CBC's Ottawa Morning Interviewed the president of AMMI about the status of Lyme disease in Canada, and the goals of the Federal Framework. Dr. Vett Lloyd, co-founder of the CLSA, provides her critique below.
In an interview on March 10, 2017, on CBC radio (Ottawa Morning), Dr. Caroline Quach, the president of Association of Medical Microbiology and Infectious Disease Canada made the following statements.
“I think that when we come up with a framework or with guidelines, what we really want is to have evidence-based data and so I think that patient experience will come in there. As you know there is a problem that needs to be addressed; now how it will be addressed is unclear to most of us right because if there’s we need to better educate the population on how to prevent Lyme disease; we also need to have money to do research, and to understand why these people are suffering, and what’s actually causing their illness. So, in terms of that framework, I think it’s a basis for a start of a conversation. Where it will end is impossible to know.”
We agree completely that this is a conversation that needs to happen. And we agree completely that the conversation and actions need to be evidence based. Regrettably, during the interview Dr. Quach made 8 statements relating to science, of which 6 were factually incorrect.
We trust that Dr. Quach did not really mean to imply that patients should be forced to participate in experimental trials when she said “aside from doing research, and from studying patients, making them enter trials, having clinics where these patients could be treated and tested, I don’t think that there’s a way to actually be able to know what’s happening.” But if the federal framework Lyme conference showed nothing else, it showed that we know very little about this disease and that there is a chasm between the research priorities of Lyme patients and AMMI. This makes it critical to include Lyme patients as equal partners in every stage of our response to this disease. This chasm needs to be breached and communication that is both respectful and accurate is required.
The comments from Dr. Quach, followed by a summary of the findings of that topic from the current peer-reviewed scientific literature are below.
1. “In fact what happens is that currently there is no scientific evidence in the medical literature that Lyme Disease can become chronic”.
“… but once treated with anti-microbials for um a maximum of 4-6 weeks, sometimes with a repeater treatment, there’s no evidence that it actually becomes chronic …”
There are numerous investigations performed by unrelated research teams that utilized a variety of model systems, both in vitro and in vivo in organisms from mice to monkeys and humans, have demonstrated evidence of residual Borrelia following acute infection and antimicrobial intervention (1-4). Although the case is far from closed, the scientific and medical communities would be deeply remiss to ignore the evidence that continues to amass.
2. Quach: “And so, that laboratory when you pay for your test to be sent there will diagnose you with Lyme, whereas it wouldn’t be picked up in and not diagnosed because it’s not Lyme.”
It is unclear which laboratory is under discussion here, however, most private Lyme disease testing includes serological diagnostics based on ELISA and Immunoblot (Western blot) testing. These methodologies are well established and routinely used in Borrelia testing, as well as for the testing of many other diseases. What is in dispute in the context of Lyme borreliosis is the algorithm used to evaluate the test results. Both the testing and the algorithms in private laboratories were well described by Fallon et al. (2014) (5). All the laboratories provided results with good sensitivities, the specificity was poor only if multiple inappropriate interpretations of the results were used. It should also be noted that no laboratories provide a diagnosis – this is provided by a physician -and that the payment is rendered for the test not the result; the payment is not altered by the test result and the implication that people purchase specific test outcomes is both incorrect and libelous.
3. “What we know is that Lyme disease is transmitted by a tick bite …”
This statement is correct, has been known for some decades(6) and is not contested. What is more problematic is the possibility of other modes of transmission.
Presenter: “On yesterday’s show we heard here that research into Lyme disease still of course very much a live topic, it’s ongoing: And we also heard that it may be possible to transmit the disease in ways not previously considered or talked about very much at least, namely that the disease may be transferred in the womb or through sexual contact or through mosquitoes. What is your feeling about that? Can Lyme Disease be transmitted in the womb, for example?”
Quach: “Well then again, there’s no evidence that that is actually um happening. And in fact even in animal models, in mice that were infected with Lyme disease did not transmit it to their offspring. So there’s no animal models to support it and hasn’t been any evidence in the, in humans that that has happened, at least not reported in the literature. I think that as for everything we have peer review journals that review articles from scientists and so as long as that data is not available to the medical literature, to us at least there’s no proof that it actually happens, so [transmission is not] from breast milk or through sexual contact or through mosquito bites.
4. Congenital transmission:
There are certainly case reports of congenital infection of Borrelia and related tick vectored diseases in humans. (7-9) These tend to be older and the power of more recent epidemiological studies in humans was insufficient to resolve this issue.(10-12) Moreover, most human studies have focused on the potential of Borreliosis to cause adverse pregnancy outcomes, and did not focus on the long-term health of the child.(33) In animal models, Gustafson et al. 1993 (13) did find congenital transmission in dogs and Burgess et al (1993) in wild mice (14). While it is correct that Silver et al (1995) (15) showed that infected mice did not pass the infection to their pups it is also important to note that they did report significant mortality of the pups of infected mothers. These findings are of obvious concern to pregnant mothers and deserves to be better assessed.
5 Sexual transmission: There is considerable evidence in animal studies of contact transmission, of which sexual transmission is one type, in diverse animals including mice, dogs, horses, cows and ducks. (16-26) There are, of course, also published papers where such evidence was not found. (27-29) There is one paper, albeit contentious (as is so much with Lyme) reporting isolation of viable B. burgdorferi in human genital secretions. (30)
6. Mosquitoes as vectors: There are certainly reports of mosquitoes carrying Borrelia sp. (31, 32) This does not mean that mosquitoes are vectors. But given the abundance of mosquitoes, it does mean that the vectoral capacity of the mosquito species present in Canada should be directly addressed rather than dismissed.
7. Breast milk: Indeed, transmission of Borrelia has not been found in cow or human breast milk but this area remains relatively poorly investigated. (14, 33)
8. Currently it’s really being transmitted through Lyme tick bites – [ticks] that need to be attached to the human for at least 36 hours..”
Cook (2015) (34) provides an extensive review on this subject. Transmission time depends on the tick species, host species and prior tick activity (interrupted feeding). Cases of transmission within 24 hours have been documented in animal studies and in humans (35).
1. Rudenko N, Golovchenko M, Vancova M, Clark K, Grubhoffer L, Oliver JH Jr. 2016. Isolation of live Borrelia burgdorferi sensu lato spirochaetes from patients with undefined disorders and symptoms not typical for Lyme borreliosis. Clin Microbiol Infect 22:267.e9–267.e15.
2. Hodzic E, Imai D, Feng S, Barthold SW. 2014. Resurgence of Persisting Non- Cultivable Borrelia burgdorferi following Antibiotic Treatment in Mice. PLoS ONE 9:e86907–12.
3. Embers ME, Barthold SW, Borda JT, Bowers L, Doyle L, Hodzic E, Jacobs MB, Hasenkampf NR, Martin DS, Narasimhan S, Phillippi-Falkenstein KM, Purcell JE, Ratterree MS, Philipp MT. 2012. Persistence of Borrelia burgdorferi in Rhesus Macaques following Antibiotic Treatment of Disseminated Infection. PLoS ONE 7:e29914.
4.Hunfeld KP, Ružić-Sabljić E, Norris DE, Kraiczy P, Strle F. 2005. In Vitro Susceptibility Testing of Borrelia burgdorferi Sensu Lato Isolates Cultured from Patients with Erythema Migrans before and after Antimicrobial Chemotherapy. Antimicrob Agents Chemother 49:1294–1301.
5. Fallon BA, Pavlicova M, Coffino SW, Brenner C. A comparison of lyme disease serologic test results from 4 laboratories in patients with persistent symptoms after antibiotic treatment. Clin Infect Dis. 2014 Dec 15;59(12):1705-10. doi: 10.1093/cid/ciu703.
6. (Burgdorfer W, Barbour AG, Hayes SF, Benach JL, Grunwaldt E, Davis JP (June 1982). "Lyme disease-a tick-borne spirochetosis?". Science. 216 (4552): 1317–9. Bibcode:1982Sci...216.1317B. doi:10.1126/science.7043737. PMID 7043737.).
7. Weber K, Bratzke H-J, Neubert U, Wilske B, Duray PH. Borrelia burgdorferi in a newborn despite oral penicillin for Lyme borreliosis during pregnancy. The Pediatric Infectious Disease Journal. 1988;7(4):286–288. doi:10.1097/00006454-198804000-00010.
8. Schlesinger PA, Duray PH, Burke BA, Steere AC, Stillman MT. Maternal-fetal transmission of the Lyme disease Spirochete, Borrelia burgdorferi. Annals of Internal Medicine. 1985;103(1):67. doi:10.7326/0003-4819-103-1-67.
9. Brzostek T. [Human granulocytic ehrlichiosis co-incident with Lyme borreliosis in pregnant woman--a case study] [in Polish] Przegl Epidemiol. 2004;58(2):289–94.
10. Strobino BA, Williams CL, Abid S, Ghalson R, Spierling P. Lyme disease and pregnancy outcome: A prospective s of two thousand prenatal patients. American Journal of Obstetrics and Gynecology. 1993;169(2):367–374. doi:10.1016/0002-9378(93)90088-z.
11. Markowitz LE, Steere AC, Benach JL, Slade JD, Broome CV. Lyme disease during pregnancy. JAMA: The Journal of the American Medical Association. 1986;255(24):3394. doi:10.1001/jama.1986.03370240064038.
12. Maraspin V, Cimperman J, Lotric-Furlan S, Pleterski-Rigler D, Strle F. Erythema migrans in pregnancy. Wiener klinische Wochenschrift. 2000;111:933–40.
13. Gustafson JM, Burgess EC, Wachal MD, Steinberg H. Intrauterine transmission of Borrelia burgdorferi in dogs. American Journal of Veterinary Research. 1993;54(6):882–890.
14. Burgess EC1, Wachal MD, Cleven TD.Borrelia burgdorferi infection in dairy cows, rodents, and birds from four Wisconsin dairy farms. Vet Microbiol. 1993 May;35(1-2):61-77.
15. Silver RM, Yang L, Daynes RA, Branch WD, Salafia CM, Weis JJ. Fetal outcome in Murine Lyme disease. Infection and Immunity. 1995;63(1):66–72.
16.Bosler EM, Schulze TL. (1986) The prevalence and significance of Borrelia burgdorferi in the urine of feral reservoir hosts. Zentralbl Bakteriol Mikrobiol Hyg A. 263(1-2):40-4.
17.Burgess EC, Amundson TE, Davis JP, et al.: Experimental inoculation of Peromyscus spp. with Borrelia burgdorferi: evidence of contact transmission. Am J Trop Med Hyg. 1986; 35(2): 355–9.
18.Burgess EC, Patrican LA: Oral infection of Peromyscus maniculatus with Borrelia burgdorferi and subsequent transmission by Ixodes dammini. Am J Trop Med Hyg. 1987; 36(2): 402–7.
19.Burgess EC: Experimental inoculation of mallard ducks (Anas platyrhynchos platyrhynchos) with Borrelia burgdorferi. J Wildl Dis. 1989; 25(1): 99–102.
20.Burgess EC: Experimentally induced infection of cats with Borrelia burgdorferi. Am J Vet Res. 1992; 53(9): 1507–11.
21.Burgess EC. (1986) Experimental inoculation of dogs with Borrelia burgdorferi. Zentralbl Bakteriol Mikrobiol Hyg A. 263(1-2):49-54.
22.Burgess EC. (1988) Borrelia burgdorferi infection in Wisconsin horses and cows. Ann N Y Acad Sci. 539:235-43.
23.Cerri D, Farina R, Andreani E, Nuvoloni R, Pedrini A, Cardini G. (1994) Experimental infection of dogs with Borrelia burgdorferi. Res Vet Sci. 57(2):256-8.
24.Renal lesions associated with Borrelia burgdorferi infection in a dog.
Grauer GF, Burgess EC, Cooley AJ, Hagee JH. J Am Vet Med Assoc. 1988 Jul 15;193(2):237-9.
25.Greene RT, Levine JF, Breitschwerdt EB, Walker RL, Berkhoff HA, Cullen J, 21Nicholson WL. (1988) Clinical and serologic evaluations of induced Borrelia burgdorferi infection in dogs. Am J Vet Res. 49(6):752-7.
26. Wright SD, Nielsen SW: Experimental infection of the white-footed mouse with Borrelia burgdorferi. Am J Vet Res. 1990; 51(12): 1980–7.
27. Appel MJ, Allan S, Jacobson RH, Lauderdale TL, Chang YF, Shin SJ, Thomford JW, Todhunter RJ, Summers BA. (1993) Experimental Lyme disease in dogs produces arthritis and persistent infection. J Infect Dis. 167(3):651-64.
28. Moody KD, Barthold SW: Relative infectivity of Borrelia burgdorferi in Lewis rats by various routes of inoculation. Amer J Trop Med Hyg. 1991; 44(2): 135–9.
29. Woodrum JE, Oliver JH Jr: Investigation of venereal, transplacental, and contact transmission of the Lyme disease spirochete, Borrelia burgdorferi, in Syrian hamsters. J Parasitol. 1999; 85(3): 426–30.
30. Middelveen MJ, Burke J, Sapi E et al. Culture and identification of Borrelia spirochetes in human vaginal and seminal secretions [version 1; referees: 1 not approved]. F1000Research 2014, 3:309
(doi: 10.12688/f1000research.5778.1)
31. Melaun C, Zotzmann S, Santaella VG, Werblow A, Zumkowski-Xylander H, Kraiczy P, Klimpel S. Occurrence of Borrelia burgdorferi s.l. in different genera of mosquitoes (Culicidae) in Central Europe. Ticks Tick Borne Dis. 2016 Mar;7(2):256-63. doi: 10.1016/j.ttbdis.2015.10.018. Epub 2015 Nov 12.
32. Kosik-Bogacka DI, Kuźna-Grygiel W, Jaborowska M.Ticks and mosquitoes as vectors of Borrelia burgdorferi s. l. in the forested areas of Szczecin. Folia Biol (Krakow). 2007;55(3-4):143-6.
33. Mylonas I. Borreliosis during pregnancy: a risk for the unborn child? Vector Borne Zoonotic Dis. 2011 Jul;11(7):891-8. doi: 10.1089/vbz.2010.0102.
34 Cook M (2015) Lyme borreliosis: a review of data on transmission time after tick attachment. Int J Gen Med 8:1–8. doi: 10.2147/IJGM.S73791
35. Hynote ED, Mervine PC, Stricker RB (2012) Clinical evidence for rapid transmission of Lyme disease following a tickbite. Diagn Microbiol Infect Dis 72:188–192. doi: 10.1016/j.diagmicrobio.2011.10.003
“I think that when we come up with a framework or with guidelines, what we really want is to have evidence-based data and so I think that patient experience will come in there. As you know there is a problem that needs to be addressed; now how it will be addressed is unclear to most of us right because if there’s we need to better educate the population on how to prevent Lyme disease; we also need to have money to do research, and to understand why these people are suffering, and what’s actually causing their illness. So, in terms of that framework, I think it’s a basis for a start of a conversation. Where it will end is impossible to know.”
We agree completely that this is a conversation that needs to happen. And we agree completely that the conversation and actions need to be evidence based. Regrettably, during the interview Dr. Quach made 8 statements relating to science, of which 6 were factually incorrect.
We trust that Dr. Quach did not really mean to imply that patients should be forced to participate in experimental trials when she said “aside from doing research, and from studying patients, making them enter trials, having clinics where these patients could be treated and tested, I don’t think that there’s a way to actually be able to know what’s happening.” But if the federal framework Lyme conference showed nothing else, it showed that we know very little about this disease and that there is a chasm between the research priorities of Lyme patients and AMMI. This makes it critical to include Lyme patients as equal partners in every stage of our response to this disease. This chasm needs to be breached and communication that is both respectful and accurate is required.
The comments from Dr. Quach, followed by a summary of the findings of that topic from the current peer-reviewed scientific literature are below.
1. “In fact what happens is that currently there is no scientific evidence in the medical literature that Lyme Disease can become chronic”.
“… but once treated with anti-microbials for um a maximum of 4-6 weeks, sometimes with a repeater treatment, there’s no evidence that it actually becomes chronic …”
There are numerous investigations performed by unrelated research teams that utilized a variety of model systems, both in vitro and in vivo in organisms from mice to monkeys and humans, have demonstrated evidence of residual Borrelia following acute infection and antimicrobial intervention (1-4). Although the case is far from closed, the scientific and medical communities would be deeply remiss to ignore the evidence that continues to amass.
2. Quach: “And so, that laboratory when you pay for your test to be sent there will diagnose you with Lyme, whereas it wouldn’t be picked up in and not diagnosed because it’s not Lyme.”
It is unclear which laboratory is under discussion here, however, most private Lyme disease testing includes serological diagnostics based on ELISA and Immunoblot (Western blot) testing. These methodologies are well established and routinely used in Borrelia testing, as well as for the testing of many other diseases. What is in dispute in the context of Lyme borreliosis is the algorithm used to evaluate the test results. Both the testing and the algorithms in private laboratories were well described by Fallon et al. (2014) (5). All the laboratories provided results with good sensitivities, the specificity was poor only if multiple inappropriate interpretations of the results were used. It should also be noted that no laboratories provide a diagnosis – this is provided by a physician -and that the payment is rendered for the test not the result; the payment is not altered by the test result and the implication that people purchase specific test outcomes is both incorrect and libelous.
3. “What we know is that Lyme disease is transmitted by a tick bite …”
This statement is correct, has been known for some decades(6) and is not contested. What is more problematic is the possibility of other modes of transmission.
Presenter: “On yesterday’s show we heard here that research into Lyme disease still of course very much a live topic, it’s ongoing: And we also heard that it may be possible to transmit the disease in ways not previously considered or talked about very much at least, namely that the disease may be transferred in the womb or through sexual contact or through mosquitoes. What is your feeling about that? Can Lyme Disease be transmitted in the womb, for example?”
Quach: “Well then again, there’s no evidence that that is actually um happening. And in fact even in animal models, in mice that were infected with Lyme disease did not transmit it to their offspring. So there’s no animal models to support it and hasn’t been any evidence in the, in humans that that has happened, at least not reported in the literature. I think that as for everything we have peer review journals that review articles from scientists and so as long as that data is not available to the medical literature, to us at least there’s no proof that it actually happens, so [transmission is not] from breast milk or through sexual contact or through mosquito bites.
4. Congenital transmission:
There are certainly case reports of congenital infection of Borrelia and related tick vectored diseases in humans. (7-9) These tend to be older and the power of more recent epidemiological studies in humans was insufficient to resolve this issue.(10-12) Moreover, most human studies have focused on the potential of Borreliosis to cause adverse pregnancy outcomes, and did not focus on the long-term health of the child.(33) In animal models, Gustafson et al. 1993 (13) did find congenital transmission in dogs and Burgess et al (1993) in wild mice (14). While it is correct that Silver et al (1995) (15) showed that infected mice did not pass the infection to their pups it is also important to note that they did report significant mortality of the pups of infected mothers. These findings are of obvious concern to pregnant mothers and deserves to be better assessed.
5 Sexual transmission: There is considerable evidence in animal studies of contact transmission, of which sexual transmission is one type, in diverse animals including mice, dogs, horses, cows and ducks. (16-26) There are, of course, also published papers where such evidence was not found. (27-29) There is one paper, albeit contentious (as is so much with Lyme) reporting isolation of viable B. burgdorferi in human genital secretions. (30)
6. Mosquitoes as vectors: There are certainly reports of mosquitoes carrying Borrelia sp. (31, 32) This does not mean that mosquitoes are vectors. But given the abundance of mosquitoes, it does mean that the vectoral capacity of the mosquito species present in Canada should be directly addressed rather than dismissed.
7. Breast milk: Indeed, transmission of Borrelia has not been found in cow or human breast milk but this area remains relatively poorly investigated. (14, 33)
8. Currently it’s really being transmitted through Lyme tick bites – [ticks] that need to be attached to the human for at least 36 hours..”
Cook (2015) (34) provides an extensive review on this subject. Transmission time depends on the tick species, host species and prior tick activity (interrupted feeding). Cases of transmission within 24 hours have been documented in animal studies and in humans (35).
1. Rudenko N, Golovchenko M, Vancova M, Clark K, Grubhoffer L, Oliver JH Jr. 2016. Isolation of live Borrelia burgdorferi sensu lato spirochaetes from patients with undefined disorders and symptoms not typical for Lyme borreliosis. Clin Microbiol Infect 22:267.e9–267.e15.
2. Hodzic E, Imai D, Feng S, Barthold SW. 2014. Resurgence of Persisting Non- Cultivable Borrelia burgdorferi following Antibiotic Treatment in Mice. PLoS ONE 9:e86907–12.
3. Embers ME, Barthold SW, Borda JT, Bowers L, Doyle L, Hodzic E, Jacobs MB, Hasenkampf NR, Martin DS, Narasimhan S, Phillippi-Falkenstein KM, Purcell JE, Ratterree MS, Philipp MT. 2012. Persistence of Borrelia burgdorferi in Rhesus Macaques following Antibiotic Treatment of Disseminated Infection. PLoS ONE 7:e29914.
4.Hunfeld KP, Ružić-Sabljić E, Norris DE, Kraiczy P, Strle F. 2005. In Vitro Susceptibility Testing of Borrelia burgdorferi Sensu Lato Isolates Cultured from Patients with Erythema Migrans before and after Antimicrobial Chemotherapy. Antimicrob Agents Chemother 49:1294–1301.
5. Fallon BA, Pavlicova M, Coffino SW, Brenner C. A comparison of lyme disease serologic test results from 4 laboratories in patients with persistent symptoms after antibiotic treatment. Clin Infect Dis. 2014 Dec 15;59(12):1705-10. doi: 10.1093/cid/ciu703.
6. (Burgdorfer W, Barbour AG, Hayes SF, Benach JL, Grunwaldt E, Davis JP (June 1982). "Lyme disease-a tick-borne spirochetosis?". Science. 216 (4552): 1317–9. Bibcode:1982Sci...216.1317B. doi:10.1126/science.7043737. PMID 7043737.).
7. Weber K, Bratzke H-J, Neubert U, Wilske B, Duray PH. Borrelia burgdorferi in a newborn despite oral penicillin for Lyme borreliosis during pregnancy. The Pediatric Infectious Disease Journal. 1988;7(4):286–288. doi:10.1097/00006454-198804000-00010.
8. Schlesinger PA, Duray PH, Burke BA, Steere AC, Stillman MT. Maternal-fetal transmission of the Lyme disease Spirochete, Borrelia burgdorferi. Annals of Internal Medicine. 1985;103(1):67. doi:10.7326/0003-4819-103-1-67.
9. Brzostek T. [Human granulocytic ehrlichiosis co-incident with Lyme borreliosis in pregnant woman--a case study] [in Polish] Przegl Epidemiol. 2004;58(2):289–94.
10. Strobino BA, Williams CL, Abid S, Ghalson R, Spierling P. Lyme disease and pregnancy outcome: A prospective s of two thousand prenatal patients. American Journal of Obstetrics and Gynecology. 1993;169(2):367–374. doi:10.1016/0002-9378(93)90088-z.
11. Markowitz LE, Steere AC, Benach JL, Slade JD, Broome CV. Lyme disease during pregnancy. JAMA: The Journal of the American Medical Association. 1986;255(24):3394. doi:10.1001/jama.1986.03370240064038.
12. Maraspin V, Cimperman J, Lotric-Furlan S, Pleterski-Rigler D, Strle F. Erythema migrans in pregnancy. Wiener klinische Wochenschrift. 2000;111:933–40.
13. Gustafson JM, Burgess EC, Wachal MD, Steinberg H. Intrauterine transmission of Borrelia burgdorferi in dogs. American Journal of Veterinary Research. 1993;54(6):882–890.
14. Burgess EC1, Wachal MD, Cleven TD.Borrelia burgdorferi infection in dairy cows, rodents, and birds from four Wisconsin dairy farms. Vet Microbiol. 1993 May;35(1-2):61-77.
15. Silver RM, Yang L, Daynes RA, Branch WD, Salafia CM, Weis JJ. Fetal outcome in Murine Lyme disease. Infection and Immunity. 1995;63(1):66–72.
16.Bosler EM, Schulze TL. (1986) The prevalence and significance of Borrelia burgdorferi in the urine of feral reservoir hosts. Zentralbl Bakteriol Mikrobiol Hyg A. 263(1-2):40-4.
17.Burgess EC, Amundson TE, Davis JP, et al.: Experimental inoculation of Peromyscus spp. with Borrelia burgdorferi: evidence of contact transmission. Am J Trop Med Hyg. 1986; 35(2): 355–9.
18.Burgess EC, Patrican LA: Oral infection of Peromyscus maniculatus with Borrelia burgdorferi and subsequent transmission by Ixodes dammini. Am J Trop Med Hyg. 1987; 36(2): 402–7.
19.Burgess EC: Experimental inoculation of mallard ducks (Anas platyrhynchos platyrhynchos) with Borrelia burgdorferi. J Wildl Dis. 1989; 25(1): 99–102.
20.Burgess EC: Experimentally induced infection of cats with Borrelia burgdorferi. Am J Vet Res. 1992; 53(9): 1507–11.
21.Burgess EC. (1986) Experimental inoculation of dogs with Borrelia burgdorferi. Zentralbl Bakteriol Mikrobiol Hyg A. 263(1-2):49-54.
22.Burgess EC. (1988) Borrelia burgdorferi infection in Wisconsin horses and cows. Ann N Y Acad Sci. 539:235-43.
23.Cerri D, Farina R, Andreani E, Nuvoloni R, Pedrini A, Cardini G. (1994) Experimental infection of dogs with Borrelia burgdorferi. Res Vet Sci. 57(2):256-8.
24.Renal lesions associated with Borrelia burgdorferi infection in a dog.
Grauer GF, Burgess EC, Cooley AJ, Hagee JH. J Am Vet Med Assoc. 1988 Jul 15;193(2):237-9.
25.Greene RT, Levine JF, Breitschwerdt EB, Walker RL, Berkhoff HA, Cullen J, 21Nicholson WL. (1988) Clinical and serologic evaluations of induced Borrelia burgdorferi infection in dogs. Am J Vet Res. 49(6):752-7.
26. Wright SD, Nielsen SW: Experimental infection of the white-footed mouse with Borrelia burgdorferi. Am J Vet Res. 1990; 51(12): 1980–7.
27. Appel MJ, Allan S, Jacobson RH, Lauderdale TL, Chang YF, Shin SJ, Thomford JW, Todhunter RJ, Summers BA. (1993) Experimental Lyme disease in dogs produces arthritis and persistent infection. J Infect Dis. 167(3):651-64.
28. Moody KD, Barthold SW: Relative infectivity of Borrelia burgdorferi in Lewis rats by various routes of inoculation. Amer J Trop Med Hyg. 1991; 44(2): 135–9.
29. Woodrum JE, Oliver JH Jr: Investigation of venereal, transplacental, and contact transmission of the Lyme disease spirochete, Borrelia burgdorferi, in Syrian hamsters. J Parasitol. 1999; 85(3): 426–30.
30. Middelveen MJ, Burke J, Sapi E et al. Culture and identification of Borrelia spirochetes in human vaginal and seminal secretions [version 1; referees: 1 not approved]. F1000Research 2014, 3:309
(doi: 10.12688/f1000research.5778.1)
31. Melaun C, Zotzmann S, Santaella VG, Werblow A, Zumkowski-Xylander H, Kraiczy P, Klimpel S. Occurrence of Borrelia burgdorferi s.l. in different genera of mosquitoes (Culicidae) in Central Europe. Ticks Tick Borne Dis. 2016 Mar;7(2):256-63. doi: 10.1016/j.ttbdis.2015.10.018. Epub 2015 Nov 12.
32. Kosik-Bogacka DI, Kuźna-Grygiel W, Jaborowska M.Ticks and mosquitoes as vectors of Borrelia burgdorferi s. l. in the forested areas of Szczecin. Folia Biol (Krakow). 2007;55(3-4):143-6.
33. Mylonas I. Borreliosis during pregnancy: a risk for the unborn child? Vector Borne Zoonotic Dis. 2011 Jul;11(7):891-8. doi: 10.1089/vbz.2010.0102.
34 Cook M (2015) Lyme borreliosis: a review of data on transmission time after tick attachment. Int J Gen Med 8:1–8. doi: 10.2147/IJGM.S73791
35. Hynote ED, Mervine PC, Stricker RB (2012) Clinical evidence for rapid transmission of Lyme disease following a tickbite. Diagn Microbiol Infect Dis 72:188–192. doi: 10.1016/j.diagmicrobio.2011.10.003
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