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Algae, macromolecules, tissue engineering, biomaterials, natural biomaterials, biocompatible, bone tissue, cardiovascular tissue
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Nurkolis F, Taslim NA, Hardinsyah H et al. Algal-derived macromolecules and their composites: From synthetic biology to biomedical applications in bone and cardiovascular tissue engineering [version 1; peer review: 1 approved with reservations]. F1000Research 2023, 12:65 (https://doi.org/10.12688/f1000research.129725.1)
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Review
Algal-derived macromolecules and their composites: From synthetic biology to biomedical applications in bone and cardiovascular tissue engineering
[version 1; peer review: 1 approved with reservations]
PUBLISHED 16 Jan 2023
OPEN PEER REVIEW
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This article is included in the Cell & Molecular Biology gateway.
Abstract
Corresponding author:
Nurpudji Astuti Taslim
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No competing interests were disclosed.
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The author(s) declared that no grants were involved in supporting this work.
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© 2023 Nurkolis F et al.
This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
How to cite: Nurkolis F, Taslim NA, Hardinsyah H et al. Algal-derived macromolecules and their composites: From synthetic biology to biomedical applications in bone and cardiovascular tissue engineering [version 1; peer review: 1 approved with reservations]. F1000Research 2023, 12:65 (https://doi.org/10.12688/f1000research.129725.1)
First published: 16 Jan 2023, 12:65 (https://doi.org/10.12688/f1000research.129725.1)
Latest published: 16 Jan 2023, 12:65 (https://doi.org/10.12688/f1000research.129725.1)
Introduction
Algae are a group of autotrophic eukaryotic organisms. They can be classified as microalgae and macroalgae, and are found in marine and freshwater environments (Borghans et al., 2008; Wang et al., 2017; Khan, Shin, and Kim, 2018; Sharma, Kanchi, and Bisetty, 2019). Algal extracts, such as polysaccharides, are frequently used as polymer binding agents in bone tissue engineering to promote tissue growth and proliferation because of their immunomodulatory, anti-inflammatory, antibacterial, and antioxidant activities (Raposo et al., 2015; Barua et al., 2019; Nour et al., 2019).
Macro- and microalgae are the latest sources of macromolecules and their alternative derivatives, such as carotenoid molecules found in the Chlorophyceae family, which includes microalgae Dunaliella, Chlorella, Muriellopsis, Haematococcus, and Chlamydomonas spp. (Berthon et al., 2017; Sayin et al., 2020; El-Chaghaby and Rashad, 2021). Furthermore, cyanobacteria also contain phycobiliproteins, accounting for 40% of these phycobiliproteins’ overall dissolved protein content (El-Chaghaby and Rashad, 2021). Macromolecule polysaccharide derivatives include chitin, fucoidans, carrageenans, and alginate, which are abundant (up to 76% of dry weight) in macroalgae species, including Ulva, Ascophyllum, Palmaria, and Porphyra sp. (Mallik et al., 2020; El-Chaghaby and Rashad, 2021). Macromolecules, especially collagen, are derived from algae and are generally complex macroproteins that comprise 20%–30% of all proteins found in living organisms (Coppola et al., 2020; Joyce et al., 2021) and represent the extracellular matrix’s main structural component in all connective and interstitial tissues of the parenchymal organs (Kim et al., 2020; Srivastava, 2022).
Collagen is well known for its uniqueness as a structural support for biomedical applications such as skin implants, medicines, cosmetics, the leather and film industries, diagnostic imaging, and therapeutic delivery (Coppola et al., 2020). Collagen can be used in various applications due to its excellent biocompatibility and degradability (Zhao et al., 2013; Wahyudi et al., 2016; Felician et al., 2018). In addition, collagen and macromolecules derived from natural biomaterials have weak immunogenicity, reducing rejection risk when ingested or injected (implanted) into different body parts (Coppola et al., 2020). Historically, most of the available collagen was extracted from the waste of the cattle and pig processing industries (Matinong et al., 2022). Nevertheless, over recent decades, the use of macromolecules derived from these sources has been restricted and prohibited (Gómez-Guillén et al., 2011; Coppola et al., 2020). This ban may be attributed to reasons such as the religious restrictions of Islam, Hindu, and Judaism, who account for 38.4% of the world’s population, and the possibility of being a disease transmission route (Coppola et al., 2020).
The current needs of tissue engineering products have not been met as there is a challenge in developing ideal materials for bone and cardiovascular tissue regeneration. Therefore, this issue emphasizes the importance of using algae as a source of macromolecules used in the biomedical field, both now and in the future. With advances in biological science and cutting-edge technology, particularly in biosynthesis and synthetic biology, algal-derived macromolecules can be used in biomedical applications using synthetic biology, transforming their chitin derivatives into biomaterials (Dyo and Purton, 2018). This natural biomaterial has been successfully used in biomedicine for various procedures (e.g., wound healing, bone repair, cell scaffolding, antimicrobial, hemostasis, and cartilage repair; Brovold et al., 2018), devices (e.g., composite heart valve material; Rastogi and Kandasubramanian, 2019), cardiovascular applications (Benko et al., 2022), and biological processes (e.g., photoelectricity, electrocatalysis, and adsorption; Bi et al., 2021). In addition to examining the most recent advancements in the biosynthesis of algal-derived biomaterials, this review aims to interpret the most recent findings regarding its potential application in bone and cardiovascular tissue engineering. Furthermore, the topics in this review have not yet been covered extensively in the literature.
Algal-derived macromolecules
The stability and nondegradable properties of synthetic polymers have recently caused the deterioration of environmental quality and highlighted the need for developing bio-based polymers, especially for biomedical purposes (Deng et al., 2021; Cywar et al., 2022). As stated in the Introduction, algae are a potential source of macromolecules and their derivatives are a potential use as biopolymers in biomedicine. The advantages of using algae over other feedstocks for sustainability and the environment are that they have a faster growth rate, resulting in more biomass, act as environmental bioremediators, and are valuable biofuel feedstocks (Banerjee, Singh and Shukla, 2016; Nasr et al., 2020).
Bar-Shai et al. (2021) successfully analyzed the biocompatibility of cellulose derived from two macroalgae seaweeds, Cladophora sp. and Ulva sp. Sargassum cristaefolium (brown macroalgae; Giriwono et al., 2019; Prasedya et al., 2019). In addition, red (Galaxaura oblongata, Corallina elongate, and Cystoseria compressa) and brown (C. compressa and Sargassum vulgare) algae powders have been successfully used and incorporated into polyhydroxyalkanoates, polycaprolactone, and polylactide to make potential biomaterials for the biomedical field (Sayin et al., 2020). They included Caulerpa racemosa, which has collagen properties, according to the latest study (Permatasari et al., 2022). Interestingly, polysaccharide derivatives or potential biopolymers such as chitin, fucoidans, sulfated fucans, sulfated l-fucose polysaccharide, carrageenans, sulfated galactan, laminaran, and alginate are abundant, even reaching 76% of the dry weight contained in macroalgae, mainly the Ulva, Ascophyllum, Palmaria, and Porphyra species (Zia et al., 2017; Azeem et al., 2017; El-Chaghaby and Rashad, 2021).
In addition to macroalgae, microalgae have great potential as a source of macromolecules and their derivatives, albeit to a lesser extent. Among the microalgae known as superfoods, Spirulina sp. contains type II collagen (Darvin et al., 2015; Elbialy et al., 2021; Sonawane et al., 2022) and nanostructured or nanofiber scaffold properties (Morais et al., 2014; Moreira et al., 2021; McCauley et al., 2022). In addition, microalgae of the Chlorophyceae family, such as Dunaliella, Chlorella, Muriellopsis, Haematococcus, and Chlamydomonas spp., contain abundant carotenoid derivatives (Berthon et al., 2017; Sayin et al., 2020; El-Chaghaby and Rashad, 2021). Spirulina also contains phycobiliproteins, which comprise 40% of these phycobiliproteins’ overall dissolved protein content (El-Chaghaby and Rashad, 2021), with promising potential as multifunctional biomaterial scaffolds (Pereira and Rodrigues, 2021). The following section elaborates on using algal-derived biomaterials.
Natural biomaterial properties of algae
One success indicator for biomaterials is their acceptability by the human body, known as biocompatibility. It is crucial for biomaterials to cause the least injury, cytotoxicity, genotoxicity, carcinogenicity, and immunogenicity in their recipients (De Jong et al., 2020; Raut et al., 2020; Hosseinpour et al., 2022). Marine macroalgae Ulva sp. and Cladophora sp. were both nontoxic to fibroblasts, with high viability up to 40 days in vitro (Bar-Shai et al., 2021). Microalgae C. reinhardtii was also highly compatible with mammalian fibroblast cells, showing photosynthetic activity and reducing hypoxia cells’ response in hypoxic simulated environments (Hopfner et al., 2014; Wangpraseurt et al., 2022).
To further simulate and mimic the physiological human extracellular matrix’s properties, polymers are used to form hydrogels. Algae can form hydrogels, especially from their polysaccharides, through physical crosslinking, defined as noncovalent bonding dependent on weak molecular interactions such as hydrogen bonds, causing reversible gel formation (Lee et al., 2012; Martin and Ballet, 2021). Various polysaccharides can form ideal hydrogels for biomedical applications, including ulvan, starch, agarose, porphyrin, and cellulose (Beaumont et al., 2021; Mandal et al., 2022; Lin et al., 2022).
Besides biocompatibility, porosity also plays an essential role in facilitating molecules transport, such as nutrients and oxygen, for cell viability and development (Chhibber et al., 2020). Furthermore, in terms of functionality, differences in porosity could influence its optimal applications, and various pore sizes could promote or hamper cell performance (Loh and Choong, 2013). Ulva sp. was reported to have intermediate pore sizes (10–30 μm), providing abundant attachment sites for cell growth, interactions, proliferation, spread, and migration in various orientations, which can be beneficial, especially to endothelial and dermal cells (Bar-Shai et al., 2021). Various approaches have also been used to produce synthetic biomaterials to match the target tissue’s demands, such as peptide and ceramic based biomaterials,, fibrous meshes, particle leaching with gas foaming methods, and phase separation (Ustunel et al., 2020). Porous bone scaffold fabrication using seaweed-derived alginate successfully created scaffolds with average pore sizes of 100 μm, falling within the trabecular bone’s natural architecture to facilitate nutrient diffusion, blood vessel permeation, and nerve innervation (Hatton et al., 2019).
Biomedical applications of algal-derived macromolecules and their composites
The exciting potential of biomaterials from algae macromolecules and their derivatives has been previously shown. Furthermore, the upcoming section discusses their potential applications in the biomedical field, especially in bone and cardiovascular tissue (Table 1). Tissue engineering is a biomedical engineering discipline that uses the appropriate combination of cells, techniques, material methods, and biochemical and physicochemical factors to restore, maintain, enhance, or replace various biological tissue types through biosynthesis or synthetic biology (Li et al., 2018).
Table 1. Studies in algae for bone and cardiovascular tissue engineering.
| Articles | Study type | Scaffold type | Tissue target | Outcome | Algae type |
|---|---|---|---|---|---|
| Turhani et al. (2005) | In vitro | Ceramic material (C GRAFT/Algipore) | Osteoblast cells | In vitro proliferation and differentiation of human osteoblast-like cells were supported on the surface of a hydroxyapatite ceramic bone substitute made from calcified red algae. The material may be suitable for scaffolds in tissue engineering in vivo. | Red algae |
| Oliveira et al. (2007) | Laboratory X-ray | Bone filler and tissue engineering scaffolds | Bone | Bioceramics derived from Coralline officinallis showed good clinical potential for bone tissue engineering applications. | Red algae |
| Changotade et al. (2008) | In vitro | Lubboc bone biomaterial | Human osteoblasts | Besides favoring cell proliferation, low-molecular-weight fucoidan increased osteoblastic differentiation marker expression (e.g., alkaline phosphatase and collagen type I) and mineral deposition, indicating that fucoidan may have therapeutic applications in bone substitutes and regeneration. | Brown algae |
| Toskas et al. (2012) | In vitro | Ulvan and chitosan scaffolds | 7F2 osteoblasts | Both ulvan and ulvan/chitosan membranes supported 7F2 osteoblasts’ adhesion and growth while preserving their morphology and survival. As prospective scaffold materials, ulvan and chitosan, each with distinctive features, may significantly influence biological applications. | Green seaweed |
| Ali and Hasan (2012) | In vitro | Extract | Bone marrow-derived mesenchymal stem cell lines | When combined directly with mesenchymal stem cells, this natural extract promoted cellular differentiation into healthy bone-forming cells. This technique can naturally strengthen bones without the unfavorable side effects of standard pharmacotherapeutic drugs. | Brown algae |
| Yeo, Jung, and Kim (2012) | In vitro | Phlorotannin-conjugated polycaprolactone (PCL)/β-tricalcium phosphate (β-TCP) composite scaffolds | MG63 osteoblast-like cells | Phlorotannin was an effective additional bioactive agent for promoting bone tissue formation in PCL/β-TCP composite scaffolds. | Brown algae |
| Barros et al. (2013) | In vitro | Polymeric components of carboxymethylesized ulvan and chitosan | Bone cement | When carboxymethyl chitosan or carboxymethyl ulvan were added to the cement formulation, they improved its mechanical properties, created non-cytotoxic cement, and encouraged the diffusion of Ca- and/or P-based moieties from the bone cement’s surface to its bulk. | Green algae |
| Wilson et al. (2017) | In vitro | Printable bioink | Mouse osteoblasts | Due to its great structural fidelity and adjustable mechanical stiffness, it may be used to 3D print intricate, substantial, cell-laden tissue structures for regenerative medicine. | Red algae |
| Singelyn et al. (2012) | In vivo | Injectable hydrogel made from decellularized ventricular extracellular matrix | Rat myocardial infarction model | Injecting the substance improved endogenous cardiomyocytes in the infarct region and preserved cardiac function without causing arrhythmias in a rat myocardial infarction model. | Brown algae |
| Duan et al. (2013) | Laboratory 3D printing | Alginate/gelatin valve hydrogel discs | Aortic root sinus smooth muscle cells and aortic valve leaflet interstitial cells | 3D bioprinting makes it possible to create conduits for the aortic valve that are heterogeneously encased and anatomically complicated. | |
| Lee et al. (2013) | Clinical trial | Algisyl-LVR | Left ventricle wall stress | Algisyl-LVR improved function and lowered left ventricular wall stress in failing hearts. | Brown algae |
| Sabbah et al. (2013) | In vivo | Alginate Hydrogel implants | Left ventricular (LV) wall thickness | Circumferential apnea-hypopnea index (AHI) wall thickness augmentation improved LV structure and function in dogs with heart failure (HF). The outcomes favored further AHI development for treating patients with advanced HF. | Brown algae |
| Haraguchi et al. (2017) | In vitro | Thicker 3D tissue | C2C12 mouse myoblasts and rat cardiac cells | Cocultivation with algae enabled the development of 160 m thick cardiac tissues by increasing the culture conditions for thicker tissues. Therefore, the authors suggested a “symbiotic recycling system” comprising mammalian cells and algae. | Green algae |
Bone tissue engineering
Bone damage or defects often result from trauma, degenerative diseases, tumor removal, and disruptions during their growth or formation (Wong, 2010). About 700,000 patients undergo open-heart surgery annually in the United States, of which 3% suffer from poor sternum healing after surgery (Wong, 2010). Bone damage that is large enough or involves extensive tissue cannot heal without critical defect intervention, and surgery is needed to reconstruct the vital defect and restore bone functionality. Bone reconstruction by surgical intervention requires a material or scaffold to aid successful reconstruction (Wong, 2010; Harb, 2022). Modern network engineering technology is developing rapidly to facilitate tissue regeneration as needed. Generally, scaffold tissue engineering technology is a factor that significantly affects bone tissue reconstruction success (Wong, 2010). Hydrogel is one often used scaffold and is a biopolymer technology with physical and chemical crosslinking (Bearzi et al., 2014; Muir and Burdick, 2020).
As previously explained, algae are a source of macromolecules and their derivatives that may be potential scaffolds for biopolymers in biomedical applications (Table 1). Various algae polysaccharide derivatives have been engineered for cartilage, intervertebral discs, and skeletal muscle (Korzeniowska et al., 2018; Perrotti et al., 2017; Sheikh et al., 2019). Sulfated polysaccharides from macroalgae (S. cristaefolium, G. oblongata, C. elongate, C. compressa, and S. vulgare) can form hydrogels and scaffolds and even imitate the extracellular matrix to increase alkaline phosphatase activity and stem cell biomineralization and differentiation for bone tissue regeneration (Venkatesan et al., 2019; Kuznetsova et al., 2020). Steffens et al. (2013) identified the mechanism underlying such functions through extensive research on mice. A Chlorococcum littorale scaffold improved C57/B16 mouse liver-derived mesenchymal stem cell adherence and proliferation (Steffens et al., 2013; Haraguchi et al., 2017; Bilge et al., 2021). In addition, using methacrylate anhydride-functionalized ulvan as a bone scaffold has also been reported (Dash et al., 2014; Zhong et al., 2021). Fucose-containing sulfated polysaccharides, often referred to as fucans and fucoidans, from brown algae can form 3D structures with stable biocompatibility and biodegradability with other composites that can trap therapeutic agents, cells, or growth factors (Pajovich and Banerjee, 2017; Nunes and Coimbra, 2019). Biosilisification and collagen layering by brown algae in biomimetic composites have been proposed to replace bone grafts producing bone morphogenetic protein-2 (BMP2) to achieve enhanced bone regeneration grafting (Lee et al., 2021). Type I and II collagen derived from microalgae Spirulina sp. (Darvin et al., 2015; Bortolini et al., 2022) has also shown promise as a biomaterial for scaffolds and hydrogels to repair bone damage (Li et al., 2021). Further clinical studies and using more advanced technological methods with algal biomaterials in the bone tissue engineering field are strongly encouraged.
Cardiovascular tissue engineering
Besides bone tissue engineering, algae rich in macromolecules have the potential to be used in cardiovascular tissue engineering. An editorial by Prof. Aikawa Elena mentioned that calcified aortic valve stenosis is a significant health burden in most countries, with valve intervention the only effective treatment, resulting in 300,000 artificial heart valves implanted annually (Elena, 2022). Therefore, further exploration is needed to maintain the sustainability and availability of these artificial valves through alternative algal-derived macromolecule uses (Rastogi and Kandasubramanian, 2019; Benko et al., 2022). Artificial heart valves are obtained through synthetic biology by engineering scaffold-based tissues from biodegradable synthetic polymer composites (Rippel, Ghanbari, and Seifalian, 2012; Long et al., 2020). At least 12% of patients aged >75 years suffer from heart valve disease (Oh et al., 2020). Patients with mechanical valves require lifelong anticoagulation due to high thromboembolism risk, while biological valve resistance is poor, rapidly leading to calcification or lobular degeneration. To address these deficiencies, researchers developed a tissue-engineered heart valve with repair and remodeling capabilities, low immunogenicity, and high durability from algal-derived macromolecules (Long et al., 2020; Chandika et al., 2020).
Natural macromolecules have weak immunogenicity, reducing rejection risk when ingested or implanted into different bodies (Coppola et al., 2020). Several studies have shown complete pericardium decellularization and the ability of macromolecules scaffold composites to induce fibroblast chemotaxis and aid anatomically correct valve-shaped construction (Tedder et al., 2008; Huang et al., 2018; Rodrigues et al., 2018). Polysaccharide derivatives, including alginates, fucoidans, chitin, porphyrin, and their derivatives, have been tested in blood vessel, heart valve, and even liver engineering (Korzeniowska et al., 2018; Bacakova, Novotná, and Parizek, 2014). Chitin, polysaccharide, and their derivatives are extracted, isolated, and calcified from algae and further made into composites with chitosan molecules with a heart valve architecture for use in vascular engineering (Ciolacu, Nicu, and Ciolacu, 2022; Albanna et al., 2012). Algal-derived macromolecules and their composites are scaffolds with promising cardiovascular tissue engineering applications, especially heart valve manufacture (Table 1). Many studies have used various models to show the preclinical relevance of tissue-engineered heart valves (Fu et al., 2017; Taramasso et al., 2015). Further innovations in the use of algal-derived macromolecules and their derivatives with other composite combinations are highly recommended.
Future directions and implications for algal-derived macromolecules
The multipotentiality of algae as biomaterials in bone and cardiovascular tissue engineering will face many challenges. First, plant-based molecules or natural macromolecules (mainly algae) encourage body tissues to synthesize macromolecules by providing the required substances. However, the question arises about algal macromolecule bioavailability and yield. Gao et al. (2013) highlighted the crucial roles of nanotechnology and nanocomposite applications in modifying macromolecules. Using nanotechnology with its improved surface-to-area volume ratio may address the low quantity of collagen extracted from algae (Mokhena et al., 2020; Lo and Fauzi, 2021). Using in vitro models or bioreactors was encouraged for research translation since the variables, composition, and target populations can be controlled and adjusted before continuing to preclinical or clinical trials (Stassen et al., 2017; Mobini et al., 2019). However, the fabrication processes significantly impact the properties of marine macromolecule-based structures, such as mechanical properties, internal pore size and structure, cell encapsulation, degradation rate, and incorporation of bio-additives into the scaffolds (Liu et al., 2022). The lower denaturation temperature of marine collagen, especially from algae, is a significant drawback since it impacts both the processing environment and the scaffold properties in vitro and in vivo (Shahidi et al., 2019; Akita et al., 2020). Iravani and Soufi (2021) also mentioned that the clinical use of scaffolds for tissue engineering applications still faces many complex problems, such as donor-site morbidity, a lack of resilience and mechanical strength, consistent volume loss, and fibrous capsular structure.
In addition, using algae as natural biomaterials also faces several challenges due to limited available studies. To fully benefit from algae in emergency medicine fields, such as orthopedic trauma and cardiovascular damage, a solid guideline regarding the use and manufacture of these products needs to be established (Vunjak-Novakovic et al., 2010; Lee and Mooney, 2012; Łabowska et al., 2020). The establishment of the guidelines is a crucial step so that the other factors in using algae, such as the products’ optical features, emission color control, and other standards, can be met to maximize their benefits (Deng, Ngo, and Guo, 2022; Fernandes et al., 2022). In the face of such challenges, more clinical trials are needed to gather sufficient data to identify the optimal method for manufacturing algae-derived macromolecules for biomedical field applications. After such guidelines have been established, more experiments in clinical settings must be conducted. Most studies in this field have presented laboratory-level evidence, with only a few performed in clinical settings (Ewers, 2005; Taemeh et al., 2020; Wang, Chen, and Zhang, 2021; Akimoto et al., 2022). Since existing technologies, such as magnetic resonance imaging and other modalities, could be used to monitor new tissue development from algal-derived macromolecules, the successes of such experiments will contribute little to forming conclusions about the benefit of such therapies due to the nature of in vivo studies using experimental animals instead of human subjects (Kotecha et al., 2017).
Moreover, adverse algal-derived macromolecule effects must also be considered and researched thoroughly to identify potential failures of such use (Hickman et al., 2018; Iravani and Varma, 2022). There is no doubt about the functions and benefits of macroalgae and microalgae, even though research is still needed to determine their usefulness and safety in human-based settings. However, this does not reduce the possible use of algal-derived macromolecules in biomedical settings, especially tissue dressings (McCauley et al., 2022). All limitations exist mainly due to the lack of proper techniques and guidelines, human research, and funding. Such studies will increase in frequency and quality provided the benefit of micro- and macro-algae continues to be researched thoroughly (De Anda-Flores et al., 2022).
Conclusions
Previous reports have used synthetic biology to show that algae rich in macromolecules and their derivatives have potential biomedical applications in bone and cardiovascular tissue engineering (Figure 1). Algae use benefits from lower immunogenicity, reducing rejection risk when ingested (implanted) into different body parts (Coppola et al., 2020). As illustrated in Figure 1, biomaterials derived from algae macromolecules have been successfully used in various biomedical fields, such as wound healing, bone repair, cell scaffolding, cartilage repair, heart valve composite materials, and other cardiovascular uses (Bi et al., 2021).
Figure 1. Algal-derived macromolecules and their composites in bone and cardiovascular tissue engineering (figure created by Fahrul Nurkolis with BioRender.com premium license – all permissions granted).
The problems in using such products arise from the lack of effective guidelines, human trials, and funding to perform the required research. Therefore, we encourage more studies on algal-derived macromolecules with a broader biomedical scope that can provide the latest innovations in their use. More in-depth research using a nanotechnology approach is needed to explore the potential of algae macromolecules as natural biomaterial scaffolds for medical applications due to their properties and benefits that will bring future developments in the medical field.
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Nurkolis F, Taslim NA, Hardinsyah H et al. Algal-derived macromolecules and their composites: From synthetic biology to biomedical applications in bone and cardiovascular tissue engineering [version 1; peer review: 1 approved with reservations]. F1000Research 2023, 12:65 (https://doi.org/10.12688/f1000research.129725.1)
NOTE: If applicable, it is important to ensure the information in square brackets after the title is included in all citations of this article.
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Greco I. Reviewer Report For: Algal-derived macromolecules and their composites: From synthetic biology to biomedical applications in bone and cardiovascular tissue engineering [version 1; peer review: 1 approved with reservations]. F1000Research 2023, 12:65 (https://doi.org/10.5256/f1000research.142428.r344711)
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Reviewer Report 05 Dec 2024
Immacolata Greco,
Universite Libre de Bruxelles, Brussels, Brussels, Belgium
Approved with Reservations
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Comment 1
The definition of biocompatibility is very broad. In page 4 it is mentioned “One success indicator for biomaterials is there acceptability by the human body, known as biocompatibility”, it would be beneficial to give more details on ... Continue reading
The definition of biocompatibility is very broad. In page 4 it is mentioned “One success indicator for biomaterials is there acceptability by the human body, known as biocompatibility”, it would be beneficial to give more details on ... Continue reading
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HOW TO CITE THIS REPORT
Greco I. Reviewer Report For: Algal-derived macromolecules and their composites: From synthetic biology to biomedical applications in bone and cardiovascular tissue engineering [version 1; peer review: 1 approved with reservations]. F1000Research 2023, 12:65 (https://doi.org/10.5256/f1000research.142428.r344711)
The direct URL for this report is:
https://f1000research.com/articles/12-65/v1#referee-response-344711
https://f1000research.com/articles/12-65/v1#referee-response-344711
NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article.
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