piesman, Karakashian, Lewengrub, Rudzinska & Spiehnan, 1986). The ‘JDl’ strain of Bo. burgdorferi, originating from Crane’s Beach, Ipswich, MA, USA., was isolated and maintained as previously described (Piesman et&., 1987). At intervals of 1, 4 and 7 months post-exposure to infected nymphs, each hamster was fed upon by larval 1. dammini derived from a laboratory colony free of Borrelia and Babesiu. These feedings constituted a form of ‘xenodiagnosis’ to determine host infectivity (Donahue, Piesman & Spielman, 1987). Replete ‘xeno’ larvae were maintained at 2 1 ‘C, 97% R.H., and allowed to molt to nymphs. Nymphal Z. dammini derived from ‘xeno’ larvae were allowed to feed on a non-infected hamster for 54 h. Subsequently, the salivary glands were dissected from each tick, stained with Feulgen’s, and examined for Ba. microti sporozoites as previously described (Piesman, Karakashian, Lewengrub, Rudzinska & Spielman, 1986). The midguts from these same ticks were examined for Bo. burgdorferi spirochetes by darkfield and directfluorescent-microscopy as previously described (Piesman, Mather, Donahue, Levine, Campbell, Karakashian & Spielman, 1986). A total of 48 ticks fed on Hamster A and 5 1 fed on Hamster B (Fig. 1). Of these 99 ticks, 68 (68.7%) became infected with Bo. burgdorferi as compared to 30 (30.3%) acquiring Ba. microti (Chisquare = 5.17, P-C 0.05). At 1 month post-hamsterinfection, the overall proportion of ticks acquiring Borrelia (85%) and Babesiu (73%) was similar. The
mouse
leucopus), are the principal reservoirs of the etiologic agents of human babesiosis (Babesia microti) and Lyme disease (Borrelia burgdorferi). In (Peromyscus
highly endemic regions of the northeastern United States, the proportion of rodents infected with Borrelia and Babesia can reach >75% (Anderson, Johnson, Magnarelli & Hyde, 1985; Spielman, Etkind, Piesman, Ruebush II, Juranek & Jacobs, 198 1). Spirochetal infection, however, is generally more prevalent in the vector tick (Zxodes dummini) than is babesial infection. In eastern Massachusetts, 24% of nymphal I. dammini were infected with Bo. burgdorferi, while only 11% were infected with Bu. microti (a ratio of 2.2 .to 1) (Piesman, Mather, Donahue, Levine, Campbell, Karakashian & Spielman, 1986). A possible explanation for the elevated prevalence of Borrelia infection, as compared to Babesiu infection, in I. dammini is that rodent reservoir hosts maintain a greater degree of infectivity for Borrelia. To test this hypothesis, we determined the intensity and duration of Borrelia and Babesia infectivity in rodent hosts. Johnson, Marek & Kodner (1984) and Piesman & Spielman (1982) have shown that hamsters are efficient laboratory hosts of Bo. burgdorferi and Ba. microti, respectively. A total of two female hamsters (50-150 g) served as hosts for individual 1. dummini nymphs dually infected with Bo. burgdorferi and Ba. microti as previously described (Piesman, Hicks, Sinsky & Obiri, 1987). The ‘GI’ strain of Ba. microti,
originating on Nantucket Is., MA, U.S.A., was isolated 687
688
J. PIESMAN
HAMSTER 100
r
100
A
r
1
months
months
postinfection
HAMSTER
4
T
postinfection
B
13 1
months FIG.
4
postinfection
months
postinfection
1. Intensity and duration of Bo. burgdo@ti and Bu. microti infectivity in two hamsters (A and B). Numbers above bars represent No. of xenodiagnostic Ixodesdammini ticks examined.
propo~on of Borrelia infected ticks at 4 months (44%) dropped to about half the level at 1 month, whereas the proportion of Babesia infected ticks at 4 months (3%) was
as infective hosts for larval I. damming during late summer-early fall (August-September). Thus, rodents must remain infective for Borrelia and Babesia for 2-4 months, in order to maintain the natural enzootic cycle of these pathogens. In the present study, the infectivity of rodents for Bo. burgdcxfkri was greater than that for Ba. microti, pa~cuIarly at 4 months post-infection, The diminished relative host infectivity of rodents infected with Babesia for 4 months may partially explain why Bo. burgdorferi infection is more prevalent in I. dammini than is Ba. microti infection. Other factors, such as the role of avian hosts (Anderson, Johnson, Magnarelli & Hyde, 1986) as secondary reservoirs of
Research Note Bo. burgdorferi,
relative prevalence mini populations.
may also contribute to the greater of Borreliu infection in I. dam-
Borrelia burgdorferi and Ba. microti are long-lived infections in rodent hosts. Johnson et al. (1984) noted that hamsters were infected with Bo. burgdorferi for at least 52 days, and Burgdorfer & Gage (1987) noted that hispid cotton rats retained infection for 55 days. Moreover, Donahue et al. (1987) observed that hamsters infected with Bo. burgdorferi were still infective for ticks at about 6 months post-infection. Similarly, Spielman et al. (198 1) observed Ba. microti infection in naturally infected P. leucopus for 4 months duration. The long-lived nature of Borrelia and Babesia infections in rodents may provide a mechanism for overwintering of these pathogens. Spielman, Wilson, Levine & Piesman (1985) have suggested that the primary overwintering mechanism of Bo. burgdorferi and Ba. microti is probably survival within nymphal I. dammini. Survival within overwintering rodents, however, may provide Bo. burgdo@ri and Ba. microti with an alternative overwintering mechanism.
REFERENCES ANDERSON J. F., JOHNSON R. C., MAGNARELLI L. A. & HYDE F. W. 1985. Identification of endemic foci of Lyme disease: isolation of Borrelia burgdo@% from feral rodents and ticks (Dermacentor v&iab&). Journal of Clinical Microbioloav 22: 36-38. ANDERSON J. F., JO&SON R. C., MAGNARELLI L. A. & HYDE F. W. 1986. Involvement of birds in the epidemiology of the Lyme disease agent Borrelia burgdo@?. Infection and Immunity 51: 394-396. BURGDORFER W. & GAGE K. L. 1987. Susceptibility of the
689
hispid cotton rat (Sigmodon hispidus) to the Lyme disease sp;ochete (Borr& burgdo&). American Journal of Trooical Medicine and Hvaiene 37: 624-628. DONA~LJE J. G., PIESMAN J.‘g SPIELMANA. 1987. Reservoir competence of white-footed mice for Lyme disease spirochetes. American Journal of Tropical Medicine and Hygiene 36: 92-96. JOHNSON R. C., MAREK N. & KODNER C. 1984. Infection of Syrian hamsters with Lyme disease spirochetes. Journal of Clinical Microbiology 20: 1099-l 101. PIESMAN J. & SPIELMAN A. 1979. Host-associations and seasonal abundance of immature Ixodes dammini in southeastern Massachusetts. Annals of the Entomological Society ofAmerica 72: 829-832. PIESMAN J. & SPIELMAN A. 1982. Babesia microti: infectivity of parasites from ticks for hamsters and whitefooted mice. Experimental Parasitology 53: 242-248. PIESMAN J., KARAKASHIANS. J., LEWENGRUB S., RUDZINSKA M. A. & SPIELMAN A. 1986. Development of Babesia microti sporozoites in adult Ixodes dammini. InternationalJournalfor Parasitology 16: 381-385. PIESMAN J., MATHER T. N., DONAHUE J. G., LEVINE J., CAMPBELL J. D., KARAKASHIAN S. J. & SPIELMAN A. 1986. Comparative prevalence of Babesia microti and Borrelia burgdorferi in four populations of Ixodes dammini in eastern Massachusetts. Acta Tropica 43: 263-270. PIESMAN J., HICKS T. C., SINSKY R. & OBIRI G. 1987. Simultaneous transmission of Borrelia burgdoeeri and Babesia microti by individual nymphal Ixodes dammini ticks. Journal of Clinical Microbiology 25: 2012-2013. SPIELMAN A., ETKIND P., PIESMAN J., RUEBUSH II T. K., JURANEK D. D. &JACOBS M. S. 1981. Reservoir hosts of human babesiosis on Nantucket Island. American Journal of Tropical Medicine and Hygiene 30: 560-565. SPIELMAN A., WILSON M. L., LEVINE J. F. & PIESMAN J. 1985. Ecology of Ixodes dammini-borne human babesiosis and Lyme disease. Annual Review of Entomology 30: 439-460.
Pamsirology
Vol. 18. No. 5, pp. 687-689,
0020-75
I98M. Q 1988
Ausrmlion
19/88 $3.00 + 0.00 Pergamon Press plc Society for Parasitology.
RESEARCHNOTE
INTENSITY AND DURATION OF BORRELIA BURGDORFERI AND BABESIA hfICRO7’I INFECTIVITY IN RODENT HOSTS JOSEPH PIESMAN Department of Epidemiology, School of public Health, University of Alabama at Birmingham, University Station, Birmingham, AL 35294, U.S.A. (Received 28 January 1988; accepted 8 February 1988) Abstract-PmMm
J. 1988. Intensity and duration of Borreliu burgdorferi and Babesia microti infectivity in rodent hosts. International Journal for Parasitology 18: 687-689. Hamsters were simultaneously infected with Borrelia burgdorferi and Babesia microti and subsequently exposed to xenodiagnostic larval Ixodes dammini at 1,4 and 7 months post-infection. The proportion of ticks acquiring Borreliu infection (1 month = 85%; 4 month = 44%; 7 month = 50%) was significantly greater than the-proportion acquiring Babesia infection (1 month = 73%; 4 month = 3%; 7 month = 16%). Hamsters maintained infectivity for Bo. burgdotferi and Ba. microti for at least 7 months.
INDEX KEY WORDS: Bubesia microti; Borrelia burgdorferi; human babesiosis; Lyme disease; infectivity; transmission; ticks; Ixodes dummini; hamsters.
RODENTS, particularly
the
white-footed
and maintained as previously described (Piesman, Karakashian, Lewengrub, Rudzinska & Spiehnan, 1986). The ‘JDl’ strain of Bo. burgdorferi, originating from Crane’s Beach, Ipswich, MA, USA., was isolated and maintained as previously described (Piesman et&., 1987). At intervals of 1, 4 and 7 months post-exposure to infected nymphs, each hamster was fed upon by larval 1. dammini derived from a laboratory colony free of Borrelia and Babesiu. These feedings constituted a form of ‘xenodiagnosis’ to determine host infectivity (Donahue, Piesman & Spielman, 1987). Replete ‘xeno’ larvae were maintained at 2 1 ‘C, 97% R.H., and allowed to molt to nymphs. Nymphal Z. dammini derived from ‘xeno’ larvae were allowed to feed on a non-infected hamster for 54 h. Subsequently, the salivary glands were dissected from each tick, stained with Feulgen’s, and examined for Ba. microti sporozoites as previously described (Piesman, Karakashian, Lewengrub, Rudzinska & Spielman, 1986). The midguts from these same ticks were examined for Bo. burgdorferi spirochetes by darkfield and directfluorescent-microscopy as previously described (Piesman, Mather, Donahue, Levine, Campbell, Karakashian & Spielman, 1986). A total of 48 ticks fed on Hamster A and 5 1 fed on Hamster B (Fig. 1). Of these 99 ticks, 68 (68.7%) became infected with Bo. burgdorferi as compared to 30 (30.3%) acquiring Ba. microti (Chisquare = 5.17, P-C 0.05). At 1 month post-hamsterinfection, the overall proportion of ticks acquiring Borrelia (85%) and Babesiu (73%) was similar. The
mouse
leucopus), are the principal reservoirs of the etiologic agents of human babesiosis (Babesia microti) and Lyme disease (Borrelia burgdorferi). In (Peromyscus
highly endemic regions of the northeastern United States, the proportion of rodents infected with Borrelia and Babesia can reach >75% (Anderson, Johnson, Magnarelli & Hyde, 1985; Spielman, Etkind, Piesman, Ruebush II, Juranek & Jacobs, 198 1). Spirochetal infection, however, is generally more prevalent in the vector tick (Zxodes dummini) than is babesial infection. In eastern Massachusetts, 24% of nymphal I. dammini were infected with Bo. burgdorferi, while only 11% were infected with Bu. microti (a ratio of 2.2 .to 1) (Piesman, Mather, Donahue, Levine, Campbell, Karakashian & Spielman, 1986). A possible explanation for the elevated prevalence of Borrelia infection, as compared to Babesiu infection, in I. dammini is that rodent reservoir hosts maintain a greater degree of infectivity for Borrelia. To test this hypothesis, we determined the intensity and duration of Borrelia and Babesia infectivity in rodent hosts. Johnson, Marek & Kodner (1984) and Piesman & Spielman (1982) have shown that hamsters are efficient laboratory hosts of Bo. burgdorferi and Ba. microti, respectively. A total of two female hamsters (50-150 g) served as hosts for individual 1. dummini nymphs dually infected with Bo. burgdorferi and Ba. microti as previously described (Piesman, Hicks, Sinsky & Obiri, 1987). The ‘GI’ strain of Ba. microti,
originating on Nantucket Is., MA, U.S.A., was isolated 687
688
J. PIESMAN
HAMSTER 100
r
100
A
r
1
months
months
postinfection
HAMSTER
4
T
postinfection
B
13 1
months FIG.
4
postinfection
months
postinfection
1. Intensity and duration of Bo. burgdo@ti and Bu. microti infectivity in two hamsters (A and B). Numbers above bars represent No. of xenodiagnostic Ixodesdammini ticks examined.
propo~on of Borrelia infected ticks at 4 months (44%) dropped to about half the level at 1 month, whereas the proportion of Babesia infected ticks at 4 months (3%) was
as infective hosts for larval I. damming during late summer-early fall (August-September). Thus, rodents must remain infective for Borrelia and Babesia for 2-4 months, in order to maintain the natural enzootic cycle of these pathogens. In the present study, the infectivity of rodents for Bo. burgdcxfkri was greater than that for Ba. microti, pa~cuIarly at 4 months post-infection, The diminished relative host infectivity of rodents infected with Babesia for 4 months may partially explain why Bo. burgdorferi infection is more prevalent in I. dammini than is Ba. microti infection. Other factors, such as the role of avian hosts (Anderson, Johnson, Magnarelli & Hyde, 1986) as secondary reservoirs of
Research Note Bo. burgdorferi,
relative prevalence mini populations.
may also contribute to the greater of Borreliu infection in I. dam-
Borrelia burgdorferi and Ba. microti are long-lived infections in rodent hosts. Johnson et al. (1984) noted that hamsters were infected with Bo. burgdorferi for at least 52 days, and Burgdorfer & Gage (1987) noted that hispid cotton rats retained infection for 55 days. Moreover, Donahue et al. (1987) observed that hamsters infected with Bo. burgdorferi were still infective for ticks at about 6 months post-infection. Similarly, Spielman et al. (198 1) observed Ba. microti infection in naturally infected P. leucopus for 4 months duration. The long-lived nature of Borrelia and Babesia infections in rodents may provide a mechanism for overwintering of these pathogens. Spielman, Wilson, Levine & Piesman (1985) have suggested that the primary overwintering mechanism of Bo. burgdorferi and Ba. microti is probably survival within nymphal I. dammini. Survival within overwintering rodents, however, may provide Bo. burgdo@ri and Ba. microti with an alternative overwintering mechanism.
REFERENCES ANDERSON J. F., JOHNSON R. C., MAGNARELLI L. A. & HYDE F. W. 1985. Identification of endemic foci of Lyme disease: isolation of Borrelia burgdo@% from feral rodents and ticks (Dermacentor v&iab&). Journal of Clinical Microbioloav 22: 36-38. ANDERSON J. F., JO&SON R. C., MAGNARELLI L. A. & HYDE F. W. 1986. Involvement of birds in the epidemiology of the Lyme disease agent Borrelia burgdo@?. Infection and Immunity 51: 394-396. BURGDORFER W. & GAGE K. L. 1987. Susceptibility of the
689
hispid cotton rat (Sigmodon hispidus) to the Lyme disease sp;ochete (Borr& burgdo&). American Journal of Trooical Medicine and Hvaiene 37: 624-628. DONA~LJE J. G., PIESMAN J.‘g SPIELMANA. 1987. Reservoir competence of white-footed mice for Lyme disease spirochetes. American Journal of Tropical Medicine and Hygiene 36: 92-96. JOHNSON R. C., MAREK N. & KODNER C. 1984. Infection of Syrian hamsters with Lyme disease spirochetes. Journal of Clinical Microbiology 20: 1099-l 101. PIESMAN J. & SPIELMAN A. 1979. Host-associations and seasonal abundance of immature Ixodes dammini in southeastern Massachusetts. Annals of the Entomological Society ofAmerica 72: 829-832. PIESMAN J. & SPIELMAN A. 1982. Babesia microti: infectivity of parasites from ticks for hamsters and whitefooted mice. Experimental Parasitology 53: 242-248. PIESMAN J., KARAKASHIANS. J., LEWENGRUB S., RUDZINSKA M. A. & SPIELMAN A. 1986. Development of Babesia microti sporozoites in adult Ixodes dammini. InternationalJournalfor Parasitology 16: 381-385. PIESMAN J., MATHER T. N., DONAHUE J. G., LEVINE J., CAMPBELL J. D., KARAKASHIAN S. J. & SPIELMAN A. 1986. Comparative prevalence of Babesia microti and Borrelia burgdorferi in four populations of Ixodes dammini in eastern Massachusetts. Acta Tropica 43: 263-270. PIESMAN J., HICKS T. C., SINSKY R. & OBIRI G. 1987. Simultaneous transmission of Borrelia burgdoeeri and Babesia microti by individual nymphal Ixodes dammini ticks. Journal of Clinical Microbiology 25: 2012-2013. SPIELMAN A., ETKIND P., PIESMAN J., RUEBUSH II T. K., JURANEK D. D. &JACOBS M. S. 1981. Reservoir hosts of human babesiosis on Nantucket Island. American Journal of Tropical Medicine and Hygiene 30: 560-565. SPIELMAN A., WILSON M. L., LEVINE J. F. & PIESMAN J. 1985. Ecology of Ixodes dammini-borne human babesiosis and Lyme disease. Annual Review of Entomology 30: 439-460.