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Detection of Leptospira kirschneri in a short-beaked common dolphin (Delphinus delphis delphis) stranded off the coast of southern California, USA

BMC Veterinary Research volume 20, Article number: 266 (2024) Cite this article

Abstract

Background

Pathogenic Leptospira species are globally important zoonotic pathogens capable of infecting a wide range of host species. In marine mammals, reports of Leptospira have predominantly been in pinnipeds, with isolated reports of infections in cetaceans.

Case presentation

On 28 June 2021, a 150.5 cm long female, short-beaked common dolphin (Delphinus delphis delphis) stranded alive on the coast of southern California and subsequently died. Gross necropsy revealed multifocal cortical pallor within the reniculi of the kidney, and lymphoplasmacytic tubulointerstitial nephritis was observed histologically. Immunohistochemistry confirmed Leptospira infection, and PCR followed by lfb1 gene amplicon sequencing suggested that the infecting organism was L.kirschneri. Leptospira DNA capture and enrichment allowed for whole-genome sequencing to be conducted. Phylogenetic analyses confirmed the causative agent was a previously undescribed, divergent lineage of L.kirschneri.

Conclusions

We report the first detection of pathogenic Leptospira in a short-beaked common dolphin, and the first detection in any cetacean in the northeastern Pacific Ocean. Renal lesions were consistent with leptospirosis in other host species, including marine mammals, and were the most significant lesions detected overall, suggesting leptospirosis as the likely cause of death. We identified the cause of the infection as L.kirschneri, a species detected only once before in a marine mammal – a northern elephant seal (Mirounga angustirostris) of the northeastern Pacific. These findings raise questions about the mechanism of transmission, given the obligate marine lifestyle of cetaceans (in contrast to pinnipeds, which spend time on land) and the commonly accepted view that Leptospira are quickly killed by salt water. They also raise important questions regarding the source of infection, and whether it arose from transmission among marine mammals or from terrestrial-to-marine spillover. Moving forward, surveillance and sampling must be expanded to better understand the extent to which Leptospira infections occur in the marine ecosystem and possible epidemiological linkages between and among marine and terrestrial host species. Generating Leptospira genomes from different host species will yield crucial information about possible transmission links, and our study highlights the power of new techniques such as DNA enrichment to illuminate the complex ecology of this important zoonotic pathogen.

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Background/introduction

Leptospirosis, the disease caused by infection with pathogenic species within the genus Leptospira, is a globally important zoonosis [1]. There are 41 pathogenic Leptospira species and hundreds of known pathogenic serovars, each with slightly different characteristics, host affinity and host–pathogen interactions [1,2,3,4,5,6,7,8]. Broadly, all mammals are believed to be susceptible to Leptospira infection, and infection has also been detected by culture, hamster inoculation, and/or polymerase chain reaction (PCR) in a range of frogs, snakes, and turtles [4, 9,10,11,12,13,14,15,16]. The full range of host–pathogen interactions for Leptospira is still being uncovered, with significant challenges arising from the diversity of pathogenic Leptospira strains, logistic hurdles in collecting samples from possible hosts, weaknesses in available tools for diagnosis and strain identification, and the broad spectrum of clinical presentations that accompany infections.

Knowledge of infection and transmission of Leptospira is based mostly on studies of terrestrial mammals. In mammalian hosts, infections can be completely subclinical, or can present with clinical signs ranging from flu-like symptoms (fever, muscle aches, headache) to pulmonary manifestations, reproductive failure, liver or renal failure, and even death [1, 2, 4, 17]. In infected hosts, leptospires ultimately colonize the kidneys and then are shed in urine; shedding can continue for months to years in some individuals or host species [4]. Leptospires may also colonize other sites, including reproductive tissues [4]. Clinical disease in infected hosts is due to the damage caused by leptospires during initial systemic infection and eventual tissue colonization, as well as the host inflammatory response against the pathogen [1]. Gross and histopathologic lesions detected in cases of leptospirosis can vary depending on host and infecting species, and reflect the bacterial virulence and host immune responses [4]. However, renal lesions are frequent and are characterized by tubulointerstitial nephritis or glomerulonephritis [2, 4, 18, 19]. The most common routes of transmission are direct contact with urine or indirect contact with urine-contaminated soil or water; intact skin is a strong barrier to infection, but damaged skin and mucous membranes are important routes of infection [20]. Vertical transmission can occur, and contact with infectious aborted tissues or sexual contact can also lead to transmission [4]. Leptospire survival in the environment likely varies by Leptospira species and genotype, as well as by environmental conditions, with survival ranging from hours to as long as months, and in some cases over a year [8, 21,22,23]. Some of the shortest reported survival times were recorded for seawater [23] and salts may be inhibitory for pathogenic Leptospira in the absence of nutrients [24].

In marine mammals, reports of Leptospira have predominantly been noted in pinnipeds, with isolated reports of infections in cetaceans. Leptospira interrogans serovar Pomona has been circulating endemically in California sea lions (Zalophus californianus), with seasonal outbreaks occurring yearly since at least 1984 [25,26,27,28,29,30]. Leptospira in other pinnipeds has also been documented, especially in the eastern Pacific Ocean, with seropositivity or infection reported in northern fur seals (Callorhinus ursinus), northern elephant seals (Mirounga angustirostris), Pacific harbor seals (Phoca vitulina richardsi), and Steller sea lions (Eumetopias jubatus) on the west coast of the United States (northeastern Pacific Ocean); South American sea lions (Otaria byronia) along the coast of Chile; and manatees (Trichechus inunguis) in the Peruvian Amazon [25,26,27, 31,32,33,34,35,36,37,38,39]. In contrast, reports of Leptospira infection in cetaceans are quite rare, and Leptospira infection or seropositivity has not been previously detected in a cetacean host in the northeastern Pacific Ocean.

Globally, only eight cetacean species have been shown definitively to be infected with Leptospira. Two isolates with 98 and 99% similarity, respectively, to L.interrogans serovar Copenhageni were cultured from kidneys of a Fraser’s dolphin (Lagenodelphis hosei) and a melon-headed whale (Peponocephala electra) from the Philippines in 2017 [40]. An isolate that is suspected to be L. interrogans based on sequence results was cultured from the kidney of a newborn southern right whale (Eubalaena australis) that stranded dead in Argentina in 2010 [41]. An isolate of L. interrogans serovar Pomona was cultured from a common bottlenose dolphin (Tursiops truncatus) that stranded along the coast of Sardinia, Italy in 2016 [42]. Torres et al. [43] detected Leptospira DNA using LipL32-PCR in a Clymene dolphin (Stenella clymene), 10 Guiana dolphins (Sotalia guianensis), seven La Plata dolphins (Pontoporia blainvillei), one rough-toothed dolphin (Stenobredanensis), and a common bottlenose dolphin. Genetic characterization using secY gene sequences of Leptospira detected in three of these PCR positive animals—one each of a Clymene, a Guiana, and a La Plata dolphin—identified them as L. interrogans with an identity > 99%, and serological classification indicated > 99% similarity with the Icterohaemorrhagiae serogroup. Serologic evidence of Leptospira infection (current or historic) and/or detection using a PCR primer that targets both pathogenic and non-pathogenic Leptospira spp. has been reported in an additional nine cetaceans [40].

Here we add to the limited body of knowledge regarding Leptospira in cetaceans. We report the first detection of Leptospira in a short-beaked common dolphin (Delphinus delphis delphis), and the first detection in any cetacean in the northeastern Pacific Ocean. We identify the species as L.kirschneri and show that infection was associated with tubulointerstitial nephritis, which was the most significant lesion observed in this animal and the likely cause of death. Given the extremely limited body of knowledge regarding Leptospira in cetaceans and the marine ecosystem in general, this provides valuable new data on host range. This report raises pertinent questions about the ecology of Leptospira in the marine environment, including how the pathogen may transmit between cetaceans and whether these obligate marine hosts play a more significant role in Leptospira circulation than is currently recognized.

Case presentation

On 28 June 2021, a 150.5 cm long female, short-beaked common dolphin (BLH0012) stranded alive along the coast of southern California (Ponto Beach, Carlsbad, San Diego County) and subsequently died. The carcass was refrigerated at 4͒°C until necropsied on 30 June 2021. Gross necropsy observations included normal body condition [44], an empty stomach, pale yellow intestinal contents, and multifocal cortical pallor within the reniculi of the kidney (Fig. 1). All other organs appeared normal on the gross exam. A standard set of tissue samples were collected and placed in 10% neutral buffered formalin, processed routinely for paraffin embedding, sectioned at 5 μm, stained with hematoxylin and eosin (H&E), and examined microscopically. The age of this dolphin was estimated to be two years old via counts of growth layers in its teeth, using methods outlined in Danil and Chivers [45]. Based on necropsy observations and estimated age, this individual was not sexually mature and was likely still nursing.

Fig. 1
figure 1

Kidneys of short-beaked common dolphins. The kidney from BLH0012, infected with Leptospira, is on the left and has multifocal cortical pallor (indicated by black arrows). On the right is a ‘normal’ kidney from a dolphin

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Histologically there was moderate lymphoplasmacytic tubulointerstitial nephritis. Multifocally, renal cortical tubules were surrounded and occasionally disrupted by moderate numbers of plasma cells and fewer lymphocytes. Some affected tubules were dilated, had attenuated epithelium, and contained pale eosinophilic granular material (Fig. 2A). No glomerular lesions were apparent. Other lesions observed in the animal were consistent with debilitation and recent inanition. Immunohistochemistry (IHC) of paraffin-embedded kidney sections was performed using a streptavidin–biotin method and a Leptospira-specific polyclonal antibody (National Veterinary Services Laboratory, Ames, Iowa, USA) directed against L. interrogans serovars Bratislava, Canicola, Copenhageni (Icterohaemorrhagiae), Hardjo, and Pomona, and L.kirschneri serovar Grippotyphosa [33]. Multiple renal tubules, both near and distant from areas of inflammation contained wispy, IHC-positive antigenic staining in the tubular lumens (Fig. 2B). No antigen was demonstrated in negative control sections.

Fig. 2
figure 2

Photomicrographs of kidney from short-beaked common dolphin (BLH0012) with leptospirosis. A Hematoxylin and eosin stained section with lymphoplasmacytic tubulointerstitial nephritis. Bar = 20 μm. B Kidney stained with a polyclonal antibody directed against Leptospira sp. There is dark brown positive staining of material within tubules. Bar = 20 μm

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We conducted real-time PCR analysis on fresh frozen kidney to detect and differentiate L. interrogans, L.kirschneri, L. borgpetersenii and L.noguchii, as described by Ferreira et al. [46] (2014), with the following modification: PerfeCTa Tough Mix Low Rox master mix (Quantabio) and appropriate thermocycling conditions for this master mix were used. We also conducted Leptospira genotyping PCR using primers targeting the lfb1 gene, followed by amplicon sequencing [47]. These methods indicated that the infecting organism most closely resembled L.kirschneri. In an effort to determine the specific Leptospira serovar and strain, dolphin kidney was cultured for growth of Leptospira spp. In brief, tissue was macerated using a Micro-Biomaster Stomacher-80 (Seward Inc., Port St Lucie, FL) with 10 mL of 7.2 pH phosphate buffered saline. The homogenate was filtered through a 0.4 µm filter. The filtrate was inoculated into the Leptospira semi-solid (modified EMJH) growth media [48]. A 1:10 dilution of the filtrate in liquid Leptospira media (modified EMJH) was also inoculated in the Leptospira semi-solid media. The cultures were incubated at 28–29 degrees C for 2 months. Cultures were visually inspected weekly for growth/Dinger zone, but no growth was observed.

To enable genomic level species identification and phylogenetic analyses, DNA extracted from the Leptospira positive kidney sample (BLH0012) was subjected to pan pathogenic Leptospira DNA capture and enrichment as described in detail elsewhere [49]. Briefly, the sample DNA was diluted to 4 ng/µL in a volume of 40µL, sonicated to an average size of 290 bp using a Q800R2 sonicator (QSonica, Newtown, CT, USA), and a short-read next-generation library was prepared using Agilent Sure-Select methodology. The library was then subjected to two rounds of DNA capture and enrichment and then sequenced on an Illumina MiSeq using a MiSeq Reagent Nano Kit v2 500 cycle kit (2 × 250).

Kidney samples from 18 additional dolphins from the Southern California Bight were submitted for PCR and all were negative. These samples were from long-beaked common dolphins (Delphinus delphis bairdii; n = 11) and short-beaked common dolphins (n = 7) collected between the years 2002—2019.

Bioinformatic methods

To estimate the percentage of Leptospira reads in the enriched sequences, reads were mapped against the standard Kraken database with Kraken v2.1.2 [50]. Reads assigned as Leptospira were then extracted and assembled using SPAdes v3.13.0 [51] with default settings. The BLH0012 assembly was placed into a genus dendrogram with Mashtree v1.2.0 [52] to confirm species membership. The large scale Blast Score Ratio (LS-BSR) tool v1.2.3 was used to identify a set of 131 DNA capture and enrichment probes that had a blast score ratio (BSR) value [53] of ≥ 0.8 in 35 L.kirschneri genomes and < 0.4 in other Leptospira genomes (n = 620). Reads from the short-beaked common dolphin Leptospira enriched genome (BLH0012) were mapped against these probes and the breadth of coverage was calculated at 3 × depth. Single nucleotide polymorphisms (SNPs) were identified among the BLH0012 enriched genome and 41 publicly available L.kirschneri genomes (GenBank accession numbers annotated in Fig. 3) by aligning reads simulated by ART vMountRainier [54] against L.kirschneri serovar Valbuzzi str. 200,702,274 (GCA_000244515.3) with minimap2 v2.22 [55] and calling SNPs from the BAM file with GATK v4.2.2 [56] using a depth of coverage ≥ 5 × and a read proportion of 0.9. All of these methods were wrapped by NASP v1.20 [57]. A maximum likelihood phylogeny was then inferred on the concatenated SNP alignments using IQ-TREE v2.2.0.3 with default parameters [58] (Minh et al. 2020), and the integrated ModelFinder method [59]; the phylogeny was rooted with L.santarosai strain LT821 (GenBank assembly accession: GCA_000313175.2). To explore the possibility that the Leptospira lineage present in this sample has been described previously but perhaps without genomic level resolution, we queried our assembly against the Leptospira pubMLST database [60], which contained 217,925 Leptospira allele sequences on the date of access [61].

Fig. 3
figure 3

Whole-genome dendrogram of Leptospira genomes, showing dolphin sequence BLH0012 within a clade of L. kirschneri isolates. The dendrogram includes representative genomes of 63 Leptospira species from the P1, P2, S1 and S2 clades. [6], three L. interrogans serovar Pomona genomes derived from isolates obtained from two California sea lions and a Channel Island fox (Urocyon littoralis), and the enriched Leptospira genome assembly from sample BLH0012 (in red)

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Phylogenetic results

Post enrichment, 81.45% of the BLH0012 sequencing reads assigned to Leptospira (1,323,517/1,624,860). The whole genome dendrogram, which included representative genomes of 63 Leptospira species from the P1, P2, S1 and S2 clades [6], three L. interrogans serovar Pomona genomes derived from isolates obtained from California sea lions and a Channel Island fox (Urocyon littoralis), and the enriched Leptospira genome assembly from the dolphin kidney sample, BLH0012, placed it closest to L.kirschneri (Fig. 3). Of 131 likely L.kirschneri-specific 120bp RNA capture probes that were included in our enrichment system, 87 were identified in the BLH0012 enrichment with ≥ 3 × coverage, providing further supporting evidence that this unknown Leptospira is most similar to L.kirschneri and falls within the phylogenetic clade of that species [62].

To more definitively assess the relationship of BLH0012 within L.kirschneri, we constructed a whole genome SNP phylogeny using the BLH0012 genome and 41 publicly-available L.kirschneri genomes previously generated from isolates. This analysis clearly placed the BLH0012 genome among the L.kirschneri genomes, confirming the species identification. However, the long branch length leading to the BLH0012 genome (7892 unique SNPs; Fig. 4) suggests it is the first representative of a previously undescribed novel lineage within L.kirschneri. In support of this conjecture, our query of the enriched BLH0012 assembly against all Leptospira loci in pubMLST revealed the closest allelic matches were to L.kirschneri but no perfect matches to any known Leptospira alleles at any locus; 6/7 loci were identified from both Leptospira MLST scheme 1 (tpiA was absent) [63] and scheme 3 (rrs was excluded in the bait design) [49, 64], and 7/7 loci were identified from scheme 2 [65]. Overall, our analyses of the Leptospira genome enriched from dolphin kidney sample BLH0012 suggest it represents a previously undescribed, divergent and novel lineage of L.kirschneri.

Fig. 4
figure 4

Phylogeny of L. kirschneri genomes, showing that the BLH0012 genome represents a divergent lineage of L. kirschneri. This whole genome SNP phylogeny included BLH0012 Leptospira sequences (in red) and 41 L. kirschneri genomes. The dolphin sequence falls among the L. kirschneri genomes, with long branch length (7893 unique SNPs) suggesting that it is a divergent lineage

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Discussion and conclusions

We report the first detection and characterization of Leptospira infection in a short-beaked common dolphin and the first detection of Leptospira in any cetacean from the northeastern Pacific Ocean. Renal lesions identified on histopathology of samples from this dolphin were consistent with clinically significant leptospirosis in other host species, including marine mammals [2, 4, 18, 19, 27, 31,32,33,34, 66]. These lesions were the most significant lesions detected, suggesting that leptospirosis most likely played a significant role in live stranding and eventual death. We identified the isolate as belonging to a divergent, previously undescribed lineage of L.kirschneri, a species that has been detected only once in the northeastern Pacific (or in any marine host): from a single northern elephant seal stranded in northern California in 2004 [31]. Although antibody reactivity against L.kirschneri serovar Grippotyphosa has been detected via microscopic agglutination testing (MAT) in a number of marine mammals from the northeastern Pacific, including Pacific harbor seals, California sea lions, and northern elephant seals [32, 33, 36, 37], titers against other Leptospira species and serovars were typically also observed in the same individuals. Thus, the MAT cannot be used to definitively identify the infecting species or serovar as Leptospira antibody cross-reaction is common [67,68,69] and not all Leptospira species are included in MAT panels. Exposure to unknown species of Leptospira has also been detected via MAT in sea otters [66, 70,71,72].

Infection with L.kirschneri distinguishes this case from other observations of Leptospira infections in marine mammals of the northeast Pacific Ocean. L. interrogans serovar Pomona has caused yearly, seasonal outbreaks in California sea lions for decades, with infections ranging from subclinical to deadly [26, 27, 25, 28,29,30, 73, 74]. Confirmed infections with L. interrogans serovar Pomona have also been detected by culture in northern elephant seals [37] and northern fur seals [34, 35], and by PCR in a Steller sea lion [31]. The different species of Leptospira indicates there is no direct connection between these observations of Leptospira in marine mammals in the northeastern Pacific, but it is important to note that sampling and testing have been limited. Further Leptospira surveillance of marine mammals, including of short-beaked common dolphins, is needed to identify other hosts carrying closely related strains of L.kirschneri, which would indicate potential intra- or interspecies transmission linkages and the host range for this novel lineage of L.kirschneri. It is also possible that the dolphin was infected by cross-ecosystem spillover transmission from a terrestrial host [75, 76]; L.kirschneri has been detected in a range of terrestrial hosts, including rodents, horses, cattle, dogs, humans and wild boar [77,78,79,80,81,82,83,84,85,86,87,88,89,90,91].

Confirmed infection of a cetacean raises interesting questions about the mechanism of transmission, given the obligate marine lifestyle of cetaceans (in contrast to pinnipeds, which spend time on land) and the commonly accepted view that Leptospira are quickly killed by salt water. If there is intraspecies transmission among short-beaked common dolphins, it could be occurring via vertical or sexual transmission, preventing exposure to salt water. In this case, sexual transmission is unlikely given the age of the dolphin; however vertical transmission may have occurred as it was likely still nursing. Expanded surveillance and testing in this species would be needed to assess whether infection prevalence, age distribution, and tissue distribution are consistent with this possibility. If transmission occurred via the environment, whether from another marine host (of the same or a different species) or cross-ecosystem spillover from a terrestrial host, the pathogen would need to survive for some period in sea water. However, Leptospira are generally understood to survive poorly in salt water [21, 23, 24]. Some researchers have reported halophilic or halotolerant pathogenic Leptospira species; yet in all of these cases isolates were cultured in nutrient rich media of varying salinity which was often less than that of sea water [40, 41, 92]. In addition, work by Trueba et al. [24] suggests that the inhibitory impacts of salinity are most important under starvation conditions (i.e., what would be experienced in the ocean), hence in the absence of nutrient rich media the reported halotolerant and halophilic species are unlikely to survive long. Finally, Saito et al. [93] showed that isolates of the pathogenic species L.kmetyi were killed within 12 h in 3% NaCl solution (i.e., the same salinity of the ocean), but were able to survive 3–4 days if incubated with soil overnight. These data, together with considerations of rapid dilution in circulating ocean water, suggest that the window of opportunity for environmental transmission would be quite short for dolphins, and would be more likely in coastal species such as bottlenose dolphins. However, under certain optimal conditions (large aggregations of animals, or behaviors involving particularly close contact with urine) intraspecific environmental transmission might occur in marine settings. This could have implications for understanding Leptospira ecology in pinnipeds as well, where transmission has broadly been assumed to occur while animals are hauled out on land.

Ultimately, to better understand the extent to which Leptospira infections occur in the marine ecosystem and the epidemiological linkages between and among marine and terrestrial host species, surveillance and sampling must be expanded across these ecosystems. Sequencing of Leptospira genomes from different host species will yield crucial information about possible transmission links, either through sequencing of isolates obtained via culture of prospective samples, or by application of DNA enrichment techniques to both banked and prospectively collected samples that test positive by PCR. The advent of these new techniques ushers in a new era for understanding and untangling the complex ecology and transmission of this important zoonotic pathogen.

Availability of data and materials

Sequence data for sample BLH0012 was deposited under BioProject PRJNA1029025; https://www.ncbi.nlm.nih.gov/bioproject/PRJNA1029025.

Abbreviations

BSR:

Blast score ratio

DNA :

Deoxyribonucleic acid

EMJH:

Ellinghausen–McCullough–Johnson–Harris

H&E:

Hematoxylin and eosin

IHC:

Immunohistochemistry

LS-BSR:

Large scale BSR

MAT:

Microscopic agglutination testing

MLST:

Multilocus sequence typing

PCR:

Polymerase chain reaction

SNP:

Single nucleotide polymorphism

References

  1. Faine S, Adler B, Bolin C, Perolat P. Leptospira and leptospirosis. 2nd ed. Melbourne: MediSci; 1999.

    Google Scholar 

  2. Zuerner RL. Host Response to Leptospira Infection. In: Adler B, editor. Leptospira and Leptospirosis. Berlin, Heidelberg: Springer Berlin Heidelberg; 2015. p. 223–50.

    Chapter  Google Scholar 

  3. Wunder EA, Eshghi A, Benaroudj N. Editorial: pathogenesis of leptospira. Front Cell Infect Microbiol. 2018;8:223.

    Article  Google Scholar 

  4. Ellis WA. Animal Leptospirosis. In: Adler B, editor. Current Topics in Microbiology and Immunology: Leptospira and Leptospirosis. Verlag Berlin Heidelberg: Springer; 2015. p. 99–137.

  5. Sykes JE, Reagan KL, Nally JE, Galloway RL, Haake DA. Role of diagnostics in epidemiology, management, surveillance, and control of leptospirosis. Pathogens. 2022;11(4):395.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Vincent AT, Schiettekatte O, Goarant C, Neela VK, Bernet E, Thibeaux R, et al. Revisiting the taxonomy and evolution of pathogenicity of the genus Leptospira through the prism of genomics. PLoS Negl Trop Dis. 2019;13(5):e0007270.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Lynch MJ, Deshpande M, Kyrniyati K, Zhang K, James M, Miller M, et al. Lysinoalanine crosslinking is a conserved post-translational modification in the spirochete flagellar hook. bioRxiv. 2023;2023.06.13.544825.

  8. Fernandes LGV, Stone NE, Roe CC, Goris MGA, Van Der Linden H, Sahl JW, et al. Leptospira sanjuanensis sp. nov., a pathogenic species of the genus Leptospira isolated from soil in Puerto Rico. Int J Syst Evol Microbiol. 2022;72(10). Available from:https://www.microbiologyresearch.org/content/journal/ijsem/10.1099/ijsem.0.005560. Cited 2023 Sep 18.

  9. Verma A, Brandt L, Runser S, Gruszynski K, Gallatin K, Morgan J, et al. Detection of pathogenic Leptospira spp. in herpetofauna in Central Appalachia. Zoonoses and Public Health. 2022. Available from: https://onlinelibrary.wiley.com/doi/full/10.1111/zph.12921.

  10. Rockwell KE, Thompson D, Maddox C, Mitchell MA. Blanding’s turtles (Emydoidea blandingii) as a reservoir for Leptospira spp. bioRxiv. 2019;14:510149.

    Google Scholar 

  11. Rodamilans GM, Fonseca MS, Paz LN, Fernandez CC, Biondi I, Lira-da-Silva RM, et al. Leptospira interrogans in wild Boa constrictor snakes from Northeast Brazil peri-urban rainforest fragments. Acta Trop. 2020;209:105572–105572.

    Article  CAS  PubMed  Google Scholar 

  12. Pérez-Flores J, López-Fernández O, Atilano D, García-Besné G, Charruau P. Serum antileptospiral agglutinins in sea turtles (Eretmochelys imbricata and Chelonia mydas) from the Gulf of Mexico. JHMS. 2021;30(4):270–6.

    Google Scholar 

  13. Glosser JW, Sulzer CR, Eberhardt M, Winkler WG. Cultural and serologic evidence of Leptospira interrogans serotype Tarassovi infection in turtles. J Wildl Dis. 1974;10(4):429–35.

    Article  CAS  PubMed  Google Scholar 

  14. Diesch SL, McCulloch WF, Braun JL, Ellinghausen HC. Leptospires isolated from frog kidneys. Nature. 1966;209(5026):939–40.

    Article  CAS  PubMed  Google Scholar 

  15. Gravekamp C, Korver H, Montgomery J, Everard CO, Carrington D, Ellis WA, et al. Leptospires isolated from toads and frogs on the Island of Barbados. Zentralbl Bakteriol. 1991;275(3):403–11.

    Article  CAS  PubMed  Google Scholar 

  16. Biscola NP, Fornazari F, Saad E, Richini-Pereira VB, Campagner MV, Langoni H, et al. Serological investigation and PCR in detection of pathogenic leptospires in snakes. Pesquisa Vet Brasil. 2011;31(9):806–11.

    Article  Google Scholar 

  17. Adler B. Leptospira and leptospirosis. 1st ed. Berlin Heidelberg: Springer-Verlag; 2015. p. 293 p (Current Topics in Microbiology and Immunology).

    Book  Google Scholar 

  18. Haake DA, Levett PN. Leptospirosis in Humans. In: Leptospira and Leptospirosis. Springer; 2015. p. 65–97.

    Chapter  Google Scholar 

  19. Haake DA, Zückert WR. The leptospiral outer membrane. Curr Top Microbiol Immunol. 2015;387:187–221.

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Gostic KM, Wunder EA, Bisht V, Hamond C, Julian TR, Ko AI, et al. Mechanistic dose–response modelling of animal challenge data shows that intact skin is a crucial barrier to leptospiral infection. Philos Trans R Soc Lond B Biol Sci. 2019;374(1782):20190367.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Bierque E, Thibeaux R, Girault D, Soupé-Gilbert ME, Goarant C. A systematic review of Leptospira in water and soil environments. PLoS One. 2020;15(1):e0227055–e0227055.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Casanovas-Massana A, Costa F, Riediger IN, Cunha M, de Oliveira D, Mota DC, et al. Spatial and temporal dynamics of pathogenic Leptospira in surface waters from the urban slum environment. Water Research. 2018;130:176–84.

  23. Khairani-Bejo S, Bahaman AR, Zamri-Saad M, Mutalib AR. The Survival of Leptospira interrogans Serovar Hardjo in the Malaysian Environment. J Anim Vet Adv. 2004;3:123–9.

    Google Scholar 

  24. Trueba G, Zapata S, Madrid K, Cullen P, Haake D. Cell aggregation: a mechanism of pathogenic Leptospira to survive in fresh water. Int Microbiol. 2004;7(1):35–40.

    PubMed  Google Scholar 

  25. Prager KC, Buhnerkempe MG, Greig DJ, Orr AJ, Jensen ED, Gomez F, et al. Linking longitudinal and cross-sectional biomarker data to understand host-pathogen dynamics: Leptospira in California sea lions (Zalophus californianus) as a case study. PLoS Negl Trop Dis. 2020;14(6):e0008407.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Lloyd-Smith JO, Greig DJ, Hietala S, Ghneim GS, Palmer L, St Leger J, et al. Cyclical changes in seroprevalence of leptospirosis in California sea lions: endemic and epidemic disease in one host species? BMC Infect Dis. 2007;7:125–36.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Gulland FMD, Koski M, Lowenstine LJ, Colagross A, Morgan L, Spraker T. Leptospirosis in California sea lions (Zalophus californianus) stranded along the central California coast, 1981–1994. J Wildl Dis. 1996;32(4):572–80.

    Article  CAS  PubMed  Google Scholar 

  28. Zuerner RL, Alt DP. Variable Nucleotide Tandem-Repeat analysis revealing a unique group of Leptospira interrogans serovar Pomona isolates associated with California sea lions. J Clin Microbiol. 2009;47(4):1202–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Zuerner RL, Cameron CE, Raverty S, Robinson J, Colegrove KM, Norman SA, et al. Geographical dissemination of Leptospira interrogans serovar Pomona during seasonal migration of California sea lions. Vet Microbiol. 2009;137(1–2):105–10.

    Article  PubMed  Google Scholar 

  30. Greig DJ, Gulland FMD, Kreuder C. A decade of live California sea lion (Zalophus califorianus) strandings along the central California coast: causes and trends, 1991–2000. Aquat Mamm. 2005;33(1):11–22.

    Article  Google Scholar 

  31. Cameron CE, Zuerner RL, Raverty S, Colegrove KA, Norman SA, Lamboum DM, et al. Detection of pathogenic Leptospira bacteria in pinniped populations via PCR and identification of a source of transmission for zoonotic leptospirosis in the marine environment. J Clin Microbiol. 2008;46(5):1728–33.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Stamper MA, Gulland FMD, Spraker T. Leptospirosis in rehabilitated Pacific harbor seals from California. J Wildl Dis. 1998;34(2):407–10.

    Article  CAS  PubMed  Google Scholar 

  33. Colegrove KM, Lowenstine LJ, Gulland FM. Leptospirosis in northern elephant seals (Mirounga angustirostris) stranded along the California coast. J Wildl Dis. 2005;41(2):426–30.

    Article  PubMed  Google Scholar 

  34. Smith AW, Brown RJ, Skilling DE, Bray HL, Keyes MC. Naturally-occurring leptospirosis in northern fur seals (Callorhinus ursinus). J Wildl Dis. 1977;13(2):144–8.

    Article  CAS  PubMed  Google Scholar 

  35. Smith AW, Prato CM, Gilmartin WG, Brown RJ, Keyes MC. A preliminary report on potentially pathogenic microbiological agents recently isolated from pinnipeds. J Wildl Dis. 1974;10(1):54–9.

    Article  CAS  PubMed  Google Scholar 

  36. Greig DJ, Gulland FMD, Smith WA, Conrad PA, Field CL, Fleetwood M, et al. Surveillance for zoonotic and selected pathogens in harbor seals Phoca vitulina from central California. Dis Aquat Org. 2014;111(2):93–106.

    Article  Google Scholar 

  37. Delaney MA, Colegrove KM, Spraker TR, Zuerner RL, Galloway RL, Gulland FMD. Isolation of Leptospira from a phocid: acute renal failure and mortality from leptospirosis in rehabilitated Northern elephant seals (Mirounga angustirostris), California, USA. J Wildlife Dis. 2014;50(3):621–7.

    Article  Google Scholar 

  38. Delgado PM, Perea NS, Garcia CB, Davila CRG. Detection of infection with Leptospira spp. in manatees (Trichechus inunguis) of the Peruvian Amazon. LAJAM. 2015;10(1):58–61.

    Article  Google Scholar 

  39. Sepúlveda MA, Seguel M, Alvarado-Rybak M, Verdugo C, Muñoz-Zanzi C, Tamayo R. Postmortem Findings in Four South American Sea Lions (Otaria byronia) from an Urban Colony in Valdivia. Chile Journal of Wildlife Diseases. 2015;51(1):279–82.

    Article  PubMed  Google Scholar 

  40. Obusan MCM, Villanueva RMD, Siringan MAT, Rivera WL, Aragones LV. Leptospira spp. and Toxoplasma gondii in stranded representatives of wild cetaceans in the Philippines. BMC Vet Res. 2019;15(1):372–372.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Grune Loffler S, Rago V, Martínez M, Uhart M, Florin-Christensen M, Romero G, et al. Isolation of a seawater tolerant Leptospira spp. from a Southern right whale (Eubalaena australis). Plos One. 2015;10(12):e0144974.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Piredda I, Palmas B, Noworol M, Tola S, Longheu C, Bertasio C, et al. Isolation of Leptospira interrogans from a Bottlenose Dolphin (Tursiops truncatus) in the Mediterranean Sea. J Wildl Dis. 2020. Available from: https://doi.org/10.7589/2019-07-186.

  43. Torres FD, Borges ALDSB, Castilho PVD, Kolesnikovas C, Domit C, Dos Santos J, et al. Molecular detection of pathogenic leptospira sp. in Cetaceans from the Brazilian Coast. Bach H, editor. Transbound Emerg Dis. 2023;2023:1–8.

    Article  Google Scholar 

  44. Joblon MJ, Pokras MA, Morse B, Harry CT, Rose KS, Sharp SM, et al. Body Condition Scoring System for Delphinids Based on Short-beaked Common Dolphins (Delphinus delphis). Journal of Marine Animals and Their Ecology. 2014;7(2):5–13.

  45. Danil K, Chivers SJ. Growth and reproduction of female short-beaked common dolphins, Delphinus delphis, in the eastern tropical Pacific. Can J Zool. 2007;85(1):108–21.

    Article  Google Scholar 

  46. Ferreira AS, Costa P, Rocha T, Amaro A, Vieira ML, Ahmed A, et al. Direct Detection and Differentiation of Pathogenic Leptospira Species Using a Multi-Gene Targeted Real Time PCR Approach. PLoS ONE. 2014;9(11):e112312.

    Article  PubMed  PubMed Central  Google Scholar 

  47. Merien F, Portnoi D, Bourhy P, Charavay F, Berlioz-Arthaud A, Baranton G. A rapid and quantitative method for the detection of Leptospira species in human leptospirosis. FEMS Microbiol Lett. 2005;249(1):139–47.

    Article  CAS  PubMed  Google Scholar 

  48. Greenlee JJ, Alt DP, Bolin CA, Zuerner RL, Andreasen CB. Experimental canine leptospirosis caused by Leptospira interrogans serovars pomona and bratislava. Am J Vet Res. 2005;66(10):1816–22.

    Article  PubMed  Google Scholar 

  49. Stone NE, McDonough RF, Hamond C, LeCount K, Busch JD, Dirsmith KL, et al. DNA capture and enrichment: a culture-independent approach for characterizing the genomic diversity of pathogenic Leptospira species. Microorganisms. 2023;11(5):1282.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Wood DE, Lu J, Langmead B. Improved metagenomic analysis with Kraken 2. Genome Biol. 2019;20(1):257.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19(5):455–77.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Katz LS, Griswold T, Morrison SS, Caravas JA, Zhang S, den Bakker HC, et al. Mashtree: a rapid comparison of whole genome sequence files. J Open Source Softw. 2019;4(44):1–6.

  53. Rasko DA, Myers GSA, Ravel J. Visualization of comparative genomic analyses by BLAST score ratio. BMC Bioinformatics. 2005;5(6):2.

    Article  Google Scholar 

  54. Huang W, Li L, Myers JR, Marth GT. ART: a next-generation sequencing read simulator. Bioinformatics. 2012;28(4):593–4.

    Article  PubMed  Google Scholar 

  55. Li H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics. 2018;34(18):3094–100.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010;20(9):1297–303.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Sahl JW, Lemmer D, Travis J, Schupp JM, Gillece JD, Aziz M, et al. NASP: an accurate, rapid method for the identification of SNPs in WGS datasets that supports flexible input and output formats. Microb Genom. 2016;2(8):e000074.

    PubMed  PubMed Central  Google Scholar 

  58. Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, von Haeseler A, et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol. 2020;37(5):1530–4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods. 2017;14(6):587–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Jolley KA, Bray JE, Maiden MCJ. Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications. Wellcome Open Res. 2018;3:124.

    Article  PubMed  PubMed Central  Google Scholar 

  61. Leptospira spp. PubMLST. https://pubmlst.org/organisms/leptospira-spp. Accessed 3 June 2022.

  62. Wagner DM, Birdsell DN, McDonough RF, Nottingham R, Kocos K, Celona K, et al. Genomic characterization of Francisella tularensis and other diverse Francisella species from complex samples. PLoS ONE. 2022;17(10):e0273273.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Boonsilp S, Thaipadungpanit J, Amornchai P, Wuthiekanun V, Bailey MS, Holden MTG, et al. A Single Multilocus Sequence Typing (MLST) Scheme for Seven Pathogenic Leptospira Species. PLoS Negl Trop Dis. 2013;7(1):e1954.

    Article  PubMed  PubMed Central  Google Scholar 

  64. Ahmed N, Devi SM, De los Á Valverde M, Vijayachari P, Machang’u RS, Ellis WA, et al. Multilocus sequence typing method for identification and genotypic classification of pathogenic Leptospira species. Ann Clin Microbiol Antimicrob. 2006;5:28.

    Article  PubMed  PubMed Central  Google Scholar 

  65. Varni V, Ruybal P, Lauthier JJ, Tomasini N, Brihuega B, Koval A, et al. Reassessment of MLST schemes for Leptospira spp. typing worldwide. Infect Genet Evol. 2014;22:216–22.

  66. Knowles S, Lynch D, Thomas N. Leptospirosis in Northern Sea Otters (Enhydra lutris kenyoni) from Washington. USA jwdi. 2020;56(2):466–71.

    Article  CAS  Google Scholar 

  67. Levett PN. Usefulness of serologic analysis as a predictor of the infecting serovar in patients with severe leptospirosis. Clin Infect Dis. 2003;36(4):447–52.

    Article  PubMed  Google Scholar 

  68. Smythe LD, Wuthiekanun V, Chierakul W, Suputtamongkol Y, Tiengrim S, Dohnt MF, et al. The Microscopic Agglutination Test (MAT) Is an Unreliable Predictor of Infecting Leptospira Serovar in Thailand. Am J Trop Med Hyg. 2009;81(4):695–7.

    Article  PubMed  Google Scholar 

  69. Murray CK, Gray MR, Mende K, Parker TM, Samir A, Rahman BA, et al. Use of patient-specific Leptospira isolates in the diagnosis of leptospirosis employing microscopic agglutination testing (MAT). Trans R Soc Trop Med Hyg. 2011;105(4):209–13.

    Article  PubMed  Google Scholar 

  70. Hanni KD, Mazet JAK, Gulland FMD, Estes J, Staedler M, Murray MJ, et al. Clinical pathology and assessment of pathogen exposure in southern and Alaskan sea otters. J Wildl Dis. 2003;39(4):837–50.

    Article  PubMed  Google Scholar 

  71. White CL, Lankau EW, Lynch D, Knowles S, Schuler KL, Dubey JP, et al. Mortality trends in northern sea otters (Enhydra lutris kenyoni) collected from the coasts of Washington and Oregon (2002–15). J Wildl Dis. 2018;54(2):238–47.

  72. Goldstein T, Gill VA, Tuomi P, Monson D, Burdin A, Conrad PA, et al. Assessment of clinical pathology and pathgen exposure in sea otters (Enhydra lutris) bordering the threatened population in Alaska. J Wildl Dis. 2011;47(3):579–92.

    Article  PubMed  Google Scholar 

  73. Prager KC, Greig DJ, Alt DP, Galloway RL, Hornsby RL, Palmer LJ, et al. Asymptomatic and chronic carriage of Leptospira interrogans serovar Pomona in California sea lions (Zalophus californianus). Vet Microbiol. 2013;164(1–2):177–83.

    Article  CAS  PubMed  Google Scholar 

  74. Buhnerkempe MG, Prager KC, Strelioff CC, Greig DJ, Laake JL, Melin SR, et al. Detecting signals of chronic shedding to explain pathogen persistence: Leptospira interrogans in California sea lions. J Anim Ecol. 2017;86(3):460–72.

    Article  PubMed  PubMed Central  Google Scholar 

  75. Borremans B, Faust C, Manlove KR, Sokolow SH, Lloyd-Smith JO. Cross-species pathogen spillover across ecosystem boundaries: mechanisms and theory. Philos Trans R Soc Lond B Biol Sci. 2019;374(1782):20180344.

    Article  PubMed  PubMed Central  Google Scholar 

  76. Helman SK, Tokuyama AFN, Mummah RO, Stone NE, Gamble MW, Snedden CE, et al. Pathogenic Leptospira are widespread in the urban wildlife of southern California. Sci Rep. 2023;13(1):14368.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Schmidt E, Obiegala A, Imholt C, Drewes S, Saathoff M, Freise J, et al. Influence of Season, Population and Individual Characteristics on the Prevalence of Leptospira spp. in Bank Voles in North-West Germany. Biology-Basel. 2021;10(9):1–19.

  78. Guyader ML, Fontana C, Simon-Dufay N, Balzer HJ, Pantchev N, Thibault JC, et al. Successful Leptospira genotyping strategy on DNA extracted from canine biological samples. J Microbiol Methods. 2020;176:1–5.

  79. Harkin KR, Hays MP. Variable-number tandem-repeat analysis of leptospiral DNA isolated from canine urine samples molecularly confirmed to contain pathogenic leptospires. Javma-Journal of the American Veterinary Medical Association. 2016;249(4):399–405.

    Article  CAS  PubMed  Google Scholar 

  80. Halliday JEB, Knobel DL, Allan KJ, Bronsvoort B Mark de C, Handel I, Agwanda B, et al. Urban Leptospirosis in Africa: a cross-sectional survey of Leptospira infection in rodents in the kibera urban settlement, Nairobi, Kenya. Am J Trop Med Hyg. 2013;89(6):1095–102.

    Article  PubMed  PubMed Central  Google Scholar 

  81. Azhari NN, Ramli SNA, Joseph N, Philip N, Mustapha NF, Ishak SN, et al. Molecular characterization of pathogenic Leptospira sp in small mammals captured from the human leptospirosis suspected areas of Selangor state. Malaysia Acta Tropica. 2018;188:68–77.

    Article  PubMed  Google Scholar 

  82. Allan KJ, Biggs HM, Halliday JEB, Kazwala RR, Maro VP, Cleaveland S, et al. Epidemiology of Leptospirosis in Africa: A Systematic Review of a Neglected Zoonosis and a Paradigm for ‘One Health’ in Africa. PLoS Negl Trop Dis. 2015;9(9):e0003899.

    Article  PubMed  PubMed Central  Google Scholar 

  83. Philip N, Bahtiar Affendy N, Ramli SNA, Arif M, Raja P, Nagandran E, et al. Leptospira interrogans and Leptospira kirschneri are the dominant Leptospira species causing human leptospirosis in Central Malaysia. PLoS Negl Trop Dis. 2020;14(3):e0008197.

    Article  PubMed  PubMed Central  Google Scholar 

  84. Soares PM, Gomes DO, Macedo FP, Soares MM, Lemes KR, Jaeger LH, et al. Serological and molecular characterization of Leptospira kirschneri serogroup Grippotyphosa isolated from bovine in Brazil. Microbial Pathogenesis. 2020;138.

  85. Iverson SA, Levy C, Yaglom HD, Venkat HL, Artus A, Galloway R, et al. Clinical, diagnostic, and epidemiological features of a community-wide outbreak of canine leptospirosis in a low-prevalence region (Maricopa County, Arizona). J Am Vet Med Assoc. 2021;258(6):616–29.

    Article  PubMed  PubMed Central  Google Scholar 

  86. Guedes IB, de Souza GO, Rocha K de S, Cavalini MB, Damasceno Neto MS, de Paula Castro JF, et al. Leptospira strains isolated from cattle in the Amazon region, Brazil, evidence of a variety of species and serogroups with a high frequency of the Sejroe serogroup. Comp Immunol Microbiol Infect Dis. 2021;74:1–5.

  87. Salaun L, Merien F, Gurianova S, Baranton G, Picardeau M. Application of multilocus variable-number tandem-repeat analysis for molecular typing of the agent of leptospirosis. J Clin Microbiol. 2006;44(11):3954–62.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Jaeger LH, Moreno LZ, Kremer FS, Dellagostin OA, Moreno AM, Lilenbaum W. Genomic characterization and comparative analysis of Leptospira kirschneri serogroup Grippotyphosa UC5/2011, a strain isolated after mare abortion: Implications for genital animal leptospirosis. Comp Immunol Microbiol Infect Dis. 2019;64:7–9.

    Article  PubMed  Google Scholar 

  89. Masuzawa T, Okamoto Y, Une Y, Takeuchi T, Tsukagoshi K, Koizumi N, et al. Leptospirosis in Squirrels Imported from United States to Japan. Emerg Infect Dis. 2006;12(7). Available from: https://wwwnc.cdc.gov/eid/article/12/7/06-0370_article. Cited 2022 Mar 30.

  90. Cilia G, Bertelloni F, Piredda I, Ponti MN, Turchi B, Cantile C, et al. Presence of pathogenic Leptospira spp. in the reproductive system and fetuses of wild boars (Sus scrofa) in Italy. PLoS Negl Trop Dis. 2020;14(12):e0008982.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Morgan J, Bornstein SL, Karpati AM, Bruce M, Bolin CA, Austin CC, et al. Outbreak of Leptospirosis among Triathlon Participants and Community Residents in Springfield, Illinois, 1998. Clin Infect Dis. 2002;34(12):1593–9.

    Article  PubMed  Google Scholar 

  92. Cilia G, Fratini F, della Buona E, Bertelloni F. Preliminary evaluation of in vitro bacteriostatic and bactericidal effect of salt on Leptospira spp. Vet Sci. 2020;7(4):154.

    Article  PubMed  PubMed Central  Google Scholar 

  93. Saito M, Miyahara S, Villanueva SYAM, Aramaki N, Ikejiri M, Kobayashi Y, et al. PCR and culture identification of pathogenic Leptospira spp. from coastal soil in Leyte, Philippines, after a storm surge during super typhoon Haiyan (Yolanda). Appl Environ Microbiol. 2014;80(22):6926–32.

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Acknowledgements

We would like to acknowledge Erin La Casella and Brittany Hanser for stranding response support, Sarah Helman for her feedback and review of the manuscript. Mike Garner, David Gasper and Judy St. Leger served as the histopathologists for cases that were selected for retrospective PCR testing of cetacean kidneys.

Funding

K.C.P. and J.O.L.-S. were supported by the US National Science Foundation (DEB-1557022) and US Cooperative Ecosystem Studies Unit (Cooperative Agreement W9132T1920006). K.C.P. was supported by the John H. Prescott Marine Mammal Rescue Assistance Grant Program (NA23NMF4390341) and US Fish and Wildlife Service American Rescue Plan Act Zoonotic Disease Initiative (F23AP00118-00).

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Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, University of California Los Angeles, Los Angeles, CA, 90095, USA

    K. C. Prager & James O. Lloyd-Smith

  2. Southwest Fisheries Science Center, National Marine Fisheries Service, NOAA, La Jolla, CA, 92037, USA

    Kerri Danil

  3. Ocean Associates Inc. Under Contract to Southwest Fisheries Science Center, National Marine Fisheries Service, NOAA, La Jolla, CA, 92037, USA

    Elyse Wurster

  4. Zoological Pathology Program, University of Illinois College of Veterinary Medicine, 3300 Golf Rd, Brookfield, IL, 60513, USA

    Kathleen M. Colegrove

  5. National Center for Emerging and Zoonotic Infectious Diseases, Centers for Diseases Control and Prevention, Atlanta, GA, 30333, USA

    Renee Galloway

  6. Veterinary Diagnostic Laboratory, College of Veterinary Medicine, Michigan State University, East Lansing, Michigan, 48825, USA

    Niesa Kettler & Rinosh Mani

  7. The Pathogen and Microbiome Institute, Northern Arizona University, Flagstaff, AZ, 86011, USA

    Ryelan F. McDonough, Jason W. Sahl, Nathan E. Stone & David M. Wagner

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Contributions

KCP wrote the initial draft of the manuscript. KD and EW conducted gross examination of the dolphin, and provided the tissues. KMC performed the histological examination of the kidney. RG conducted initial PCR of the tissues. NK and RM conducted PCR targeting lfb1 genes and amplicon sequencing. DW and NS conducted gene enrichment and genome sequencing. JWS assembled the Leptospira genome and built the phylogeny. KCP, KD, EW, RG, NK, RFM, JLS, NS and DW contributed to study design, RG, NK and RM contributed to diagnostic approaches, KCP, JLS, RG, NK, RM, NS and DW contributed to interpretation of results. All contributed to writing the manuscript.

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Correspondence to K. C. Prager.

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Prager, K.C., Danil, K., Wurster, E. et al. Detection of Leptospira kirschneri in a short-beaked common dolphin (Delphinus delphis delphis) stranded off the coast of southern California, USA. BMC Vet Res 20, 266 (2024). https://doi.org/10.1186/s12917-024-04111-x

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BMC Veterinary Research

ISSN: 1746-6148

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