Skip to main content
  • ASM
    • Antimicrobial Agents and Chemotherapy
    • Applied and Environmental Microbiology
    • Clinical Microbiology Reviews
    • Clinical and Vaccine Immunology
    • EcoSal Plus
    • Eukaryotic Cell
    • Infection and Immunity
    • Journal of Bacteriology
    • Journal of Clinical Microbiology
    • Journal of Microbiology & Biology Education
    • Journal of Virology
    • mBio
    • Microbiology and Molecular Biology Reviews
    • Microbiology Resource Announcements
    • Microbiology Spectrum
    • Molecular and Cellular Biology
    • mSphere
    • mSystems
  • Log in
  • My alerts
  • My Cart

Main menu

  • Home
  • Articles
    • Current Issue
    • Accepted Manuscripts
    • COVID-19 Special Collection
    • Archive
    • Minireviews
  • For Authors
    • Submit a Manuscript
    • Scope
    • Editorial Policy
    • Submission, Review, & Publication Processes
    • Organization and Format
    • Errata, Author Corrections, Retractions
    • Illustrations and Tables
    • Nomenclature
    • Abbreviations and Conventions
    • Publication Fees
    • Ethics Resources and Policies
  • About the Journal
    • About JCM
    • Editor in Chief
    • Editorial Board
    • For Reviewers
    • For the Media
    • For Librarians
    • For Advertisers
    • Alerts
    • RSS
    • FAQ
  • Subscribe
    • Members
    • Institutions
  • ASM
    • Antimicrobial Agents and Chemotherapy
    • Applied and Environmental Microbiology
    • Clinical Microbiology Reviews
    • Clinical and Vaccine Immunology
    • EcoSal Plus
    • Eukaryotic Cell
    • Infection and Immunity
    • Journal of Bacteriology
    • Journal of Clinical Microbiology
    • Journal of Microbiology & Biology Education
    • Journal of Virology
    • mBio
    • Microbiology and Molecular Biology Reviews
    • Microbiology Resource Announcements
    • Microbiology Spectrum
    • Molecular and Cellular Biology
    • mSphere
    • mSystems

User menu

  • Log in
  • My alerts
  • My Cart

Search

  • Advanced search
Journal of Clinical Microbiology
publisher-logosite-logo

Advanced Search

  • Home
  • Articles
    • Current Issue
    • Accepted Manuscripts
    • COVID-19 Special Collection
    • Archive
    • Minireviews
  • For Authors
    • Submit a Manuscript
    • Scope
    • Editorial Policy
    • Submission, Review, & Publication Processes
    • Organization and Format
    • Errata, Author Corrections, Retractions
    • Illustrations and Tables
    • Nomenclature
    • Abbreviations and Conventions
    • Publication Fees
    • Ethics Resources and Policies
  • About the Journal
    • About JCM
    • Editor in Chief
    • Editorial Board
    • For Reviewers
    • For the Media
    • For Librarians
    • For Advertisers
    • Alerts
    • RSS
    • FAQ
  • Subscribe
    • Members
    • Institutions
Bacteriology

Demonstration of Bartonella grahamii DNA in Ocular Fluids of a Patient with Neuroretinitis

F. T. Kerkhoff, A. M. C. Bergmans, A. van der Zee, A. Rothova
F. T. Kerkhoff
Department of Ophthalmology, F. C. Donders Institute, University Hospital, Utrecht, and
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
A. M. C. Bergmans
Laboratory of Molecular Microbiology, St. Elisabeth Hospital, Tilburg, The Netherlands
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
A. van der Zee
Laboratory of Molecular Microbiology, St. Elisabeth Hospital, Tilburg, The Netherlands
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
A. Rothova
Department of Ophthalmology, F. C. Donders Institute, University Hospital, Utrecht, and
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
DOI: 10.1128/JCM.37.12.4034-4038.1999
  • Article
  • Figures & Data
  • Info & Metrics
  • PDF
Loading

ABSTRACT

We describe the clinical and laboratory features of a 55-year-old human immunodeficiency virus-negative female patient who presented with bilateral intraocular inflammatory disease (neuroretinitis type) and behavioral changes caused by a Bartonella grahamiiinfection. Diagnosis was based on the PCR analysis of DNA extracted from the intraocular fluids. DNA analysis of the PCR product revealed a 100% identity with the 16S rRNA gene sequence of B. grahamii. The patient was successfully treated with doxycycline (200 mg/day) and rifampin (600 mg/day) for 4 weeks. This is the first report that demonstrates the presence of a Bartonellaspecies in the intraocular fluids of a nonimmunocompromised patient and that indicates that B. grahamii is pathogenic for humans.

The spectrum of diseases attributed to Bartonella species is still expanding; so far, four species, B. henselae, B. quintana, B. bacilliformis, and B. elizabethae, have been identified as causes of human disease (16). B. grahamii(formerly known as Grahamella) has been found in small rodents, but was, to our knowledge, never implicated in human infections (3, 11).

Ocular involvement in the course of Bartonella infections is being recognized with increasing frequency, with B. henselaebeing the most frequently encountered species (9, 18). In the past, ophthalmological manifestations such as Parinaud's oculoglandular syndrome, papillitis, multifocal chorioretinitis, and, mainly, neuroretinitis have been associated with cat-scratch disease (CSD), especially in children and young adults (5, 18). In addition, various reports have described intraocular inflammation associated with highly positive antibody titers against B. henselae in patients who lacked the systemic symptoms and signs typical of generalized CSD (12, 24).

The exact pathogenesis of ocular involvement in bartonellosis is still obscure. Although the presence of B. henselae DNA has been described in the retina of an AIDS patient, it is not known whether in immunocompetent patients the Bartonella species directly cause intraocular infection or whether ocular involvement represents a secondary (auto)immune reaction (29). We describe a patient with neuroretinitis and high levels of immunoglobulin G (IgG) againstB. henselae in serum. PCR and sequence analysis of the PCR product identified the presence of B. grahamii DNA in the patient's eye.

CASE REPORT

A 55-year-old female patient was referred to our uveitis clinic for an analysis of her bilateral neuroretinitis, which was accompanied by behavioral changes.

The patient had a history of insulin-dependent diabetes mellitus from the age of 35 years and hypothyroidism, for which she was treated with insulin and levothyroxine. One year before the referral, the patient had consulted an ophthalmologist because of a progressive decrease of visual acuity in both eyes and sudden onset of headache. Behavioral changes such as irritability and anxiety were noticed by the family members. The patient was admitted to the district hospital for further evaluation. Ophthalmological examination at that time revealed visual acuity of 20/125 in the right eye (RE) and 20/50 in the left eye (LE), inflammatory cells in the anterior chambers, posterior synechiae, vitreitis, and papillitis (Fig. 1), with macular edema and retinal vasculitis in both eyes. There were no signs of diabetic retinopathy or thyroid orbitopathy.

Fig. 1.
  • Open in new tab
  • Download powerpoint
Fig. 1.

Fluorescein angiogram of the right eye (A) and the left eye (B) showing a classic neuroretinitis with an extremely hyperfluorescent optic nerve with discrete peripapillary leakage of fluorescein and small peripapillary hemorrhages.

On general examination, no abnormalities were noticed; specifically, no signs of systemic vasculitis were present. The results of laboratory evaluations for erythrocyte and leukocyte counts and renal and liver function tests were within the normal limits, the patient was negative for HLA-B27, a test for antinuclear antibody was positive with a titer of 1:40, and the erythrocyte sedimentation rate was 66 mm per h. There was no serological evidence of infection with herpes simplex virus (HSV), varicella-zoster virus (VZV), or Borrelia burgdorferi. Her diabetes and thyroid status were adequately controlled.

Neurological examination disclosed no apparent abnormalities; the patient was well oriented in place and time but reacted slowly to external stimuli. A computed tomographic scan of the cerebrum showed no abnormalities. The cerebrospinal fluid (CSF) revealed a pleiocytosis without oligoclonal bands, and further microbiological analysis of the CSF disclosed no evidence of infection with HSV, VZV, enteroviruses, orB. burgdorferi.

A presumed diagnosis of viral encephalouveitis was made, and the patient was given a course of oral prednisone (initial dose, 90 mg, together with 250 mg of acetazolamide three times daily for retinal edema). Her visual acuity and mental condition slowly improved, but her ocular inflammatory disease persisted and the patient was referred to our institution.

On presentation at our institution, her visual acuity was 20/80 in the RE and 20/30 in the LE. Anterior eye segments were normal, and old posterior synechiae were present. Posterior subcapsular opacities were noted in the lens. On dilated fundus examination, occasional cells and dense opacities were located in the vitreous humor; the optic disc and retina appeared normal except for slight macular edema and sporadic atrophic scars in the peripheral retinas of both eyes. The fluorescein angiography revealed leakage from the optic disc and moderate cystoid macular edema. The reevaluation for uveitis included tests for erythrocyte sedimentation rate; erythrocyte and leukocyte counts; serum angiotensin-converting enzyme levels; and syphilis,Borrelia, and Bartonella serology as well as chest radiography. Except for the Bartonella serological test, the results of all tests were within the normal limits. The human immunodeficiency virus (HIV) serological test was negative. The patient owned a dog and had no contact with cats. The PCR was positive forBartonella and was negative for all other microorganisms evaluated.

A diagnosis of ocular bartonellosis was made, and the patient was treated with doxycycline at 200 mg/day and rifampin at 600 mg/day for 4 weeks. On ophthalmic examination 3 months after the treatment was completed, the intraocular inflammation appeared to be extinguished. Due to cataract development, however, the visual acuity had decreased (20/300 in the RE and 20/100 in the LE) and extraction of the cataract from the RE was performed. The intraocular fluid collected during the surgery was reexamined for the presence of Bartonella DNA. The visual acuity of the RE increased to 20/30 after cataract extraction.

MATERIALS AND METHODS

Serological analysis.Within a 6-month period in 1998, three serum samples were taken from the patient (Fig.2). The first two serum samples were taken before antibiotic treatment; the third was taken 3 months after the treatment was completed (during the cataract surgery). The serum and CSF taken during the initial phase of the patient's disease were not stored and therefore could not be examined retrospectively. All serum samples were tested for the presence of IgG and IgM antibodies against B. henselae in an enzyme immunoassay (EIA) and in an indirect fluorescence assay (IFA) with B. henselae as the antigen, as described earlier (2). In our laboratory, the cutoff values for positive serology were 1:900 for IgG EIA, 1:250 for IgM EIA, 1:128 for IgG IFA, and 1:16 for IgM IFA (2).

Fig. 2.
  • Open in new tab
  • Download powerpoint
Fig. 2.

Time course of clinical manifestations and detection ofB. grahamii DNA in intraocular fluids and B. henselae antibodies in serum. *, determined retrospectively; pos., positive; neg., negative; Persist., persistent.

DNA analysis with anterior chamber fluid.Within a 3-month period, two anterior chamber fluid samples were collected by a standard procedure (Fig. 2) (26). The first one was collected during active ocular inflammation and before the antibiotic treatment was initiated, and the second one was collected 3 months after the treatment was completed (during the cataract surgery, when there were no signs of intraocular inflammatory activity).

DNA was extracted from anterior chamber fluid with a commercially available DNA purification kit (QIAamp Blood Kit; QIAGEN AG, Basel, Switzerland). A PCR analysis was performed with the extracted DNA and with the Bartonella-specific primers p24E and p12B described by Relman et al. (20), but without the 5′ restriction site sequences. The PCR product was hybridized by programs with a 5′-biotinylated, B. henselae-specific oligonucleotide probe (5′-ATTTGGTTGGGCACTCTAGGGG-3′) (1). The DNA sequence of the Bartonella PCR product was determined with fluorescent dye dideoxide terminators in the cycling sequencing system (Applied Biosystems, Perkin-Elmer, Nieuwerkerk a.d. IJssel, The Netherlands). The DNA sequencing data were compared with the sequences in the EMBL and GenBank nucleotide sequence databases by using the FastA and BLAST comparison programs with a 5′-biotinylated, B. henselae-specific oligonucleotide.

RESULTS

Serological analysis.By EIA, the titers of IgG antibodies against B. henselae were 1:1,000 in all three serum samples, and IgM antibodies were absent. The IFA with B. henselae as the antigen revealed IgG titers of 1:64 and 1:32 in the serum samples before antibiotic treatment and titers of 1:32 after the treatment. By IFA, the IgM antibody titers remained less than 1:8.

Analysis of DNA from anterior chamber fluid.PCR with theBartonella-specific primers and with DNA extracted from the anterior chamber fluid yielded a PCR fragment of the expected size of 300 bp. The PCR product did not hybridize with the B. henselae-specific oligonucleotide probe. DNA sequence analysis of the PCR product and comparison of the sequence with those present in the EMBL and GenBank nucleotide sequence databases revealed a 100% identity of DNA from the first anterior chamber fluid sample with the 16S rRNA gene sequence of B. grahamii (accession no.Z31349 ). PCRs with intraocular fluids for detection of HSV, VZV, andToxoplasma gondii were also performed, and the results were negative for all microorganisms studied. With the second anterior chamber fluid sample, the PCR for B. grahamii was negative.

DISCUSSION

In the study described in this report we demonstrated the presence of B. grahamii DNA in the eye of an HIV-negative patient with neuroretinitis, which indicates the direct involvement ofBartonella species in neuroretinitis and further documents the possibility of B. grahamii infection in humans.

Uveitis, an intraocular inflammatory disease, is an important cause of severe visual impairment and blindness and causes significant morbidity in the economically active young adult population (25). Infectious processes play an important role in the pathogenesis of uveitis; specifically, herpesviruses and T. gondii are common causative agents in immunocompetent as well as in immunocompromised patients (8). The recognition of an infectious etiology of uveitis is important because of the consequences of the treatment; while immunosuppressive medication is essential for the majority of patients with noninfectious uveitis, this treatment modality may induce a fulminant course of infection without specific antimicrobial treatment (21). The recently achieved ability to detect microbial DNA has led to the recognition of various infectious agents as causes of intraocular inflammatory disease (7, 8).

The route of B. grahamii infection in our patient is unclear. Various animals have been recognized as reservoirs forBartonella species. B. grahamii was isolated from rodents in North America and Europe (3, 11). Domestic cats are a major reservoir for B. henselae, and a recently described subspecies, B. clarridgeiae, was also found in cats (13, 14). B. vinsonii has been cultured from the blood of a dog with endocarditis (4). Furthermore, studies suggested that not only fleas but also the human body louse, the sand fly, and ticks are possible vectors in the transmission ofBartonella species (16). Our patient described here owned a dog but had a negative history of cat ownership or cat scratches and had never been bitten or been in contact with small rodents. The existence of nonfeline infectious sources may explain the occurrence of ocular bartonellosis in the absence of previous contact with cats.

In previous studies, ocular bartonellosis was mainly associated withB. henselae infections; however, this association was predominantly based solely on serological grounds (9, 12, 18). The present case suggests that ocular bartonellosis might also be caused by other Bartonella species, and therefore, ocular bartonellosis may also be present in patients lacking the systemic symptoms of CSD. The presence of IgG against B. henselae in the serum of our patient, as determined by EIA, is probably due to cross-reactivity between B. henselae andB. grahamii. Cross-reactivity between differentBartonella species has been described earlier (28).

The diagnosis of human bartonellosis may be extremely troublesome, since the typical clinical features are not always present and the interpretation of the results of serological tests is difficult, as cross-reactivity between different Bartonella species has been observed (2, 28). Therefore, the diagnosis of bartonellosis should preferably rely on the detection of the infectious agent or the DNA of the infectious agent in the affected tissue. As patients with intraocular inflammation do not have tissues that are easily available for biopsy, diagnostic vitrectomy and retinal biopsy are recommended for patients with severe cases that threaten visual acuity (29). However, these surgical procedures are invasive and have considerable complication rates (27). Analysis of aqueous humor collected by anterior chamber tap, which was reported to be a safe diagnostic procedure for patients with uveitis, had diagnostic value even for patients with inflammatory lesions located in the posterior segment of the eye, such as the lesions associated with toxoplasmosis (7, 8, 26). In the previous studies, PCR analysis of intraocular fluids was specifically recommended for patients with early infections (and for immunosuppressed patients), since PCR positivity was mainly found for samples collected within 2 weeks after the onset of the disease (7, 8). TheBartonella PCR is usually performed with pus aspirates and lymph nodes from patients in the acute stages of the disease (1). A study of CSD encephalitis also showed that a PCR for detection of B. henselae in CSF was predominantly positive early in the course of the disease (23). In our patient, 1 year after the onset of the disease, B. grahamii DNA was present in the eye. The pathogenesis of intraocular inflammatory disease in patients with bartonellosis is not clear. The direct involvement of B. henselae in uveitis was supported by the detection of B. henselae DNA in a retinal lesion of an AIDS patient. In immunocompetent patients, ocular disease usually develops after systemic involvement has subsided, suggesting that ocular involvement represents a late complication of the disease (9, 18). However, this assumption cannot be confirmed by previous studies, because serology was performed mainly by IFA and no specific IgM titers were determined for these patients (6, 9, 19, 30). The late manifestation of ocular involvement might be explained by the persistence of bacteria in the eye, which is shielded from the peripheral circulation by the blood-ocular barrier. This presumably occurred in our patient. An alternative hypothesis for the development of uveitis in a late stage of systemic bartonellosis may be that the bacteria have an indirect role, in that they induce a late (auto)immune reaction. The presence of B. grahamii DNA in our patient indicates that the direct microbial involvement may occur in HIV-negative patients. The late onset of intraocular inflammation in patients with systemic infections is a well-known phenomenon in uveitic disease; it is characteristic for herpetic retinopathies and toxoplasmic retinitis (25). In patients with bacterial infections such as syphilis, tuberculosis, leptospirosis, and borreliosis, the late involvement also occurs and is usually associated with the presence of bacteria or bacterial DNA in the eye (10, 15, 17, 22).

We demonstrated B. grahamii DNA in the intraocular fluids of a patient with neuroretinitis who was subsequently treated and reacted well to antibiotic therapy and who would otherwise be treated with immunosuppressive medication. Therefore, we would include bartonellosis in the differential diagnosis of patients with intraocular inflammatory disease, especially in those patients with neuroretinitis. Depending on the clinical manifestations and outcomes of laboratory examinations, we recommend that intraocular fluids be tested for infectious agents before initiating immunosuppressive treatment as a result of the symptomatology, especially in those patients with an unexplained cause of intraocular inflammation and clinical features suggesting an infectious disease. Future studies are needed to establish the involvement of different Bartonella species in human ocular disease.

FOOTNOTES

    • Received 26 April 1999.
    • Returned for modification 4 June 1999.
    • Accepted 24 August 1999.
  • Copyright © 1999 American Society for Microbiology

REFERENCES

  1. 1.↵
    1. Bergmans A. M. C.,
    2. Groothedde J. W.,
    3. Schellekens J. F. P.,
    4. van Embden J. D. A.,
    5. et al.
    Etiology of cat scratch disease: comparison of polymerase chain reaction detection of Bartonella (formerly Rochalimea) and Afipia felis DNA with serology and skin tests.J. Infect. Dis.1711995916923
    OpenUrlCrossRefPubMedWeb of Science
  2. 2.↵
    1. Bergmans A. M. C.,
    2. Peeters M. F.,
    3. Schellekens J. F. P.,
    4. Vos M. C.,
    5. Sabbe L. J. M.,
    6. Ossewaarde J. M.,
    7. Verbakel H.,
    8. Hooft H. J.,
    9. Schouls L. M.
    Pitfalls and fallacies of cat scratch disease serology: evaluation of Bartonella henselae-based indirect fluorescence assay and enzyme-linked immunoassay.J. Clin. Microbiol.35199719311937
    OpenUrlAbstract/FREE Full Text
  3. 3.↵
    1. Birtles R. J.,
    2. Harrison T. G.,
    3. Molyneux D. H.
    Grahamella in small woodland mammals in the U.K.: isolation prevalence and host specificity.Ann. Trop. Med. Parasitol.8881994317327
    OpenUrl
  4. 4.↵
    1. Breitschwerdt E. B.,
    2. Kordick D. L.,
    3. Malakey D. E.,
    4. Keene B.,
    5. Hadfield T. L.,
    6. Wilson K.
    Endocarditis in a dog due to infection with a novel Bartonella subspecies.J. Clin. Microbiol.331995154160
    OpenUrlAbstract/FREE Full Text
  5. 5.↵
    1. Carithers H. A.
    Oculoglandular disease of Parinaud.Am. J. Dis. Child.132197811951200
    OpenUrlCrossRefPubMed
  6. 6.↵
    1. Cohen S. M.,
    2. Davis J. L.,
    3. Gass D. M.
    Branch retinal arterial occlusion in multifocal retinitis with optic nerve edema.Arch. Ophthalmol.113199512711276
    OpenUrlCrossRefPubMedWeb of Science
  7. 7.↵
    1. de Boer J. H.,
    2. Luyendijk L.,
    3. Rothova A.,
    4. Kijlstra A.
    Analysis of ocular fluids for local antibody production in uveitis.Br. J. Ophthalmol.791995610616
    OpenUrlFREE Full Text
  8. 8.↵
    1. de Boer J. H.,
    2. Verhagen C.,
    3. Bruinenberg M.,
    4. Rothova A.,
    5. et al.
    Serologic and polymerase chain reaction analysis of intraocular fluids in the diagnosis of infectious uveitis.Am. J. Ophthalmol.1211996650658
    OpenUrlCrossRefPubMedWeb of Science
  9. 9.↵
    1. Golnik K. C.,
    2. Marotto M. E.,
    3. Fanous M. M.,
    4. et al.
    Ophthalmic manifestations of Rochalimaea species.Am. J. Ophthalmol.1181994145151
    OpenUrlPubMedWeb of Science
  10. 10.↵
    1. Hira S. K.,
    2. Shukla S. M.,
    3. Mubanga M. R.
    Uveitis in secondary syphilis: a report of treponemes in aqueous humor.Eur. J. Sex. Transm. Dis.81985107109
    OpenUrl
  11. 11.↵
    1. Hofmeister E. K.,
    2. Kolbert C. P.,
    3. Abdulkarim A. S.,
    4. Magera J. M. H.,
    5. et al.
    Cosegregation of a novel Bartonella species with Borrelia burgdorferi and Babasia micoti in Peromyscus leucopus.J. Infect. Dis.1771998409416
    OpenUrlCrossRefPubMedWeb of Science
  12. 12.↵
    Kerkhoff, F. T., J. M. Ossewaarde, W. S. de Loos, and A. Rothova. Presumed ocular bartonellosis. Br. J. Ophthalmol., in press.
  13. 13.↵
    1. Koehler J. E.,
    2. Glaser C. A.,
    3. Tappero J. W.
    Rochalimaea henselae infection. A new zoonosis with the domestic cat as reservoir.JAMA71994531535
    OpenUrl
  14. 14.↵
    1. Kordick D. L.,
    2. Hilyard E. J.,
    3. Hadfield T. L.,
    4. Wilson K. H.,
    5. Steigerwaldt A. G.,
    6. Brenner D. J.,
    7. Breitschwerdt E. B.
    Bartonella clarridgeiae, a newly recognized zoonotic pathogen causing inoculation papules, fever, and lymphadenopathy (cat scratch disease).J. Clin. Microbiol.35199718131818
    OpenUrlAbstract/FREE Full Text
  15. 15.↵
    1. Kox L. F. F.,
    2. Jansen H. M.,
    3. Kuijper S.,
    4. Kolk A. H. J.
    Multiplex PCR assay for immediate identification of the infecting species in patients with mycobacterial disease.J. Clin. Microbiol.35199714921498
    OpenUrlAbstract/FREE Full Text
  16. 16.↵
    1. Maurin M.,
    2. Birtles R. J.,
    3. Raoult D.
    Current knowledge of Bartonella species.Eur. J. Clin. Microbiol. Infect. Dis.161997487506
    OpenUrlCrossRefPubMedWeb of Science
  17. 17.↵
    1. Merien F.,
    2. Perolar P.,
    3. Mancel E.,
    4. Persan D.,
    5. Baraton G.
    Detection of Leptospira DNA by polymerase chain reaction in aqueous humour of a patient with unilateral uveitis.J. Infect. Dis.168199313351336
    OpenUrlCrossRefPubMed
  18. 18.↵
    1. Ormerod D.,
    2. Skolnick K. A.,
    3. Menesky M. M.,
    4. Pavan P. R.,
    5. Pon D. M.
    Retinal and choroidal manifestations of cat-scratch disease.Ophthalmology105199810241031
    OpenUrlCrossRefPubMedWeb of Science
  19. 19.↵
    1. Regnery R. L.,
    2. Olson J. G.,
    3. Perkins B. A.,
    4. Bibb W.
    Serological response to “Rochalimaea henselae” antigen in suspected cat-scratch disease.Lancet339199214431445
    OpenUrlCrossRefPubMedWeb of Science
  20. 20.↵
    1. Relman D. A.,
    2. Loutit J. S.,
    3. Schmidt T. M.,
    4. Falkow S.,
    5. Tompkins L. S.
    The agent of bacillary angiomatosis. An approach to the identification of uncultured pathogens.N. Engl. J. Med.323199015731580
    OpenUrlCrossRefPubMedWeb of Science
  21. 21.↵
    1. Sabates R.,
    2. Pruett R. C.,
    3. Brockhurst R. J.
    Fulminant ocular toxoplasmosis.Am. J. Ophthalmol.921981497503
    OpenUrlCrossRefPubMed
  22. 22.↵
    1. Schubert H. D.,
    2. Greenebaum E.,
    3. Neu H. C.
    Cytologically proven seronegative Lyme choroiditis and vitritis.Retina1419943942
    OpenUrlPubMed
  23. 23.↵
    1. Schwatrzman W. A.,
    2. Patnaik M.,
    3. Barka N. E.,
    4. Peter J. B.
    Rochalimaea antibodies in HIV-associated neurologic disease.Neurology44199413121316
    OpenUrlAbstract/FREE Full Text
  24. 24.↵
    1. Soheilian M.,
    2. Markomichelakis N.,
    3. Foster C. S.
    Intermediate uveitis and retinal vasculitis as manifestations of cat scratch disease.Am. J. Ophthalmol.1221996582583
    OpenUrlPubMedWeb of Science
  25. 25.↵
    1. Suttorp M. S. A.,
    2. Rothova A.
    The possible impact of uveitis in blindness, a literature survey.Br. J. Ophthalmol.801996844848
    OpenUrlFREE Full Text
  26. 26.↵
    1. van der Lelij A.,
    2. Rothova A.
    Diagnostic anterior chamber paracentesis in uveitis: a safe procedure? Br. J. Ophthalmol. 81 1997 976 979
    OpenUrlAbstract/FREE Full Text
  27. 27.↵
    1. Verbraeken H.
    Diagnostic vitrectomy and chronic uveitis.Graefes Arch. Clin. Exp. Ophthalmol.2341996S2S7
    OpenUrl
  28. 28.↵
    1. Waldvogel K.,
    2. Regnery R. L.,
    3. Anderson R.,
    4. Caduff R.,
    5. Caduff J.,
    6. Nadal D.
    Disseminated cat-scratch disease: detection of Rochalimea henselae in affected tissue.Eur. J. Pediatr.15319942327
    OpenUrlPubMedWeb of Science
  29. 29.↵
    1. Warren K.,
    2. Goldstein E.,
    3. Hung V. S.,
    4. Koehler J. E.,
    5. Richardson W.
    Use of retinal biopsy to diagnose B. henselae retinitis in an HIV-infected patient.Arch. Ophthalmol.1161998937940
    OpenUrlPubMedWeb of Science
  30. 30.↵
    1. Zacchei A. C.,
    2. Newman N. J.,
    3. Sternberg P.
    Serous retinal detachment of the macula associated with cat scratch disease.Am. J. Ophthalmol.1201995769770
    OpenUrl
PreviousNext
Back to top
Download PDF
Citation Tools
Demonstration of Bartonella grahamii DNA in Ocular Fluids of a Patient with Neuroretinitis
F. T. Kerkhoff, A. M. C. Bergmans, A. van der Zee, A. Rothova
Journal of Clinical Microbiology Dec 1999, 37 (12) 4034-4038; DOI: 10.1128/JCM.37.12.4034-4038.1999

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Print

Alerts
Sign In to Email Alerts with your Email Address
Email

Thank you for sharing this Journal of Clinical Microbiology article.

NOTE: We request your email address only to inform the recipient that it was you who recommended this article, and that it is not junk mail. We do not retain these email addresses.

Enter multiple addresses on separate lines or separate them with commas.
Demonstration of Bartonella grahamii DNA in Ocular Fluids of a Patient with Neuroretinitis
(Your Name) has forwarded a page to you from Journal of Clinical Microbiology
(Your Name) thought you would be interested in this article in Journal of Clinical Microbiology.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Share
Demonstration of Bartonella grahamii DNA in Ocular Fluids of a Patient with Neuroretinitis
F. T. Kerkhoff, A. M. C. Bergmans, A. van der Zee, A. Rothova
Journal of Clinical Microbiology Dec 1999, 37 (12) 4034-4038; DOI: 10.1128/JCM.37.12.4034-4038.1999
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
  • Top
  • Article
    • ABSTRACT
    • CASE REPORT
    • MATERIALS AND METHODS
    • RESULTS
    • DISCUSSION
    • FOOTNOTES
    • REFERENCES
  • Figures & Data
  • Info & Metrics
  • PDF

KEYWORDS

Aqueous Humor
Bartonella
Bartonella Infections
DNA, Bacterial
Eye Infections, Bacterial
Optic Neuritis

Related Articles

Cited By...

About

  • About JCM
  • Editor in Chief
  • Board of Editors
  • Editor Conflicts of Interest
  • For Reviewers
  • For the Media
  • For Librarians
  • For Advertisers
  • Alerts
  • RSS
  • FAQ
  • Permissions
  • Journal Announcements

Authors

  • ASM Author Center
  • Submit a Manuscript
  • Article Types
  • Resources for Clinical Microbiologists
  • Ethics
  • Contact Us

Follow #JClinMicro

@ASMicrobiology

       

ASM Journals

ASM journals are the most prominent publications in the field, delivering up-to-date and authoritative coverage of both basic and clinical microbiology.

About ASM | Contact Us | Press Room

 

ASM is a member of

Scientific Society Publisher Alliance

 

American Society for Microbiology
1752 N St. NW
Washington, DC 20036
Phone: (202) 737-3600

 

Copyright © 2021 American Society for Microbiology | Privacy Policy | Website feedback

Print ISSN: 0095-1137; Online ISSN: 1098-660X