Mechanical induced wounds in fish – a review on models and healing mechanisms

Abstract

Skin wounds and injuries are frequently occurring in farmed fish, particularly in more intensive production systems. Any disruptions of the skin, such as mucus removal, scale loss or deeper incisions, are negatively correlated with barrier functions and disease resistance. In this review, the current knowledge on mechanically induced wounds in fish is dedicated to five areas of focus: (i) The anatomy and functions of fish skin, (ii) Techniques to inflict mechanical skin damage in farmed and laboratory fish for experimental purposes, (iii) Healing mechanisms of deep wounds, (iv) In vitro models for wound healing studies and (v) Wound care, with focus on factors that may enhance or delay skin regenerative processes. The aim of the review was to presents key points for a better understanding of skin resilience and fish robustness, with focus on Atlantic salmon, Salmo salar, in Norwegian coastal production environment.

Keratinocytes Drive the Epithelial Hyperplasia Key to Sea Lice Resistance in Coho Salmon

“…Neural crest cells were characterized by multiple pigment cell genes (Table 1) including ltk , which directs multipotent neural crest cell development into pigment cells in zebrafish [56], suggesting these cells are pigment cell progenitors. The detection of neural crest cells, red blood cells, and muscle cells predominately in trunk skin samples (Fig.1 e,f), is consistent with expectations of greater abundance of these cell types in the trunk skin than in the fins [30] given the potential to cut deeper into the dermal layer. Additionally, several clusters of neuronal and glial cells were observed, but most were observed in a single sample per species (Fig.1 e,f ) suggesting they comprise neural structures which are present sporadically throughout the skin (e.g., peripheral axons [34], or the lateral line).…”

“…Keratinocytes were among the most abundant cell types. Three keratinocyte clusters were identified: basal keratinocytes, superficial keratinocytes and a third cluster of “intermediate keratinocytes”, likely located between the former two keratinocyte layers and consistent with the three layers of keratinocytes observed in fish skin [29, 30]. Keratinocytes were abundant in all samples, but notably increased at 48h and 60h post infection only in coho salmon (Fig.1 e,f).…”

“…The detection of neural crest cells, red blood cells, and muscle cells predominately in trunk skin samples (Fig. 1 e,f), is consistent with expectations of greater abundance of these cell types in the trunk skin than in the fins [30] given the potential to cut deeper into the dermal layer. Additionally, several clusters of neuronal and glial cells were observed, but most were observed in a single sample per species (Fig.…”

Keratinocytes Drive the Epithelial Hyperplasia Key to Sea Lice Resistance in Coho Salmon

“…Neural crest cells were characterized by multiple pigment cell genes (Table 1) including ltk , which directs multipotent neural crest cell development into pigment cells in zebrafish [56], suggesting these cells are pigment cell progenitors. The detection of neural crest cells, red blood cells, and muscle cells predominately in trunk skin samples (Fig.1 e,f), is consistent with expectations of greater abundance of these cell types in the trunk skin than in the fins [30] given the potential to cut deeper into the dermal layer. Additionally, several clusters of neuronal and glial cells were observed, but most were observed in a single sample per species (Fig.1 e,f ) suggesting they comprise neural structures which are present sporadically throughout the skin (e.g., peripheral axons [34], or the lateral line).…”

“…Keratinocytes were among the most abundant cell types. Three keratinocyte clusters were identified: basal keratinocytes, superficial keratinocytes and a third cluster of “intermediate keratinocytes”, likely located between the former two keratinocyte layers and consistent with the three layers of keratinocytes observed in fish skin [29, 30]. Keratinocytes were abundant in all samples, but notably increased at 48h and 60h post infection only in coho salmon (Fig.1 e,f).…”

“…The detection of neural crest cells, red blood cells, and muscle cells predominately in trunk skin samples (Fig. 1 e,f), is consistent with expectations of greater abundance of these cell types in the trunk skin than in the fins [30] given the potential to cut deeper into the dermal layer. Additionally, several clusters of neuronal and glial cells were observed, but most were observed in a single sample per species (Fig.…”

Histological and Transcriptomic Characterization of Full-Thickness Skin Wound Healing in Maraena Whitefish (Coregonus maraena Bloch, 1779)

“…In fishes, the repair tissue typically consists of connective tissue, fibroblasts, myofibroblasts, inflammatory and immune cells, and blood vessels. The granulation tissue also exhibits hyperpigmentation due to melanocytes infiltration [ 3 ], which was similarly observed in the present study. An inflammatory response was detected in experimentally injured maraena whitefish alongside granulation tissue formation.…”

Novel Antimicrobial Protein Fibroblast Growth Factor 8 Accelerates Skin Wound Healing via Directly Inhibiting Bacteria and Activating Glycolysis

“…In general, skin damage in fish is negatively correlated with their disease resistance. [28] Consistent with this, we found that after skin wounds, the bacterial load at the wound site significantly increased in grass carp (Figure 4A), especially the pathogenic bacteria Aeromonas (Figure 4B). Subsequently, as shown in Figure S5A,B (Supporting Information), HE staining revealed severe tissue damage and bleeding after skin wounds, consistent with the sepsis symptoms induced by Aeromonas.…”

Keratinocytes Drive the Epithelial Hyperplasia Key to Sea Lice Resistance in Coho Salmon

“…Neural crest cells were characterized by multiple pigment cell genes (Table 1) including ltk , which directs multipotent neural crest cell development into pigment cells in zebrafish [56], suggesting these cells are pigment cell progenitors. The detection of neural crest cells, red blood cells, and muscle cells predominately in trunk skin samples (Fig.1 e,f), is consistent with expectations of greater abundance of these cell types in the trunk skin than in the fins [30] given the potential to cut deeper into the dermal layer. Additionally, several clusters of neuronal and glial cells were observed, but most were observed in a single sample per species (Fig.1 e,f ) suggesting they comprise neural structures which are present sporadically throughout the skin (e.g., peripheral axons [34], or the lateral line).…”

“…Keratinocytes were among the most abundant cell types. Three keratinocyte clusters were identified: basal keratinocytes, superficial keratinocytes and a third cluster of “intermediate keratinocytes”, likely located between the former two keratinocyte layers and consistent with the three layers of keratinocytes observed in fish skin [29, 30]. Keratinocytes were abundant in all samples, but notably increased at 48h and 60h post infection only in coho salmon (Fig.1 e,f).…”

“…The detection of neural crest cells, red blood cells, and muscle cells predominately in trunk skin samples (Fig. 1 e,f), is consistent with expectations of greater abundance of these cell types in the trunk skin than in the fins [30] given the potential to cut deeper into the dermal layer. Additionally, several clusters of neuronal and glial cells were observed, but most were observed in a single sample per species (Fig.…”

Histological and Transcriptomic Characterization of Full-Thickness Skin Wound Healing in Maraena Whitefish (Coregonus maraena Bloch, 1779)

“…In fishes, the repair tissue typically consists of connective tissue, fibroblasts, myofibroblasts, inflammatory and immune cells, and blood vessels. The granulation tissue also exhibits hyperpigmentation due to melanocytes infiltration [ 3 ], which was similarly observed in the present study. An inflammatory response was detected in experimentally injured maraena whitefish alongside granulation tissue formation.…”

Novel Antimicrobial Protein Fibroblast Growth Factor 8 Accelerates Skin Wound Healing via Directly Inhibiting Bacteria and Activating Glycolysis

“…In general, skin damage in fish is negatively correlated with their disease resistance. [28] Consistent with this, we found that after skin wounds, the bacterial load at the wound site significantly increased in grass carp (Figure 4A), especially the pathogenic bacteria Aeromonas (Figure 4B). Subsequently, as shown in Figure S5A,B (Supporting Information), HE staining revealed severe tissue damage and bleeding after skin wounds, consistent with the sepsis symptoms induced by Aeromonas.…”

Keratinocytes Drive the Epithelial Hyperplasia Key to Sea Lice Resistance in Coho Salmon

“…Neural crest cells were characterized by multiple pigment cell genes (Table 1) including ltk , which directs multipotent neural crest cell development into pigment cells in zebrafish [56], suggesting these cells are pigment cell progenitors. The detection of neural crest cells, red blood cells, and muscle cells predominately in trunk skin samples (Fig.1 e,f), is consistent with expectations of greater abundance of these cell types in the trunk skin than in the fins [30] given the potential to cut deeper into the dermal layer. Additionally, several clusters of neuronal and glial cells were observed, but most were observed in a single sample per species (Fig.1 e,f ) suggesting they comprise neural structures which are present sporadically throughout the skin (e.g., peripheral axons [34], or the lateral line).…”

“…Keratinocytes were among the most abundant cell types. Three keratinocyte clusters were identified: basal keratinocytes, superficial keratinocytes and a third cluster of “intermediate keratinocytes”, likely located between the former two keratinocyte layers and consistent with the three layers of keratinocytes observed in fish skin [29, 30]. Keratinocytes were abundant in all samples, but notably increased at 48h and 60h post infection only in coho salmon (Fig.1 e,f).…”

“…The detection of neural crest cells, red blood cells, and muscle cells predominately in trunk skin samples (Fig. 1 e,f), is consistent with expectations of greater abundance of these cell types in the trunk skin than in the fins [30] given the potential to cut deeper into the dermal layer. Additionally, several clusters of neuronal and glial cells were observed, but most were observed in a single sample per species (Fig.…”

Histological and Transcriptomic Characterization of Full-Thickness Skin Wound Healing in Maraena Whitefish (Coregonus maraena Bloch, 1779)

“…In fishes, the repair tissue typically consists of connective tissue, fibroblasts, myofibroblasts, inflammatory and immune cells, and blood vessels. The granulation tissue also exhibits hyperpigmentation due to melanocytes infiltration [ 3 ], which was similarly observed in the present study. An inflammatory response was detected in experimentally injured maraena whitefish alongside granulation tissue formation.…”

Novel Antimicrobial Protein Fibroblast Growth Factor 8 Accelerates Skin Wound Healing via Directly Inhibiting Bacteria and Activating Glycolysis

“…In general, skin damage in fish is negatively correlated with their disease resistance. [28] Consistent with this, we found that after skin wounds, the bacterial load at the wound site significantly increased in grass carp (Figure 4A), especially the pathogenic bacteria Aeromonas (Figure 4B). Subsequently, as shown in Figure S5A,B (Supporting Information), HE staining revealed severe tissue damage and bleeding after skin wounds, consistent with the sepsis symptoms induced by Aeromonas.…”