Volume 16, Number 3—March 2010
Bartonella spp. Transmission by Ticks Not Established
Highlight and copy the desired format.
|EID||Telford SR, Wormser GP. Bartonella spp. Transmission by Ticks Not Established. Emerg Infect Dis. 2010;16(3):379-384. https://dx.doi.org/10.3201/eid1603.090443|
|AMA||Telford SR, Wormser GP. Bartonella spp. Transmission by Ticks Not Established. Emerging Infectious Diseases. 2010;16(3):379-384. doi:10.3201/eid1603.090443.|
|APA||Telford, S. R., & Wormser, G. P. (2010). Bartonella spp. Transmission by Ticks Not Established. Emerging Infectious Diseases, 16(3), 379-384. https://dx.doi.org/10.3201/eid1603.090443.|
Bartonella spp. infect humans and many animal species. Mainly because PCR studies have demonstrated Bartonella DNA in ticks, some healthcare providers believe that these microorganisms are transmitted by ticks. B. henselae, in particular, is regarded as being present in and transmissible by the Ixodes scapularis tick. The presence of a microbial agent within a tick, however, does not imply that the tick might transmit it during the course of blood feeding and does not confer epidemiologic importance. After a critical review of the evidence for and against tick transmission, we conclude that transmission of any Bartonella spp. by ticks, to animals or humans, has not been established. We are unaware of any well-documented case of B. henselae transmission by I. scapularis ticks.
Infections with Bartonella spp. appear to be widespread in many animal species besides cats (1). Some evidence has been advanced in support of the possibility of tick transmission. Such findings have resulted in diagnostic testing and empiric therapies directed at B. henselae infection that are of dubious value with respect to illnesses thought to be caused by deer tick exposure. We critically examined the reported findings regarding tick transmission of Bartonella spp.
Bartonella spp. are common bacterial hemoparasites of mammals; for as long as 100 years, 2 species have been known to cause infections of public health significance. Trench fever, caused by B. quintana (formerly Rochalimaea quintana) and transmitted by body lice, affected hundreds of thousands of soldiers or displaced persons during World War I and to this day affects homeless persons. Oroya fever (and its chronic manifestation verruga peruana), caused by infection with B. bacilliformis and transmitted by phlebotomine sandflies, is a potentially severe febrile disease. Although it is geographically restricted to the high altitudes of the Andes and affects only a relatively small number of persons, the high case-fatality rate brought attention to this apparent anthroponosis as early as the late 1800s.
B. henselae causes cat-scratch disease, the most common Bartonella spp. infection in the United States (2). The hallmark of cat-scratch disease is enlargement and tenderness of lymph nodes draining the site of inoculation of the microorganism (3). In addition, a skin or mucous membrane lesion may be observed at the site of inoculation for 25% to >90% of patients (3,4). Extranodal clinical manifestations (e.g., encephalopathy, neuroretinitis, arthritis, and lytic bone lesions) occur in ≈10% of patients (3–6). Cats are the main reservoir of B. henselae. In a study from San Francisco, 25 (41%) of 61 pet, pound, or stray cats (Felis domesticus) were found to have B. henselae bacteremia (7). Bites or scratches from infected cats are associated with development of cat-scratch disease. The gut of cat fleas is commonly infected, and exposure to feces of infected fleas is the presumed route of transmission to uninfected cats and a possible route of transmission to humans.
Parasitologists focusing on blood parasites have long noted the ubiquity of Bartonella spp. within mammals, particularly rodents, and by the late 1960s nearly 2 dozen species had been described within the genus Grahamella (8). The genera Rochalimaea and Grahamella were subsumed into the genus Bartonella (9), and many of the validly published Grahamella spp. have been excluded from the list of approved bacterial taxa (10). These actions tended to foster ignorance of the history of the diversity of Bartonella spp. and to promote a fallacy in pathogen discovery (11); namely, if a DNA sequence is not present in GenBank, surely it must represent something novel, the extensive classical literature on a likely identical organism known only by morphology notwithstanding. The significance of such a fallacy is that a large body of literature that may provide critical details on the biology of a “novel” agent is completely overlooked or dismissed.
Seminal studies by Richard Pearson Strong and the members of the American Red Cross trench fever commission (12) conclusively demonstrated biological as opposed to mechanical transmission of the trench fever agent by body lice. Feeding experiments on human volunteers established that lice may transmit by bite or by fecal contamination of abraded skin; that an infected louse remains infectious for at least 2 weeks; that the agent is not inherited by the progeny of infected lice; and that transmission may be extremely efficient, causing trench fever in 75% of volunteers after 1 exposure to a feeding box containing ≈50 lice that had previously fed on patients with trench fever.
Although initially Oroya fever was epidemiologically associated with ticks (13), it rapidly became evident that phlebotomine sandflies (particularly Lutzomyia verrucarum) were the vectors. Sandflies were the only blood-feeding arthropods that were peridomestic in their habits and occurred in the “bartonella zone,” >2,000 m elevation. Experimentally, sandflies acquired infection from blood-smear positive patients and transmitted infection by bite to those without evidence of Bartonella spp. infection (14).
Grahamellae (now bartonellae) of rodents have long been known to be transmitted by fleas (15–17). Such studies have noted the difficulty with which experimental infections may be established by means other than inoculation of flea homogenates, the persistence within the rectal sac of the flea, and the likely mode of perpetuation of the bacteria by larval fleas ingesting dried infected blood. In addition, grahamellae-infected rodents were noted to exist in the absence of ticks, demonstrating that ticks were not required to perpetuate these particular bacteria.
Ticks are notorious vectors of a variety of agents that cause zoonotic infections (11), including viruses, bacteria, and protozoans. Like all animals, ticks have a diverse microflora. Recent analyses, using cloning and sequencing broad-range 16S rDNA amplification products, have documented a large bacterial flora within northeastern populations of Ixodes scapularis ticks that bite humans as nymphs, hereafter referred to as deer ticks (18,19). Amebas, mycoplasma, fungi, and helminths have been detected in these ticks by microscopy or other standard methods. However, the presence of a microbial agent within a tick does not imply that the tick might transmit it during the course of blood feeding or that it is pathogenic.
During early investigations of the causes of Oroya fever, Noguchi (20) demonstrated that B. bacilliformis could be experimentally transmitted between monkeys by the bites of Dermacentor andersoni ticks. However, the ticks that had been fed for a few days on infected monkeys were removed and allowed to reattach and complete their blood meal on uninfected animals, which became infected. Noguchi concluded that mechanical transmission had been demonstrated (perhaps by contamination of mouthparts or by regurgitation of the infectious partial blood meal), but persistence of viable bacteria or transstadial passage had not, and thus ticks were not biologic vectors.
Based on the volume of studies, the most compelling argument in favor of a tick vector for Bartonella spp. is that these microorganisms are sometimes detected in field-collected ticks (Table 1) (15). Although at least 20 studies have provided evidence for the presence of Bartonella spp. in primarily Ixodes spp. ticks collected at various locations in the United States and Europe, only 1 study has confirmed the presence of Bartonella spp. by culture (15,21,22). Caution is warranted when interpreting such data, however, because acquisition of Bartonella spp. from animal sources through a blood meal would be anticipated given the ubiquity of the microorganism in domestic animals and wildlife. In New England, as many as 60% of white-footed mice are blood-smear positive for Grahamella spp. (now Bartonella), regardless of collection site, including those trapped within the house of 1 of the authors where a tick life cycle was not present (S.R. Telford III, unpub. data); prevalence would probably reach unity if more sensitive modes of detection were used. The mere presence of Bartonella spp. or their DNA in ticks does not prove vector competence or confer epidemiologic significance (15), but it should serve as the impetus to rigorously perform the studies necessary to establish vector competence of ticks. At the least, viability should be established for bartonellae detected within ticks by means of in vitro cultivation.
To date, no report has documented transmission of B. henselae or any other Bartonella spp. to an animal after a tick bite (Table 2). The strongest evidence that ticks might be competent vectors for bartonellae was reported in a recent study in which I. ricinus ticks were infected with B. henselae in spiked (artificially infected) ovine blood by using an artificial feeding system (23). The ticks maintained infection throughout the molt, thereby establishing transstadial transmission. The experimentally infected ticks were also able to transmit B. henselae during a subsequent blood meal, again through the artificial feeding system; the dissected salivary glands from such ticks, when introduced into a cat, produced typical B. henselae infection, proving viability. Serious questions exist, however, as to whether these experiments are relevant to establishing vector competence. The ticks were fed continuously on blood meals with 109 CFU/mL, representing a bacteremia that would rarely be seen in natural infections of cats. Given that Ixodes spp. nymphs ingest a total of ≈15 μL blood (24), each nymph may have ingested 106–107 bacteria, a large dose. In addition, the Houston-1 strain of B. henselae used in this study may not represent strains found in nature. It is highly adapted to the laboratory and readily grows in vitro, whereas primary isolates are extremely fastidious and grow slowly.
A more straightforward experiment to establish vector competence would be to feed an uninfected Ixodes sp. tick on a B. henselae–infected cat and then, after the tick has molted, determine whether B. henselae can be transmitted by tick bite to an uninfected cat. However, even if such an experiment were to prove vector competence, additional data would be needed to conclude that Ixodes spp. ticks are epidemiologically relevant as B. henselae vectors.
Do epidemiologic data that support tick transmission of Bartonella spp. in animals exist? One study correlated canine seropositivity to B. vinsonii subsp. berkhoffii with tick exposure and with seropositivity to other tick-borne pathogens (25). However, the dogs in that study were also heavily exposed to fleas, and according to findings with cats, flea transmission is as likely a possibility as tick transmission in dogs, if not more so (15,25,26). A study in the United Kingdom reported an association between seropositivity to B. henselae and to Borrelia burgdorferi in feral cats (27). The method used to detect antibodies to B. burgdorferi was not precisely described. However, the fact that the rate of seropositivity to B. henselae was nearly the same for domestic and feral cats, despite domestic cats having much less tick exposure than feral cats, raises questions about the epidemiologic relevance of tick transmission. In another study, a “novel” Bartonella subspecies was detected more often in white-footed mice concurrently infected with the tick-borne pathogens B. burgdorferi or Babesia microti (1), but this analysis failed to compare the likelihood that the Bartonella spp. might also commonly co-occur with rodent trypanosomes, which are maintained by fleas. Epidemiologic arguments must carefully control for confounding, and none to date argues convincingly for tick transmission of Bartonella spp.
Certain authors have interpreted their studies as providing epidemiologic support for tick transmission of Bartonella spp. These data are, however, largely anecdotal and inconclusive (28,29). Culture-confirmed B. henselae infection was reported in 3 US patients who had been bitten by a tick within a few weeks of onset of illness (28,30); 2 of these patients had been in contact with a cat and may have been infected by this animal or its fleas. The tick species causing the bites was not identified for any of the patients but was unlikely to have been deer ticks because of the locations (Arkansas, Oklahoma, and probably North Carolina) (30), in which deer tick bites would be rare. Bartonella spp. have rarely (2 of ≈500 ticks) been detected in Amblyomma americanum ticks, the most common tick species to parasitize humans in these 3 states (22), but the finding was based on 1 PCR reaction and not confirmed with a second target or any other assay.
A more recent study described 3 patients from Europe for whom a scalp eschar and neck lymphadenopathy were attributed to tick transmission of B. henselae (31). Molecular detection of the microorganism by PCR of a biopsy specimen from the eschar, in conjunction with a high serum antibody titer by immunofluorescence assay, document B. henselae infection for 2 of the patients; a tick bite at the lesion site was presumed but not proven for either patient. Both had been in contact with cats that may well have transmitted this infection because the clinical features were indistinguishable from those of cat-scratch disease. The third patient, who had no cat exposure, had a documented bite from a Dermacentor marginatus tick that had PCR evidence of B. henselae infection. Whether the patient actually had B. henselae infection is questionable because PCR testing of tissue from the eschar was negative and antibodies to B. henselae could not be detected by immunofluorescence assay. The sole stated basis for the diagnosis was a positive Western blot result, but neither the interpretive criteria used nor the specificity of this testing were provided. When associated with a documented tick bite, the most common cause for a scalp eschar and neck lymphadenopathy is Rickettsia slovaca, but other rickettsia and even Francisella tularensis are possible causes, and in at least 25% of cases no pathogen can be identified (31).
Univariate analysis in a case–control study of cat-scratch disease in Connecticut found a significant association between having found a tick on the body and cat-scratch disease (32). This association, however, did not remain significant on multivariate (bivariate) analysis after controlling for exposure to kittens.
A 2001 report from New Jersey described 3 patients believed to have nervous system co-infection with B. henselae and B. burgdorferi (33). The authors suggested that bartonellae were transmitted by infected deer ticks because of the co-infection with B. burgdorferi and because the investigators detected B. henselae in a deer tick found in the household of 1 of these co-infected patients and in several deer ticks found on the pet cat of a fourth patient believed to have only B. henselae infection. PCR detection of DNA of both B. burgdorferi and B. henselae in the cerebrospinal fluid of these patients was the primary basis for the diagnosis of co-infection. An accompanying editorial, however, raised concerns about the validity of the diagnosis of both neuroborreliosis and neurobartonellosis in these patients (34). The clinical features were atypical for either infection, and the laboratory test results in support of these infections showed inconsistencies. In addition, 2 of the 3 authors had a potential conflict of interest; they were associated with a commercial laboratory that stood to gain financially from laboratory testing for B. henselae. The PCRs used by these investigators and others need careful scrutiny. In a later publication (35), the authors of the original NJ report conceded that the primers that they had used to amplify B. henselae DNA were insufficiently specific to warrant the conclusion that B. henselae was detected. BLAST (www.ncbi.nlm.nih.gov/blast/Blast.cgi) analysis of their primer P12B demonstrates identity with mouse mitochondrial DNA; also, what might be amplified if the PCR reaction were not stringent enough (e.g., lower annealing temperature) is not clear. In addition, their primer P24E contains a large proportion of α-proteobacterial 3′ terminus 16S rDNA consensus sequence. Because the specificity of PCR testing depends on target selection and reaction conditions, molecular detection using current primer sets may identify yet-undescribed genera of environmental bacteria distinct from Bartonella spp. Future examination of field-collected ticks for Bartonella spp. DNA should use a minimum of 2 independent PCR targets, preferably those that include larger portions of phylogenetically informative genes; to demonstrate viability, Bartonella spp. cultures should be attempted from all DNA-positive ticks. The deer ticks were unlikely to have been actually infected with B. henselae unless one postulates that feral cats serve as common hosts to larval or nymphal deer ticks. Indeed, the relatively high prevalence of reported Bartonella spp. infection (35) suggests that these ticks feed on cats as frequently as they do on mice. Although cats certainly serve as hosts for deer ticks of all stages, their contribution to feeding these vectors relative to all other animals remains to be defined and is likely to be minimal compared with rodents or birds. Given how frequently deer ticks feed on mice, B. vinsonii arupensis (previously known as Grahamella peromysci), which was isolated from a febrile, encephalopathic patient as well as from a patient who died from endocarditis, should more commonly infect persons in Lyme disease–endemic sites. This agent, however, has not been detected in deer ticks in any survey to date. Nevertheless, that B. henselae infection is a potential deer tick-transmitted co-infection in patients with possible Lyme disease is still widely accepted by the “chronic Lyme disease” counterculture (i.e., those physicians, patients, and activists who believe that patients with unexplained subjective symptoms have chronic B. burgdorferi infection even in the absence of exposure to a disease-endemic area or credible laboratory evidence of infection) (36).
Anecdotal accounts of B. henselae co-infection with B. burgdorferi in patients have been reported from Poland (37), Russia (29), and North Carolina (38). The report from North Carolina relied solely on immunoglobulin (Ig) M seroreactivity to B. burgdorferi to support a diagnosis of neuroborreliosis (38). The relatively poor specificity of IgM serologic testing (39) and the fact that the case was from outside Lyme disease–endemic regions of the United States raise concerns about the validity of the diagnosis of B. burgdorferi infection in this patient.
A straightforward approach to address whether B. henselae is transmitted by deer ticks would be seroepidemiologic studies to compare the prevalence of B. henselae antibodies in patients with Lyme disease with those in appropriate control groups, but such studies have not been performed. A study in Slovenia found that only 1 of the 86 children in whom febrile illness developed after a tick bite had Lyme disease in conjunction with seroconversion for IgG antibodies to both B. henselae and B. quintana (40).
In the United States alone, >20,000 cases of Lyme disease and about the same number of cases of cat-scratch disease occur annually (2). Thus, co-infections may occur occasionally by chance alone, without cotransmission by a tick vector. If the bite of a deer tick is a common route for B. henselae transmission, the absence of reports of the typical lymph node findings of cat-scratch disease proximal to the bite site of this tick species seems puzzling. The seasonality of cat-scratch disease, in which most cases in temperate regions occur in autumn and early winter (when peak breeding of cat fleas and birth of kittens occur), provides further evidence against a major role for ticks in transmission of B. henselae (32).
Tick transmission of any Bartonella spp. to either animals or humans has not been established. B. henselae in particular is unlikely to be transmitted by deer ticks, and, to our knowledge, no well-documented case of transmission by this tick species in humans or animals has been reported.
Dr Telford is an associate professor in the Division of Infectious Diseases at the Cummings School of Veterinary Medicine at Tufts University. His research interests are related to the evolutionary ecology of tick-transmitted infections, with an emphasis on tick-pathogen interactions.
Dr Wormser is chief of the Division of Infectious Diseases, vice chairman of the Department of Medicine, and professor of medicine and pharmacology at New York Medical College. He is also chief of the Section of Infectious Diseases at Westchester Medical Center and director and founder of the Lyme Disease Diagnostic Center. His main research interests are Lyme disease, human granulocytic anaplasmosis, and babesiosis.
We thank Lisa Giarratano and Lenise Banwarie for their assistance.
S.R.T. is supported by National Institutes of Health RO1 AI 064218.
- Hofmeister EK, Kolbert CP, Abdulkarim AS, Magera JM, Hopkins MK, Uhl JR, Cosegregation of a novel Bartonella species with Borrelia burgdorferi and Babesia microti in Peromyscus leucopus. J Infect Dis. 1998;177:409–16.
- Jackson LA, Perkins BA, Wenger JD. Cat scratch disease in the United States: an analysis of three national databases. Am J Public Health. 1993;83:1707–11.
- Carithers HA. Cat scratch disease. An overview based on a study of 1,200 patients. Am J Dis Child. 1985;139:1124–33.
- Margileth AM, Wear DJ, English CK. Systemic cat-scratch disease: report of 23 patients with prolonged or recurrent severe bacterial infection. J Infect Dis. 1987;155:390–402.
- Wheeler SW, Wolf SM, Steinberg EA. Cat-scratch encephalopathy. Neurology. 1997;49:876–8.
- Maman E, Bickels J, Ephros M, Paran D, Comaneshter D, Metzkor-Cotter E, Musculoskeletal manifestations of cat scratch disease. Clin Infect Dis. 2007;45:1535–40.
- Koehler JE, Glaser CA, Tappero JW. Rochalimaea henselae infection: a new zoonosis with the domestic cat as a reservoir. JAMA. 1994;271:531–5.
- Kreier JP, Ristic M. Haemobartonellosis, eperythrozoonosis, grahamellosis, and ehrlichiosis. In: Weinman D, Ristic M, editors. Infectious blood diseases of man and animals, Vol. II. New York: Academic Press; 1968. p 387–472.
- Birtles RJ, Harrison TG, Saunders NA, Molyneux DH. Proposals to unify the genera Grahamella and Bartonella, with descriptions of Bartonella talpae comb. nov., Bartonella peromysci comb. nov., and three new species, Bartonella grahamii sp. nov., Bartonella taylorii sp. nov., and Bartonella doshiae sp. nov. Int J Syst Bacteriol. 1995;45:1–8.
- Skerman VBD, McGowan V, Sneath PHA. Approved lists of bacterial names (amended edition). Washington: American Society for Microbiology; 1989.
- Telford SR, Goethert HK. Emerging and emergent tick borne infections. In: Bowman AS, Nuttall PA, editors. Ticks: biology, disease and control. New York: Cambridge University Press; 2008. p. 344–76
- Strong RP, Tyzzer EE, Brues CT, Sellards AW, Gastiaburu JC. Report of the first expedition to South America, 1913. Cambridge (MA): Harvard University Press; 1915.
- Townsend CHT. The possible and probable etiology and transmission of verruga fever. J Econ Entomol. 1913;6:211–25.
- Hertig M. Phlebotomus and Carrión’s disease. Am J Trop Med. 1942;22(suppl):2–81.
- Billeter SA, Levy MG, Chronel BB, Breitschwerdt EB. Vector transmission of Bartonella species with emphasis on the potential for tick transmission. Med Vet Entomol. 2008;22:1–15.
- Krampitz HE, Kleinschmidt A. Grahamella brumpt: biologische und morphologische untersuchungen. Z Tropenmed Parasitol. 1911;11:336–52.
- Fay FG, Rausch RL. Parasitic organisms in the blood of arvicoline rodents in Alaska. J Parasitol. 1969;55:1258–65.
- Benson MJ, Gawronski JD, Eveleigh DE, Benson DR. Intracellular symbionts and other bacteria associated with deer ticks (Ixodes scapularis) from Nantucket and Wellfleet, Cape Cod, Massachusetts. Appl Environ Microbiol. 2004;70:616–20.
- Moreno CX, Moy F, Daniels TJ, Godfrey HP, Cabello FC. Molecular analysis of microbial communities identified in different developmental stages of Ixodes scapularis ticks from Westchester and Dutchess Counties, New York. Environ Microbiol. 2006;8:761–72.
- Noguchi H. Etiology of Oroyo fever: V. the experimental transmission of Bartonella bacilliformis by ticks (Dermacenter andersoni). J Exp Med. 1926;44:729–34.
- Kruszewska D, Tylewska-Wierzbanowska S. Unknown species of rickettsiae isolated from Ixodes ricinus tick in Walcz. Rocz Akad Med Bialymst. 1996;41:129–35.
- Billeter SA, Miller MK, Breitschwerdt EB, Levy MG. Detection of two Bartonella tamiae–like sequences in Amblyomma americanum (Acari: Ixodidae) using 16S–23S intergenic spacer region–specific primers. J Med Entomol. 2008;45:176–9.
- Cotté V, Bonnel S, Le Rhun D, Le Naour E, Chauvin A, Boulouis HJ, Transmission of Bartonella henselae by Ixodes ricinus. Emerg Infect Dis. 2008;14:1074–80.
- Balashov YS. Blood sucking ticks (Ixodoidea)—vectors of diseases of man and animals. Miscellaneous publications of the Entomological Society of America. 1972;8:161–376.
- Pappalardo BL, Correa MT, York CC, Peat CY, Breitschwerdt EB. Epidemiologic evaluation of the risk factors associated with exposure and seroreactivity to Bartonella vinsonii in dogs. Am J Vet Res. 1997;58:467–71.
- Sreter-Lancz Z, Tornyai K, Szell Z, Sreter T, Marialigeti K. Bartonella infections in fleas (Siphonaptera: Pulicidae) and lack of bartonellae in ticks (Acari: Ixodidae) from Hungary. Folia Parasitol (Praha). 2006;53:313–6.
- Barnes A, Bell SC, Isherwood DR, Bennett M, Carter SD. Evidence of Bartonella henselae infection in cats and dogs in the United Kingdom. Vet Rec. 2000;147:673–7.
- Lucey D, Dolan MJ, Moss CW, Garcia M, Hollis DG, Wegner S, Relapsing illness due to Rochalimaea henselae in immunocompetent hosts: implication for therapy and new epidemiologic associations. Clin Infect Dis. 1992;14:683–8.
- Morozova OV, Chernovsova NY, Morozov IV. Detection of the Bartonella DNA by the method of nested PCR in patients after tick bites in Nov-Osibirsk region. Mol Gen Mikrobiol Virusol. 2005;4:14–7.
- Breitschwerdt EB, Maggi RG, Nicholson WL, Cherry NA, Woods CW. Bartonella sp. bacteremia in patients with neurological and neurocognitive dysfunction. J Clin Microbiol. 2008;46:2856–61.
- Angelakis E, Pulcini C, Waton J, Imbert P, Socolovschi C, Edourard S, Scalp eschar and neck lymphadenopathy caused by Bartonella henselae after tick bite. Clin Infect Dis. 2010 Jan 13; [Epub ahead of print].
- Zangwill KM, Hamilton DH, Perkins BA, Regnery RL, Plikaytis BD, Hadler JL, Cat scratch disease in Connecticut. Epidemiology risk factors and evaluation of a new diagnostic test. N Engl J Med. 1993;329:8–13.
- Eskow E, Rao R-VS, Mordechai E. Concurrent infection of the central nervous system by Borrelia burgdorferi and Bartonella henselae. Evidence for a novel tick-borne disease complex. Arch Neurol. 2001;58:1357–63.
- Halperin JJ, Wormser GP. Of fleas and ticks on cats and mice…. Arch Neurol. 2001;58:1345–7.
- Adelson ME, Rao R-VS, Tilton RC, Cabets K, Eskow E, Fein L, Prevalence of Borrelia burgdorferi, Bartonella species, Babesia microti and Anaplasma phagocytophila in Ixodes scapularis ticks collected in northern New Jersey. J Clin Microbiol. 2004;42:2799–801.
- Feder HM Jr, Johnson BJ, O’Connell S, Shapiro ED, Steere AC, Wormser GP, A critical appraisal of “chronic Lyme disease.”. N Engl J Med. 2007;357:1422–30.
- Podsiadly E, Chmielewski T, Tylewska-Wierzbanowska S. Bartonella henselae and Borrelia burgdorferi infections of the central nervous system. Ann N Y Acad Sci. 2003;990:404–6.
- Gupta PK, Patel R, Bhatti MJ. Neuroretinitis secondary to concurrent infection with cat scratch disease and Lyme disease. Eye (Lond). 2009;23:1607.
- Weinstein A. Editorial commentary: laboratory testing for Lyme disease: time for a change? Clin Infect Dis. 2008;47:196–7.
- Arnez M, Luznik-Bufon T, Avsic-Zupanc T, Ruzic-Sabljic E, Petrovec M, Lotric-Furlan S, Causes of febrile illnesses after a tick bite in Slovenian children. Pediatr Infect Dis J. 2003;22:1078–83.
- Table 1. Reasons that Bartonella species might be transmitted by ticks
- Table 2. Reasons that transmission of Bartonella henselae by deer ticks is unlikely or unproven
Please use the form below to submit correspondence to the authors or contact them at the following address:
Gary P. Wormser, New York Medical College, Division of Infectious Diseases, Munger Pavilion, Rm 245, Valhalla, NY 10595, USA
Comment submitted successfully, thank you for your feedback.
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.
- Page created: December 14, 2010
- Page last updated: December 14, 2010
- Page last reviewed: December 14, 2010
- Centers for Disease Control and Prevention,
National Center for Emerging and Zoonotic Infectious Diseases (NCEZID)
Office of the Director (OD)