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The first case of imported Borrelia miyamotoi disease concurrent with Lyme disease
J Infect Chemother xxx (2017) 1e3
Contents lists available at ScienceDirect
Journal of Infection and Chemotherapy journal homepage: http://www.elsevier.com/locate/jic
Case Report
The first case of imported Borrelia miyamotoi disease concurrent with Lyme disease Rentaro Oda a, *, Satoshi Kutsuna b, Yoshiyuki Sekikawa a, Igen Hongo a, Kozue Sato c, Makoto Ohnishi c, Hiroki Kawabata c a b c
Division of Infectious Diseases, Musashino Red Cross Hospital, Japan National Center for Global Health and Medicine, Disease Control and Prevention Center, Japan National Institute of Infectious Diseases, Bacteriology-I, Japan
a r t i c l e i n f o
a b s t r a c t
Article history: Received 5 October 2016 Received in revised form 22 December 2016 Accepted 23 December 2016 Available online xxx
Borrelia miyamotoi disease (BMD) is an emerging infectious disease caused by B. miyamotoi. Although BMD has been reported in the United States, Europe, and Japan, no case of imported BMD has been described in the world. Here, we report a 63-year-old American man living in Japan who presented with malaise, headache, myalgia, and arthralgia. We suspected Lyme disease because of his travel history to Minnesota and presence of erythema migrans. Serologic analysis supported our diagnosis, and doxycycline was administered for 14 days. However, we also suspected coinfection with BMD because of his fever, elevated liver function test results and his travel history. The patient was seropositive for the immunoglobulin M antibody to recombinant glycerophosphodiester phosphodiesterase, and was diagnosed with coinfection with BMD. This case suggests that BMD should be considered in febrile travelers returning from the Northeastern and Midwestern regions of the United States, and that BMD and Lyme disease coinfection should be considered to detect cases of imported BMD. © 2017 Japanese Society of Chemotherapy and The Japanese Association for Infectious Diseases. Published by Elsevier Ltd. All rights reserved.
Keywords: Borrelia miyamotoi Lyme disease Vector-borne disease Zoonotic disease
1. Introduction
2. Case report
Borrelia miyamotoi disease (BMD) is a systemic infectious disease caused by B. miyamotoi, a spirochete belonging to the relapsing fever group Borrelia. Although the relapsing fever group Borrelia genus are transmitted by soft ticks or body lice, B. miyamotoi is transmitted by hard ticks. B. miyamotoi was first identified in Japan in 1995 [1]; however, its pathogenesis was not determined until 2011, and human infection was first reported in 2011 in Russia [2]. Patients with BMD generally present with acute, nonspecific, flulike symptoms, such as fever, headache, general malaise, myalgia, and arthralgia [3]. However, BMD also can cause severe disease; 2 cases of meningoencephalitis in immunocompromised hosts have been reported [4,5]. Although BMD is an important emerging infectious disease in the United States, Europe, and Japan [6], no case of imported BMD has been reported in the world. Here, we describe the first case of imported BMD.
A previously healthy 63-year-old American man living in Japan visited the emergency department of our hospital on August 14, 2013, with malaise, headache, myalgia, and arthralgia, which began 10 days prior to his visit. He was referred to the outpatient department of internal medicine of our hospital the following day. He reported being bitten by ticks several times while staying with his family at his summer house in the state of Minnesota in the United States from July 25 to August 9, 2013. He appeared to be ill with a high fever (39.2 C) and relative bradycardia (77 beats/min). Physical examination revealed erythema migrans on the right buttock (Fig. 1). Laboratory test results showed normal white blood cell (5700/mL) and platelet counts (27.2 104/mL), slightly elevated aspartate aminotransferase and alanine aminotransferase levels (39 IU/L and 77 IU/L, respectively), and elevated C-reactive protein level (7.73 mg/dL). Blood culture results on August 14 were negative. We suspected Lyme disease and initiated doxycycline treatment at 100 mg twice a day. The patient demonstrated defervescence the following day, and his symptoms gradually improved. The doxycycline treatment was administered for a total of 14 days. Serologic analysis performed on
* Corresponding author. Division of Infectious Diseases, Musashino Red Cross Hospital, 1-26-1 Kyonan-cho, Musashino-shi, Tokyo 180-8610, Japan. Fax: þ81 422 32 3525. E-mail address: [email protected] (R. Oda).
http://dx.doi.org/10.1016/j.jiac.2016.12.015 1341-321X/© 2017 Japanese Society of Chemotherapy and The Japanese Association for Infectious Diseases. Published by Elsevier Ltd. All rights reserved.
Please cite this article in press as: Oda R, et al., The first case of imported Borrelia miyamotoi disease concurrent with Lyme disease, J Infect Chemother (2017), http://dx.doi.org/10.1016/j.jiac.2016.12.015
2
R. Oda et al. / J Infect Chemother xxx (2017) 1e3
analysis be considered positive if two of the following three bands are present: 24 kDa (OspC), 39 kDa (BmpA), and 41 kDa (Fla) [7]. In this case, the patient's serum showed a positive reaction to all three of these antigens (OspC, p39, and p41). Reactivity to Lyme disease borreliae also was elevated on August 19 (Fig. 2a). Although the skin rash and laboratory findings suggested acute Lyme disease, the patient's high fever and elevated liver function test results are uncommon for Lyme disease [8]. Therefore, we investigated his seroreactivity to recombinant glycerophosphodiester phosphodiesterase (rGlpQ) to identify possible coinfection with relapsing fever borreliae, especially B. miyamotoi. Western blotting using serum from the patient performed on August 15 and 19 confirmed seropositivity for the IgM antibody to rGlpQ (Fig. 2b). Thus, Lyme disease and BMD coinfection was diagnosed. Fig. 1. Erythema migrans on the right buttock.
August 15 using a commercial kit for immunoglobulin (Ig) M (recomLine Borrelia IgG/IgM; Mikrogen, Neuried, Germany) showed reactivity with 4 antigens (p100, p41, p39, and OspCs) of Lyme disease borreliae. It has been recommended that IgM immunoblot
3. Discussion Many reports of BMD have originated from the United States and Europe [3,6], and Lyme disease is currently endemic in the Northeastern and Midwestern regions of the United States, including Minnesota [9]. Furthermore, both B. miyamotoi and Borrelia burgdorferi are transmitted by Ixodes scapularis, a common vector in
Fig. 2. Serum reactivity to Lyme disease borreliae and the recombinant glycerophosphodiester phosphodiesterase (rGlpQ) antigen. (A) Serodiagnosis for Lyme disease with a commercial kit (recomLine Borrelia IgG/IgM; Mikrogen, Neuried, Germany). The test was performed according to the manufacturer's instructions. (B) Reactivity to rGlpQ. rGlpQ was separated with 12.5% polyacrylamide gel (Wako Pure Chemical Industries Inc., Osaka, Japan) and used for the immunoblot analysis [12]. The antigen was stained with Coomassie Brilliant Blue (CBB; left). Molecular weight markers (62e17) are shown on the left in kilodaltons (kDa).
Please cite this article in press as: Oda R, et al., The first case of imported Borrelia miyamotoi disease concurrent with Lyme disease, J Infect Chemother (2017), http://dx.doi.org/10.1016/j.jiac.2016.12.015
R. Oda et al. / J Infect Chemother xxx (2017) 1e3
these areas [6]. The incidence of concomitant Lyme disease and BMD is reportedly 14%e19% in United States [3,10], while a recent report showed that 3.2% of patients with suspected Lyme disease also were positive for B. miyamotoi antibody in United States [11]. These reports suggest that Lyme disease and BMD coinfection is not rare, and that patients with BMD living in Lyme disease endemic areas are at risk for misdiagnosis with Lyme disease. Patients with BMD present with nonspecific clinical symptoms. Fever is more common among patients with BMD than in those with Lyme disease, while erythema migrans occurs less frequently (98% vs. 32% and 9% vs. 89%, respectively) [2,3]. However, this does not mean that BMD alone shows erythema migrans, because this report included coinfection with Lyme disease. Although BMD without coinfection typically does not present erythema migrans, further investigation is required. In addition, hematological examination of BMD often reveal leukopenia, thrombocytopenia, and elevated aminotransferase levels [3], whereas these findings are uncommon in Lyme disease. Based on these characteristics, BMD and Lyme disease coinfection was considered in this case. Although definitive diagnosis of BMD is established primarily via polymerase chain reaction (PCR) assay, antibody tests also may be useful [3]. The accuracy of GlpQ serodiagnosis was originally designated by Schwan et al. [12], and is an alternative method when bacterial DNA is not detected [3]. In this case, the PCR result was negative, and diagnosis was based on antibody test results and the patient's travel history. Although the finding of a positive reactivity to rGlpQ was found in patients with relapsing fever [13], this patient had not traveled to the Western region of the United States, where relapsing fever is endemic. Furthermore, BMD is only the endemic relapsing fever in the Eastern United States [12]. In addition, the patient remembered being bitten by ticks in Minnesota before onset of his illness, and he had never visited Hokkaido, Japan, where cases of BMD have been reported [14]. These epidemiologic data suggest that he might have been infected with B. miyamotoi in Minnesota. Although it is considered that treatment for Lyme disease is also effective for BMD, the data are limited. Treatment for uncomplicated BMD is generally doxycycline (100 mg twice a day) for 7e14 days. Amoxicillin, cefuroxime, and macrolide also may be effective [6]. Treatment for BMD with meningoencephalitis should include intravenous ceftriaxone (2 g every 24 h) [4,6]. This is the first imported case of BMD concurrent with Lyme disease from the United States. This case suggests that BMD should be considered in febrile travelers returning from the Northeastern and Midwestern regions of the United States, and that BMD and Lyme disease coinfection should be considered to detect cases of imported BMD.
3
Conflict of interest None. Acknowledgment This research was supported by the Research Program on Emerging and Re-emerging Infectious Diseases Project of the Japan Agency for Medical Research and Development (15fk0108010h0001, 16fk0108210j0102). References [1] Fukunaga M, Takahashi Y, Tsuruta Y, Matsushita O, Ralph D, McClelland M, et al. Genetic and phenotypic analysis of Borrelia miyamotoi sp. nov., isolated from the ixodid tick Ixodes persulcatus, the vector for Lyme disease in Japan. Int J Syst Bacteriol 1995;45:804e10. [2] Platonov AE, Karan LS, Kolyasnikova NM, Makhneva NA, Toporkova MG, Maleev VV, et al. Humans infected with relapsing fever spirochete Borrelia miyamotoi, Russia. Emerg Infect Dis 2010;17:1816e23. [3] Molloy PJ, Telford 3rd SR, Chowdri HR, Lepore TJ, Gugliotta JL, Weeks KE, et al. Borrelia miyamotoi disease in the northeastern United States: a case series. Ann Intern Med 2015;163:91e8. [4] Gugliotta JL, Goethert HK, Berardi VP, Telford 3rd SR. Meningoencephalitis from Borrelia miyamotoi in an immunocompromised patient. N Engl J Med 2013;368:240e5. [5] Hovius JW, de Wever B, Sohne M, Brouwer MC, Coumou J, Wagemakers A, et al. A case of meningoencephalitis by the relapsing fever spirochaete Borrelia miyamotoi in Europe. Lancet 2013;382:658. [6] Krause PJ, Fish D, Narasimhan S, Barbour AG. Borrelia miyamotoi infection in nature and in humans. Clin Microbiol Infect 2015;21:631e9. [7] Centers for Disease Control and Prevention. Notice to readers recommendations for test performance and interpretation from the second national conference on serologic diagnosis of Lyme disease. MMWR 1995;44: 590e1. [8] Nadelman RB, Nowakowski J, Forseter G, Goldberg NS, Bittker S, Cooper D, et al. The clinical spectrum of early Lyme borreliosis in patients with cultureconfirmed erythema migrans. Am J Med 1996;100:502e8. [9] Centers for Disease Control and Prevention. Lyme disease data tables. Reported cases of Lyme disease by state or locality, 2005e2014. Available at: http://www.cdc.gov/lyme/stats/tables.html. [Accessed 21 January 2016]. [10] Krause PJ, Narasimhan S, Wormser GP, Barbour AG, Platonov AE, Brancato J, et al. Borrelia miyamotoi sensu lato seroreactivity and seroprevalence in the northeastern United States. Emerg Infect Dis 2014;20:1183e90. [11] Krause PJ, Narasimhan S, Wormser GP, Rollend L, Fikrig E, Lepore T, et al. Human Borrelia miyamotoi infection in the United States. N Engl J Med 2013;368:291e3. [12] Schwan TG, Schrumpf ME, Hinnebusch BJ, Anderson Jr DE, Konkel ME. GlpQ: an antigen for serological discrimination between relapsing fever and Lyme borreliosis. J Clin Microbiol 1996;34:2483e92. [13] Centers for Disease Control and Prevention. Cases of tick-borne relapsing feverdUnited States, 1990e2011. Available at: http://www.cdc.gov/ relapsing-fever/distribution/index.html. [Accessed 21 January 2016]. [14] Sato K, Takano A, Konnai S, Nakao M, Ito T, Koyama K, et al. Human infections with Borrelia miyamotoi. Jpn Emerg Infect Dis 2014;20:1391e3.
Please cite this article in press as: Oda R, et al., The first case of imported Borrelia miyamotoi disease concurrent with Lyme disease, J Infect Chemother (2017), http://dx.doi.org/10.1016/j.jiac.2016.12.015
Contents lists available at ScienceDirect
Journal of Infection and Chemotherapy journal homepage: http://www.elsevier.com/locate/jic
Case Report
The first case of imported Borrelia miyamotoi disease concurrent with Lyme disease Rentaro Oda a, *, Satoshi Kutsuna b, Yoshiyuki Sekikawa a, Igen Hongo a, Kozue Sato c, Makoto Ohnishi c, Hiroki Kawabata c a b c
Division of Infectious Diseases, Musashino Red Cross Hospital, Japan National Center for Global Health and Medicine, Disease Control and Prevention Center, Japan National Institute of Infectious Diseases, Bacteriology-I, Japan
a r t i c l e i n f o
a b s t r a c t
Article history: Received 5 October 2016 Received in revised form 22 December 2016 Accepted 23 December 2016 Available online xxx
Borrelia miyamotoi disease (BMD) is an emerging infectious disease caused by B. miyamotoi. Although BMD has been reported in the United States, Europe, and Japan, no case of imported BMD has been described in the world. Here, we report a 63-year-old American man living in Japan who presented with malaise, headache, myalgia, and arthralgia. We suspected Lyme disease because of his travel history to Minnesota and presence of erythema migrans. Serologic analysis supported our diagnosis, and doxycycline was administered for 14 days. However, we also suspected coinfection with BMD because of his fever, elevated liver function test results and his travel history. The patient was seropositive for the immunoglobulin M antibody to recombinant glycerophosphodiester phosphodiesterase, and was diagnosed with coinfection with BMD. This case suggests that BMD should be considered in febrile travelers returning from the Northeastern and Midwestern regions of the United States, and that BMD and Lyme disease coinfection should be considered to detect cases of imported BMD. © 2017 Japanese Society of Chemotherapy and The Japanese Association for Infectious Diseases. Published by Elsevier Ltd. All rights reserved.
Keywords: Borrelia miyamotoi Lyme disease Vector-borne disease Zoonotic disease
1. Introduction
2. Case report
Borrelia miyamotoi disease (BMD) is a systemic infectious disease caused by B. miyamotoi, a spirochete belonging to the relapsing fever group Borrelia. Although the relapsing fever group Borrelia genus are transmitted by soft ticks or body lice, B. miyamotoi is transmitted by hard ticks. B. miyamotoi was first identified in Japan in 1995 [1]; however, its pathogenesis was not determined until 2011, and human infection was first reported in 2011 in Russia [2]. Patients with BMD generally present with acute, nonspecific, flulike symptoms, such as fever, headache, general malaise, myalgia, and arthralgia [3]. However, BMD also can cause severe disease; 2 cases of meningoencephalitis in immunocompromised hosts have been reported [4,5]. Although BMD is an important emerging infectious disease in the United States, Europe, and Japan [6], no case of imported BMD has been reported in the world. Here, we describe the first case of imported BMD.
A previously healthy 63-year-old American man living in Japan visited the emergency department of our hospital on August 14, 2013, with malaise, headache, myalgia, and arthralgia, which began 10 days prior to his visit. He was referred to the outpatient department of internal medicine of our hospital the following day. He reported being bitten by ticks several times while staying with his family at his summer house in the state of Minnesota in the United States from July 25 to August 9, 2013. He appeared to be ill with a high fever (39.2 C) and relative bradycardia (77 beats/min). Physical examination revealed erythema migrans on the right buttock (Fig. 1). Laboratory test results showed normal white blood cell (5700/mL) and platelet counts (27.2 104/mL), slightly elevated aspartate aminotransferase and alanine aminotransferase levels (39 IU/L and 77 IU/L, respectively), and elevated C-reactive protein level (7.73 mg/dL). Blood culture results on August 14 were negative. We suspected Lyme disease and initiated doxycycline treatment at 100 mg twice a day. The patient demonstrated defervescence the following day, and his symptoms gradually improved. The doxycycline treatment was administered for a total of 14 days. Serologic analysis performed on
* Corresponding author. Division of Infectious Diseases, Musashino Red Cross Hospital, 1-26-1 Kyonan-cho, Musashino-shi, Tokyo 180-8610, Japan. Fax: þ81 422 32 3525. E-mail address: [email protected] (R. Oda).
http://dx.doi.org/10.1016/j.jiac.2016.12.015 1341-321X/© 2017 Japanese Society of Chemotherapy and The Japanese Association for Infectious Diseases. Published by Elsevier Ltd. All rights reserved.
Please cite this article in press as: Oda R, et al., The first case of imported Borrelia miyamotoi disease concurrent with Lyme disease, J Infect Chemother (2017), http://dx.doi.org/10.1016/j.jiac.2016.12.015
2
R. Oda et al. / J Infect Chemother xxx (2017) 1e3
analysis be considered positive if two of the following three bands are present: 24 kDa (OspC), 39 kDa (BmpA), and 41 kDa (Fla) [7]. In this case, the patient's serum showed a positive reaction to all three of these antigens (OspC, p39, and p41). Reactivity to Lyme disease borreliae also was elevated on August 19 (Fig. 2a). Although the skin rash and laboratory findings suggested acute Lyme disease, the patient's high fever and elevated liver function test results are uncommon for Lyme disease [8]. Therefore, we investigated his seroreactivity to recombinant glycerophosphodiester phosphodiesterase (rGlpQ) to identify possible coinfection with relapsing fever borreliae, especially B. miyamotoi. Western blotting using serum from the patient performed on August 15 and 19 confirmed seropositivity for the IgM antibody to rGlpQ (Fig. 2b). Thus, Lyme disease and BMD coinfection was diagnosed. Fig. 1. Erythema migrans on the right buttock.
August 15 using a commercial kit for immunoglobulin (Ig) M (recomLine Borrelia IgG/IgM; Mikrogen, Neuried, Germany) showed reactivity with 4 antigens (p100, p41, p39, and OspCs) of Lyme disease borreliae. It has been recommended that IgM immunoblot
3. Discussion Many reports of BMD have originated from the United States and Europe [3,6], and Lyme disease is currently endemic in the Northeastern and Midwestern regions of the United States, including Minnesota [9]. Furthermore, both B. miyamotoi and Borrelia burgdorferi are transmitted by Ixodes scapularis, a common vector in
Fig. 2. Serum reactivity to Lyme disease borreliae and the recombinant glycerophosphodiester phosphodiesterase (rGlpQ) antigen. (A) Serodiagnosis for Lyme disease with a commercial kit (recomLine Borrelia IgG/IgM; Mikrogen, Neuried, Germany). The test was performed according to the manufacturer's instructions. (B) Reactivity to rGlpQ. rGlpQ was separated with 12.5% polyacrylamide gel (Wako Pure Chemical Industries Inc., Osaka, Japan) and used for the immunoblot analysis [12]. The antigen was stained with Coomassie Brilliant Blue (CBB; left). Molecular weight markers (62e17) are shown on the left in kilodaltons (kDa).
Please cite this article in press as: Oda R, et al., The first case of imported Borrelia miyamotoi disease concurrent with Lyme disease, J Infect Chemother (2017), http://dx.doi.org/10.1016/j.jiac.2016.12.015
R. Oda et al. / J Infect Chemother xxx (2017) 1e3
these areas [6]. The incidence of concomitant Lyme disease and BMD is reportedly 14%e19% in United States [3,10], while a recent report showed that 3.2% of patients with suspected Lyme disease also were positive for B. miyamotoi antibody in United States [11]. These reports suggest that Lyme disease and BMD coinfection is not rare, and that patients with BMD living in Lyme disease endemic areas are at risk for misdiagnosis with Lyme disease. Patients with BMD present with nonspecific clinical symptoms. Fever is more common among patients with BMD than in those with Lyme disease, while erythema migrans occurs less frequently (98% vs. 32% and 9% vs. 89%, respectively) [2,3]. However, this does not mean that BMD alone shows erythema migrans, because this report included coinfection with Lyme disease. Although BMD without coinfection typically does not present erythema migrans, further investigation is required. In addition, hematological examination of BMD often reveal leukopenia, thrombocytopenia, and elevated aminotransferase levels [3], whereas these findings are uncommon in Lyme disease. Based on these characteristics, BMD and Lyme disease coinfection was considered in this case. Although definitive diagnosis of BMD is established primarily via polymerase chain reaction (PCR) assay, antibody tests also may be useful [3]. The accuracy of GlpQ serodiagnosis was originally designated by Schwan et al. [12], and is an alternative method when bacterial DNA is not detected [3]. In this case, the PCR result was negative, and diagnosis was based on antibody test results and the patient's travel history. Although the finding of a positive reactivity to rGlpQ was found in patients with relapsing fever [13], this patient had not traveled to the Western region of the United States, where relapsing fever is endemic. Furthermore, BMD is only the endemic relapsing fever in the Eastern United States [12]. In addition, the patient remembered being bitten by ticks in Minnesota before onset of his illness, and he had never visited Hokkaido, Japan, where cases of BMD have been reported [14]. These epidemiologic data suggest that he might have been infected with B. miyamotoi in Minnesota. Although it is considered that treatment for Lyme disease is also effective for BMD, the data are limited. Treatment for uncomplicated BMD is generally doxycycline (100 mg twice a day) for 7e14 days. Amoxicillin, cefuroxime, and macrolide also may be effective [6]. Treatment for BMD with meningoencephalitis should include intravenous ceftriaxone (2 g every 24 h) [4,6]. This is the first imported case of BMD concurrent with Lyme disease from the United States. This case suggests that BMD should be considered in febrile travelers returning from the Northeastern and Midwestern regions of the United States, and that BMD and Lyme disease coinfection should be considered to detect cases of imported BMD.
3
Conflict of interest None. Acknowledgment This research was supported by the Research Program on Emerging and Re-emerging Infectious Diseases Project of the Japan Agency for Medical Research and Development (15fk0108010h0001, 16fk0108210j0102). References [1] Fukunaga M, Takahashi Y, Tsuruta Y, Matsushita O, Ralph D, McClelland M, et al. Genetic and phenotypic analysis of Borrelia miyamotoi sp. nov., isolated from the ixodid tick Ixodes persulcatus, the vector for Lyme disease in Japan. Int J Syst Bacteriol 1995;45:804e10. [2] Platonov AE, Karan LS, Kolyasnikova NM, Makhneva NA, Toporkova MG, Maleev VV, et al. Humans infected with relapsing fever spirochete Borrelia miyamotoi, Russia. Emerg Infect Dis 2010;17:1816e23. [3] Molloy PJ, Telford 3rd SR, Chowdri HR, Lepore TJ, Gugliotta JL, Weeks KE, et al. Borrelia miyamotoi disease in the northeastern United States: a case series. Ann Intern Med 2015;163:91e8. [4] Gugliotta JL, Goethert HK, Berardi VP, Telford 3rd SR. Meningoencephalitis from Borrelia miyamotoi in an immunocompromised patient. N Engl J Med 2013;368:240e5. [5] Hovius JW, de Wever B, Sohne M, Brouwer MC, Coumou J, Wagemakers A, et al. A case of meningoencephalitis by the relapsing fever spirochaete Borrelia miyamotoi in Europe. Lancet 2013;382:658. [6] Krause PJ, Fish D, Narasimhan S, Barbour AG. Borrelia miyamotoi infection in nature and in humans. Clin Microbiol Infect 2015;21:631e9. [7] Centers for Disease Control and Prevention. Notice to readers recommendations for test performance and interpretation from the second national conference on serologic diagnosis of Lyme disease. MMWR 1995;44: 590e1. [8] Nadelman RB, Nowakowski J, Forseter G, Goldberg NS, Bittker S, Cooper D, et al. The clinical spectrum of early Lyme borreliosis in patients with cultureconfirmed erythema migrans. Am J Med 1996;100:502e8. [9] Centers for Disease Control and Prevention. Lyme disease data tables. Reported cases of Lyme disease by state or locality, 2005e2014. Available at: http://www.cdc.gov/lyme/stats/tables.html. [Accessed 21 January 2016]. [10] Krause PJ, Narasimhan S, Wormser GP, Barbour AG, Platonov AE, Brancato J, et al. Borrelia miyamotoi sensu lato seroreactivity and seroprevalence in the northeastern United States. Emerg Infect Dis 2014;20:1183e90. [11] Krause PJ, Narasimhan S, Wormser GP, Rollend L, Fikrig E, Lepore T, et al. Human Borrelia miyamotoi infection in the United States. N Engl J Med 2013;368:291e3. [12] Schwan TG, Schrumpf ME, Hinnebusch BJ, Anderson Jr DE, Konkel ME. GlpQ: an antigen for serological discrimination between relapsing fever and Lyme borreliosis. J Clin Microbiol 1996;34:2483e92. [13] Centers for Disease Control and Prevention. Cases of tick-borne relapsing feverdUnited States, 1990e2011. Available at: http://www.cdc.gov/ relapsing-fever/distribution/index.html. [Accessed 21 January 2016]. [14] Sato K, Takano A, Konnai S, Nakao M, Ito T, Koyama K, et al. Human infections with Borrelia miyamotoi. Jpn Emerg Infect Dis 2014;20:1391e3.
Please cite this article in press as: Oda R, et al., The first case of imported Borrelia miyamotoi disease concurrent with Lyme disease, J Infect Chemother (2017), http://dx.doi.org/10.1016/j.jiac.2016.12.015