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The fish was a wild-type strain purchased from a commercial tropical fish vendor and was being held in quarantine at the time it became ill.
The fish were hatched Sept and submitted to the diagnostic laboratory March The infection was initially detected in 2 of 13 moribund fish submitted to the ZIRC diagnostic service in June of This quarantine facility is physically separated from the main fish holding room, with isolated recirculating water systems, ultraviolet treatment of effluent post-filtration, restricted access, and dedicated equipment.
Fish are moved from quarantine into the main facility as eggs after being disinfected in 30 ppm sodium hypochlorite for 2 min and transfered to sterile water.
After this discovery, more fish in this facility were screened for the parasite. First, 10 live fish from the same stock in which the initial infection was detected were shipped live to Oregon State University for histology.
All of these animals, many of which presented obvious clinical signs of infection, tested positive for the parasite by histology.
An additional 13 individuals from the subsequent F3 generation of CG1 in this facility were examined and confirmed as positive for the infection by histology.
Finally, infections were detected in three more fish in August , two more from the F3 generation of the CG1 strain and another fish from a separate population of WIK strain zebrafish.
All three of these animals had been exposed to sublethal doses of gamma radiation to suppress the immune system before tissue transplantation Traver et al The WIK fish in this facility were imported as described for the CGI line and had been maintained internally for many generations, with no known history of exposure to fish outside of the colony.
At 6 months, all of these fish were euthanized and examined by histology. A single fish from this group was positive for P.
The one infected fish from Lab 1 showed no obvious clinical or macroscopic changes. The one infected fish from Laboratory 2 was sluggish, appeared bloated, and exhibited a white area in the integument below the dorsal fin that was obvious in the swimming fish when examined from above.
In Lab 3, large, depigmented regions in the central dorsal fin area were observed in infected fish while still swimming in tanks.
Some fish also displayed spinal curvatures. Examination of infected fish with a dissecting microscope revealed multifocal to coalescing white-gray, slightly raised regions where the skin appeared depigmented Fig 1.
Removal of the skin showed that the underlying skeletal muscle was white, soft, and edematous Fig 1. The one positive AB fish from the Lab 3 sentinel group appeared normal when euthanized.
Zebrafish infected with P. Upper image shows mottled appearance with light areas arrows on flanks. Lower image is same fish with skin removed, exhibiting opaque regions in muscle arrows representing massive infection.
Wet-mount preparations of skeletal muscle from infected fish revealed numerous sporophorous vesicles, many which contained fully developed spores.
Histopathologic changes were consistent from all three laboratories and thus are described together. However, in several of the fish examined as a part of this study, the severity of infection was much more pronounced and was associated with severe chronic inflammation.
Skeletal muscle degeneration, denoted by loss of cross-striations as well as fragmented, hypereosinophilic myofibers and centralized nuclei, was also observed among the affected myofibers.
In sections, muscle myofibers contained from 2 to plus P. The affected skeletal muscle myofibers were frequently surrounded by large numbers of intermixed histiocytes and lymphocytes with fewer eosinophilic granular cells, which tracked along the endomysial connective tissue and were accompanied by marked endomysial edema that widely separated myofibers.
Regenerating myofibers characterized by enhanced sarcoplasmic basophilia and nuclear rowing were frequently adjacent to many of the necrotic myofibers data not shown.
Numerous liberated mature spores within the endomysial spaces were surrounded by dense aggregates of histiocytes and lymphocytes Fig.
Phagocytized mature spores were occasionally seen within activated histiocytes. Wet mount of P. Note prominent posterior vacuole arrow.
Histological sections of zebrafish infected with P. Numerous sporophorous vesicles with spores and developmental stages within myocytes.
Spores in phagocytes associated with chronic infections and myolysis demarked by arrows. Mixed infection with P.
Accustain Gram. Meronts m , and developing and mature spores sp in sporophorous vesicles. Some fully developed spores stain deep blue arrows.
Mature spores stain deep blue to purple arrows , developmental stages are light orange arrow heads.
Lillie Twort Gram. Numerous spores arrows throughout all layers of the intestine and mesenteries. Masses of spores in phagocytes arrows in ovaries.
The parasitic infection in the single fish from Lab 1 was limited to the skeletal muscles; however in the fish from the other two laboratories, spores within phagocytes were also detected in various other organs, including the kidney interstitium, spleen, ovaries, intestine, and mesenteries.
Massive numbers of spores within phagocytes were frequently observed in the connective tissues of the ovary, but never within ova Fig.
Aggregates of spores were observed in all layers of the intestine, extending through the serosal surface and into mesenteric connective tissue.
Smooth and cardiac muscle were not affected in any of the fish examined. Both Gram stain methods were effective for distinguishing spores.
With the Accustain method, mature spores stained deep blue while immature spores appeared to take up less of the stain Fig. With the Lillie-Twort method, fully formed spores stained deep blue to purple Fig 3e.
All seven of the fish from Lab 3 examined by histology exhibited a mixed infection with Pseudoloma neurophilia Fig 3c. This microsporidium was easily distinguished from P.
The maximum likelihood and Bayesian analyses produced phylogenetic trees with identical topology Figure 4. The topology is also consistent with other phylogenetic analyses of fish microsporidian parasites Moran et al Phylogenetic tree of Pleistophora hyphessobryconis obtained from neon tetra and related microsporidia based on small subunit rRNA gene sequences.
Maximum likelihood tree is shown. Genus names shown are as recorded in GenBank with new genus designations in parentheses. The microsporidian parasite, Pseudoloma neurophilia was selected as an outgroup taxa.
A total of bp position 1 to of the small subunit rRNA gene was sequenced from P. Both moribund zebrafish collected from the group exposed to infected neon tetra tissue exhibited massive muscle infections based on wet mount observations at 20 days postexposure.
Histological examination of the remaining fish collected at 30 days showed infections in five of eight fish.
These fish had light infections exhibiting various stages of development. Among those are zebrafish Opitz and the dwarf danio, D.
Here we found the infection in three separate zebrafish research colonies with no known movement of fish between the facilities.
Confirmation of host ranges of parasites with limited morphological characters such as Microsporidia often requires cross transmission studies or sequence comparisons.
There are reports of experimental transmission experiments of P. Here we confirmed that the infection in zebrafish was P. This is consistent with intraspecific variation in this region of the small subunit rRNA for other Pleistophora spp.
The intraspecific pairwise distance between other available sequences from multiple individuals in GenBank are as follows: P. Further, we found an average pairwise interspecific distance of 0.
The minor, but consistent, differences seen between the three zebrafish sequences compared to that of neon tetra might suggest different strains of the parasite.
Regardless, the parasite from neon tetra was easily transmitted to zebrafish. Our findings agree with previous transmission studies, confirming the broad host specificity of this microsporidium Canning et al It was noted previously that the genus Pleistophora does not form a monophyletic clade Nilsen et al In fact, ultrastructural characterization and molecular analyses of the small subunit rRNA gene sequences have resulted in the movement of P.
Prior ultrastructural descriptions of P. However, phylogenetic analyses of P. Interestingly, unlike the members of Ovipleistophora, this species does not infect oocytes but rather myocytes as does the type species of this genus, P.
Comprehensive analysis of the genus is beyond the scope of this study but further investigation appears to be needed.
The three facilities had no history of sharing fish and are located in different areas of the United States. Thus we presume that the infections arose in three independent instances by exposure to other species of infected aquarium fishes.
The affected fish from Lab 2 had also been purchased from a pet store and the maternal parent of the infected fish at Lab 1 had been purchased from a vendor that supplied fish to the commercial pet trade.
As stated above, transmission of P. As with other microsporidia, it is assumed that infection is initiated by ingestion of spores.
Spores released from dead fish are a likely source of infection, but could also be released from the intestines. Schäperclaus suggested that spores may be released from the skin or urinary tract of infected fish.
Zebrafish spawn frequently within aquaria, and tank mates quickly eat available eggs Lawrence , Spence et al Although spores were not found within eggs, the massive numbers seen within ovaries of some infected zebrafish suggest that infectious spores could be released during spawning and thus would be available to fish feeding on eggs or to infect the next generation of fish.
Schäperclaus suggested the possibility of maternal transmission as he found infections in 8-day-old neon tetras derived from infected parents.
Once established in zebrafish, it is conceivable that the infection could be maternally transferred to the next generation.
This could even occur with spores outside the egg as microsporidian spores are very resistant to chlorine Ferguson et al This provides one explanation for the occurrence of the infection in fish derived from surface-disinfected eggs.
Alternatively, these fish may have become infected by an unrecognized breach in biosecurity protocols. The infected fish from Lab 1 was the month-old offspring of a female fish that had been purchased from an outside vendor and brought into the laboratory.
If this fish was infected as an embryo, this would mean that the fish was subclinically infected for more than 1 year. All of the fish purchased from the vendor had been removed from Lab 1 more than 7 months before the infected fish was detected.
Even if the fish had not been infected as an embryo but instead at a later time through accidental cross-contamination with an infected fish from the group purchased from the vendor, it indicates that this fish was subclinically infected for more than 7 months.
As with other microsporidian infections, it is likely that immune status influences susceptibility of zebrafish to P.
Recently, Ramsay et al. Ramsay et al showed that stress enhances infections of P. Infections by P. The microsporidium was also found in fish CG1 and WIK that were irradiated and thus were immune compromised.
Although immune status likely affects the susceptibility and progression of the disease in zebrafish, apparently immunocompetent fish can become infected as demonstrated by reports of P.
The latter were exposed at days old, a time at which fish have innate immunity but adaptive immunity has not fully developed Lam et al , Trede et al The most remarkable pathological feature of P.
Parasites within myocytes were not associated with inflammation; however, mature spores released from degenerate myofibers into interstitial spaces were consistently associated with inflammation, and these liberated spores were often engulfed by phagocytes.
This is similar to that seen with other intramuscular parasites of fishes, such as Kudoa thyrsites of salmon Moran et al Microsporidian spores remain intact within phagocytes, and thus may be transported to sites beyond where they originally developed Kent et al The occurrence of large numbers of spores of P.
Spores of Microsporidia are gram positive in histological sections Gardiner et al , Bruno et al Both Lilly-Twort and Accustain Gram stains were very effective for demonstrating spores and particularly useful for visualizing individual spores within visceral organs.
Some infected zebrafish exhibited concurrent infections by Pseudoloma neurophilia , a common microsporidium parasite of zebrafish that demonstrates myelinotropic behavior and is directly associated with encephalomyelitis and polyneuritis involving the peripheral nerves and spinal nerve roots.
The two microsporidian infections can be easily differentiated by histology. Skeletal muscle is the primary site of development P. In contrast, the central and peripheral nervous systems are the primary sites of infection for P.
In cases of myositis attributed to P. In the case of coinfections, the opaque, depigmented muscle lesions were clearly caused by P.
However, it is possible that P. Given the potential for severe infections and long-term subclinical chronic infections, P.
As suggested for Pseudoloma neurophilia Kent et al , the most feasible strategy would be to hold brood fish in quarantine and screen them and their progeny for the infection using a PCR test specific to the parasite.
Sentinel fish programs and sampling of moribund fish are also recommended as a means of surveillance of colony health.
Notably, two of these cases were from fish that had been in contact with commercial pet store fish. It would be prudent to not mix zebrafish used in research with other aquarium fishes.
Further studies on the role of maternal transmission, susceptibility of spores to disinfectants, and the role of age and fish strain in severity of disease are all warranted.
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Opinions, interpretations, conclusions, and recommendations stated are those of the authors and are not necessarily endorsed by the U.
We thank Dr. Sanders, University of Washington for manuscript review, Dr. Schuster for assistance in translation of German references, and K.
Berkenkamp for histology slide preparation and technical support. National Center for Biotechnology Information , U. Dis Aquat Organ.
Author manuscript; available in PMC Sep 5. Murray , 5 and Michael L Kent 1. Jeffrey F. Katrina N. Author information Copyright and License information Disclaimer.
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