Praca oryginalna Original paper
Bartonellosis is a disease caused by the Bartonella spp. bacteria. These are small pleomorphic, gram-negative, intracellular bacilli that belong to the order of Rickettsiales (17). This disease is a zoonosis. The etiologic agents of bartonellosis in cats are B.
hense-lae, B. clarridgeiae and B. koehlerae, with the disease
being most frequently caused by B. henseale in cats in Europe. There are at least two genotypes of B.
hense-lae: Houston-1 and Marseille. The Houston-1 genotype
is common in Asia, whereas the Marseille one occurs mainly in Europe, the United States and Australia (9). Infections caused by these microbes are most com-monly reported in cats under one year of age living in large groups (e.g. shelters).
The main vectors of bartonellosis are external para-sites, such as fleas and ticks (24). After penetrating into the body, the bacteria adhere to epithelial cells, includ-ing vascular endothelium, and proliferate inside them in phagosomes. They also attack bone marrow pro-genitor cells (25). B. henselae forms large aggregates, which bind to the cell surface and are absorbed, thereby creating a vacuole inside, called an ‘invasome’. During divisions, the bacteria release proinflammatory factors, growth factors and apoptosis inhibitors. This activity may result in the proliferation of the host’s cells and
the formation of tumorous structures in the vascular endothelium. Then, the bacteria are released into the blood, where they attack erythrocytes. In the course of the disease, bacteraemia may persist for weeks or even years (17). In cats, the first signs of bartonellosis are fever and enlarged lymph nodes (19, 26). Additionally, fertility disorders may occur, and endocarditis as well as myocarditis may develop (5, 30). It is presumed that infections with these microorganisms may be respon-sible for the development of various feline pathological conditions that were earlier considered as idiopathic, such as inflammations of the lower respiratory tract (12, 29), pancreatitis (4), choroiditis (12, 13), gingivitis (6, 16, 29) and rhinosinusitis (7).
Since data on the occurrence and course of bartonel-losis in cats in Poland are rather scant, the aim of the study was to analyse the clinical course of bartonellosis in 24 cats with Bartonella henselae infection confirmed by molecular tests.
Material and methods
Animals used in the study. The study included a group
of 24 cats numbered 001-024 (10 males and 14 females aged from 4 months to 17 years) from eastern Poland in which bartonellosis was confirmed by molecular tests. All
Clinical course of bartonellosis in 24 cats
ŁUKASZ MAZUREK1, OLIWIER TEODOROWSKI2, PIOTR DĘBIAK3, KLAUDIUSZ
SZCZEPANIAK4, ANNA WILCZYŃSKA1, STANISŁAW WINIARCZYK1, ŁUKASZ ADASZEK1
1Department of Epizootiology and Clinic of Infectious Diseases, Faculty of Veterinary Medicine, University of Life Sciences, Głęboka 30, 20-612 Lublin, Poland
2Veterinary Clinic „Teodorowscy”, Żwirki i Wigury 5, 43-190 Mikołów, Poland
3Department and Clinic of Animal Surgery, Laboratory of Radiology and Ultrasonography, Faculty of Veterinary Medicine, University of Life Sciences, Głęboka 30, 20-612 Lublin, Poland
4Sub-Department of Parasitology and Invasive Diseases, Faculty of Veterinary Medicine, University of Life Sciences, Akademicka 13, 20-950 Lublin, Poland
Received 02.11.2020 Accepted 03.01.2021
Mazurek Ł., Teodorowski O., Dębiak P., Szczepaniak K., Wilczyńska A., Winiarczyk S., Adaszek Ł.
Clinical course of bartonellosis in 24 cats Summary
The aim of this study was to analyse clinical cases of bartonellosis. Medical records of cats naturally infected with Bartonella henselae were retrospectively evaluated with regard to clinical signs and laboratory abnormalities at the time of presentation, therapy and course of disease. The most common clinical abnormalities in B. henselae-positive cats included in the study were flea allergic dermatitis (29.5%), fever (25%) and diarrhoea (12.5%). Thrombocytopenia was the most common laboratory abnormality (50%).The results of the study indicate that B. henselae infection must be considered in differential diagnosis in patients with thrombocytopenia and flea invasion.
cats were fed with commercial food. The animals were reported to the Clinic of Infectious Diseases with various problems. The feature shared by all animals was the pres-ence of fleas and/or ticks found on the body by the owners or veterinarians.
All animals were subjected to a routine clinical exami-nation. Blood for haematological tests, molecular tests for bartonellosis, erlichiosis/anaplasmosis, and speed tests for feline leukaemia virus (FeLV), feline immunodeficiency virus (FIV) and feline coronavirus infection was obtained from the sick animals.
Blood analysis. Blood for haematological tests was
placed in 3 ml test tubes with ethylenediamine tetra-acetic acid (EDTA), shaken and tested (about 300 µl) in an Exigo (Boule) analyser.
The blood for biochemical tests was collected into clot-ting accelerator tubes. Serum biochemical tests (the assess-ment of urea concentration, creatinine concentration, ALT, AST and ALP activity) were carried out with a BS 120 Mindray analyser.
Tests for FeLV, FIV and feline coronavirus infection were performed according to the manufacturer’s instruc-tions (Vetexpert Poland).
Molecular tests. DNA extraction for molecular tests
was performed using a DNA Blood kit (A&A Biotechnol-ogy Gdańsk, Poland). Extracted DNA was subjected to PCR for Bartonella and Ehrlichia/Anaplasma. PCR for Bartonella was performed with primers targeting frag-ments of the citrate synthase gene: one generic forward primer (BART- LC-GEN-F: 5’-ATGGGTTTTGGTCATC-GAGT-3’), one species-specific reverse B. henselae, primer (BART-LC-HEN-R: 5’-AA ATCGACATTAGGGTA-AAGTTTTT-3’) and one species-specific reverse B. clar-ridgeiae primer (BART-LC-CLA-R: 5’-CAAGAAGTG-GATCATCTTGG-3’), according to a method described by Staggemeter et al. (28), that is, an initial denaturation of 2 min at 95°C, followed by 37 cycles consisting of dena-turation at 96°C for 60 s, annealing at 55°C for 60 s and elongation at 72°C for 90 s. Reaction mixture (50 µL) con-tained 100 µM of each dNTP, 1.6 mM of MgCl2, 0.25 µM of each primer, 2.5 U of Taq DNA polymerase and 5 µL of DNA template. The negative control consisted of distilled water, and the positive control was DNA extracted in the previous study (24).
The size of each PCR product was analysed by electro-phoresis in a 1.5% agarose gel stained with ethidium bro-mide. PCR products were purified using QIA quick spin columns (Qiagen) and eluted in 50 µl of Tris 10 mM, pH 7.6. The DNA sequence was determined on both strands using the primers employed earlier for PCR at a DNA sequenc-ing core facility (Institute of Biochemistry and Biophys-ics, Polish Academy of Sciences, Warsaw, Poland). DNA sequences were assembled and edited using SeqMan (DNA-star, Lasergene, Madison, USA) and ClustalV alignments. PCR for Ehrlichia/Anaplasma was performed according to a method described by Adaszek et al. (1) with the prim-ers EHR 521 (5’-TGT AGG CGG TTC GGT AAG TTA AAG-3’) and EHR 747 (5’-GCA CTC ATC GTT TAC AGC GTG-3’), which made it possible to amplify the 16S rRNA gene fragment of Anaplasma/Ehrlichia spp. with
a size of 247 bp. For use as the positive control, the DNA of A. phagocytophilum was obtained from the National Reference Center for Borrelia of the Max von Pettenkofer Institute. Pure water was used as the negative control.
Skin scraping examination. Animals in which a
clini-cal examination showed skin lesions (alopecia, abrasion or skin area bitten off) accompanied with itching had a skin scraping collected from affected areas to confirm or exclude ectoparasite infestation. The material was collected from the edges of skin lesions observed in the clinical examination, covered with 10% KOH and then viewed in a light micro-scope under magnification (40 ×).
Parasitological examination of faeces. In animals with
diarrhoea signs, a parasitological examination of faeces was performed by direct smear methods, flotation with saturated NaCl solution and sucrose, Baermann technique and com-mercial immunochromatographic assays (R-Biopharm AG, Darmstadt, Germany) for detection of the copro-antigens of protozoa of the Cryptosporidium, Giardia and Entamoeba genera.
Imaging (chest x-ray and abdominal ultrasound).
Animals with dyspnoea signs were subjected to a chest X-ray. The examination was performed with Zoomax HF in a system of direct digital radiography. Patients were examined in two views: dorsal-abdominal and lateral in the right-side position. The radiographs were evaluated using the DICOM PACS DXR software. Pulmonary aeration, mediastinal area (tracheal width and heart size) and possible lesions in the pleural cavity or thoracic wall were assessed.
The abdominal ultrasound examination of cats with gastrointestinal signs was performed with EsaoteMyLab twice, using a 10-13 MHz linear transducer and a 6-9 MHz microconvex.
Echocardiography. In cats with dyspnoea and exercise
intolerance which had a heart enlargement on X-ray, addi-tional echocardiography was performed. The echocardiog-raphy was performed on the subject in a standing position with an ESAOTE MyLab Class C (with probe Esaote Phased PA112) device. The heart structure and function were assessed. Various imaging procedures were used, includ-ing two-dimensional imaginclud-ing (2D), M-mode procedure and Doppler technique. Two-dimensional imaging covered long and short axes views from the right parasternal acoustic window and the left parasternal acoustic window. These views made it possible to quantitatively evaluate the heart cavities and the heart’s systolic function, as well as to deter-mine the proportion of the left atrium to the left aorta (LA/ Ao). M-mode echocardiography assessed the size of the left ventricle lumen, the thickness of the interventricular septum and the free wall of the left ventricle in the end-diastolic and end-systolic phases. Doppler echocardiography evaluated laminar and possible turbulent blood flow through the aorta valves, the pulmonary valve and the bicuspid and tricuspid aortic valves. A quantitative evaluation of the speed and volume of the blood flow was also performed.
Statistical analysis. Statistical analyses were performed
with the SPSS v15.0 software (SPSS Inc., Chicago, IL, USA). Descriptive statistical methods were used to calculate minimum, maximum, median, mean and standard deviation values for haematological and biochemical parameters.
Results and discussion
Clinical examination results. A general
deteriora-tion in the condideteriora-tion of all cats taking part in the clini-cal trial was observed. Internal body temperature was increased by 0.5-1°C in three cats and by more than 1°C in two cats. The heart rate was increased by 20% in two cats and by 50% in further two cats, in which subsequent echocardiography revealed myocardial in-sufficiency due to hypertrophic cardiomyopathy. Based on the clinical course of the disease, six groups were distinguished. Group I consisted of seven cats (001, 008, 0012, 015, 013, 016, 020) in which only fever was observed. Group II comprised three cats (010, 021, 022) with signs of chronic diarrhoea. In group III, there were seven cats (003, 004, 005, 006, 007, 014, 017,) with signs of flea allergy dermatitis (FAD). Group IV consisted of four cats (011, 013, 018, 019) with signs of dyspnoea. Group V was composed of three cats (002, 009, 023) with confirmed feline leuke-mia and immunodeficiency viral infections. In Group VI, there was only one cat (024), which did not show any clinical signs, but whose owners were diagnosed with cat scratch disease (the disease developed after the cat scratched the owner).
Haematological examination showed mild leukocy-tosis in six cats (001, 008, 012, 014, 016, 02), anaemia in three animals (002, 005, 009) and thrombocytopenia in 12 cats (003, 004, 005, 006, 008, 010, 012, 013, 015, 016, 020, 024). Serum biochemical tests showed an increase in AST activity in seven animals (002, 005, 006, 009, 0021, 022, 023), in ALT in five cats (005, 006, 021, 022, 023) and in ALP in five animals (002, 007, 010, 015, 023). Serum urea concentration was elevated in six cats (002, 007, 008, 011,
019, 021) and creatinine in five (002, 008, 011, 019, 021).
The results of haematologi-cal and biochemihaematologi-cal tests are summarized in Tables 1 and 2.
Results of parasitologi-cal examination and skin scrapings. The parasitological
examination of faeces, both microscopic and with the use of rapid immunochromato-graphic tests, showed no pres-ence of adult parasite forms, their eggs or antigens in any of the animals with signs of diar-rhoea (n = 3) in their faeces. All of these animals also tested normal for pancreas-specific lipase. Microscopic examina-tion of skin scrapings collected from seven cats with FAD signs (group III) showed no presence of external parasites
(Sarcoptes scabiei, Demodex) in this material, and skin mycoses were excluded. However, the presence of flea faeces was found in all samples.
Imaging test results. The X-ray imaging
exami-nation in cats with respiratory problems (011, 013, 018, 019) showed moderately disseminated, irregular, poorly delimited areas of peribronchial and pulmonary tissue densities, which were the cause of decreased lung aeration. On the other hand, in all animals with diarrhoea (010, 021, 022), the abdominal ultrasound examination showed the thickening of the small intestine wall, increased mucosal echogenicity and hyperechoic mucosal bands.
Echocardiography results. In two cats with
dys-pnoea signs (011 and 019), echocardiography revealed concentric left ventricular hypertrophy, significantly reducing the left ventricular lumen in diastole (HCM).
Molecular test results. The presence of Bartonella
genetic material was shown by the PCR technique in blood samples from all cats. The amplified product was 250 bp. The sequences of the gene amplicons showed 99-100% similarity with B. henselae sequences ob-tained in earlier tests (3).
No Anaplasma or Ehrlichia genetic material was found in the blood of any cat.
Efficacy of treatment. The treatment of all cats
started with amoxicillin with clavulanic acid (12.5 mg/ kg bw P.O. for seven days once a day) and meloxicam (0.05 mg/kg bw for three days) in syrup. As a result of the therapy, recovery was observed in 21 out of 24 cats in which bartonellosis was confirmed by PCR. Three animals (002, 009, 023) were euthanised due to poor clinical condition (all of them belonged to group V,
Tab. 1. Results of haematological examination in cats (n = 24)
Parameter Reference range Mean deviationStandard
Number of animals with an elevated value
of the parameter a decreased value of the parameter
WBC (109/l) 5.5-19.5 0.45 13-93 6 5 LYM (109/l) 1.8-7.0 0.375 2-25 0 9 GRAN (109/l) 2.8-13.0 0.5 14-18 6 6 RBC (1012/l) 5.0-11.0 0.167 2-44 1 3 HCT (%) 25.0-45.0 0.25 0-08 2 4 HGB (g/dl) 8.0-15.0 0.46 2-03 8 3 PLT (109/l) 200.0-500.0 0.54 80-20 1 12
Tab. 2. Results of biochemical examination (n = 24)
Parameter Reference range Mean deviationStandard
Number of animals with an elevated value
of the parameter a decreased value of the parameter
ALT (u/l) 20.00-107.00 0.20 72-4 0 5
AST (u/l) 6.00-44.00 0.29 36-1 0 7
CREA (mg/dl) 1.00-1.80 0.33 55-4 3 5
UREA (mg/dl) 25.00-70.00 0.25 5-5 0 6
in which bartonellosis was accompanied by FeLV or FIV infections).
In patients with cardiological signs (HCM), amlodip-ine (0.25 mg/kg P.O./once a day) was additionally ad-ministered, as a result of which their general condition stabilized and echocardiography showed an increase of the left ventricular lumen in diastole.
This article describes the clinical course of bartonel-losis in the feline population in Poland. The disease is rarely diagnosed in this species in our country, and data on its clinical signs is incomplete (23).
In general, the first signs of bartonellosis are fever and enlarged lymph nodes (26). As the disease ad-vances, fertility disorders may occur, and endocarditis as well as myocarditis may develop. The bacterial DNA was isolated from the blood, inflammatory lesions of the wrist and metacarpal bones and from the heart (7, 30). It is presumed that infections with Bartonella spp. in cats may be responsible for the development of various pathological conditions that were earlier considered in research.
Most infected cats show no abnormalities in haema-tological or biochemical blood tests (15). Our research also showed that the deviations from the physiologi-cal norm in haematologiphysiologi-cal and biochemiphysiologi-cal serum parameters in sick animals were not very specific. The most common abnormality found in haematological ex-amination was thrombocytopaenia, which occurred in 12 animals and is also described by other authors (12). Anaemia, which occurs in some cats with Bartonella infections (20), developed in only three individuals in our study.
As already mentioned, fever is considered to be the first and permanent sign of feline bartonellosis, although in our study it was found in only six animals (25%) in group I. Lappin et al. (21) conducted a study on 81 cats with fever and 81 cats without fever. After excluding that the temperature increase in the group of animals with fever was induced by stress or envi-ronmental factors, all animals were tested by PCR for infectious agents. The DNA of Bartonella spp. was detected in 17.3% of cats with fever and in only 7.4% of cats without fever. The results of Bradbury et al. (10) also confirm that Bartonella can induce fever in cats. These authors exposed cats to fleas infected with
B. henselae rickettsia, which resulted in the
develop-ment of high, long-lasting fever in 50% of animals used in the experiment.
Besides fever, the most common abnormality re-corded in the course of bartonellosis in cats in our study was flea allergy dermatitis, which occurred in 29.5% of the animals (cats in group III). This is not surprising, because the main vector of Bartonella in cats are fleas (23). Similar skin reactions to the presence of fleas in cats with bartonellosis are also reported by other au-thors (7, 16). It should be noted that in all animals of this group the presence of flea faeces was revealed by microscopic examination of skin scrapings.
In groups II and IV, the dominant signs were diar-rhoea and dyspnoea, respectively. These disorders were probably caused by the formation of inflammatory foci in the gastrointestinal tract (intestines) and in the lungs, the presence of which was confirmed by imag-ing. Such foci, due to bartonellosis, are often found by histopathological examination in dead animals in the peripheral lymph nodes, spleen, liver, heart and kidneys. Focal hyperplasia in the lymph nodes and spleen may indicate an unspecific tissue response to chronic antigen stimulation (10). Additionally, in two cats from group IV, cardiological abnormalities were found: concentric left ventricular hypertrophy (HCM). Hypertrophic cardiomyopathy and endocarditis are severe complications of bartonellosis, which may cause death in affected animals. The first reports of cardiac disorders induced by Bartonella spp. infection in cats come from Australia. These microbes were isolated from the aortic valve of sick individuals, although no direct link between the disease and the infection was demonstrated in the described cases (2, 22). Several years later, a cat from California was diagnosed with endocarditis with B. henselae (13). Its clinical exami-nation and auscultation revealed loud heart murmurs and cardiac arrhythmias, while X-rays showed a sig-nificant enlargement of the heart. Echocardiography showed hypertrophic cardiomyopathy, as in patients in our study, a significant enlargement of the left atrium and significant thickening of the aortic valve cusps. It should also be noted that cardiac disorders are a com-mon complication of bartonellosis in humans (11).
The zoonotic potential of this unit is demonstrated by the case of the cat from group VI, which did not show clinical signs of bartonellosis, yet the disease developed in its owner, who had been scratched by the animal.
B. henselae in humans causes a purulent reaction.
Microbes cause the development of various disor-ders in infected individuals, including multifocal angioproliferative lesions, optic nerve inflammation, haemorrhages in the liver and spleen, and sometimes endocarditis. In children, infections with B. henselae can lead to encephalopathy. Some studies suggest that CSD is related to breast cancer in women (3, 8, 27). All forms of bartonellosis may be accompanied by general signs, such as fever, feeling unwell, headaches and weight loss. Around 10% of patients develop unusual signs, such as Parinaud’s syndrome manifested by visual disturbances, atypical pneumonia, arthralgia, osteomyelitis, abdominal pain and loss of appetite (14).
In all animals in our study, the infections were con-firmed by molecular studies. Currently, the diagnosis of bartonellosis is based on serological tests and PCR-based tests. Commercial serological tests are available only for some species, such as B. henselae, B. quintana and B. vinsonii subsp. berkhoffii, but these tests do not show 100% specificity, and their result depends on the time elapsed since the infection (9, 24).
Amoxicillin with clavulanic acid was used in the treatment of sick animals to good effect. The most common chemotherapeutics used in dogs and cats to treat bartonellosis alongside amoxicillin are ampicillin, gentamicin, doxycycline and azithromycin. It should be noted that B. henselae has been described as resistant to azithromycin and fluoroquinolones (20).
The description of the present cases indicates that
B. henselae infection must be considered in
differen-tial diagnoses in cats living in Poland, especially in individuals with thrombocytopenia and flea invasions.
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Corresponding author: Łukasz Mazurek, DVM, Department of Epi- zootiology and Clinic of Infectious Diseases, University of Life Sciences, Głęboka 30, 20-612 Lublin, Poland; e-mail: lukaszmazurek92@gmail.com
