Swim bladder-derived biomaterials: structures, compositions, properties, modifications, and biomedical applications

Abstract

Animal-derived biomaterials have been extensively employed in clinical practice owing to their compositional and structural similarities with those of human tissues and organs, exhibiting good mechanical properties and biocompatibility, and extensive sources. However, there is an associated risk of infection with pathogenic microorganisms after the implantation of tissues from pigs, cattle, and other mammals in humans. Therefore, researchers have begun to explore the development of non-mammalian regenerative biomaterials. Among these is the swim bladder, a fish-derived biomaterial that is rapidly used in various fields of biomedicine because of its high collagen, elastin, and polysaccharide content. However, relevant reviews on the biomedical applications of swim bladders as effective biomaterials are lacking. Therefore, based on our previous research and in-depth understanding of this field, this review describes the structures and compositions, properties, and modifications of the swim bladder, with their direct (including soft tissue repair, dural repair, cardiovascular repair, and edible and pharmaceutical fish maw) and indirect applications (including extracted collagen peptides with smaller molecular weights, and collagen or gelatin with higher molecular weights used for hydrogels, and biological adhesives or glues) in the field of biomedicine in recent years. This review provides insights into the use of swim bladders as source of biomaterial; hence, it can aid biomedicine scholars by providing directions for advancements in this field.

Keywords: Biological adhesive; Cardiovascular repair; Hydrogel; Swim bladder; Tissue repair.

Fig. 1

An overview of the structures, compositions, properties, modifications, and biomedical applications of swim bladder-derived biomaterials

Fig. 2

Summary of relevant reports on swim bladder-derived materials retrieved from Web of Science (WOS) on the topic, among which the number of review papers is counted (A, January 1, 1900–December 31, 2023). Statistical data of publications per 20-year span containing the words "swim bladder" B or "fish bladder" C and "material" (January 1, 1900–December 31, 2023), and the data between January 1, 2014, and December 31, 2023 (inserted images in B and C)

Fig. 3

Shape, composition, and relative position of the swim bladder in fish (A). Reproduced with permission from Ref. [53]. Copyright 2006, Wiley-Liss, Inc. Scheme of the structures and compositions of the posterior chambers (B)

Fig. 4

Schematic of the mechanism of GA crosslinking (A). Reprinted with permission from Ref. [111]. Copyright 2007, Wiley Periodicals, Inc. Mechanical properties of the swim bladder and bovine pericardium before and after crosslinking (B, C); Staining of tissue to show calcification after implantation into sheep pulmonary valve (D). B is the circumferential direction and C is the axial direction. BP, bovine pericardium; SB, swim bladder; UN, un-crosslinked; and GA, glutaraldehyde. The upper and lower borders of the box represent upper and lower quartiles, respectively. The horizontal line indicates the median value. Statistical significance is indicated as follows: *, p < 0.05; **, p < 0.01; and ***, p < 0.001. Reprinted with permission from Ref. [85]. Copyright 2021, Royal Society of Chemistry

Fig. 5

Schematic diagram of the reaction mechanism of BDDGE crosslinking. Reprinted with permission from Ref. [123]. Copyright 1999, John Wiley & Sons, Inc

Fig. 6

Representative histological images of wound sections taken after 7, 14, 21, and 28 days of Masson’s trichrome staining. Swim bladder tissue was implanted on to a skin surface wound in New Zealand white rabbits. BV, blood vessel; D, dermis; E, epithelial layer; F, fibroblasts. Reprinted with permission from Ref. [115]. Copyright 2015, Elsevier B.V

Fig. 7

Schematic representation of the self-crosslinking mechanism with EDC/NHS (A). Morphology of L929 cells on crosslinked swim bladder with GA (GLUT) and self-crosslinked swim bladder with EDC/NHS (EDC) (B). Calcification of subcutaneous implants in rats (alizarin red staining, C scale bar = 100 mm. Reprinted with permission from Ref. [48]. Copyright 2021, IOP Publishing, Ltd

Fig. 8

Experimental results of acellular swim bladder-loaded AgNPs: Optical photographs of swim bladder before and after decellularization and impregnation with AgNPs (A), where a1, a2, and a3 represent fresh swim bladder, decellularized, and AgNP-soaked samples, respectively; histological staining analysis of fresh swim bladder before (b1, b4, and b7) and after decellularization with 0.5% SDS (b2, b5, and b8) and 1.0% SDS (b3, b6, and b9) (B), among which b1–b3, b4–b6, and b7–b9 are H&E, picro-fuchsin, and orcein-picroindigocarmine staining, respectively; bacterial experiment results (C), in which BS, EC, PA, ST and SA represent Bacillus subtilis, Escherichia coli, Pseudomonas aeruginosa, Salmonella typhimurium and Staphylococcus aureus, respectively. Reprinted with permission from Ref. [27]. Copyright 2020, Elsevier B.V

Fig. 9

Swim bladder tissue treated using different decellularized methods: Details of different decellularized treatment methods (A); DAPI staining before and after decellularized treatment (B), where (a) is fresh swim bladder, and (b–f) correspond to groups A–E in (A), respectively; the physical structure of the tissue was observed using H&E staining before and after decellularized treatment (C); DNA test results after decellularized treatment (D); hemolysis rate after decellularized treatment (E); in vitro co-culture assay with mouse embryonic fibroblasts (MEFs) (F), in which (a, c) and (b, d) are groups E and B in image A; immunogenic assessment of three months after dural repair (G), in which a is the overall appearance of the excised material and b-d show the fibroblast distribution and inflammation at the dural repair site. Reprinted with permission from Ref. [47]. Copyright 2019, Taylor & Francis

Fig. 10

Schematic diagram of the preparation of swim bladder-derived small-diameter vascular grafts by the rolling process (A) and the histological staining and morphological observation results of the extracts after celiac artery replacement in rats (B). Reprinted with permission from Ref. [12]. Copyright 2019, Wiley–VCH GmbH

Fig. 11

"Dry membrane" material (A) made of swim bladder-derived biomaterial. Reprinted with permission from Ref. [48]. Copyright 2021, IOP Publishing, Ltd. Overall appearance (B) of the pulmonary valves implanted in sheep. Reprinted with permission from Ref. [85]. Copyright 2021, Royal Society of Chemistry

Fig. 12

Performance comparison of SBC hydrogel (SBC gel) with calf skin collagen hydrogel (CSC gel) and porcine skin collagen hydrogel (PSC gel). Photographic and polarizing microscope images (POM) of SBC gel (A); photographic and POM images of CSC gel (B); photographic and POM images of PSC gel (C); SEM images of SBC solution (SBC sol), SBC gel, CSC gel, and PSC gel (D); differential scanning calorimetry (DSC) results of SBC sol, SBC gel, CSC solution (CSC sol), CSC gel, PSC solution (PSC sol), and PSC gel (E); rheological test results of SBC gel (F). Reprinted with permission from Ref. [181]. Copyright 2015, Royal Society of Chemistry

Fig. 13

Preparation and bonding effect of fish swim bladder glue (FSG): Schematic diagram of preparation and mechanism (A), adhesive property of FSG on rat skin, and the effect of promoting wound healing (B). Reprinted with permission from Ref. [36]. Copyright 2021, Wiley–VCH GmbH