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Journal of Feline Medicine and Surgery logoLink to Journal of Feline Medicine and Surgery
. 2016 Jun 24;2(1):61–68. doi: 10.1053/jfms.2000.0067

Bartonella spp Antibodies and DNA in Aqueous Humour of Cats

M R Lappin 1, D L Kordick 2, E B Breitschwerdt 2
PMCID: PMC10829198  PMID: 11716593

Abstract

Bartonella spp antibodies were measured in the serum and aqueous humour of cats with and without uveitis and polymerase chain reaction (PCR) for Bartonella spp DNA was performed on aqueous humour from most of the cats. Serum and aqueous humour were assayed from 49 client-owned cats with uveitis, 49 healthy shelter cats, and nine cats experimentally inoculated with either B henselae or B clarridgeiae, 454 days after inoculation. An aqueous antibody coefficient (C value) was calculated for cats positive for Bartonella spp antibodies in the aqueous humour. Ocular production of Bartonella spp IgG (C value >1) was detected in seven of 49 cats with uveitis, none of 49 healthy shelter cats, and four of nine experimentally inoculated cats. The organism was detected by PCR in the aqueous humour of three of 24 cats with uveitis, one of 49 healthy shelter cats, and four of nine experimentally inoculated cats. Bartonella spp infect the eyes of some cats following natural exposure or experimental inoculation and may cause uveitis in some cats.

Intra-ocular inflammation in cats has been most commonly associated with neoplasia, degeneration of the lens, and infections with Toxoplasma gondii, feline infectious peritonitis virus, feline leukaemia virus, feline immunodeficiency virus, feline herpesvirus 1, parasites or systemic mycoses (Lappin et al 1992, Williams 1994, Maggs et al 1999). Histopathological studies of eyes from cats with uveitis show the majority to have infiltrates of lymphocytes and plasma cells in the iris and ciliary body without obvious aetiological agents (Davidson et al 1991, Peiffer & Wilcock 1991). These cell infiltrates could represent immune-mediated inflammation against unrecognised infectious agents. Viral agents are too small to be detected by light microscopy and other infectious agents could be inadvertently missed by histopathology due to sampling error or inappropriate stain selection. For example, T gondii was not detected in ocular tissues of cats with uveitis by histopathological examination (Davidson et al 1991, Peiffer & Wilcock 1991), but was detected in the aqueous humour of 18.6% of cats with uveitis (Lappin et al 1996a) by polymerase chain reaction (PCR).

In some geographical areas, up to 54.6–81% of cats have serum antibodies against Bartonella henselae, indicating exposure to the organism (Chomel et al 1995, Jameson et al 1995). Chronic and relapsing bacteraemia occurs in experimentally and naturally B henselae infected cats (Kordick et al 1995). Bartonellosis has been associated with intra-ocular inflammation in people (Fish et al 1992, Golnick et al 1994, Wong et al 1995, Soheilian et al 1996, Rothova et al 1998). A cat was suspected to have uveitis due to bartonellosis based on local production of antibody in aqueous humour, exclusion of other known causes of uveitis and response to doxycycline (Lappin & Black 1999). Fever, lymphadenopathy and neurological disease occurred in some cats experimentally inoculated with B henselae (Guptill et al 1997, Kordick & Breitschwerdt 1997, Guptill et al 1997). There is seroepidemiological evidence that Bartonella spp infection is associated with gingivitis, lymphadenopathy and urinary tract disorders (Ueno et al 1996, Glaus et al 1997). Based on these findings, it appears that B henselae infection of cats may occasionally cause clinical disease. Cats can also be infected by B clarridgeiae; serological cross-reactivity between this organism and B henselae is variable (Kordick et al 1997, 1999). The purpose of this study was to evaluate the relationship between Bartonella spp and uveitis in cats by assaying aqueous humour from cats with and without uveitis for Bartonella spp antibodies and for presence of Bartonella spp DNA by PCR.

Materials and methods

Naturally exposed cats

Serum and aqueous humour were collected from 49 client-owned cats with uveitis and 49 healthy shelter cats with normal ocular examinations. The majority of the client-owned cats were examined by veterinary ophthalmologists. The shelter source cats were examined and samples collected by a practising veterinarian (courtesy of Dr Allen Riley, Becker Animal Clinic, Birmingham, AB, USA).

The cats with uveitis had no obvious exogenous cause of uveitis or intra-ocular masses. The shelter cats were from Birmingham (AB, USA); cats with uveitis came from diverse geographical regions throughout the USA. Serum and aqueous humour samples were stored at −20 or −70°C until evaluated in this study.

Experimentally inoculated cats

In a separate, independent study nine specific pathogen free (SPF) cats were experimentally inoculated with B clarridgeiae or B henselae to study clinical, immunological and pathological changes resulting from long-term infection. The principal findings of that study were previously published and describe in detail the experimental design (Kordick & Breischwerdt 1997, Kordick et al 1999), while the results of the ocular examinations and testing are reported here. At the end of the study on day 454 after primary inoculation serum, and aqueous humour were collected from all nine cats and were stored at −70°C until use in this study. Serum and aqueous humour were assayed for antibodies at Colorado State University and Bartonella DNA at HESKA® Veterinary Diagnostic Laboratory (Fort Collins, CO, USA). Clinical ophthalmic examinations had been performed on days 84, 118, 191 (cat 8 only), 274 and 436 post-inoculation. Prior to euthanasia on day 454, blood cultures and whole blood PCR (North Carolina State University) were performed as previously described (Kordick et al 1999). After euthanasia, ocular tissues were removed and examined histopathologically In the original study, three experiments were performed which may have had an impact on the results described herein. Methylprednisolone acetate (20 mg/kg, im) had been administered to each cat on day 363. Challenge inoculation of seven cats (cats 1 and 3–8) with B henselae or B clarridgeiae had been performed on day 370 (Kordick et al 1999). Lastly, cats 1–7 and 9 received six 0.5 ml intradermal injections of B henselae skin test antigen at dilutions of 1:1000, 1:500; 1:100, 1:50, 1:25 and 1 × on day 447.

Bartonella henselae antigen preparation

Bartonella henselae was initially grown on rabbit blood heart infusion agar from the blood of a clinically infected human (Regnery et al 1992; courtesy of Dr Russ Regnery, Centers for Disease Control, Atlanta GA and Dr Jane Rooney, Heska Corporation, Fort Collins, CO, USA). The organism was suspended in 0.01 M phosphate-buffered saline solution (PBSS; pH 7.2) at a concentration of 108 organisms/ml. Soluble antigens were obtained by lysing 5 × 107 ice-bath-cooled organisms with 50% duty time intermittent ultrasonic pulsations at 33% power for 10 min, followed by removal of insoluble material by centrifugation at 14 000 × g for 5 min. Soluble antigens were dialysed (Dialysis tubing, Sigma Chemical Co., St. Louis, MO, USA) against 1l of PBSS overnight at 4°C. The protein concentration of this antigen preparation was 10 mg/dl. Glycerol was added to make a 20% solution and the soluble antigens were stored at −70°C until used.

Bartonella spp ELISA

Appropriate wells of a microtitration plate (Immulon 2, Dynatech Laboratories, Chantilly, VA, USA), were sensitised with 50 μl of B henselae antigen diluted 1:200 in 0.01 M PBSS (pH 7.2). After a 24-h incubation at 4°C, the plate was washed three times with 200 μl/well 0.01 M PBSS (pH 7.2) containing 0.05% Tween 20 (PBSS-TW). Positive controls, negative controls, serum samples and aqueous humour samples were diluted 1:10 in PBSS-TW and 50 μl were pipetted into quadruplicate wells. The plates were incubated for 30 min at 37°C and washed as before in PBSS-TW. Anti-feline IgG (1:500, peroxidase-labelled, goat anti-feline IgG, heavy chain; Kirkegaard and Perry Laboratories, Gaithersburg, MD, USA), anti-feline IgM (1:500, peroxidase-labelled, goat anti-feline IgM, heavy chain; Kirkegaard and Perry Laboratories) or anti-feline IgA (1:100, peroxidase-labelled, goat anti-feline IgA, heavy chain; Bethyl Laboratories, Montgomery, Texas) were diluted in PBSS-TW and 50 μl were added to appropriate wells. Following a 30-min incubation at 37°C, the plates were washed as described. A 1:1000 dilution of ophenylenediamine solution in 0.05 M sodium acetate buffer (pH 4.5) plus 0.001% hydrogen peroxide was added to all wells (50 μl/well). After incubation for 30 min at 20°C in the dark, 25 μl of 8 N sulphuric acid (H2SO4) was added to each well to stop the colour reaction. Absorbance of each dilution was measured by an automated microELISA reader equipped with a 492 nm filter. Enzyme and substrate control wells were assessed on each plate.

Bartonella ELISA titration experiments

Serum and aqueous humour from adult, arthropod-free, SPF cats had previously been collected and stored frozen at −70°C. Samples from four cats were collected prior to inoculation with T gondii. Samples from four different cats were collected on week 8 PI with T gondii at which time each aqueous humour sample had T gondii-specific antibody production. These aqueous humour samples were chosen to assess the effect of ocular antibody production against another pathogen on results of the Bartonella spp ELISA. Each serum and aqueous humour sample was diluted 1:10 in PBSS-TW and assayed in quadruplicate wells in the optimised Bartonella spp IgG, IgM, and IgA ELISA. None of the eight aqueous humour samples had an absorbance value >0.008 in the Bartonella spp IgG, IgM, or IgA ELISA. The mean absorbance plus 2 sd of the sera was calculated for each ELISA; the negative control used on all subsequent plates was one that approximated the mean plus 2 sd of these sera. To be considered positive in the Bartonella spp ELISA, the mean absorbance value of suspect serum or aqueous humour sample wells had to exceed the mean of the negative control wells.

Bartonella aqueous humour antibody coefficient

Serum and aqueous humour samples were assayed for calicivirus IgG (naturally exposed cats; Hill et al 1995) or total IgG (experimentally inoculated cats; Lappin et al 1992). In studies of feline toxoplasmosis, the calicivirus antibody-based aqueous humour antibody coefficient has been shown to be more accurate than that based on total IgG (Hill et al 1995). However, the total IgG assay was required for the cats experimentally inoculated with Bartonella spp since they did not have calicivirus antibodies in serum.

Serum and aqueous humour Bartonella IgG, IgM, and IgA ELISA results were converted to %ELISA as follows: sample absorbance minus the negative control absorbance/positive control absorbance minus the negative control absorbance multiplied by 100. The IgM, IgG or IgA Bartonella spp aqueous humour antibody coefficient (Bartonella spp C value) was calculated as follows: aqueous humour Bartonella IgG, IgM, or IgA %ELISA/serum Bartonella IgG, IgM, or IgA %ELISA multiplied by the serum total IgG or calicivirus IgG/aqueous humour total IgG or calicivirus IgG. A Bartonella spp C value >1 was considered evidence for ocular production of Bartonella antibodies; a Bartonella spp C value <1 was considered evidence for leakage of serum antibody into aqueous humour from breakdown of the blood ocular barrier due to inflammation.

Bartonella spp. aqueous humour PCR

Aqueous humour samples were available for testing from the 49 shelter source healthy cats, nine experimental cats, and 24 of 49 cats with uveitis. The volume of aqueous humour assayed was based on sample availability; however, for the majority of samples 50 μl were available. Aqueous humour samples were submitted to the HESKA®; Veterinary Diagnostic Laboratories for Bartonella spp PCR analysis (Jensen et al 1999). This PCR amplifies B henselae, B clarridgeiae, and B vinsonii (subspecies berkhoffii) but does not amplify other common bacteria which infect cats. The PCR analysis was repeated three times on each sample and a minimum of two positive assays was necessary to designate a sample as positive.

Statistical evaluation

Bartonella spp seroprevalence rates were compared between groups by chi-square analysis. Significance was defined as P<0.005. Shelter cats from Alabama were chosen as the healthy control group as outdoor cats in the region have a high incidence of bartonellosis (Jameson et al 1995). Thus, if clinically affected cats had statistically higher seroprevalences, the results would unlikely to be from geographical variation.

Results

Naturally exposed cats

Multiple combinations of Bartonella spp IgG, IgM and IgA were detected in serum of cats with uveitis and healthy shelter cats (Table 1). The prevalence of Bartonella spp IgG, IgM or IgA in serum was similar in cats with uveitis (39 of 49 cats) and the healthy shelter cat group (35 of 49 cats). Bartonella spp IgM (chi-square=5.518; P<0.025) and IgA (chi-square=5.926; P<0.025) were detected more frequently in serum from cats with uveitis than from healthy shelter cats (Table 1).

Table 1.

Bartonella spp serological test results in naturally exposed cats with and without uveitis

ELISA test result Cats with uveitis (n=49) n (%) Healthy shelter cats (n=49) n (%)
IgG 14 (28.6) 24 (49.0)
IgM 1 (2.0) 0 (0)
IgA 2 (4.1) 0 (0)
IgG, IgM 4 (8.2) 2 (4.1)
IgG, IgA 6 (12.2) 4 (8.2)
IgM, IgA 1 (2.0) 1 (2.0)
IgG, IgM, IgA 11 (22.4) 4 (8.2)
Any IgG 35 (71.4) 34 (69.4)
Any IgM 17 (34.7) 7 (14.3)
Any IgA 20 (40.8) 9 (18.4)
Any antibody positive 39 (79.6) 35 (71.4)
Antibody negative 10 (20.4) 14 (28.6)
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Bartonella spp IgA C value >1 was not detected in the aqueous humour of any cat (Table 2). Bartonella spp IgM or IgG C values >1 were detected in nine of 49 (18.4%) cats with uveitis but not in any healthy shelter cat (Table 2).

Table 2.

Bartonella henselae antibody in aqueous humour of client-owned cats with uveitis and humane shelter source healthy cats

Group n (%)
Test status* Uveitis (n=49) Healthy (n=49)
Seropositive, IgG C >1 7 (14.3) 0 (0)
Seropositive, IgG C <1, IgM C >1 2 (4.1) 0 (0)
Seropositive, IgG and IgM C <1 10 (20.4) 0 (0)
Seropositive, any C >1 9 (18.4) 0 (0)
Total seropositive, aqueous antibody positive 19 (38.8) 0 (0)
Total seropositive, aqueous AB negative 16 (32.7) 35 (71.4)
Total seronegative, aqueous AB negative 10 (20.4) 14 (28.6)
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*

Bartonella-specific IgA was not detected in the aqueous humour of any cat.

Bartonella henselae was detected by PCR in aqueous humour from three of 24 cats with uveitis and one of 49 healthy shelter cats; there was no significant difference in the rate of detection among the two groups (Table 3). All four PCR-positive cats were seropositive for Bartonella spp antibodies but three had Bartonella spp C value <1.

Table 3.

Bartonella henselae in aqueous humour of cats

Test status
PCR Serum AB C value Cats with uveitis Normal shelter cats Total
+ + >1 1 0 1
+ + <1 2 1 3
+ – <1 0 0 0
– + >1 4 0 4
– + <1 13 34 47
– – <1 4 14 18
Total tested 24 49 73
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Seropositive=Bartonella spp IgM, IgG, or IgA antibodies in serum; Bartonella C value=any combination of IgM or IgG results.

Experimentally inoculated cats

All nine cats were PCR-positive in whole blood for Bartonella spp; four cats were positive by culture of lysed whole blood. The nine PCR-positive cats were Bartonella spp IgG seropositive but negative for IgA and IgM. Bartonella spp IgM or IgA were not detected in the aqueous humour of any experimentally inoculated cat. Bartonella spp IgG C values >1 were detected in aqueous humour from both eyes of four of nine (44.4%) experimentally inoculated cats (Table 4). Each of these cats had received intradermal inoculations of B henselae skin test antigen 1 week prior to sampling, as a component of another study (Kordick et al 1999). One experimentally inoculated cat had perilenticular vitreal degeneration noted on ophthalmoscopic examination on post-inoculation day 191; the cat had been febrile and disoriented several weeks earlier. Anterior or posterior segment cataracts were detected ophthalmoscopically in four cats. Although detection of cataracts did not uniformly correlate with Bartonella spp C value >1 (two of four cats), Bartonella spp DNA was detected in aqueous humour from three of four cats with cataracts. Of the four experimentally inoculated cats with Bartonella spp IgG C value >1, three were concurrently positive for Bartonella spp in whole blood by culture, whereas one blood culture positive cat did not have local antibody production in aqueous humour.

Table 4.

Bartonella spp antibody and DNA in aqueous humour of experimentally inoculated cats

Bartonella IgG C value Aqueous humour PCR*
Cat OS OD OS OD Whole blood culture Whole blood PCR Ophthalmic examination
1 Negative Negative Negative Negative B clarridgeiae B clarridgeiae Normal
2 59.7 53.1 Negative Negative B henselae B henselae Normal
3** 424.8 389.6 Positive Negative B henselae B henselae Sutural cataract
4 Negative Negative Negative Negative Negative B henselae Normal
5 Negative Negative Positive Negative Negative B henselae Sutural cataract
6 1.5 22.2 Positive Negative Negative B henselae Normal
7 Negative Negative Negative Negative Negative B henselae Posterior cortical cataract
8*** Negative Negative Positive Positive Negative B henselae Anterior/posterior cortical cataract
9 36.4 45.8 Negative Negative B henselae B henselae Normal
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Cats 1 and 3–8 were challenged with B henselae or B clarridgeiae on day 370; cats 2 and 9 were not challenged. Samples were collected on day 454 after primary inoculation.

*

Aqueous humour PCR performed at the Heska Corporation using 16S/23S intergenic spacer region primers; whole blood PCR performed at NCSU using 16S primers.

**

Mild perilenticular vitreal degeneration detected at day 191 PI (15 weeks after defervesence (Tmax 40.3) and central nervous system signs).

***

Non-localising central nervous system signs.

Bartonella spp DNA was detected by PCR in aqueous humour from one or both eyes of four experimentally inoculated cats, of which only one cat was concurrently blood culture positive (Table 4). Of these four aqueous humour PCR-positive cats, two had Bartonella spp IgG C values >1 and two had Bartonella spp IgG C values <1. All four aqueous humour PCR-positive cats had been challenged 84 days prior to sample collection; however, three aqueous humour PCR-negative cats received an identical challenge.

Discussion

Detection of local production of antibodies by the eyes of people and cats has been used as indirect evidence of ocular infection by a number of infectious agents including T gondii (Turunen et al 1983, Lappin et al 1992) and herpesviruses (Yamamoto et al 1996, Maggs et al 1999). Local production of Bartonella spp antibodies in cerebrospinal fluid has been used to aid the diagnosis of bartonellosis in people with central nervous system disease (Schwartzman et al 1994) and in a cat with uveitis (Lappin & Black 1999). Antibody in the aqueous humour can also result from serum leakage due to breakdown of the blood–ocular barrier. Aqueous humour antibody coefficients (C values) compare the serum to aqueous humour ratio of specific antibodies to the aqueous humour to serum ratio of a reference protein not usually produced by the eye; total IgG or IgG against a non-ocular pathogen are commonly used. A C value >1 suggests that the specific antibody detected in aqueous humour is present in a concentration too great to be explained by serum leakage into the eye. Detection of intra-ocular antibody production does not definitively prove ocular infection and it is possible that Bartonella-sensitised lymphocytes migrate to the eye from distant sites. However, simultaneous detection of both intra-ocular antibody production and Bartonella spp DNA in several cats in this study supports the hypothesis that Bartonella spp can invade the eyes during the course of infection. Although detection of DNA does not confirm the presence of viable Bartonella organisms, concurrent production of antibody suggests that invasion and replication within intra-ocular tissues is likely.

Bartonella spp IgG C value >1 occurred in cats with and without clinically apparent uveitis. Thus, positive results using this assay do not prove that ocular disease is due to bartonellosis. Toxoplasma gondii IgG C value >1 can be detected for at least 4 months after primary inoculation and can recur following challenge inoculation in cats without uveitis (Chavkin et al 1994). The detection of Bartonella spp IgG C values >1 in two of the experimentally inoculated cats (cats 3 and 6) may have been from the challenge inoculation 12 weeks earlier; however, two other cats (cats 2 and 9) with IgG C values >1 were not challenged, suggesting that the findings were from the primary inoculation. Alternately, all four experimentally inoculated cats in this study with Bartonella spp C values >1 had received killed B henselae antigen intradermally 1 week before sampling which may have enhanced the ocular immune responses. Some cats with chronic toxoplasmosis can be induced to have T gondii IgG C value >1 by SQ inoculation of killed tachyzoites (Lappin et al 1996b). Based on the results of that study, it appears likely that once ocular infections occur, antigen-sensitised lymphocytes remain and can be induced to produce antibodies at a later date.

Bartonella spp IgM C values >1 were only detected in cats with uveitis and Bartonella spp IgM and IgA antibodies were detected in serum of a greater number of cats with uveitis than in healthy shelter cats. Toxoplasma gondii IgM C values >1 have been detected in many cats with uveitis (Lappin et al 1992) but not in experimentally inoculated cats (Chavkin et al 1994) and serum IgM antibodies are detected more frequently in cats with uveitis than healthy cats (Chavkin et al 1992). Perhaps the IgM antibody class is superior to IgG as a marker of recent infection or disease in cats.

Of the eight PCR-positive aqueous humour samples in this study, only three were from cats with clinically apparent uveitis. Thus, detection of the organism in aqueous humour cannot be used alone to document definitively ocular bartonellosis. Toxoplasma gondii can be detected in aqueous humour of healthy cats by PCR following primary and secondary inoculation (Burney et al 1998). As pre-challenge aqueous humour was not available in this study, it cannot be determined whether the positive PCR results in experimentally inoculated cats resulted from persistent primary infection or challenge infection. However, positive aqueous humour PCR results were obtained only from cats that had been challenged 84 days previously.

When the results from three groups of cats were combined, three of nine cats with Bartonella C values >1 were aqueous humour PCR-positive. It is possible that the antibody response cleared the organism from aqueous humour or suppressed infection below the level of detectability in the six PCR-negative cats. Alternately, the organism may have only been present in tissue or the volume of aqueous humour tested was too small. Bartonella spp DNA was detected in aqueous humour of five seropositive cats with Bartonella spp C values <1. These aqueous humour PCR-positive, seropositive, but aqueous humour antibody-negative cats may have had peracute infection. Alternately, administration of topical or systemic glucocorticoids may have lessened Bartonella spp antibody production in the cats with uveitis; further clinical history from these cats is unavailable. Administration of methylprednisolone acetate 91 days before sample collection may have resulted in failure to detect Bartonella spp antibodies in the aqueous humour of two PCR-positive experimentally inoculated cats.

It is also possible that seropositive, aqueous humour PCR-positive cats with Bartonella C values <1 had contamination of aqueous humour by B henselae during aqueous paracentesis. Since B henselae parasitises red blood cells, minimal blood contamination of aqueous humour during aqueous paracentesis could result in positive PCR results (Kordick & Breitschwerdt 1995). Cats with uveitis commonly have hyphaema, and given that large numbers of cats in the USA have Bartonella spp bacteraemia, positive PCR results from blood contamination from ocular paracentesis or uveitis will presumably occur. However, since all cats in the experimental cat group were PCR positive in whole blood but four cats were aqueous humour PCR-negative, confounding blood contamination does not always occur during ocular paracentesis.

While uveitis was not documented histologically in the experimentally inoculated cats in this study, anterior or posterior cataracts were detected in some cats. Nutritional or congenital cataracts have not been observed previously in this line of SPF cats, therefore it is possible that cataract formation was potentially related to infection with Bartonella spp. The results of this study support those of others which suggest that Bartonella spp may induce chronic insidious disease manifestations in cats (Ueno et al 1996, Glaus et al 1997, Guptill et al 1997, Kordick & Breitschwerdt 1997). Potentially, co-infection with feline immunodeficiency virus, T gondii or other pathogens is required to induce pronounced disease manifestations. Alternatively, as B henselae has more than one subtype, it is plausible that cats developing ocular inflammation may be infected by pathogenic strains (Matar et al 1993, Bergmans et al 1996) as was recently suggested for T gondii (Glasner et al 1992).

Acknowledgements

Supported by grants from the HESKA Corporation, Fort Collins CO, Pfizer Animal Health, Exton PA, and Bayer AG/Institute of Biology, Leverkusen, Germany. The authors thank Dr Michael Davidson for performing the opthalmoscopic examinations on experimentally inoculated cats and Drs Frank Geoly and Talmage Brown for performing histopathological examination of ocular tissues.

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