The impact of co-infections on fish: a review.

Co-infections are very common in nature and occur when hosts are infected by two or more different pathogens either by simultaneous or secondary infections so that two or more infectious agents are active together in the same host. Co-infections have a fundamental effect and can alter the course and the severity of different fish diseases. However, co-infection effect has still received limited scrutiny in aquatic animals like fish and available data on this subject is still scarce. The susceptibility of fish to different pathogens could be changed during mixed infections causing the appearance of sudden fish outbreaks. In this review, we focus on the synergistic and antagonistic interactions occurring during co-infections by homologous or heterologous pathogens. We present a concise summary about the present knowledge regarding co-infections in fish. More research is needed to better understand the immune response of fish during mixed infections as these could have an important impact on the development of new strategies for disease control programs and vaccination in fish.

Differential modulation of host immune genes in the kidney and cranium of the rainbow trout (Oncorhynchus mykiss) in response to Tetracapsuloides bryosalmonae and Myxobolus cerebralis co-infections.

BACKGROUND: Most of the studies on fish diseases focus on single infections, although in nature co-infections occur more often. The two freshwater myxozoan parasites of salmonids, having high economic and ecologic relevance are Tetracapsuloides bryosalmonae (Malacosporea), the etiological agent of proliferative kidney disease, and Myxobolus cerebralis (Myxosporea), the etiological agent of whirling disease. The present study aims to investigate immune modulation in rainbow trouts (Oncorhynchus mykiss) during single and co-infections by these parasites. METHODS: Fish were initially infected with T. bryosalmonae (one group) and M. cerebralis (another group) separately. At 30 days post-exposure (dpe), both the single species infected groups were co-infected, respectively, with the other parasite. Posterior kidney and cartilage cranium samples were collected at 30, 60, 90 and 120 dpe and RT-qPCR was performed on them to assess the transcription of suppressors of cytokine signaling (SOCS) -1 and -3, Janus kinase-1 (JAK-1) and signal transducer and activator of transcription-3 (STAT-3) genes. RESULTS: Kidney samples from the T. bryosalmonae-infected group showed upregulation of all immune genes tested between 60-120 dpe. Crania from the single M. cerebralis-infected group and the M. cerebralis and T. bryosalmonae co-infected group exhibited upregulation of SOCS-1 and JAK-1 between 60-120 dpe and SOCS-3 at 120 dpe. However, only in the single M. cerebralis-infected group, was a statistically significant expression of STAT-3 observed at 30 and 60 dpe. CONCLUSIONS: The results of this study indicate that both T. bryosalmonae and M. cerebralis induce overexpression of SOCS-1 and SOCS-3 genes and modulate the host immune response during the development of parasite to cause immunosuppression.

The impact of Tetracapsuloides bryosalmonae and Myxobolus cerebralis co-infections on pathology in rainbow trout.

BACKGROUND: Myxozoan parasites pose emerging health issues for wild and farmed salmonid fish. Rainbow trout (Oncorhynchus mykiss) is a particularly susceptible species to Tetracapsuloides bryosalmonae (Malacosporea), the etiological agent of Proliferative Kidney Disease (PKD), and to Myxobolus cerebralis (Myxosporea), the etiological agent of Whirling Disease (WD). The objective of this study was to investigate the impact of myxozoan co-infections on the pathogenesis of PKD and WD in the rainbow trout. METHODS: Two groups of rainbow trout (96 fish each) were primarily infected with T. bryosalmonae and triactinomyxons of M. cerebralis; after 30 days half of the fish in each group were co-infected with these parasites vice versa and remaining half was continued as single infection. Mortalities and clinical signs were recorded at different time points. Histopathology and immunohistochemistry were performed to assess the extent of each infection and estimate the parasite burden between groups. RESULTS: Fish firstly infected with M. cerebralis and co-infected with T. bryosalmonae exhibited exacerbated pathological changes of both parasitic diseases and elicited a higher mortality rate. A higher kidney swelling index (grade 4) appeared together with more severe cartilage destruction and displacement, when compared to the pathological changes in fish upon single infections with T. bryosalmonae or M. cerebralis. Conversely, fish firstly infected with T. bryosalmonae and co-infected with M. cerebralis also exhibited typical pathological changes of both parasitic diseases, but with a lower mortality rate, similar as caused by the single T. bryosalmonae or M. cerebralis infection. WD clinical signs were milder, without skeletal deformities, while kidney swelling index was similar to single infection with T. bryosalmonae (grade 2 to 3). CONCLUSIONS: In this study, a co-infection with myxozoan parasites was for the first time successfully achieved in the laboratory under controlled conditions. The impact of co-infections in concurrent myxozoan infections mainly depends on the primary pathogen infecting the host, which could alter the outcomes of the secondary pathogen infection. The primary M. cerebralis infection followed by T. bryosalmonae had a much more serious impact and elicited a synergistic interaction. Contrasting results were instead seen in rainbow trout primarily infected with T. bryosalmonae and then co-infected with M. cerebralis.