leptospirosis in cats current literature review to guide diagnosis and management

Leptospirosis in cats: Current literature review to guide diagnosis and management

Affiliations.

1 Departament de Medicina i Cirurgia Animals, Facultat de Veterinària, Universitat Autònoma de Barcelona, 08193 Bellaterra, Cerdanyola del Vallès, Barcelona, Spain.
2 OIE and National Collaborating Centre for Reference and Research on Leptospirosis (NRL), Amsterdam UMC, University of Amsterdam, Medical Microbiology, Meibergdreef 39, 1105 AZ, Amsterdam, Netherlands.
PMID: 32093581
DOI: 10.1177/1098612X20903601

Practical relevance: Literature on the clinical presentation of leptospirosis in cats is scarce, although it has been demonstrated that cats are susceptible to infection and are capable of developing antibodies. The prevalence of antileptospiral antibodies in cats varies from 4% to 33.3% depending on the geographical location. Urinary shedding of leptospires in naturally infected cats has been reported, with a prevalence of up to 68%. Infection in cats has been associated with the consumption of infected prey, especially rodents. Thus, outdoor cats have a higher risk of becoming infected.

Clinical challenges: Clinical presentation of this disease in cats is rare and it is not known what role cats have in the transmission of leptospirosis. Ongoing work is needed to characterise feline leptospirosis.

Audience: This review is aimed at all veterinarians, both general practitioners who deal with cats on a daily basis in private practice, as well as feline practitioners, since both groups face the challenge of diagnosing and treating infectious and zoonotic diseases.

Evidence base: The current literature on leptospirosis in cats is reviewed. To date, few case reports have been published in the field, and information has mostly been extrapolated from infections in people and dogs. This review is expected to serve as a guide for the diagnosis and management of the disease in cats.

Keywords: Leptospirosis; microscopic agglutination test; real-time PCR; zoonosis.

Publication types

Cat Diseases / diagnosis*
Cat Diseases / therapy*
Leptospirosis / diagnosis
Leptospirosis / therapy
Leptospirosis / veterinary*

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Murillo Picco A | 0000-0002-7630-6116
Pastor J | 0000-0003-1702-9531

Journal of Feline Medicine and Surgery , 01 Mar 2020 , 22(3): 216-228 https://doi.org/10.1177/1098612x20903601 PMID: 32093581

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Leptospirosis in cats: Current literature review to guide diagnosis and management

2020, Journal of Feline Medicine and Surgery

Global importance: Leptospirosis is the most widespread zoonosis worldwide. Mammals (eg, rats, horses, cows, pigs, dogs, cats and aquatic species, such as sea lions and northern elephant seals) can all be infected by leptospires. Infection in animals occurs through contact with urine or water contaminated with the bacteria. In people, the disease is acquired mainly from animal sources or through recreational activities in contaminated water. Practical relevance: Literature on the clinical presentation of leptospirosis in cats is scarce, although it has been demonstrated that cats are susceptible to infection and are capable of developing antibodies. The prevalence of antileptospiral antibodies in cats varies from 4% to 33.3% depending on the geographical location. Urinary shedding of leptospires in naturally infected cats has been reported, with a prevalence of up to 68%. Infection in cats has been associated with the consumption of infected prey, especially rodents. Thus, outdoor c...

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Molecular and serological epidemiology of Leptospira infection in cats in Okinawa Island, Japan

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Bacterial infection
Infectious-disease epidemiology

Leptospirosis is a zoonosis caused by pathogenic Leptospira spp. Cats have been reported to be infected with Leptospira spp. and shed the bacteria in the urine. However, the importance of cats as an infection source for humans remains unclear. In this study, Leptospira infection in cats in Okinawa Prefecture, Japan, where leptospirosis is endemic, was investigated by leptospiral antibody and DNA detection using microscopic agglutination test and nested PCR, respectively. Moreover, multilocus sequence typing (MLST) and whole genome sequencing (WGS) were conducted on the Leptospira borgpetersenii serogroup Javanica isolated from cats, black rats, a mongoose, and humans. Anti- Leptospira antibodies were detected in 16.6% (40/241) of the cats tested, and the predominant reactive serogroup was Javanica. The leptospiral flaB gene was detected in 7.1% (3/42) of cat urine samples, and their sequences were identical and identified as L. borgpetersenii . MLST and WGS revealed the genetic relatedness of L. borgpetersenii serogroup Javanica isolates. This study indicated that most seropositive cats had antibodies against the serogroup Javanica and that cats excreted L. borgpetersenii in the urine after infection. Further, genetic relatedness between cat and human isolates suggests that cats may be a maintenance host for L. borgpetersenii serogroup Javanica and a source for human infection.

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Introduction

Leptospirosis is a zoonotic disease caused by infection with pathogenic spirochetes of the genus Leptospira , composed of 64 species divided into 24 serogroups and more than 300 serovars 1 , 2 , 3 , 4 . Leptospira spp. colonize the proximal renal tubules of maintenance hosts, including wild animals such as rats and boars, livestock such as cattle and pigs, and companion animals such as dogs, and are shed in their urine 2 , 5 , 6 . Humans are infected percutaneously or permucosally with Leptospira spp. by direct contact with the urine of maintenance hosts or by indirect contact with soil or water contaminated with infected urine 3 , 6 , 7 .

Cats have not been considered an important source of Leptospira infection for humans. Besides antibody detection, however, several recent studies from various regions reported that Leptospira spp. were isolated or leptospiral DNAs were detected from cat urine or kidney samples 8 , 9 , 10 , 11 , 12 , 13 , 14 , 15 , 16 , 17 , 18 , 19 , 20 , 21 ; carriage rate was related to some factors such as rearing style (cat external behavior), climate, and living environment (urban or rural) 15 , 20 . Moreover, leptospiral DNA was continuously detected in the urine of naturally infected cats for 8 months 20 . Although symptomatic cases with polyuria, polydipsia, hematuria, ascites, and diarrhea have been reported, the clinical presentation of leptospirosis in cats is rare, usually mild, or subclinical, and symptoms in feline leptospirosis remain undefined 9 , 13 , 14 , 17 , 20 , 22 . These studies suggest that cats can carry and shed pathogenic Leptospira in urine for a long period after infection. Asymptomatic or uncertain symptoms of infected cats make the diagnosis and appropriate treatment difficult and prevent infected cats from becoming a chronic carrier, resulting in a potential infection source for humans.

Cats are the most common companion animal in Japan. According to a survey conducted by the Japan Pet Food Association, the number of cats has been increasing year by year, and the number of cats raised in Japan is estimated to be 9,778,000 in 2019, higher than that of dogs 23 . Canine leptospirosis and its causative Leptospira spp. have been recently reported 24 , 25 , but the current status of Leptospira infection in cats in Japan remains limited. In the southern Kyushu District, the prevalence of anti- Leptospira antibodies in domestic cats was reported to be 7.7% 26 . In Okinawa Prefecture, the southernmost part of Japan, where leptospirosis is endemic, it was reported 30 years ago that the seroprevalence and isolation rate of Leptospira spp. among cats ranged from 4.8 to 9.1% and 1.0% to 3.1%, respectively 27 , 28 . Although Leptospira spp. were isolated, molecular characterization of the isolates was not performed in these studies.

Understanding the Leptospira genotype-host association in maintenance hosts is important for elucidating and controlling the source for human infection. Currently, molecular typing methods, such as multilocus sequence typing (MLST) and multilocus variable-number tandem repeat analysis (MLVA), are the main methods for characterizing Leptospira isolates 1 . As a genotyping method having higher resolution, whole genome sequencing (WGS) has been rapidly developed in recent years. These methods have enabled the understanding of host specificity of certain Leptospira genotypes as well as the geographic structuring of genetic diversity and host switching event in Leptospira spp 29 , 30 , 31 , 32 .

In this study, to clarify Leptospira infection and carriage in cats in Okinawa Island (Okinawa Main Island), anti-leptospiral antibodies in cats were investigated by the microscopic agglutination test (MAT) using 13 reference strains. Leptospiral DNA was detected from cat urine samples by nested PCR. Moreover, MLST and WGS were performed to gain further insights into the genetic relatedness of Leptospira isolates from cats, mongooses, rats, and humans.

Antibodies against Leptospira spp. were detected in 40 of 241 cats (16.6%) included in the analysis. Thirty-seven cats and one cat had antibodies against serogroups Javanica and Hebdomadis, respectively, and two samples were positive for multiple serogroups (Table 1 ). The reciprocal antibody titers for serogroup Javanica ranged from 160 to 2560 (Table 1 ). The antibody-positive samples in the northern, central, and southern regions of Okinawa Island were 15.0% (26/173), 22.0% (9/41), and 18.5% (5/27), respectively. Of the 40 anti-leptospiral antibody-positive cats, 23 were male (19.3%) and 17 were female (13.9%). There were no significant differences between seropositivity and capture area nor between seropositivity and sex. In contrast, the seropositivity varied among the age groups based on weight: 3% (1/33) in kittens, 12.1% (7/58) in juveniles, and 21.3% (32/150) in adults. There was a statistically significant difference in the seropositivity among the age groups ( p = 0.021), and a trend toward an increase in seropositivity with age was observed ( p = 0.006).

Leptospiral flaB was detected in 3 of 42 urine samples (7.1%, see Supplementary Fig. S1 online) included in the analysis. All three PCR-positive cats were also positive for antibody against serogroup Javanica with the titers of 320 (2 animals) and 640 (1 animal). All three flaB sequences were identical and identified as L. borgpetersenii (DDBJ accession numbers LC596932–LC596934). Amplification of all seven housekeeping genes for MLST was succeeded in two of the three flaB -positive urine samples (FU18017 and FU18027) and nine strains of L. borgpetersenii serogroup Javanica (Table 2 ). Their sequence types (STs) were all assigned as ST143 (Fig. 1 ). There were no gross abnormalities in the autopsy findings in the three cats.

MST of L. borgpetersenii detected from cat urine samples and L. borgpetersenii serogroup Javanica strains in this study and 182 L. borgpetersenii strains based on the allelic profiles of the MLST seven housekeeping genes. Each circle represents an individual ST, and the numbers represent ST numbers. Circle sizes correspond to the numbers of strains in each ST. The thickness and the dotting of lines indicate the distance between the circles: a thicker line indicates a closer distance than a thin line, and a thin line denotes a closer distance than a dotted line. The green-colored circle and the ST number in red represent L. borgpetersenii serogroup Javanica strains and DNAs determined in this study.

Of the six strains subjected to WGS, enough data for comparison were obtained from four strains, OHJ2008-88U, FK-118, 058031, and 078065. Strains isolated from a cat, a mongoose, and humans were clustered with L. borgpetersenii serogroup Javanica strains isolated from black rats in Okinawa Island sequenced in a previous study 30 (Fig. 2 ).

Core genome SNP-based maximum likelihood tree of L. borgpetersenii serogroup Javanica strains isolated in Japan. The strain Piyasena, belonging to serogroup Javanica serovar Ceylonica, was used as the reference, omitted from the tree. WGS of strains 058031, 078065, FK-118, and OHJ2008-88U was performed in this study, and strains named WFA have been analyzed in a previous study 30 . Black, human isolate; blue, black rat isolate; green, mongoose isolate; red, cat isolate.

Identification of prevalent serovar(s) and their maintenance host(s) and seroprevalence in the host(s) is important for understanding the epidemiology of leptospirosis in a particular geographic region 33 . In the Okinawa Island, which has a subtropical climate, Leptospira spp. have been isolated or detected from various animals such as rat, mouse, shrew, mongoose, wild boar, and dog 24 , 34 , 35 , 36 . The animals excrete the bacteria into the environment where Leptospira spp. can survive and remain infective for several weeks 7 . Humans can get infected with Leptospira spp. through contact with the contaminated environment during recreational activities in rivers and agricultural activities 37 . Therefore, the approach of “One Health” recognizing the interconnection between humans, animals, and their shared environment is important to elucidate the epidemiology of leptospirosis in this island. In this study, we demonstrated that free-roaming stray cats in Okinawa Island were predominantly infected with L. borgpetersenii serogroup Javanica and shed the bacterium in urine, suggesting a potential role of cats in transmitting leptospirosis to humans.

The prevalence of anti- Leptospira antibodies and the detection of leptospiral DNA among cats worldwide range from 4 to 33% and 0% to 67.8%, respectively 9 , 10 , 11 , 12 , 13 , 14 , 15 , 16 , 18 , 19 , 20 , 21 . In this study, the seropositivity was 16.6%, and more than 90% of the cat serum samples reacted with serogroup Javanica (Table 1 ). Pathogenic Leptospira DNA was detected in three cat urine samples (7.1%, 3/42). The seropositivity in this study was slightly higher than that in previous studies done in Okinawa Prefecture (mainly in the Okinawa Island) 30 years ago (4.8% and 9.1%), but reactive serogroups were much diverse in the previous studies 27 , 28 . Previous studies reported that Leptospira spp. were isolated from 1.0% and 3.1% of the cats tested, lower than the DNA detection in this study, but success in isolation is generally lower than that in DNA detection. The positive rate of anti-leptospiral antibodies and leptospiral DNA detection in cats could be affected by various factors, such as age, rearing styles, season, geographical region, presence of maintenance hosts, panel of serovars, and/or cutoff value used for MAT, sensitivity, and specificity of the primer (and probe) set used for PCR 9 , 15 , 16 , 38 , which may be true for this study, and primer sets for other genes may be able to detect leptospiral DNA in more samples. This study employed reciprocal MAT titer 160 as the cutoff value because MAT titer 100 is generally accepted to indicate a previous infection 3 , 5 . Under this definition, there was no significant association between seropositivity and capture area in Okinawa Island. A previous report indicated that the prevalence of anti-leptospiral antibodies in cats was higher in rural areas than in urban areas 9 . The southern part of Okinawa Island is an urban area, and it changes to rural areas as it moves northward. In addition, human leptospirosis is often reported in the northern area due to recreational activities in rivers 37 . These facts suggest no regional difference in the risk of leptospiral infection in cats in Okinawa Island. The previous study mentioned above included only domestic cats 9 , whereas this study included free-roaming, stray cats. Stray cats have more risk of contact with maintenance hosts than pet cats, even in urban areas, resulting in discrepant results between the two studies. In addition, as more than 90% of seropositive cats had antibodies against serogroup Javanica, the transmission of L. borgpetersenii serogroup Javanica may easily occur between cats. A significant association between seropositivity and cat age groups based on weight was shown in this study ( p = 0.021), and seropositivity tended to increase with age ( p = 0.006). This is consistent with the previous report describing that older cats had higher seroprevalence due to an increased opportunity for exposure to the source of infection 16 .

Each serovar tends to be maintained in specific animal species: host-maintained infections of global importance are Icterohaemorrhagiae in the brown rat, Hardjo in cattle and sheep, Canicola in dogs, and Bratislava in pigs 5 . Infections with several serovars/serogroups have been identified in cats, such as Australis, Autumnalis, Ballum, Bataviae, Bratislava, Canicola, Copenhageni, Cynopteri, Grippotyphosa, Hardjo, Icterohaemorrhagiae, Javanica, Panama, Pomona, Pyrogenes, Rachmati, or Shermani 9 , 12 , 14 , 15 , 16 , 18 , 19 , 20 . A serological survey revealed that cats were predominantly infected with serogroup Javanica in Okinawa Island (Table 1 ). Serogroup Javanica has also been isolated from black rats and mongooses in the northern part of Okinawa Island 34 . MLST revealed that L. borgpetersenii detected in urine samples and isolated from cats, black rats, a mongoose, and humans all belonged to ST143. Although ST143 has been isolated from mongooses, L. interrogans serogroup Hebdomadis is the predominant strain isolated from mongooses 34 . Since cats are carnivorous and avoid water, they are more likely to be infected by rat predation than by waterborne infections 39 . These facts suggest an infection cycle between cats and rats in Okinawa Island. Monitoring acute leptospirosis in dogs as sentinels is suggested to aid in estimating the risk to humans in specific areas 40 . Cats may also act as sentinels, but their clinical manifestations seem to be less apparent than those of dogs 9 , 13 , 14 , 22 and their implications may need further verification.

Conversely, all urine PCR-positive cats showed high antibody titer against serogroup Javanica, indicating that they shed leptospires in urine for some period after infection. Therefore, infected stray cats contaminate the environment and can be a source for infection to humans. In this study, more than 90% of seropositive cats had antibodies against serogroup Javanica (Table 1 ), although a variety of Leptospira serogroups/serovars exist on the island 24 , 34 , 35 , 36 , 37 . In cases of leptospirosis in humans on this island during 2007–2016, Hebdomadis was the most frequently detected serogroup (40.1%, 57/142), whereas Javanica was rare (2.8%, 4/142) 37 . Urine PCR-positive DNA samples showed the presence of L. borgpetersenii ST143, which was the same ST with cat isolates on this island; furthermore, the serogroup of these isolates was Javanica (Table 2 ). It has been reported that naturally infected cats subclinically shed leptospires (leptospiral DNAs) for 8 months after infection 20 . These results suggest that this genotype of L. borgpetersenii serogroup Javanica can be easily transmitted among cats and that cats may act as their maintenance host. Antibodies against serogroup Javanica were also detected from cats in Taiwan 12 . Although no genetic information on serogroup Javanica strain from cats was obtained, the same L. borgpetersenii serogroup Javanica genotype has been isolated from rats in Taiwan and in other Asian countries, such as China, Indonesia, Laos, Thailand, and Sri Lanka 30 (PubMLST; https://pubmlst.org/organisms/leptospira-spp ). These facts suggest that cats may carry L. borgpetersenii serogroup Javanica in other Asian countries.

In addition to MLST, WGS revealed that L. borgpetersenii serogroup Javanica isolated from a cat, a mongoose, black rats, and humans in Okinawa Island belonged to the same cluster, supporting their genetic relatedness and the geographic structuring of genetic diversity of Leptospira species as with the previous studies 30 , 31 (Fig. 2 ). The previous report indicated that this genotype of L. borgpetersenii serogroup Javanica could infect various rodent species, suggesting that they are a generalist pathogen 30 . Moreover, this study supports this L. borgpetersenii serogroup Javanica as a generalist, as they can colonize the kidney tissues of cats and mongooses. In this study, only one cat and mongoose succeeded in WGS. WGS of more cat and mongoose isolates could identify animal species-specific characteristics, which may gain new insights into the mechanism of renal colonization and evolution of Leptospira spp. in different animals. It could also identify the precise animal source for human infection.

In conclusion, this study reports that cats are commonly infected with and excrete L. borgpetersenii serogroup Javanica that are genetically closely related to those isolated from black rats, mongooses, and humans in Okinawa Island, Japan. Although genetic relatedness suggests that black rats and mongooses are the source of infection for cats, a high proportion of serogroup Javanica infection and urinary excretion of L. borgpetersenii after infection also suggest that cats may be a maintenance host of L. borgpetersenii serogroup Javanica and the source for human infection.

Sample collection

There were 241 serum samples and 42 urine samples collected in Okinawa Island, the main island of Okinawa Prefecture, Japan. Of these, 121 serum samples and 42 urine samples were collected from free-roaming, stray cats captured/accommodated at the Okinawa Prefectural Animal Protection and Control Center from June 2012 to November 2018, based on the Act on Welfare and Management of Animals. Cats were euthanized by carbon dioxide gas inhalation under the Act, not for this study, and all methods were performed in accordance with the American Veterinary Medical Association guidelines. Autopsy findings, body weight, sex, and capture area were recorded. Blood was collected in a serum separation tube by cardiocentesis and centrifuged at 1710 × g for 15 min to separate the serum. Urine was aseptically collected directly from the bladder using a syringe. Blood and urine collection from euthanized cats was conducted with permission from the Okinawa Prefectural Animal Protection and Control Center.

The other 120 serum samples were derived from the residual blood collected from free-roaming, stray cats during the free-roaming neutering program in the northern part of Okinawa Island from 2016 to 2018 carried out by a nonprofit organization. Serum was separated as described above, and the body weight, sex, and capture area of cats were recorded.

The study was carried out in compliance with the ARRIVE guidelines ( https://arriveguidelines.org/ ).

Antibody detection from cats

To detect anti- Leptospira antibodies in serum samples, MAT was performed using 13 reference strains of serogroups: Australis (serovar Australis), Autumnalis (Autumnalis and Rachmati), Ballum (Castellonis), Bataviae (Bataviae), Canicola (Canicola), Grippotyphosa (Grippotyphosa), Hebdomadis (Hebdomadis), Icterohaemorrhagiae (Icterohaemorrhagiae), Javanica (Javanica), Pomona (Pomona), Pyrogenes (Pyrogenes), and Sejroe (Hardjo). These reference strains were cultivated in Ellinghausen-McCullough-Johnson-Harris medium at 30°C 7 . Twenty-five microliters of twofold serially diluted serum samples [1:80–1:5120 by phosphate-buffered saline] were incubated with the same volume of leptospiral cultures for 3 h at 30 °C. The endpoint was determined by ≥ 50% decrease of free, unagglutinated leptospires compared with the control suspension 3 . Reciprocal MAT titer 160 was used for the cutoff antibody titer.

DNA detection from cat urine samples

DNA was extracted from 200 µL urine using the QIAamp DNA Blood Mini Kit (Qiagen, Hilden, Germany) and subjected to nested PCR targeting flaB for the pathogenic Leptospira spp. First, 5 µl of extracted DNA were used for the first PCR using the primer set L- flaB -F1 5′-CTCACCGTTCTCTAAAGTTCAAC-3′ and L- flaB -R1 5′-TGAATTCGGTTTCATATTTGCC-3′ in a 50 µl reaction volume. Then, 1 µl of the first PCR product was added to 19 µl of the second PCR mixture with the primer set L- flaB -F2 5′-TGTGGACAAGACGATGAAAGC-3′ and L- flaB -R2 5′-AACATTGCCGTACCACTCTG-3′. The positive first PCR samples (FU18017, FU18027, and FU18028) were subjected to DNA sequencing using the BigDye Terminator v3.1 Cycle Sequencing Kit (Applied Biosystems, Foster City, CA, USA).

MLST was performed for the flaB -positive DNA samples (FU18017, FU18027, and FU18028) and DNA samples extracted from nine strains of Leptospira borgpetersenii serogroup Javanica isolated from cats, a mongoose, black rats, and humans using the QIAamp DNA Blood Mini Kit, which were stored at − 80 °C at the Okinawa Prefectural Institute of Health and Environment 27 , 28 (Table 2 ). MLST using seven housekeeping genes ( glmU , pntA , sucA , tpiA , pfkB , mreA , and caiB ) for the isolates was performed as previously described 40 . MLST for the flaB -positive DNAs, FU18017 and FU18028, was performed via nested PCR as previously described 42 . For FU18027, since five of the seven genes were not amplified using the original primer sets 41 , 42 , new primer sets were designed based on L. borgpetersenii sequences (accession numbers CP000350, CP012029, CP015044, CP015046, CP015048, CP015050, CP015052, CP015814, CP021412, CP026671, and CP033440) as described in Table 3 . glmU , sucA , tpiA , pfkB , and caiB were amplified by nested PCR while pntA and mreA were amplified by the first PCR alone. Nucleotide sequences of the amplicons were determined using the BigDye Terminator v3.1 Cycle Sequencing Kit. The concatenated sequences were aligned in MEGA10, and STs were assigned through the MLST database ( https://pubmlst.org/organisms/leptospira-spp ). A minimum spanning tree (MST) based on the allelic profiles determined in this study and those of 182 L. borgpetersenii strains registered in the MLST database was created using BioNumerics Software (version 7.6; Applied-Maths, Sint Maartens-Latem, Belgium) with default settings (MST for categorical data).

Genomic DNA from the six strains in Table 2 was prepared as described above. Genomic DNA libraries were prepared using the Nextera XT DNA Library Prep Kit (Illumina, San Diego, CA, USA) according to the manufacturer’s instructions and sequenced on MiSeq (Illumina) with 300 bp paired-end reads. Core genome single nucleotide variants (SNVs) were extracted using BactSNP v.1.1.037 43 with the genome of L. borgpetersenii serogroup Javanica serovar Ceylonica strain Piyasena as the reference (GenBank accession no. CP026671.1 and CP026672.1). For phylogenetic analysis, SNVs in the recombinogenic regions detected using Gubbins version 2.3.4 44 and those in the repetitive regions of the Piyasena genome identified using MUMmer v.3.2259 45 were excluded. Phylogenetic relationships were determined by reconstructing a phylogenetic tree via the maximum likelihood method using IQ-TREE 46 with 1000 ultrafast bootstrap replicates. The data have been deposited with links to BioProject accession number PRJDB10861 in the DDBJ BioProject database.

Statistical methods

To define the capture areas, the island was divided into northern, central, and southern areas. Cats were categorized according to three age groups based on weight as previously described 47 : male: kitten, < 1.0 kg; juvenile, 1–2.4 kg; and adult, ≥ 2.5 kg and female: kitten, < 1.0 kg; juvenile, 1–1.9 kg; and adult, ≥ 2.0 kg. Associations of seropositivity with capture area, sex, and age based on weight were analyzed using χ 2 test or 2 × 3 Fisher’s exact test and χ 2 test for trend.

Ethics declarations

No ethical approval was required as the samples were collected from cats sacrificed under an act or derived from residual blood from health examinations.

Data availability

The flaB sequences have been deposited in a public database (DDBJ accession numbers LC596932–LC596934). The WGS data have been deposited with links to BioProject accession number PRJDB10861 in the DDBJ BioProject database.

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Acknowledgements

We thank Okinawa Prefectural Animal Protection and Control Center and Okinawa Wildlife Federation for collecting the samples. We are grateful to Kanako Oba for her technical assistance. This work was supported by the Research Program on Emerging and Re-emerging Infectious Diseases (JP21fk0108139) from the Japan Agency for Medical Research and Development (AMED) (N.K.).

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Present address: Regional Health Division, Department of Public Health and Medical Care, Okinawa Prefectural Government, 1-2-2 Izumizaki, Naha-shi, Okinawa, 900-8570, Japan

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Department of Biological Sciences, Okinawa Prefectural Institute of Health and Environment, 17-1 Kanekadan, Uruma-shi, Okinawa, 904-2241, Japan

Tetsuya Kakita, Yumani Kuba, Hisako Kyan & Sho Okano

Department of Bacteriology I, National Institute of Infectious Disease, 1-23-1 Toyama, Shinjuku-ku, Tokyo, 162-8640, Japan

Masatomo Morita & Nobuo Koizumi

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T.K. and N.K. conceived and designed the study. T.K., Y.K., S.O., M.M., and N.K. conducted the experiments. T.K., M.M., and N.K. analyzed the data. H.K. supervised the study. T.K., M.M., and N.K. wrote the manuscript. All authors read and approved the final manuscript.

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Kakita, T., Kuba, Y., Kyan, H. et al. Molecular and serological epidemiology of Leptospira infection in cats in Okinawa Island, Japan. Sci Rep 11 , 10365 (2021). https://doi.org/10.1038/s41598-021-89872-3

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Received : 27 December 2020

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DOI : https://doi.org/10.1038/s41598-021-89872-3

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Trop Med Infect Dis

Feline Susceptibility to Leptospirosis and Presence of Immunosuppressive Co-Morbidities: First European Report of L. interrogans Serogroup Australis Sequence Type 24 in a Cat and Survey of Leptospira Exposure in Outdoor Cats

Elisa mazzotta.

1 Istituto Zooprofilattico Sperimentale delle Venezie (IZSVe), Viale dell’Università 10, 35020 Legnaro, Italy

Gabrita De Zan

Monia cocchi, maria beatrice boniotti.

2 National Reference Centre for Animal Leptospirosis (NRCL), Istituto Zooprofilattico Sperimentale della Lombardia ed Emilia Romagna “Bruno Ubertini”, Via Bianchi 7/9, 25121 Brescia, Italy

Cristina Bertasio

Tommaso furlanello.

3 Veterinary Clinic and Laboratory San Marco, Viale dell’Industria, 35030 Veggiano, Italy

Laura Lucchese

Letizia ceglie, laura bellinati, alda natale, associated data.

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

Leptospirosis is one of the most widespread zoonotic diseases and can infect both humans and animals worldwide. The role of the cat as a susceptible host and potential environmental reservoir of Leptospira is still not well understood, due to the lack of obvious clinical signs associated with Leptospira spp. infection in this species. This study aims to describe the first European detection of Leptospira interrogans serogroup Australis ST 24 in a young outdoor cat with a severe comorbidity (feline panleukopenia virus). In addition, the results of a preliminary study conducted in 2014–2016 are presented (RC IZSVE 16/12), which reports an investigation of Leptospira exposure of outdoor cats in Northeast Italy by means of serological investigation and molecular evaluation of urine. The animals included in the survey are part of samples collected during active and passive surveillance (diagnostic samples). The study reported a seroprevalence of 10.5% among outdoor cats and the serogroups identified were Grippotyphosa, Icterohaemorrhagiae, Bratislava, Canicola and Ballum. Symptomatic cats reported high MAT titres (ranging from 1:800 to 1:1600) towards antigens belonging to the serovars Grippotyphosa (1:800), Bratislava (1:1600), Icterohaemorrhagiae (1:200) and Copenhageni (1:200–1:800). In one subject, urine tested positive for Leptospira PCR. Cats with high antibody titres for Leptospira and/or positivity on molecular test suffered from immunosuppressive comorbidities (feline immunodeficiency virus and feline leukaemia virus; feline herpesvirus and lymphoma; hyperthyroidism). The overall prevalence of serum antibodies against Leptospira found in free-ranging cats (10.53%, 95% CI: 4.35–16.70%) and the identification of L. interrogans ST 24 in a young cat with immunosuppressive disease (feline panleukopenia virus) suggest the possibility of natural resistance to clinical leptospirosis in healthy cats. In a One Health perspective, further studies are needed to better define the pathogenesis of leptospirosis in cats and their epidemiological role as environmental sentinels or possible carriers of pathogenic Leptospira .

1. Introduction

Leptospirosis is caused by spirochaetal bacteria of the genus Leptospira and is an almost endemic disease worldwide. Leptospira spp. potentially affects all mammals that can act either as primary/defective hosts, which develop the acute disease, or as carrier hosts, which are primarily responsible for spreading the disease. The genus Leptospira is currently divided into three phylogenetic clusters, which supposedly correlate with the virulence of the bacteria [ 1 , 2 ]. To date, at least 64 Leptospira species have been described, and these have been classified into four subclades (S1, S2, S3 and S4), including more than 300 serovars [ 3 , 4 , 5 ]. Recently, 43 novel species of Leptospira were isolated from tropical soils, suggesting a highly unexplored biodiversity in the genus [ 4 , 6 , 7 ]. Leptospirosis occurrence is related to specific climatic conditions (i.e., moist soils with neutral pH and warm temperature around 25 °C) that could allow leptospires to persist and remain infectious for several months, leading to potentially relevant environmental contamination [ 1 , 4 , 8 , 9 ].

The serogroups Australis, Autumnalis, Ballum, Canicola, Grippotyphosa, Icterohaemorrhagiae, Pomona and Sejroe are the most frequently reported among cats in Europe, although with significant regional variation, both in terms of serovars and hosts distribution [ 9 , 10 ]. The overall prevalence reported worldwide by microscopic agglutination tests (MAT) ranges from 4% to 33.3%, whereas molecular assays have reported widely different prevalence values, probably influenced by the molecular techniques employed (i.e., PCR-primers) and the characteristics of the geographical area [ 9 ]. Antibodies against Leptospira spp. are mostly reported in older, outdoor, urban cats with hunting behaviour [ 9 , 11 , 12 , 13 ]. In addition, a recent serologic and urinary survey in Canada reported that exposure to Leptospira was unexpectedly relevant in feral cats [ 14 ].

Cats are now considered to represent a possible zoonotic risk, although the clinical course of the disease related to the pathogenesis of leptospirosis in this species is still not fully elucidated [ 8 , 9 , 10 ]. Previous literature reported that the cat could be a potential chronic reservoir host, since, in urine, Leptospira can be isolated and its DNA can be identified for more than 8 months, even when the infected cat presents detectable specific serum antibodies [ 15 ]. Concerning the cat’s natural exposure to pathogenic Leptospira , the most recent literature reported that in Europe, the serological prevalence of anti- Leptospira antibodies varies geographically: 14% in Andalusia [ 16 ], 12.8% in Estonia [ 17 ], 4.1% in Spain [ 18 ] and 9.2% in the Czech Republic [ 19 ]. Previous studies reported a Leptospira serological positivity of 18.2% in Austria (Tyrol’s districts) [ 20 ] and 9.2% in Scotland [ 11 ]. Recently, a seroprevalence of 17.9% was described in Germany in outdoor cats, with titres ranging from 1:100 to 1:6400. The most common serovars were Australis (8.7%, MAT titres range 1:100–1:6400), Bratislava (7.2%, range 1:100–1:400) and Grippotyphosa (5.6%, range 1:100–1:400) [ 21 ].

Reports of clinical leptospirosis in cats are rare: the clinical presentation is characterised by a plethora of signs ranging from asymptomatic to fulminant disease, making the diagnostic process challenging. Specifically, the acute clinical disease mainly involves the young incidental host infected by haemolysin-producing Leptospira species, but in the majority of cases clinical signs are likely to be mild [ 10 , 22 ]. Experimentally described clinical signs include polyuria, polydipsia, haematuria, uveitis, lethargy, anorexia, weight loss, ascites, vomiting, diarrhoea, pain on handling, inflammatory lesions on the skin and digits, cavity effusions, and nephritis, although infection in cats is not always associated with suggestive symptoms [ 10 , 23 , 24 ]. Clinicopathologic changes are a fluctuating leukocytes count, azotaemia, hypokalaemia, hyperphosphatemia, hyposthenuria, haematuria and proteinuria. Therefore, while the interstitial nephritis appears a common clinical manifestation, the liver dysfunction is not reported as frequently as in dogs [ 9 , 24 , 25 ].

Outdoor behaviour and predatory activity seem to be the most relevant risk factors. In addition, living in rural areas in close contact with livestock farms, contact with synanthropic or wildlife species and the presence of other cats in the household are also associated with an increased risk of leptospirosis [ 9 , 12 ]. Further environmental risk factors have been identified, such as living in flooded areas where agricultural activities use water flowing in streams or backwaters [ 26 ]. Accordingly, in tropical countries, the frequency of clinical manifestations of leptospirosis in people is strongly correlated with rainy seasons: flooding contributes strongly to disease transmission, since a high degree of flooding leads to more infected individuals [ 27 , 28 ].

The presence of diseases associated with immunosuppression or immune system deficiency can lead to decreased resistance to infection, debilitation and other complications of illness. Varieties of infectious and non-infectious diseases, stress, poor nutrition, drugs, toxins and medical procedures have been associated with immunosuppression in dogs and cats [ 29 ]. Specifically, the viral agents that could commonly affect outdoor and shelter cats are feline panleukopenia virus (FPV), feline herpesvirus, feline caliciviruses (FCV), feline infectious peritonitis virus (FIPV), feline leukaemia virus (FeLV) and feline immunodeficiency virus (FIV) [ 30 ]. FIP is caused by a feline coronavirus (FCoV) in which the immune system is known to play a crucial, but complex, role in the pathogenesis. This role is still not fully understood, with involvement of both host and viral factors [ 31 ]. Young cats of less than 2 years of age seem especially vulnerable, and it has been estimated that 0.3% to 1.4% of feline deaths at veterinary institutions are caused by FIP [ 32 ]. FeLV and FIV infections are reported in cats worldwide. Both infections are associated with a variety of clinical signs and can impact quality of life and affect longevity [ 33 ]. The major route of FIV transmission is through bite wounds that introduce saliva containing virus and FIV-infected white blood cells. Following the primary phase of the infection, cats enter a long asymptomatic stage that can last for many years. During this chronic stage, progressive dysfunction of the immune system can occur. Thus, FIV-infected cats are predisposed to chronic and recurrent infections. Moreover, neoplasia is about five times more common than in uninfected cats [ 34 ]. Infection with FeLV is transmitted through close contact among cats. Commonly, it is spread vertically and horizontally from infected queens to their kittens and horizontally among cats that live together or that fight [ 34 ]. The prevalence in individually kept cats is usually less than 1%; differently, in multi-cat households, this figure may be 20%: the high density of cat populations represents a facilitating factor [ 35 ]. Immune suppression in FeLV infections is more complex and severe than the more selective effects caused by FIV. Whether showing clinical signs or not, every FeLV-viraemic cat is immune suppressed, with retarded and decreased primary and secondary antibody responses [ 36 ]. FPV may affect cats of all ages, but kittens are most susceptible. FPV has become less frequent in the domestic cat population over the last decades because of vaccination. However, outbreaks in shelter cats are commonly reported and often associated with a high number of fatalities [ 37 ]. Signs of disease include diarrhoea, lymphopenia and neutropenia, followed by thrombocytopenia and anaemia, immunosuppression (transient in adult cats), cerebellar ataxia (in kittens only) and abortion [ 38 ]. Feline panleukopenia mortality is 25–90% in cats with the acute form of the disease and up to 100% in hyperacute infections [ 39 ].

To the best of the author’s knowledge, there are no recent studies about the possible association between immunosuppressive infectious disease and clinical leptospirosis. A proportion of the cat population in Italy has outdoor access, where they have the opportunity to hunt prey [ 40 ]. Therefore, a large population of outdoor cats could be exposed to Leptospira spp. and might play a role in the complex epidemiology of the disease. Only a few recent studies have described the most commonly circulating strains of Leptospira spp. among dogs in Northeast Italy [ 41 ], whereas no recent reports of serological investigation are known in cats in these regions.

The present study reports the first identification of L. interrogans serogroup Australis ST 24 in an immunocompromised young cat and describes four suspected clinical cases of feline leptospirosis. Furthermore, the results of a preliminary serological and epidemiological survey of Leptospira in free-roaming cats in Northeast Italy are described.

2. Materials and Methods

2.1. diagnostic in a young cat referred for sudden death.

A 4-month-old cat was referred from the veterinarian practitioner to the Istituto Zooprofilattico Sperimentale delle Venezie (IZSVE) laboratory for post-mortem examination. The cat was a young free-roaming male domestic short hair from a shelter. The cat had been receiving itraconazole (Itrafungol ® , Virbac, Milan, Italy) for dermatomycosis, which was previously diagnosed by the veterinary surgeon. The cat presented severe and acute gastrointestinal syndrome with vomiting, haemorrhagic diarrhoea, anorexia and dehydration, which rapidly deteriorated, leading to his death within hours.

2.1.1. Microbiological Analysis

Based on the necropsy findings, selected organs were sampled for further diagnostic investigations. Specifically, swabs from faeces, liver and lung were submitted to laboratory routine aerobic and anaerobic culture; faeces and a pool of visceral organs (liver, gall bladder and spleen) were analysed for Salmonella spp. isolation, according to the World Organization for Animal Health (WOAH), Chapter 3.10.07 [ 42 ]. Bacterial identification was phenotypically performed using a routine test.

Leptospira isolation was attempted on liver, kidney and lung tissue. A sample of 1 cm 3 of these organs was homogenized with a pestle and mortar and added to 9 mL of liquid Ellinghausen–McCullough–Johnson–Harris (EMJH) medium, according to WOAH, Chapter 3.1.12 [ 3 ].

2.1.2. Molecular Analysis and Genome Sequencing

The liver, lung and kidney tissue samples were assessed via a pathogen-specific Leptospira TaqMan real-time polymerase chain reaction (real-time PCR) kit. The tissue samples were homogenized at a 1:10 dilution in 600 µL of PBS, with TissueLyser II (QIAGEN, Hilden, Germany), and DNA isolation from 100 µL of tissue homogenate was performed after a prelysis treatment with 2.5 μL of lysozyme (10 mg/mL in 10 mM of Tris-HCl, pH 8.0) and an incubation period of 15 min at +37 °C. The DNA extraction was performed on the KingFisher™ Flex Purification System (Life Technologies, Carlsbad, CA, USA) platform using the ID Gene ® Mag Universal Extraction Kit (IDvet, Grabels, France), in accordance with the manufacturer’s instructions. Every DNA extraction included a negative process or extraction control (water). To detect the presence of pathogenic species of Leptospira , a screening real-time PCR targeting a 87 bp fragment that corresponds to a portion of the gene encoding the 16S rDNA was applied [ 43 ]. The real-time PCR was performed in a 25 µL final volume, containing 3 µL of extracted DNA, 12.5 µL of 2× Master Mix TaqMan Universal 2× (Thermo Fisher Scientific, Waltham, MA, USA), 300 nM of each primer, and 100 nM of a 5′ 6-carboxyfluorescein (FAM)–3′-tetramethylrhodamine (TAMRA) probe. The amplification assay included a negative control (water), a negative bacterial genomic control (DNA of Leptospira biflexa sv Patoc), the negative extraction control and a positive control (DNA of L. interrogans sv Icterohaemorrhagiae). The assay was performed with the following thermal conditions: a holding step at 95 °C for 10 min, and 45 cycles of 95 °C for 15 s and 60 °C for 60 s. Samples with cycle threshold (Ct) < 38 were considered positive. Samples with Ct values within the 38–40 range were considered doubtful, whereas samples with no FAM fluorescence signal or with Ct ≥ 40 were considered negative.

The positive samples were referred to the Istituto Zooprofilattico Sperimentale della Lombardia e dell’Emilia Romagna (IZSLER) National Reference centre for Leptospirosis for the genomic characterization with the multi locus sequence typing (MLST) technique. The genotyping was performed using the 7-loci scheme proposed by Boonsilp in 2013 [ 44 ], which is based on the housekeeping genes glmU, pntA, sucA, tpiA, pfkB, mreA and caiB, as previously described [ 41 ].

For allelic number and ST identification, the assembled and trimmed sequences were queried against the Bacterial Isolate Genome Sequence Database (BIGSdb) available on the Leptospira MLST website ( https://pubmlst.org/leptospira/ , accessed on 1 March 2022), sited at the University of Oxford [ 45 ]. Comparisons between the STs found and those present in BIGSdb as reference isolates were used to deduce the species of the Leptospira being tested. To perform comparisons among historical serological studies (where serovars and serogroups were defined) and genotyping data (where species and genomic profiles were defined), we chose to assign to each identified ST a classification at the serogroup and serovar levels obtained from BIGSdb, knowing that this information was deduced and did not result from active serological typing.

A pool of tissue samples from the stomach and small intestine were submitted to quantitative molecular testing for FPV [ 46 ]. The tissue samples were homogenized at a 1:10 dilution in 800 µL of PBS supplemented with antibiotics (PBS-A: 10,000 IU/mL of penicillin G, 10 mg/mL of streptomycin, 5000 IU/mL of nystatin and 0.25 mg/mL of gentamicin sulphate), with TissueLyser II (QIAGEN, Hilden, Germany) at 30 Hz for 3 min. The DNA extraction was performed on the KingFisher™ Flex Purification System (Life Technologies, Carlsbad, CA, USA) platform using the ID Gene ® Mag Universal Extraction Kit (IDvet, Grabels, France), in accordance with the manufacturer’s instructions, adding a pre-treatment with 20 µL of Proteinase K(QIAGEN, Hilden, Germany) for 10 min at 70 °C before the extraction. Every DNA extraction included a negative control (water). A real-time PCR on a conserved region of gene VP2 of FPV [ 46 ] was carried out in a final volume of 25 µL, consisting of 5 µL of eluted DNA, 5 µL of Quantifast Pathogen Master Mix 5× (QIAGEN, Hilden, Germany), 2.5 µL of Internal Control Assay 10× (QIAGEN, Hilden, Germany), 600 nM of each primer and 200 nM of probe. The assay was performed with the following thermal conditions: a holding step at 95 °C for 5 min, followed by 40 cycles at 95 °C for 15 s and 59 °C for 30 s. The real-time PCR was performed on a Biorad CFX96 instrument (Biorad, Hercules, CA, USA). Samples with cycle threshold (Ct) < 35 were considered positive, whereas samples with no FAM fluorescence signal or with Ct ≥ 35 were considered negative.

2.2. Ricerca Corrente IZSVE 16/12: Sample Collection from 2014 to 2016

The study design involved the collection of samples according to both active and passive epidemiological survey. Ninety-five samples were collected from free-roaming cats with no suspected Leptospira infection reported (active surveillance), while four cases were reported as cases of suspected leptospirosis (passive surveillance). Leptospira investigation of the free-roaming cats ( n = 95) was conducted by retrospectively testing the cat samples collected for other purposes (health status control, pre-surgery investigation, other diagnostics investigations) and enrolled for the study. The test included Leptospira antibody detection by means of a microscopic agglutination test (MAT) on serum [ 3 ] and a real-time PCR on urine for the detection of pathogenic Leptospira , as previously described. The samples were collected from 2014 to 2016 by the veterinary service of the health authority in Northeast Italy (Veneto region) and by veterinary private practices: the samples were submitted to the laboratory of IZSVE and tested for Leptospira through serological and/or molecular methods, as reported above. Anamnestic data, including the clinical features, of the cats enrolled for the study were collected when available. The average age of these subjects was 5.95 years (standard deviation ± 3.75), accounting for 34 young cats (age from 1 to 3 y/o), 42 adult cats (age from 4 to 8 y/o) and 19 senior cats (age > 9 y/o). The study population enrolled 47 female cat (47/95, 49.67%, 95% CI: 36.42–59.53%), and 48 male cat (48/95, 50.53%, 95% CI: 40.47–60.58%).

Moreover, as part of the passive surveillance, samples from suspected clinical cases came from veterinary clinical practices. The clinical symptoms included polyuria, polydipsia, kidney disease and dehydration. The samples (EDTA-whole blood, serum and urine) were collected during routinely diagnostic procedures carried out by the veterinary surgeons. In this context, considering the specific case, it was not deemed necessary to submit a specific request to the Ethics Committee. All procedures complied with the ethical standards of the relevant national and European regulations on animal welfare. Data concerning the cat’s clinical features and the presence of co-morbidities were reported by the attending veterinarians.

Serological Analysis: Micro Agglutination Test (MAT)

All the collected serum samples ( n = 99, active and passive surveillance) were submitted to MAT, according to the WOAH method (Chap 3.1.12) [ 3 ]. The antigen panel included 8 serogroups and 9 serovars distributed by the Italian Reference Centre for Animal Leptospirosis as antigens in the routine diagnostic MAT ( L . interrogans serogroup (sg) Australis serovar Bratislava; L . interrogans sg Canicola serovar Canicola; L . kirschneri sg Grippotyphosa serovar Grippotyphosa; L . interrogans sg Icterohaemorrhagiae serovar Copenhageni; L . interrogans sg Icterohaemorrhagiae serovar Icterohaemorrhagiae; L . interrogans sg Pomona serovar Pomona; L . interrogans sg Sejroe serovar Hardjo; L . borgpetersenii sg Tarassovi serovar Tarassovi; L . borgpetersenii sg Ballum serovar Ballum) [ 47 ].

The serum samples were pretested at the final dilution of 1:100. Samples with 50% agglutination were retested to determine an endpoint using dilutions of serum beginning at 1:100 through to 1:6400. Serum samples with the widely accepted minimum significant titre of 1:100 (reciprocal of the final dilution of serum with 50% agglutination) were assessed as positive. In cases of clinically suspected Leptospira infection, urine samples were collected and analysed for bacterial culture and Leptospira isolation ( n = 2). In addition, these urine samples were assessed via a pathogen-specific Leptospira TaqMan (real-time PCR) kit [ 43 ], as previously described [ 41 ].

3.1. Leptospira Interrogans Serogroup Australis ST 24 in an Immunocompromised Cat

The gross pathology main findings included moderate, acute, catarrhal-haemorrhagic gastritis with areas of erosion in the pyloric region, as well as severe segmental catarrhal-haemorrhagic enteritis of the proximal enteric tracts (duodenum and digiunum). Moderate hepatomegaly was observed in association with mild and diffuse prominence of the parenchyma, as well as multifocal and irregular areas of greyish discoloration with ill-defined margins. The kidney showed multifocal areas of poorly defined cortico-medullary demarcation. The renal cortex was prominent with multifocal, rarely coalescing, bright red radial striations. A moderate quantity of sero-haemorrhagic pleural effusion was reported in both hemithorax, and the lungs were bilaterally characterized by multifocal to locally diffuse, dark-red, irregular and haemorrhagic areas associated with pulmonary edema. In addition, an extensive area of adhesion between the middle and caudal lobes of the right lung was described, associated with pleural fibrin and a moderate increase in parenchymal consistency ( Figure 1 ). Finally, the mucous membranes appeared pale and the peripheral lymph nodes and tonsils were moderately increased in volume with prominent follicles on the cut surface. Unfortunately, histopathology was not performed, as reported in the study limitation paragraph.

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Gross findings of the kitten positive for FPV and Leptospira interrogans serogroup Australis ST 24. Left kidney dorsal and longitudinal section: multifocal, ill-defined cortico-midline demarcation and a prominent renal cortex with multifocal, rarely coalescent, bright red radial striations ( A , B ). ( B ) Stomach and proximal intestine (duodenum): catarrhal-haemorrhagic gastritis, erosive alteration of the mucosa of the pyloric region. ( C ) Increased size of the liver with blurred margins and slight diffuse prominence of the parenchyma. ( D ) Severe pulmonary edema and haemorrhagic suffusions: area of adhesion between the middle and caudal lobes of the right lung (arrow) ( E ).

Bacteriological samples from intestine, liver and lung were positive for Escherichia coli, whereas Salmonella spp. analysis tested negative. Finally, gastrointestinal samples tested positive for the molecular detection of FPV (Ct 23.01) (stomach and small intestine tissue samples).

Bacterial culture tested negative for Leptospira spp. (kidney, lung and liver).

The molecular analysis reported positivity for Leptospira spp. only in the kidney tissues (Ct 35.95), while lung and liver resulted negative. The Leptospira DNA, submitted to an MLST analysis, was typed as Leptospira ST 24, which identifies L . interrogans serogroup Australis.

3.2. Survey on the Exposure to Leptospira spp. of Feline Populations in Northeast Italy (2014–2016): RC IZSVE 16/12

3.2.1. leptospira investigation in free-roaming cats: active surveillance.

Ninety-five free-roaming cats were tested for anti- Leptospira antibodies (MAT) and for pathogenic Leptospira detection in urine (real-time PCR). The MAT was positive in 10 out 95 cats (10.53%, 95% CI: 4.35–16.70%), and the most representative serogroups were Grippotyphosa ( n = 6/95; 6.32%, 95% CI: 1.42–11.21%), Icterohaemorrhagiae ( n = 2/95; 2.11%, 95% CI: 0.00–4.99%) and Bratislava ( n = 3/95; 3.16%, 95% CI: 0.00–6.67%). None of these cats tested positive in urine and blood by real-time PCR. The animals reported low antibody titres (<1:200), both against L. kirschneri sg Grippotyphosa serovar Grippotyphosa and L. interrogans sg Icterohaemorrhagiae serovar Icterohaemorrhagiae. One cat reported antibodies against L. interrogans sg Australis serovar Bratislava (titre 1:200) and one cat showed positivity for L. interrogans Canicola serovar Canicola (titre 1:100). One young and pregnant queen showed antibody titres against L. kirschneri sg Grippotyphosa serovar Grippotyphosa (titre 1:100), L. interrogans sg Icterohaemorrhagiae serovar Icterohaemorrhagiae (titre 1:100) and L. interrogans sg Icterohaemorrhagiae serovar Copenhageni (titre 1:100). Finally, a pregnant adult queen reported low titres for L. borgpetersenii sg Ballum serovar Ballum (titre 1:100) ( n = 1/95, 1.05%, 95%CI 0.00–3.10) ( Table 1 ). The real-time PCR on the urine samples tested negative.

MAT titres detected during the survey in cats (study RC 16/12); the significant clinical features and concurrent diseases (active surveillance). Clinically symptomatic cats tested positive for Leptospira spp. MAT and/or real-time PCR, and the presence of clinical signs and concurrent diseases (passive surveillance).

Sexual condition is indicated when information was available. (*): the cat was treated with antibiotics. (**): no urine samples were available for molecular and microbiological assay. NP: not performed.

3.2.2. Leptospira Investigation in Free-Roaming Cats with Clinical Symptoms: Passive Surveillance

Among the four cats selected by passive surveillance showing clinical symptoms suggestive of possible Leptospira infection, high MAT titres (>1:400) were recorded towards serogroup/serovars Grippotyphosa ( n = 2/5; 40%, 95% CI: 0.00–82.9%) and Bratislava ( n = 2/5; 40%, 95% CI: 0.00–82.9%). MAT titres of 1:200 were reported for Icterohaemorrhagiae ( n = 1/5, 20%, 95% CI 0.00–55.06%) and Copenhageni ( n = 2/5; 40%, 95% CI: 0.00–82.9%). Moreover, two cats reported a co-presence of different serovars ( L. Grippotyphosa, L. Icterohaemorrhagiae and L. Copenhageni; L. Bratislava and L . Copenhageni, respectively). Interestingly, the cats that were positive for Leptospira (high antibody titres and/or molecular positivity) presented severe immunocompromising co-morbidities, such as FIV and FeLV, FHV-1 infection and hyperthyroidism, and lymphoma. ( Table 1 ).

4. Discussion

Leptospirosis in cats still has several unclear aspects. Epidemiological studies and the identification of serovars of Leptospira circulating in this species help to fill the gaps in the definition of the eco-pathological picture of leptospirosis and the role of the cat. Although outdoor cats are potentially easily exposed to the pathogen (predatory behaviour, contact with reservoirs and contaminated environments), they appear to be less prone to the development of clinical disease than other susceptible animals. It is not completely clarified which serovars can cause incidental infections in cats. Based on previously published reports of acute leptospirosis in cats, serovars belonging to Autumnalis, Australis, Icterohaemorrhagiae, Grippotyphosa, Pomona and Sejroe serogroups seem to be mostly involved [ 9 ]. Interestingly, during an ongoing study conducted by these authors’ research team (Mazzotta E., et al.), L . interrogans Australis ST 24 was detected in hedgehogs, mice and foxes in Northeast Italian regions, suggesting a possible prey–predator epidemiological scenario (preliminary unpublished data).

The present study describes the identification of L. interrogans Australis ST 24 in a kitten with severe immunosuppressive co-morbidity (FPV). The clinical symptoms (haemorrhagic diarrhoea) and the gross pathology findings (haemorrhagic enteritis) were highly suggestive of FPV infection [ 48 , 49 ], as confirmed by the positive real-time PCR result. FPV is transmitted via the faecal–oral route, and the infected subject is able to shed high titres of virus, rapidly contaminating the environment. Feline panleukopenia represents a severe disease, common signs of which include lymphopenia and neutropenia, followed by thrombocytopenia and anaemia, immunosuppression (transient in adult cats), neurological and reproductive symptoms [ 50 ]. In addition, this cat reported both pulmonary severe diffuse haemorrhagic lesions and hepatic alterations: bacteriological identification revealed in both lung and liver samples showed a positive high load for E . coli . The identification may indicate an extra intestinal localization of this bacterium, likely related to the poor immunity of the kitten.

In this context, the shelter condition/household, the young age of the cat, the expected presence of immune dysfunction due to FPV and the possible presence of bacterial co/secondary infection, could likely have favoured the occurrence of Leptospira infection. As previously reported in the literature [ 9 , 12 ], this cat could be more likely considered as an incidental host rather than a chronic carrier for leptospirosis.

Concerning the epidemiological evaluation among free-roaming cats in Northeast Italy, these authors reported an apparently reassuring situation in clinically healthy cats, with sporadic seropositivity at low titres and no direct detection of Leptospira . Conversely, a different scenario appeared in four clinically suspected cases: these cats showed suggestive symptoms of clinical leptospirosis, high MAT antibody titres, and one animal tested positive in a real-time PCR analysis on the urine sample. All these cases presented severe systemic co-morbidities (i.e., FPV, FIV, FeLV and lymphoma).

To the best of the authors’ knowledge, a specific correlation between Leptospira ST and immunosuppressive co-morbidities has not been demonstrated, but significant associations with an inflammatory condition and stress response were reported in cats exposed to Leptospira spp. In Leptospira spp. antibody-positive cats, alterations in CBC (anaemia, neutrophilia, monocytosis and eosinopenia), in inflammation markers (i.e., hypoalbuminemia and hyperglobulinemia) and increased ALT activity have been reported [ 51 ]. Previous case reports described three confirmed, naturally infected clinical cases of feline leptospirosis, in which the major clinical findings were different stages of renal insufficiency without any liver involvement [ 24 , 52 ]. Dissimilar information is available about the correlation between chronic kidney disease and serological positivity for Leptospira [ 10 , 53 ]. Although further investigations are needed, it is possible that the lack of an adequate immune response in animals with immunosuppressive diseases may have favoured the development of systemic leptospirosis, in association with a clinically evident condition in the most severe cases.

The free-roaming cats found positive for Leptospira antibodies but without any suggestive clinical symptoms reported low serological titres (>1:100): these findings would be suggestive of exposure, possibly recurrent, to pathogenic Leptospira or subclinical and chronic infection, since it has been previously reported that cats can demonstrate positive serology of leptospirosis months after the suspected time of infection/exposure [ 9 ]. Thus, it is possible that cats may develop clinical signs after a longer period than what has been documented experimentally [ 23 ]. Unfortunately, it was not possible to evaluate the animals afterwards, so no follow-up data are available.

The most frequent serovars involved in feline leptospirosis in Europe, based on serological investigations and according to the European consensus statement on leptospirosis, belong to serogroups Australis, Autumnalis, Ballum, Canicola, Grippotyphosa, Icterohaemorrhagiae, Pomona and Sejroe [ 10 ]. According to this, our study showed the presence of antibodies against Grippotyphosa, Icterohaemorrhagiae, Canicola and Australis, despite these low serological titres being suggestive of exposure or subclinical infection. The comparison of the serological data available in the literature about anti- Leptospira antibodies in cats is likely biased by geographical origin, sampling method and the diagnostic technique applied [ 24 , 53 , 54 ]. Environmental factors, such as outdoor habits, the presence of livestock and farm animals that may shed Leptospira in the neighbourhood, wild animals’ Leptospira reservoirs, and seasonality, may result in different degrees of exposure to pathogenic Leptospira , thus, potentially justifying the broad ranges of antibody prevalence reported in the literature. A recent study conducted in cats in southern Italy reported antibodies against serovars Poi, Arborea and Mini, among others [ 51 ]. This study also described the spring season as the only risk factor for urinary Leptospira shedding, detected in 9% of urine samples. Moreover, laboratory variability determined by both the use of different methods and the application of different cut off values (≥1:100), and variations in host-specific humoral immune responses, can be a hindrance to the correct identification of positive results. Many different Leptospira antigens were tested in the immunoassay, but false-negative results occur when the infecting serogroups are not included. Furthermore, the significance and duration of Leptospira species antibodies, as detected by the MAT in cat sera, are largely unknown. It is even possible that seroconversion in cats is expressed at a lower titre compared to dogs [ 55 ]. However, the MAT is believed to be specific for Leptospira species antibodies, even if it is unknown whether antibodies against other spirochetes in feline sera can lead to falsely positive results. Although not completely elucidated, it has recently been experimentally assessed that antibodies produced following infection by other spirochetes in cats (i.e., Borrelia burgdorferi ) are not detected in Leptospira MAT [ 55 ].

The evaluation of serological tests in cats is a challenge: cross-reactivity with non-vaccine serogroups has been demonstrated in dogs, as well as in cats, and antibody production after infection in cats appears to be serogroup-specific, although immune protection is not clearly understood [ 14 ]. The seroprevalence against Leptospira observed in our study was 10.53%, falling within the previous intervals (4% to 33.3%) described worldwide [ 18 , 26 , 55 , 56 , 57 ].

The cat’s role as a possible cause of Leptospira environmental contamination and source of exposure for people is not fully understood [ 9 ], whereas it is a susceptible host for Leptospira spp. and could potentially present a chronic leptospirosis infection with urinary shedding. Feline leptospirosis is likely to be underdiagnosed: it is common for leptospirosis not to be considered as a possible differential diagnosis, even in animals with clinical symptoms suggestive of acute Leptospira infection (i.e., acute renal failure). Moreover, the possible underestimation of leptospirosis in cats may be due to other factors, such as the challenging clinical diagnosis related to mild or atypical clinical signs, and difficulties in serological or molecular analysis. These circumstances may impact the scarcity of official reports and the perceived low prevalence of the infection within this species [ 58 ]. Therefore, the lack of a large serological survey and molecular detection among Leptospira spp.-positive cats does not adequately define the zoonotic risk factors nor the epidemiological role of this species.

5. Conclusions

The detection of new ST in cats highlights the need to consider the challenge of better understanding the effect of exposure to or infection with pathogenic Leptospira spp. in felines, and the need to define their epidemiological role as sentinel hosts or environmental reservoirs. Outdoor and shelter cats that are free-roaming and hunt prey would be a population worthy of special attention: although they may not explicitly manifest symptoms of leptospirosis, they may instead reveal circulating strains of Leptospira in a domestic–shelter (cat–prey) or domestic–domestic (cat–dog or other susceptible domestic mammals) context. To date, many questions remain to be clarified, particularly concerning the cat’s ability to be a chronic carrier rather than an environmental sentinel. In addition, as highlighted by the serological survey in outdoor cats, further studies are needed to increase knowledge about the host-immune response following infection or exposure to specific Leptospira serovars within the feline population. Furthermore, the evaluation of the possible aetiopathogenic link between clinical leptospirosis and immunosuppressive diseases, and the analysis of the immune pathways, would be useful to improve the diagnostic techniques.

Acknowledgments

This paper is dedicated to the memory of Carmelo Furnari. The authors would like to thank Ben Adler for his advice and scientific support.

Funding Statement

Ministero della Salute, Ricerca Corrente IZSVE 16/12 grant number B28C13000510001.

Author Contributions

Conceptualization, E.M. and G.D.Z.; methodology, L.B. and L.C.; formal analysis, G.D.Z., M.C. and L.L.; investigation, E.M. and T.F.; resources, A.N., T.F., M.B.B., C.B. and L.C.; data curation, E.M., G.D.Z. and L.L.; writing—original draft preparation, E.M. and G.D.Z.; writing—review and editing, E.M., G.D.Z., L.B., T.F., C.B. and L.L.; visualization, A.N. and M.B.B.; supervision, A.N.; project administration, A.N.; funding acquisition, A.N. All authors have read and agreed to the published version of the manuscript.

Institutional Review Board Statement

The study received Ethics Committee IZSVE approval (CE_IZSVE 17/2022). Biological samples were collected by clinicians for diagnostic purposes and from stray cats undergoing spaying surgery sampled to perform pre-operative profile tests. No animals were sampled exclusively for the purposes of this study. Necropsy was performed on request of the legal manager of the shelter, as an official diagnostic surveillance of the veterinary service of the health authority. Animal care and procedures are in accordance with the Guide for the Care and Use of Laboratory Animals and Directive 2010/63/EU for animal experiments (National law: D.L. 26/2014).

Informed Consent Statement

The processing of biological material, data, anamnestic and epidemiological information of the animals were authorized as a part of the research project (RC IZSVE 16/12).

Data Availability Statement

Conflicts of interest.

The authors declare no conflict of interest.

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Leptospirosis in cats: Current literature review to guide diagnosis and management
The current literature on leptospirosis in cats is reviewed. To date, few case reports have been published in the field, and information has mostly been extrapolated from infections in people and dogs. This review is expected to serve as a guide for the diagnosis and management of the disease in cat …
Leptospirosis in cats: Current literature review to guide diagnosis and
This review is expected to serve as a guide for the diagnosis and management of the disease in cats. Clinical signs of leptospirosis in cats based on published studies of acute disease Figures ...
Leptospirosis in cats: Current literature review to guide diagnosis and
Leptospirosis in cats: Current literature review to guide diagnosis and management. Sign in | Create an account. https://orcid.org. Europe PMC ... Search life-sciences literature (43,447,177 articles, preprints and more) Search. Advanced search. Feedback Complete Survey Survey.
Leptospirosis in cats: Current literature review to guide diagnosis and
Leptospirosis in cats: Current literature review to guide diagnosis and management. ... Search worldwide, life-sciences literature Search. Advanced Search Coronavirus articles and preprints Search examples: "breast cancer" Smith J Recent history ...
Leptospirosis in cats: Current literature review to guide diagnosis and
Global importance: Leptospirosis is the most widespread zoonosis worldwide. Mammals (eg, rats, horses, cows, pigs, dogs, cats and aquatic species, such as sea lions and northern elephant seals) can all be infected by leptospires.
Leptospirosis in cats: Current literature review to guide diagnosis and
Global importance: Leptospirosis is the most widespread zoonosis worldwide. Mammals (eg, rats, horses, cows, pigs, dogs, cats and aquatic species, such as... Leptospirosis in cats: Current literature review to guide diagnosis and management
Leptospirosis in cats: Current literature review to guide diagnosis and
216_228_Murillo2.qxp_FAB 03/02/2020 12:44 Page 216 JournalofFelineMedicineandSurgery (2020) 22, 216-228 CLINICAL REVIEW LEPTOSPIROSIS IN CATS Current literature review to guide diagnosis and management Global importance: Leptospirosis is the most widespread zoonosis worldwide.
Leptospirosis in cats: Current literature review to guide diagnosis and
The current literature on leptospirosis in cats is reviewed. To date, few case reports have been published in the field, and information has mostly been extrapolated from infections in people and dogs. This review is expected to serve as a guide for the diagnosis and management of the disease in cats.
Molecular and serological epidemiology of Leptospira infection in cats
Leptospirosis is a zoonosis caused by pathogenic Leptospira spp. Cats have been reported to be infected with Leptospira spp. and shed the bacteria in the urine. However, the importance of cats as ...
Leptospira Species Infection in Cats: ABCD guidelines on prevention and
In experimental and naturally infected cats, nephritis has been reported. 16-18,21 In one study, a relationship was found between polyuria/polydipsia and the presence of antibodies against Leptospira species. 15,19 A recently published case series of three cats with leptospirosis reported that all three cats suffered from renal failure, while ...
Molecular and serological epidemiology of Leptospira infection in cats
Leptospirosis is a zoonosis caused by pathogenic Leptospira spp. Cats have been reported to be infected with Leptospira spp. and shed the bacteria in the urine. However, the importance of cats as an infection source for humans remains unclear. In this study, Leptospira infection in cats in Okinawa Prefecture, Japan, where leptospirosis is endemic, was investigated by leptospiral antibody and ...
Feline Susceptibility to Leptospirosis and Presence of
Reports of clinical leptospirosis in cats are rare: the clinical presentation is characterised by a plethora of signs ranging from asymptomatic to fulminant disease, making the diagnostic process challenging. ... Pastor J. Leptospirosis in Cats: Current Literature Review to Guide Diagnosis and Management. J. Feline Med. Surg. 2020; 22:216-228 ...
[PDF] Feline leptospirosis prevalence worldwide: A systematic review
A systematic review and meta-analysis of leptospirosis in domestic cats indicated a significantly higher pooled seroprevalence of leptospirosis in domestic cats compared with infection prevalence, while wild cats had no significant differences in any of the subgroups. Background and Aim: Leptospirosis in felids (domestic and wild cats) presents an ongoing challenge in our understanding ...
Leptospirosis in dogs and cats: new challenges from an old bacteria
Use of renal replacement therapy should be considered for severe renal leptospirosis. This is only available at some referral centres in the UK. In-contact dogs should be treated with the same schedule of doxycycline as infected dogs. There is no current recommendation to treat in-contact cats.
PDF Leptospirosis in cats: Current literature review to guide diagnosis and
Evidence base: The current literature on leptospirosis in cats is reviewed. To date, few case reports have been published in the field, and information has mostly been extrapolated from infections in people and dogs. This review is expected to serve as a guide for the diagnosis and management of the disease in cats.
Evaluation of Leptospira infection and exposure in free-roaming cat
Banked serum specimens were obtained from free-roaming cats that had been euthanized for management purposes at a large shelter in the Rio Grande Valley region of Texas throughout 2017. ... POC assays may have value in the diagnosis of leptospirosis in cats. ... Ahmed A, et al. Leptospirosis in cats: current literature review to guide diagnosis ...
Leptospirosis in cats: Current literature review to guide diagnosis and
Leptospirosis in cats: Current literature review to guide diagnosis and management. Andrea Murillo, Marga Goris, Ahmed Ahmed, Rafaela Cuenca *, Josep Pastor * Autor corresponent d'aquest treball. Departament de Medicina i Cirurgia Animals; Universiteit van Amsterdam;
European consensus statement on leptospirosis in dogs and cats
The aim of this consensus statement is to raise awareness of leptospirosis and to outline the current knowledge on the epidemiology, clinical features, diagnostic tools, prevention and treatment measures relevant to canine and feline leptOSPirosis in Europe. Leptospirosis is a zoonotic disease with a worldwide distribution affecting most mammalian species. Clinical leptospirosis is common in ...
Evaluation of Leptospira infection and exposure in free-roaming cat
Banked serum specimens were obtained from free-roaming cats that had been euthanized for management purposes at a large shelter in the Rio Grande Valley region of Texas throughout 2017. ... POC assays may have value in the diagnosis of leptospirosis in cats. ... Ahmed A, et al. Leptospirosis in cats: current literature review to guide diagnosis ...
Leptospirosis in Cats: Current Literature Review To Guide Diagnosis and
2020 Leptospirosis en gatos.pdf - Free download as PDF File (.pdf), Text File (.txt) or read online for free.
Leptospirosis in cats: Current literature review to guide diagnosis and
Leptospirosis in cats: Current literature review to guide diagnosis and management. Andrea Murillo, Marga Goris, Ahmed Ahmed, Rafaela Cuenca *, Josep Pastor * Autor correspondiente de este trabajo. Departamento de Medicina y Cirugía Animal; Universiteit van Amsterdam;

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Feline Susceptibility to Leptospirosis and Presence of Immunosuppressive Co-Morbidities: First European Report of L. interrogans Serogroup Australis Sequence Type 24 in a Cat and Survey of Leptospira Exposure in Outdoor Cats.

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Feline Susceptibility to Leptospirosis and Presence of Immunosuppressive Co-Morbidities: First European Report of L. interrogans Serogroup Australis Sequence Type 24 in a Cat and Survey of Leptospira Exposure in Outdoor Cats

Gabrita De Zan

Cristina Bertasio

Laura Lucchese

1. Introduction

2. Materials and Methods

2.1.1. Microbiological Analysis

2.1.2. Molecular Analysis and Genome Sequencing

2.2. Ricerca Corrente IZSVE 16/12: Sample Collection from 2014 to 2016

Serological Analysis: Micro Agglutination Test (MAT)

3.1. Leptospira Interrogans Serogroup Australis ST 24 in an Immunocompromised Cat

3.2. Survey on the Exposure to Leptospira spp. of Feline Populations in Northeast Italy (2014–2016): RC IZSVE 16/12

3.2.2. Leptospira Investigation in Free-Roaming Cats with Clinical Symptoms: Passive Surveillance

4. Discussion

5. Conclusions

Acknowledgments

Funding Statement

Author Contributions

Institutional Review Board Statement

Informed Consent Statement

Data Availability Statement

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