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Article

Photobacterium damselae subsp. damselae in Stranded Cetaceans: A 6-Year Monitoring of the Ligurian Sea in Italy

by
Roberta Battistini
1,
Chiara Masotti
1,
Federica Giorda
1,
Carla Grattarola
1,
Simone Peletto
1,
Camilla Testori
1,
Simona Zoppi
1,
Enrica Berio
2,
Maria Ines Crescio
1,
Nicola Pussini
1,
Laura Serracca
1,* and
Cristina Casalone
1
1
Istituto Zooprofilattico Sperimentale del Piemonte, Liguria e Valle d’Aosta, Via Bologna 148, 10154 Torino, Italy
2
ASL 1 Sistema Sanitario Regione Liguria, Via Aurelia Ponente 97, 18038 Sanremo, Italy
*
Author to whom correspondence should be addressed.
Animals 2024, 14(19), 2825; https://doi.org/10.3390/ani14192825
Submission received: 8 August 2024 / Revised: 17 September 2024 / Accepted: 26 September 2024 / Published: 30 September 2024
(This article belongs to the Special Issue Advances in the Pathology and Infectious Diseases of Marine Mammals)
Versions Notes

Abstract

:

Simple Summary

Photobacterium damselae subsp. damselae (Pdd) is a marine bacterium that can infect a variety of marine animals and humans. Although this bacterium has been isolated from several stranded dolphins and whales, its pathogenic role in cetaceans is still unclear and very limited information exists on its occurrence in these animals. In this study, we report data relating to the presence of Pdd in marine mammals stranded within the Liguria Pelagos Sanctuary from 2017 to 2022. Our findings show a 41.5% (22/53) Pdd prevalence in stranded cetaceans, where 22.7% (5/22) of these were positive in at least one of the Pdd virulence factors which, in previous studies, have been related to Pdd pathogenicity. Our results also revealed that in all cases where cetaceans tested positive for Pdd, other well-known pathogens for these species were also present. This finding supports the hypothesis that Pdd is an opportunistic agent that might contribute to the worsening of health conditions in subjects already compromised by other pathogens, contributing to their death. However, further studies are necessary to investigate and deepen this hypothesis.

Abstract

Photobacterium damselae subsp. damselae (Pdd) is an increasingly common bacterium in post-mortem diagnostics of beached marine mammals, but little is known about its precise etiological responsibility. To estimate the prevalence of Pdd in stranded cetaceans from 2017 to 2022 on the Ligurian coast (Pelagos Sanctuary), we tested tissues from 53 stranded individuals belonging to four cetacean species. DNA extracts from cetacean tissue were screened using a polymerase chain reaction (PCR) assay targeting the Pdd ureC gene. Positive samples were screened by PCR for dly, hlyApl and hlyAch hemolysin genes, which were confirmed by sequencing. Twenty-two out of 53 (41.5%) cetaceans analyzed by PCR were confirmed for Pdd DNA in at least one tissue among those analyzed. Five of these cetaceans were positive for at least one of the hemolysin genes tested. In all Pdd-positive cetaceans, other pathogens that were considered responsible for the causa mortis of the animals were also found. The results provide new information on the spread of Pdd in cetaceans and support the thesis that Pdd might be an opportunistic agent that could contribute to worsening health conditions in subjects already compromised by other pathogens. However, further studies are needed to investigate and deepen this hypothesis.

1. Introduction

Photobacterium damselae subsp. damselae (Pdd) is a halophilic gram-negative bacterium within the family Vibrionaceae. Like other Vibrionaceae species, its natural habitat is the aquatic ecosystem [1,2]. Pdd is considered a primary pathogen for a wide range of aquatic species, including molluscs, crustaceans, reptiles, and, more frequently, aquaculture fish [1,3,4,5]. Its role as a minor zoonotic agent, responsible for severe necrotizing fasciitis in humans, is also known [6,7,8]. The pathogenicity of Pdd has been correlated to its ability to produce several virulence proteins, such as hemolysins and histamine, and to the presence of an iron uptake system [9,10]. In particular, it has been reported that hemolytic strains produce a chromosome-encoded hemolysin, named HlyAch, and highly hemolytic strains also harbor the virulence plasmid pPHDD1, which encodes for two other different hemolysins—damselysin (Dly) and HlyApl [10]—and was recently renamed phobalysin (PhlyP) [11]. The entry route of this bacterium in animal species is still poorly investigated. However, there is evidence that the infection is transmitted through water in the presence of skin lesions as a port of entry [1,12]. Pdd can survive in seawater and sediments for a long period, maintaining infectivity and pathogenic properties [13]. New host individuals can be infected through water when temperature and salinity are favorable [12,14,15]. The spread of the disease appears to depend mainly on water temperature; in fact, some reports have associated the presence of Pdd epidemics in fish with unusual increases in water temperature [16,17,18]. Therefore, the occurrence of diseases caused by this pathogen is likely to increase in the future due to the expected increase in seawater temperature resulting from global climate change [19].
In cetaceans, this bacterium has been isolated from healthy and stranded dolphins and whales [20,21], and it is commonly considered an opportunistic agent without a clear explanation of its possible pathogenic role [22]. In recent years, its presence has been more frequently identified in stranded cetaceans of the Mediterranean Sea [22,23,24,25,26]. The increase in infection reports may be due to increased surveillance efforts focused on stranding cetaceans, improved diagnostic approaches, or increased disease prevalence. Understanding the impacts of disease in cetacean populations relies on postmortem diagnosis of disease limited by the small number of carcasses recovered. The occurrence of Pdd in marine mammals remains a poorly understood phenomenon, since very little information exists. In this work, data relating to the presence of Pdd in marine mammals stranded in the Liguria Pelagos Sanctuary from 2017 to 2022 are reported.

2. Materials and Methods

2.1. Samples Collection

Between January 2017 and December 2022, 53 cetaceans were stranded and found dead along the Ligurian coast of Italy. The cetaceans included 37 striped dolphins (Stenella coeruleoalba), 13 bottlenose dolphins (Tursiops truncatus), two Cuvier’s beaked whales (Ziphius cavirostris), and one pilot whale (Globicephala melas). The animals were examined and submitted to complete postmortem examination, routine pathological analysis, and cause-of-death assessment by the Italian National Reference Center for diagnostic activities in stranded marine mammals (C.Re.Di.Ma.) according to standard protocols [27]. Investigations also regarded the presence of relevant pathogens, including bacterial, viral, fungal, protozoan, and helminthic agents. Bacteriological analyses were performed on all main organs onto a non-selective blood-based agar medium (BAB, Liofilchem Italy s.r.l.), and confirmation of grown bacterial species was initially performed by using matrix-assisted laser desorption ionization time-of-flight mass spectrometry (MALDI-TOF MS) according to the manufacturer’s protocol. Specific bacteriological procedures were also applied in order to screen for Listeria spp., Salmonella spp., and Brucella spp. [28]. Carcass recovery information and individual data of each stranded cetacean were also recorded. All these data are available in the annual stranding reports of C.Re.Di.Ma. [29,30,31,32,33,34]. A few cases have also been previously published [35,36,37,38,39,40].
In particular, for Pdd detection, when available, spleen, liver, lymph nodes, lung, kidney, and brain samples were collected during the routine postmortem investigations and submitted for biomolecular analysis in parallel with the bacteriological analysis already described above. The presence of virulence factors was also investigated by biomolecular methods in the cetaceans that tested positive for Pdd in cetaceans. The presence of macro and micro hemorrhagic lesions was also assessed. The procedure for the biomolecular identification of Pdd and virulence factors is described below.

2.2. DNA Extraction

A small portion of each tissue sample (25–30 mg) was added to sterile phosphate buffered saline (pH 7.2) (300 µL) and then physically disrupted on a TissueLyser II homogenizer (Qiagen, Hilden, Germany) by high-speed stirrer in plastic tubes with stainless steel beads (5 mm in diameter). An aliquot of the resulting supernatant (200 μL) from each sample was used to extract DNA using the IndiSpin Pathogen Kit (Indical Bioscience, Leipzig, Germany), as described in the manufacturer’s instructions, and the eluted nucleic acids (100 μL) were stored at −20 °C until use.

2.3. PCR Amplification of Pdd

Genome amplification for the detection of Pdd was performed using a PCR that amplifies a 448 bp fragment of ureC gene [41]. The PCR assays used a reaction solution containing PCR buffer 1× (Invitrogen, Waltham, MA, USA), 2.5 mmol·L–1 MgCl2 (Invitrogen, Waltham, MA, USA), 0.2 mmol·L–1 dNTPs (Sigma-Aldrich, St Louis, MO, USA, 1 µmol·L–1 of primers (Metabion International Ag, Planegg, Germany), 1 U Platinum Taq DNA polymerase (Invitrogen, Waltham, MA, USA), 2 μL of DNA template, and ultra-pure water up to 50 μL. Amplification conditions were as follows: 2 min at 94 °C, 50 cycles of 30 s at 95 °C, 30 s at the primer annealing temperature (65 °C), 1 min at 72 °C, and a final extension of 10 min at 72 °C. Reactions were carried out in a C1000 Touch thermal cycler (Bio-Rad, Hercules, CA, USA). The negative and positive controls (DNA of Pdd ATCC 33539) were included in each amplification series. The PCR products were analyzed by electrophoresis on 2% agarose gel (Sigma-Aldrich, St Louis, MO, USA) containing Gel Green Nucleic Acid Gel Stain 10,000× (Biotium, Fremont, CA, USA) in comparison with molecular weight markers, and then photographed on a Gel-Doc UV transilluminator system (Bio-Rad, Hercules, CA, USA).

2.4. PCR Amplification of Hemolysin Genes

Samples testing positive for Pdd were screened by PCR for hemolysin genes (dly, hlyApl, and hlyAch) using primers and thermal cycling conditions as previously described [42]. The amplification reactions for dly and hlyAch genes were performed in a final volume of 25 µL containing 0.625 U of Platinum Taq DNA polymerase (Invitrogen, Waltham, MA, USA), 400 nM of each primer, 1× PCR Buffer, 3 mM MgCl2, 0.4 mM dNTPs, 1 µL of DNA sample, and sterile water to volume. The PCR for hlyApl gene was performed using a mixture containing 1×PCR buffer, 3 mM MgCl2, 0.2 mM dNTPs each, 1 µM of each primer, 1 U of Platinum Taq DNA polymerase (Invitrogen, Waltham, MA, USA), 2 µL of the DNA sample, and water to a final volume of 50 µL. All reactions were carried out in a C1000 Touch thermal cycler (Bio-Rad, Hercules, CA, USA) and PCR products were separated by electrophoresis on 2% agarose gel stained with 10,000× Gel Green Nucleic Acid Gel Stain (Biotium, Fremont, CA, USA) and visualized under ultraviolet (UV) illumination. The presence of hemolysin DNA in a sample was indicated by the presence of a band of the appropriate size 549 bp (dly), 767 bp (hlyApl), and 353 bp (hlyAch) with concordant negative and positive controls.

2.5. Sequencing

Amplification products were purified with the QIAquick Gel Extraction kit (Qiagen) and sequenced using a BrilliantDye Terminator v.3.1 kit (NimaGen, Nijmegen, The Netherlands) according to the manufacturer’s instructions. The amplicons were purified with an AutoSeq G-50 Dye Terminator Removal kit (GE Healthcare, Chicago, IL, USA) and run on a SeqStudio Genetic Analyzer (Applied Biosystems, Foster City, CA, USA). Obtained forward and reverse sequences were aligned using the SeqMan software from the Lasergene package v. 7.2 (DNASTAR Inc., Madison, WI, USA). The resulting consensus sequences were aligned to detect any nucleotide variation and matched with available sequences retrieved from the National Center for Biotechnology Information (NCBI) database using the BLAST tool against the sequence records available in GenBank to confirm species identification.

2.6. Data Analysis

Data on the date of stranding, species, and positivity found in different organs were subjected to descriptive analysis. Subsequently, a univariate analysis was performed using the chi-square test to assess whether there were differences in prevalence among species and among tissues in the individuals which tested as Pdd positive. Finally, the presence of infection seasonality was assessed by analysis-of-variance (ANOVA).

3. Results

Between January 2017 and December 2022, samples from 53 cetaceans stranded on the Ligurian coastline (Italy) were tested for Pdd DNA by PCR. A total of 272 tissue samples were analyzed. Twenty-two animals out of 53 (41.5%) tested positive for Pdd DNA in at least one tissue, including the brain, lung, lymph nodes, kidney, liver, and spleen (Table 1 and Table 2). All positive samples were confirmed by sequencing. The sequence analysis revealed that almost all ureC and all hemolysin gene sequences shared 100% nucleotide identity when compared to each other as well as the sequence records available in GenBank. The only exception was the ureC sequence of sample ID 6, which showed 92.4% similarity with the other sample sequences. Moreover, microbiological examinations allowed the isolation of Pdd from seven out of 19 (36.8%) of the tested animals, mainly from the lung, lymph nodes, and brain samples (Table 3). The chi-square test showed no differences when Pdd prevalences were compared between tissues in positive animals.
Of the 22 positive cetaceans, 15 were striped dolphins, and seven were bottlenose dolphins (Table 1). The chi-square test showed no differences when Pdd prevalences were compared between striped dolphins and bottlenose dolphins.
Three PCR-positive cetaceans were stranded, respectively, in 2017, 2018, 2020, 2021, and 2022, and seven were stranded in 2019 (Table 1). Most positive cetaceans were stranded during summer, followed by winter, spring, and autumn (Table 3), but no seasonality was found in the Pdd prevalence according to statistical analysis.
Of the five cetaceans PCR-positive for the hlyAch hemolysin gene, one was also positive for hlyApl and dly hemolysin genes. The hlyApl and dly genes were detected only in one out of 22 (4.5%) cetaceans testing positive to Pdd (Table 1). Only one cetacean (4.5%) was positive for all three of the considered genes in the lymph node, while the spleen was positive for hlyAch and dly together (Table 2). Hemorrhagic lesions were observed in tissue samples, which resulted in a positive for hemolysins only in samples ID 16 and ID 17 (Table 3).
Of the 22 PCR-positive cetaceans, 11 were adults, five were sub-adults, four were juveniles, and two were calves (Table 3). Sex was not determined in one animal, while five were female and 16 were male. Among the 22 cetaceans that tested positive for Pdd, other pathogen microorganisms were found in co-presence. Cetacean Morbillivirus (CeMV) was the most prevalent (10/22), followed by herpesvirus (7/22), Toxoplasma gondii (5/22), and in fewer numbers of Salmonella 1,4,[5],12:i:-(2/22), Clostridium perfringens (2/22), and others (refer to Table 3). Therefore, in 13 of these animals (59%), the causa mortis after necroscopy was correlated to an infectious origin. In some of the six animal tissues (ID: 5, 6, 11, 16, 17, 20, 22) that tested positive for the molecular investigation of Pdd, hemorrhagic lesions were also present mainly in the lymph nodes. In two of these cases (ID 16 and 22), where the Pdd was isolated, the pathological condition found was compatible with the presence of Pdd hemolytic strain and Clostridium sordelli in one case, and Pdd and Brucella spp. in the other case (Table 3).

4. Discussion

Our study presents available data on Pdd prevalence in cetaceans stranded during the last six years along the Ligurian coastline, part of the Pelagos Sanctuary.
The prevalence of Pdd over such a long period of time has never been reported in marine mammals except for one study [21] that found 4% of cetaceans positive for Pdd from the northeast USA and 8% from cetaceans stranded along southwest Florida Gulf coasts [21]. In fact, positivity for Pdd is usually reported in cetaceans linked to a single stranding [23,24] or, in some cases, associated with mass mortality events [22,43]. Casalone et al. 2014 [22] reported a Pdd prevalence of 62% of the stranded dolphins in an unusual mortality event that occurred along the Tyrrhenian Sea coast of Italy during the first three months of 2013.
In our study, Pdd DNA was detected by PCR in 41.5% of cetaceans stranded from January 2017 to December 2022, and 22.7% (5/22) of these PCR-positive cetaceans were also positive for at least one of the hemolysin genes tested. In particular, four out of five (80%) cetaceans showed positivity only for the hlyAch gene, which seems to be the one with the lower pathogenicity based on experimental studies conducted on mice [10]. In one out of five (20%) cetaceans positive for Pdd virulence factors, the co-presence of the three hemolysins investigated was found, a condition correlated to the highest level of mortality in experimental animals. Previous investigations have demonstrated that strains of Pdd characterized by greater virulence correspond to those capable of inducing more significant hemorrhagic lesions in fish, thus establishing a relationship between hemolysis and virulence [44]. On the contrary, in the matrices of our study in which high and medium pathogenic hemolysins (dly and hlyApl) were confirmed, no hemorrhagic lesions were observed either at a macroscopic or histopathological level. However, in a previous report, strains of Pdd having the chromosomal PhlyC gene (hlyAch), in the absence of the dly gene, caused severe chronic suppurative pneumonia in dead dolphins [23], supporting previous indications that this virulence factor is not essential for pathogenesis [45]. Furthermore, it should be considered that Pdd is a pathogen mainly for fish, while the potential to cause disease in humans and mammals is an accidental condition. A recent study shows that mammalian body temperature represents a stress condition for this microorganism, unlike that of fish, which are cold-blooded animals. When Pdd grows at 37 °C, the genes involved in virulence are repressed, including iron acquisition systems, and the virulence factor dly is four-fold downregulated at this temperature [46].
Analysis of ureC gene sequences revealed that most positive samples shared the same nucleotide sequence. However, this sequence showed 100% identity with only three records in GenBank, specifically three Pdd isolates from South Korea (Acc. Nos. CP035458, CP021152, CP063050) collected in Yangtze finless porpoises (Neophocena asiaorientalis) and Beluga whale (Delphinapterus leucas) in 2017 and 2020, respectively. The ureC of sample ID 6, however, was different from the other sequences (92.4% similarity), but a number of 100% identical records were found in the GenBank database. Most of the Pdd strains identified by molecular testing were not identified by culture tests. In healthy carriers, the bacterial load can persist in low numbers, and it is therefore very difficult to isolate them with classical culture methods [47]. Furthermore, the isolation of Pdd when it grows at mammalian body temperature can be difficult as already reported by another study [46]. In fact, the stress conditions at this temperature compromise the cells’ vitality and shape control [46]. PCR has been able to detect the presence of DNA of these microorganisms even when present in low numbers and significantly reduce identification times. However, it does not provide us with information on the microorganisms’ viability and is not able to test phenotypic hemolytic activity. The rapidity of PCR testing is a potential advantage over cultures. Molecular methods maintain an advantage, at least theoretically, over time, and they are more sensitive than cultures. Furthermore, this technique can produce a more accurate and feasible diagnosis [48,49,50,51]. Therefore, by combining the two techniques, it is possible to obtain as much information as possible about the bacterial strain.
The present study also examined several different tissue samples for each cetacean. This extensive analysis shows that most of the animals were infected in multiple tissues at the same time, with the lymph node being the most frequently infected tissue
In our study, the hypothesis of causa mortis in 13 of the 22 cetaceans positive for Pdd was correlated to an infectious origin, mainly of a viral and bacterial nature, and, to a lesser extent, a parasitic one. In two cases, an anthropic cause related to fishery interaction was identified; however, it was in the presence of underlying pathologies. It is interesting to note that, in all cases where cetaceans tested positive for Pdd, other well-known pathogens for these species, such as CeMV, T. gondii, and α-herpesvirus, were also present. These pathogens are responsible for serious systemic infections in the examined subjects, often accompanied by severe histopathological lesions.
The coinfection of Pdd and other pathogens has been previously described in stranded cetaceans [22,24,52], and CeMV-induced immunosuppression has been suggested to act as a predisposing factor to Pdd infections [43].
The prevalence of Pdd in live cetaceans has never been directly investigated. However studies on the microbial community profile in dolphins reveal the presence of this bacterium also in healthy cetaceans [53,54]. In a study of wild dolphins from the Gulf of Mexico and two Atlantic Ocean locations, V. damselae (later renamed Pdd) resulted in the most commonly recovered bacteria (64.1% of all animals tested) from both anal/fecal and blowhole samples [54].
Numerous other aerobic microorganisms of clinical significance were also isolated from healthy cetacean samples [21,53,54,55]. Other studies indicate that debilitated animals are characterized by a greater number of opportunists than healthy animals [21]. Therefore, based on existing studies, many potential pathogens occur in a commensal or transient state in healthy wild dolphin populations. To better investigate this aspect, it would therefore be appropriate for future research to perform molecular or cultural screening for Pdd not only in deep invasive tissue samples, but also in non-invasive samples such as skin, blowhole, genitalia, rectum, or feces of stranded cetaceans. The common presence of coinfection in stranded dolphins, as highlighted in our study, would seem to support the hypothesis that in the case of a weakening of the immune system of cetaceans due to other infections or other causes, these opportunistic pathogens may take over, increasing the state of debilitation of the individual with consequent death and/or stranding.
Dolphins are gregarious animals and move over large distances, which makes it possible to disseminate bacteria to other individuals of the same social group and perhaps to other groups, in new geographic areas and, perhaps, to new animals. The dissemination of these pathogens in the marine environment also represents a potential threat to public health since Pdd causes infections also in humans [1], and Pdd has been associated with drug resistance in aquaculture [56] and in human clinical settings [57]. This fact highlights the importance of monitoring the presence of this and other pathogens in marine mammals and deepening the analyses with further information, such as the acquisition of the presence of antibiotic resistance genes in Pdd strains isolated from cetaceans, since, at the moment, there are no data in the literature.

5. Conclusions

The pathogenic role of Pdd has not been clarified yet in cetaceans [22,24]; however, the presence of virulence factors, and not just the identification of the bacterium, in association with important cetacean pathogens could lay the ground for evaluating the role of Pdd in the worsening of conditions already characterized by serious impairment. However, further studies are necessary to investigate and deepen this initial hypothesis.

Author Contributions

The individual author contributions are as follows: Conceptualization, C.G. and L.S.; formal analysis, R.B. and M.I.C.; investigation, R.B., C.M., F.G., C.G., C.T., S.Z., S.P., E.B. and N.P.; resources, C.G., L.S. and N.P.; data curation, C.G. and F.G.; writing—original draft preparation, R.B.; writing—review and editing, R.B., F.G., C.G., N.P. and S.Z.; supervision, C.C. and L.S.; project administration, C.G. and F.G.; funding acquisition, C.G. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Italian Ministry of Health, grant number IZS PLV 06/21 RC. The APC was funded by IZS PLV 06/21 RC.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

All data supporting the present study are reported in this study. Further inquiries can be directed to the corresponding author.

Acknowledgments

The authors wish to thank Walter Mignone and Fulvio Garibaldi for their support in the recovery of cetacean carcasses and necropsy investigations. The authors are also grateful to Mariella Goria for biomolecular investigation and to Pite Ledi for the English language review.

Conflicts of Interest

The authors declare no conflicts of interest.

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Table 1. Pdd and hemolysins DNA presence in cetaceans stranded on the Ligurian coast (from 2017 to 2022).
Table 1. Pdd and hemolysins DNA presence in cetaceans stranded on the Ligurian coast (from 2017 to 2022).
YearTotal Animals TestedPddSpecies (No. Pdd Positive; %)Pdd Positive/Haemolysin
Positive (Type)
No.%
20175360.0Stenella coeruleoalba (3/5; 60.0)3/0
20189333.3Stenella coeruleoalba (3/8; 27.5)3/0
Tursiops truncatus (0/1; 0.0)-
201911763.6Stenella coeruleoalba (4/6; 66.7)4/0
Tursiops truncatus (3/4; 75.0)3/0
Globicephala melas (0/1; 0.0)-
202011327.3Stenella coeruleoalba (2/9; 22.2)2/1 (hlyAch)
Tursiops truncatus (1/1; 100.0)1/1 (hlyAch; hlyApl; dly)
Ziphius cavirostris (0/1; 0.0)-
202111327.3Stenella coeruleoalba (1/5; 20.0)1/1 (hlyAch)
Tursiops truncatus (2/6; 33.3)2/1 (hlyAch)
20226350.0Stenella coeruleoalba (2/4; 50.0)2/0
Tursiops truncatus (1/1; 100.0)1/1 (hlyAch)
Ziphius cavirostris (0/1; 0.0)-
Total532241.5Stenella coeruleoalba (15/37; 40.5)22/5 (5 hlyAch; 1 hlyApl; 1 dly)
Tursiops truncatus (7/13; 53.8)
Ziphius cavirostris (0/2; 0.0)
Globicephala melas (0/1; 0.0)
Table 2. Pdd and hemolysins DNA presence in tissues of cetaceans stranded on the Ligurian coastline (Italy) from 2017 to 2022.
Table 2. Pdd and hemolysins DNA presence in tissues of cetaceans stranded on the Ligurian coastline (Italy) from 2017 to 2022.
Tissue Type Total Tested Pdd Haemolysin Positive/Pdd Positive
No.%No. and Type%
Spleen 41 9 22.0 2/9 (1 hlyAch; dly) 22.2
(1 hlyAch)
Liver 46 11 24.00/11 0.0
Lymph node(s) 47 16 34.03/16 (1 hlyAch; 1 hlyApl; 1 dly) 18.7
(2 hlyAch)
Lung 50 14 28.03/14 (hlyAch) 21.4
Kidney 45 7 15.61/7 (hlyAch) 14.3
Brain 42 9 21.42/10 (hlyAch) 20.0
Total 272 66 24.3 11/67 (11 hlyAch; 1 hlyApl; 2 dly) 14.9
Table 3. Pathogen microorganisms found in stranded cetaceans recovered from the Ligurian coastline from 2017 to 2022 that tested positive for Pdd and hemolysin DNA, Pdd culture, and cause of death after necroscopy. M: male, F: female, n.d: not determined, J: juvenile, A: adult, S.A.: sub-adult, C: newborn-calf. n.t.: not tested.
Table 3. Pathogen microorganisms found in stranded cetaceans recovered from the Ligurian coastline from 2017 to 2022 that tested positive for Pdd and hemolysin DNA, Pdd culture, and cause of death after necroscopy. M: male, F: female, n.d: not determined, J: juvenile, A: adult, S.A.: sub-adult, C: newborn-calf. n.t.: not tested.
IDLaboratory
Reference		Stranding DateSpecies (Sex and Age Class)Tissue Pdd PCR +
(Hemolysin)/
Tissue Culture +		Tissue Positive for Pdd with Hemorrhagic LesionsOther MicroorganismsCause of DeathRef.
11676916 February 2017S. coeruleoalba (M, J)Liver, lung, brain/--CeMV, Brucella ceti,
T. gondii, Sarcocystis spp.,
Monorygma sp. (cysts)		Bacterial/viral/
parasitic infection		[29,35,36,37]
27898314 September 2017S. coeruleoalba (F, A)Kidney/--CeMV, α-herpesvirus,
Salmonella 1,4,[5],12:i:-,
T. gondii, Phyllobotrium sp., Monorygma sp., Pennella sp.		Bacterial/viral/
parasitic infection		[29,36,37,38]
39070416 October 2017S. coeruleoalba (F, A)Liver, lymph nodes, lung, brain/--α-herpesvirusViral infection[29]
4512920 January 2018S. coeruleoalba (M, A)Liver, kidney, brain/--CeMV, α-herpesvirus,
Salmonella 1,4,[5],12:i:-,
Phyllobotrium sp.,
Monorygma sp.		Bacterial/viral
infection		[30,38,39]
5538621 January 2018S. coeruleoalba (M, A)Liver, lung/-LiverCeMV, ƴ-herpesvirus,
Salmonella tsevie,
pulmonar nematodes (Pseudaliidae),
Pholeter sp. (cysts), Phyllobotrium sp., Monorygma sp.		Viral infection[30]
68755829 October 2018S. coeruleoalba (F, J)Spleen, liver, lymph nodes, lung, kidney/-LungCeMV, Listeria innocuaBacterial/viral
infection		[30,37,39]
71801323 February 2019T. truncatus
(M, J)		Lymph nodes, lung/--α-herpesvirus, Enterococcus faecium, Staphylococcus spp., mycetes (mucorales)n.d.[31,40]
8217245 March 2019S. coeruleoalba (F, A)Lymph nodes, lung/lung-CeMV, Moraxella spp.,
Phyllobotrium sp. (cysts), Monorygma sp. (cysts)		Viral infection[31,37,39]
9332124 April 2019S. coeruleoalba (M, J)Lung, kidney/n.t.-Pulmonar nematodes,
Pholeter sp. (cysts)		n.d[31]
10424727 May 2019T. truncatus
(M, A)		Brain/n.t.-CeMVAnthropic cause: vessel collision[31,39,40]
11592604 July 2019T. truncatus
(M, A)		Spleen, liver, lymph nodes, lung, brain/-BrainCeMV, T. gondiiBacterial/viral/
parasitic infection		[31,37,39,40]
126287721 July 2019S. coeruleoalba (M, A)Spleen, lymph nodes, lung, kidney, brain/--CeMV,
Phyllobotrium spp. (cysts),
Monorygma spp. (cysts)		Bacterial/viral/
parasitic infection		[31,39]
136355823 July 2019S. coeruleoalba (M, C)Spleen, liver, lymph nodes, lung, brain/--T. gondiiBacterial/parasitic infection[31]
145135213 July 2020T. truncatus
(M, A)		Spleen (hlyAch; dly), lymph nodes (hlyAch; hlyApl; dly), lung (hlyAch), brain(hlyAch)/liver, lymph nodes, lung, brain-T. gondii, α-herpesvirus,
Listeria grayi,
C. perfringens,
Penicillium spp.		Anthropic cause: by catch (consequence of underlying pathologies)[32,36,40]
155565430 July 2020S. coeruleoalba (M, C)Spleen, liver, lymph nodes/brain--Natural cause[32]
166066923 August 2020S. coeruleoalba (M, S.A)Spleen (hlyAch), liver, lymph nodes (hlyAch), kidney (hlyAch)/lymph nodes, brainLymph nodesClostridium sordelli,
Phyllobotrium sp.		Bacterial infection[32]
17612822 January 2021S. coeruleoalba (M, A)Lymph nodes, lung (hlyAch)/lymph nodes, lungLungα-herpesvirus, Pholeter sp.(cysts), Campula spp.
Phyllobotrium sp. (cysts), Monorygma sp.		Natural cause[33]
183043429 March 2021T. truncatus
(M, A)		Lymph nodes (hlyAch)/lymph nodes, lung, brain-Listeria seeligeri,
Carnobacterium spp.,
Cetacean poxvirus 1,
Phyllobotrium sp.,
Intestinal trematodes,
Serratia spp., Pholeter sp.		Anthropic cause: by catch (consequence of underlying pathologies)[33]
197395110 September 2021T. truncatus
(F, S.A)		Lymph nodes, lung/--T. gondii, CeMV,
Erysipelothrix rhusiopathiae, Phyllobotrium sp., Pholeter sp.		n.d.[33,39,40]
20831930 January 2022S. coeruleoalba (M, S.A)Spleen, liver, lymph nodes/-Lymph nodesα-herpesvirus, C. perfringens, Monorygma sp., Pholeter sp.Bacterial/viral
infection		[34]
21638312 August 2022T. truncatus
(M, S.A)		Lymph nodes, lung (hlyAch), brain (hlyAch)/n.t.-Pholeter sp.n.d.[34]
228588924 October 2022S. coeruleoalba (n.d., S.A)Spleen, liver, lymph nodes, kidney, brain/kidneyLymph nodes, brainBrucella spp., Pholeter sp., Phyllobotrium sp.Bacterial infection[34]
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Battistini, R.; Masotti, C.; Giorda, F.; Grattarola, C.; Peletto, S.; Testori, C.; Zoppi, S.; Berio, E.; Crescio, M.I.; Pussini, N.; et al. Photobacterium damselae subsp. damselae in Stranded Cetaceans: A 6-Year Monitoring of the Ligurian Sea in Italy. Animals 2024, 14, 2825. https://doi.org/10.3390/ani14192825

AMA Style

Battistini R, Masotti C, Giorda F, Grattarola C, Peletto S, Testori C, Zoppi S, Berio E, Crescio MI, Pussini N, et al. Photobacterium damselae subsp. damselae in Stranded Cetaceans: A 6-Year Monitoring of the Ligurian Sea in Italy. Animals. 2024; 14(19):2825. https://doi.org/10.3390/ani14192825

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Battistini, Roberta, Chiara Masotti, Federica Giorda, Carla Grattarola, Simone Peletto, Camilla Testori, Simona Zoppi, Enrica Berio, Maria Ines Crescio, Nicola Pussini, and et al. 2024. "Photobacterium damselae subsp. damselae in Stranded Cetaceans: A 6-Year Monitoring of the Ligurian Sea in Italy" Animals 14, no. 19: 2825. https://doi.org/10.3390/ani14192825

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