Degradable metallic biomaterials for cardiovascular applications 13 K. Sangeetha1, A.V. Jisha Kumari2, Jayachandran Venkatesan3, Anil Sukumaran4, S. Aisverya1 and P.N. Sudha1 1 PG & Research Department of Chemistry, D.K.M. College for Women, Vellore, Tamil Nadu, India, 2Department of Chemistry, Tagore Engineering College, Chennai, Tamil Nadu, India, 3Department of Marine Bio Convergence Science and Marine Bioprocess Research Center, Pukyong National University, Busan, South Korea, 4Department of Preventive Dental Sciences, College of Dentistry, Prince Sattam Bin Abdulaziz University, Alkharj, Saudi Arabia Abstract In the last decade, the use of biomaterials has proven to improve the quality of life. Several metallic biomaterials have been developed and applied in the medical fields. The idea of biodegradable implants came into existence after getting the awareness that there is a need for an implant to naturally degrade after fulfilling its objectives. This chapter concentrates especially on degradable metals, although there are also materials made of polymers and ceramics for cardiovascular applications. The bioresorbable material “metal” is more advantageous in cardiovascular application over polymers and ceramic due to their remarkable properties including high impact strength, high ductility, and high strain energy. In this chapter we glance over the cardiovascular applications of metals including heart valves, stents, pacemaker, etc. From the various sources of literature reviews, in this chapter it can be confidently declared that biocompatible metals will continue to be used in various cardiovascular applications in near future with further advancements and new uprising biofunctionalities. We also discussed the new challenges and directions of metals in cardiovascular research. Keywords: Coronary artery; stent; pacemaker; stent grafting 13.1 Introduction The development of metallic biomaterials for the application of cardiovascular is one of the trending fields in material science. In the early years the implantation of metals experienced several drawbacks such as corrosion, insufficient strength Fundamental Biomaterials: Metals. DOI: https://doi.org/10.1016/B978-0-08-102205-4.00013-1 © 2018 Elsevier Ltd. All rights reserved. 286 Fundamental Biomaterials: Metals problems, etc. [1]. Shortly after the introduction of 18-8 stainless steel in the 1920s and titanium alloys, again the metal implantation was of great interest to researchers. These metals were nondegradable and in the case of permanent implanting it required a second surgery for removing the implant [2]. This major limitation urged the necessity for the evolution of the next generation metal implantation. The concept of using metals as a biodegradable material over polymers was a new and much more recent technique than that of polymers. The first metal to be successfully implanted as a cardiovascular implant was magnesium in the year 1938 by McBride. In the early years the corrosion of metal was considered as a huge drawback. In certain cases such as magnesium and iron the corrodibility results in implanting them as biodegradable implants. These metals will perform the healing of the affected tissues followed by generation of new tissues and will start to degrade slowly. The metal should participate in the healing process without showing any adverse effect. Nowadays the more advanced metallic biomaterials comprised of nontoxic and allergy-free elements have also been developed and have revolutionized cardiovascular surgery [3]. When a biomaterial is implanted in the body, whether it is inert or degradable, the biomaterial will induce reactions with the surrounding tissues which are termed as “host responses.” This host response was considered as a parameter to access the biocompatibility of the material which will be expected to show minimal toxicity and inflammatory reactions both locally and systematically [4]. The International Organization for Standardization (ISO) and the American Society of Testing and Material (ASTM), establish guidelines to assess the biocompatibility of implant materials and these have undergone in vitro, in vivo tests prior to the clinical human study [5]. 13.1.1 Cardiovascular disease Cardiovascular disease is the prime cause of mortality in the industrialized society and it is considered as a worldwide public health problem. Cardiovascular disease physically damages the cardiac function of heart [6]. The major risk factors associated with cardiovascular disease include smoking, hypertension, obesity, cholesterol, and blood pressure [7] and hence the modification of these risk factors will prevent the mortality due to cardio problems. The World Health Organization (WHO) has reported that the two most frequent types of vascular disease, i.e., ischemic heart disease and stroke, are the most common causes of death worldwide and three out of every 10 deaths is because of cardiovascular disease (WHO, 2014). Cardiac disease is treated by approaches ranging from medications to surgical interventions. In this chapter a broad review of cardiovascular therapy based on different metallic implantations is briefly discussed. Degradable metallic biomaterials for cardiovascular applications 287 13.1.2 Need for using degradable metallic materials in cardiovascular devices The implantation of cardiovascular devices are associated with certain issues like thrombogenesis and extended endothelial dysfunction, and if it implanted into children they cannot adapt as the children grow which requires repeated surgery. In order to overcome these issues the usage of degradable metallic materials were adopted for clinical surgery. Generally in implantation technique, the implants (metal) are in contact with living tissues and hence the implants should be biocompatible and biodegradable. The implantation of cardiovascular devices includes artificial valves, stents, pacemaker cases, and stent grafts. Most of the artificial metal implants are subjected to loads either by static or repetitive and this condition requires an excellent combination of strength and ductility. This is the superiority of metals over ceramics and polymers. For cardiovascular implants the sign of degradation will start only after 1 month of implantation. Among the various metals Mg alloy shows the faster rate of degradation and the process completes within 6 12 months whereas the alloys of iron are completely degraded within 12 36 months [8]. The degradation is associated with corrosion—the oxidation and the dissolution of metals. 13.2 Concept of degradation In the early years bare metals were used as implants which had some major drawbacks such as permanent physical irritation, mismatches in mechanical behavior between the implanted metal vessels and normal vessel areas, and inability to adapt to growth in infant patients [9] which led to later surgical operations to replace the metal at each stages of the patient’s growth. To overcome these major disadvantages the concept of degradable metallic implants was developed in order to improve clinical efficacy. Biodegradable metals (BMs) can be defined as the metals expected to corrode gradually in vivo, with an appropriate host response elicited by released corrosion products, then dissolve completely upon fulfilling the mission to assist with tissue healing with no implant residues. The two main characteristics associated with biodegradable metals are (i) temporary support and (ii) degradation. The metal should possess a positive effect during the process of healing followed by degradation. Hence a considerable amount of components in the metallic implants should be metabolized in the human body with significant degradation rates and modes in the human body [10]. Biodegradable metallic implants have emerged as a promising alternative and will result in reducing the risk of post-implantation side effects and this supports the rapid recovery of blood vessels [11]. Generally the biodegradable metal-based stents have shorter degradation periods of time than the polymer-based implants. Some metals such as magnesium, zinc, and iron already exist in the human body in various amounts which marks them as highly biocompatible [12]. 288 13.3 Fundamental Biomaterials: Metals Classes of biodegradable metals The biodegradable metals are categorized into three main classes and the newly developed metal implants will eventually fall in one of these classes: 1. magnesium-based biodegradable metals; 2. iron-based biodegradable metals; and 3. zinc-based biodegradable metals. 13.4 Metals used in cardiovascular treatment Chemically nonreactive metals are extensively used in the medical field due to their strength and biocompatibility. In the cardiovascular arena other than heart transplantation, metals are used in a wide variety of treatment methods, such as replacement of heart valves, stents for opening of lumen in obstructed blood vessel, in tissue repairing and healing, and treatment of various heart areas such as the septal wall for ventricles and valves [13]. Metals are considered as more suitable compared to polymers for some specific applications which require high strength to bulk ratio. Metals are also extensively used in the replacement of heart valves. Heart valves are constructed from metals such as stainless steel or titanium [14]. Mechanical valves can last the lifetime of a patient, although anticoagulant medications are required for the remainder of their lives because of the higher chance for blood clot formation [15]. Newer stents utilizing cobalt chromium or platinum chromium alloys are used widely for their greater strength [16,17]. Nitinol stents made from a nickel and titanium alloy dominated the market in the past because of their shape-memory properties, but nickel allergies have since eliminated their use [18]. Stents made of nickel titanium alloys are used extensively as they possess unique shape-memory or superelastic properties. Noble metals such as platinum iridium are used in making pacemaker electrodes. Noble metals, stainless steel, and tantalum are used in sensing (nonpacing) electrodes. For most of the cardiovascular treatments, the fatigue life is critical and in such cases metallic alloys are used. Alloys are also used in the preparation of endovascular stents. Magnesium- and Fe-based alloys are the two classes of metals which are mainly used in cardiovascular applications. Several Mg-based alloys have been investigated, including Mg Al [19 22], Mg rare earth [23,24,36,25] and Mg Ca [26] based alloys. Fe-based alloys have been studied, including pure Fe [27,28] and Fe Mn alloys [29,30]. 13.4.1 Revolutionary treatment of coronary artery disease The first revolutionary method widely used in coronary heart disease was balloon angioplasty or percutaneous transluminal coronary angioplasty (PTCA). It was a nonsurgical procedure that relieves narrowing and obstruction of the arteries to the muscle of the heart (coronary arteries). A long thin tube called a catheter is inserted Degradable metallic biomaterials for cardiovascular applications 289 into coronary artery and the balloon is inflated at the blockage site to flatten the plague against the artery wall [31]. Up to 30% 40% of restenosis was observed within 6 months [32] and this higher rate of restenosis led to the second revolutionary treatment called stenting. The coronary stenting has the limitations of thrombosis and hyperplasia [33]. The third revolutionary method was based on coating antiproliferation drugs onto the stent leading to the development of drug-eluting stents (DES). Drug-eluting stents were found to trigger late stent thrombosis due to denudation once the coating washed away [34,35]. And finally the fourth generation was the introduction of biodegradable stents. Nowadays, stainless steel or chrome cobalt or nickel titanium is known as the gold standard for metallic materials for cardiac stents (Fig. 13.1). 13.4.2 Coronary stents Stents are coils serving as a scaffold and are implanted in the artery during angioplasty process in order to limit the negative remodeling of a stented artery. The short- and long-term efficiency of stenting is limited by in-stent restenosis and thrombosis [36,37]. The primary role of a stent is to reduce the risk of restenosis after angioplasty but in about 25% of stenting cases, the restenosis problem still remains which is called as “in-stent restenosis” [38]. In order to avoid these complications the degradable stents were used as an efficient and valid alternative. The proper design with appropriate mechanical and degradation properties is key for the development of this new class of medical device. Angioplasty is a procedure to open the clogged heart arteries also called coronary arteries. After angioplasty the stent should have the ability to minimize the tendency of vessel restenosis which leads to the shrinkage of the lumen [39] and Angioplasty Revolutionary Treatment of Coronary Artery Disease 1st 2nd 3rd Balloon Angioplasty Stenting Drug eluting stents Mechanical Insufficient 1964 1977 Thrombosis Hyperplasia 4th Late in-stent thrombosis 1986 Figure 13.1 Revolutionary treament of coronary artery disease. 2003 Biodegradable stents Avoid: In-stent restenosis prolonged angioplasty drug Mismatch secondary surgery 290 Fundamental Biomaterials: Metals hence more attention was needed in choosing a proper material to act as a scaffold while maintaining mechanical integrity to withstand the forces of the vessel wall. The principal advantage of using a stent is that it does not require open heart surgery and each year more than one million stents are implanted in the world. Commercially more than 40 different types of stents are available and they are made of stainless steel, Nitinol shape-memory alloy, cobalt chromium alloys, platinum, tantalum, or gold which provide sufficient strength and they minimize blood flow blockage. For cardiovascular stent application, some of the potential candidates reported so far are pure iron, Fe 35 Mn alloy, magnesium alloy, and others. Each type of metal shows some unique properties and they are employed depending on the suitability of the environment and the patients’ need. However there are some clinical problems associated with metallic stents, i.e., the metal ions can be released following processes such as electrochemical corrosion and mechanically accelerated electrochemical processes, i.e., stress corrosion, corrosion fatigue, and fretting corrosion [40]. 13.4.3 Application of biodegradable metals in coronary artery The application of biodegradable metals in coronary arteries was an innovative approach to treat heart diseases. For patients with coronary artery diseases, the options of treatment include medication, percutaneous coronary interventions (PCI), and coronary artery bypass surgery. When coronary artery disease is detected at an early stage and is less severe, then medication and a change in lifestyle is prescribed to control the disease from further progression. Stents are usually made of metals but fabric type stents are also available. Stents prevent the artery from renarrowing and from being blocked again (restenosis) [41]. The gold-coated stents were used for coronary circulation from the year 1995, and the experimental studies suggest that the coating of gold to the metallic stent resulted in reduced thrombogenicity, smaller thrombus mass, and decreased neointimal formation [42]. These stents also possess superior visibility in fluoroscopy [43]. As gold enhances the opaque nature of the stent, the coating of metallic stents with gold was carried out by many researchers and became one of the hot topics during PCI [44]. But later on, the short- and mid-term follow-up studies showed that these patients required frequent repeated revascularization procedures, and thus the use of stents coated with a layer of gold could be considered a failure in clinical terms. Kastrati et al. [45] made a comparative study on steel stents with and without a gold coating for coronary artery disease. They picked the patients randomly and assessed their angiographic outcome after coronary placement. They monitored the performance of both the stents at regular intervals of time and after a year of stent implantation the patients with steel stent showed a more positive improvement than the gold-stent group, of the order of 73.9% for steel stent versus 62.9% for goldstent. Kastrati and his coworkers concluded “one-year event-free survival was significantly less favorable in the gold-stent group” (versus the steel stent group) with the increase in the risk of restonosis. Following Kastrati Kastrati et al., Gehman Degradable metallic biomaterials for cardiovascular applications 291 [46] explained the possible mechanism for the poorer clinical performance of the gold-coated stent than the result expected from previous work was due to the significant radiation deposition mechanism between the gold and the tissues. A similar clinical study was demonstrated by Pache et al. [47] by implanting gold-coated stents in patients and a 5-year clinical follow-up was monitored carefully by selecting the patients randomly. A similar trend of results showing higher restenosis risk was obtained for gold-coated stents supporting the observations of Kastrati et al. [45]. Tang et al. [48] prepared a zinc-based alloy containing copper at different weight percentages and studied these for biodegradable stent application. The presence of copper element in the stent enhances the acceleration of the endothelialization process and the copper possesses excellent antibacterial effect which helps to reduce the risk of infection during surgery [49]. These particular zinc copper alloy stents are cytocompatible to human endothelial cells with perfect antibacterial effect in in vivo tests and hence Tang and his workers suggest this binary alloy can be used as an excellent implant in cardiovascular application. The in vitro and in vivo biocompatibility of the ternary Mg 0.3Sr 0.3Ca alloy was investigated by Bornapour and his coworkers [50]. The in vivo test was conducted by implanting a tubular Mg 0.3Sr 0.3Ca stent along with a WE43 control stent into the right and left femoral artery of a dog. After 5 weeks of implantation, the histological analysis and post-implantation results showed no sign of thrombosis with the Mg 0.3Sr 0.3Ca stent while an excessive thrombosis and occlusion was observed in the artery implanted with WE43 stent. The in vitro biocompatibility was evaluated by cytotoxicity assays using HUVECs, no toxicity was observed and there is increase in the viability of HUVECs after 1 week of implantation. From these observations it was concluded that the surface of the magnesium-based stent was protected interfacially in both in vitro and in vivo studies. Erbel et al. [51] evaluated the performance of magnesium stents by implanting them in 63 patients. The stents achieved immediate angiographic response similar to other metallic stents and they were safely degraded after 4 months. Waksman et al. [52] conducted a short-term implantation of Fe and Co Cr (control) stent by implanting them in the coronary arteries of juvenile domestic pigs. In comparison to the control the iron stent exhibited better intimal thickness, intimal area, and percentage of occlusion compared to the control (Co Cr). Waksman et al. concluded that the iron was a safer metal to be used as stent in humans. Even though the property of biodegradation was considered as a primary property to be considered for the vascular stent it is important to note the clinical safety concerns by conducting trial experiments. Recently the FDA approved the first commercialization of the fully biodegradable stent for coronary arteries. The Absorb GT1TM BVS System (Abbott Vascular, Santa Clara, CA, United States) was approved at July, 2016. Generally the Fe- and Mg-based stents exhibit superior mechanical properties than the other metals. The properties of high radial strength and elastic modulus enable the use of these metals to fabricate thinner struts. When compared to 292 Fundamental Biomaterials: Metals polymeric stents there is no limit for stent geometry for degradable metallic stents and hence they show enhanced clinical efficiency with reduced adverse effects [53]. The biological responses towards material implantation were well explained by in vivo model compared to the in vitro model. The inability to explain the complex systems of cellular interactions, hormones, dynamic blood circulation, excretions, etc., which are absent within the in vivo model leads to false negative results. Moreover the cells in the in vitro tests were not as dense as those within the in vivo model and thus the cells are more vulnerable within the in vitro model as the extent of cell cell cooperation was minimal [54]. On taking into account the convenience and low cost, animals such as rodent and rabbits are used to study the animal model. However their cardiovascular system does not closely resemble the human system and hence their biological responses within cardiovascular system will be different. The most widely used animal model to study cardiovascular system is porcine as it more closely resembles that of humans. 13.4.4 Stent grafting Endovascular stent grafting or endovascular aneurysm repair (EVAR) is a minimally invasive surgical method to treat an aortic aneurysm [55]. Aortic aneurysm is a disease that causes local weakening and dilatation, and it can develop at various locations of the aorta. The most common location is the abdominal aorta. With this stent-graft therapy the stent is placed inside the aneurysm using a catheter without a surgical opening. The stent graft reinforces the weakened section of the aorta to prevent the aneurysm from rupturing. The surgery takes 2 4 h to complete which is much shorter than the open surgery aneurysm repair. The endovascular stent grafting is performed if the aneurysm is not ruptured and the size is 5 cm or more in size. The recent developments of endovascular aortic stent-grafting for aortic aneurysm and thoracic aortic aneurysm (TAA) offer a less-invasive option for treating this type of disease. Common examples of stent-graft include Endurant (polyester with Nitinol stents, Medtronic), Zenith (polyester with 316L stainless steel self-expanding stent support), and Excluder (expanded polytetrafluoroethylene and fluorinated ethylene propylene with Nitinol wire stent support) [56]. The metal vascular scaffold material prepared using magnesium has been reported as a promising material in most of the research works [57]. Critical limb ischemia is an end-stage manifestation of peripheral artery disease. Compared to infrageniculate bypass surgery (IBS), treating with endovascular therapy was an alternate option offering the advantages of reduced cost and shorter stay in the hospital compared to IBS [58]. Peeters et al. [24] conducted a pilot human trial using magnesium metal vascular scaffold for treating 20 patients suffering from critical limb ischemia. It was successful for all the 20 patients with a clinical patency rate of 89.5% for the initial 3 months and a patency rate of 72.4% for the 12-month period. Degradable metallic biomaterials for cardiovascular applications 293 Maier et al. [59] evaluated the functional integrity of vascular walls by applying magnesium to maintain endothelial functions. The magnesium showed a protective effect by facilitating the healing of vascular injuries, hypertension, and preventing atherosclerosis. It plays a vital role in promoting the growth of collateral vessels in chronic ischemia. The presence of magnesium induces the synthesis of nitric oxide thereby reducing hypertension as well as in preventing thrombosis. 13.4.5 Implantable pacemakers Heart rhythm disorders will disturb the contraction of heart which leads to insufficient pumping of blood into the body. A normal resting heartbeat ranges from 60 to 100 beats/min. The treatment of heart rhythm disorders include medication management, catheter ablation, and the implantation of cardioverter-defibrillators, known as pacemakers. The pacemakers are implantable devices used to treat hearts that beat slower than the normal range of beating. In 1958, Senning implanted a pacemaker using stainless steel and lead; proper functioning lasted for only 7 days [60]. Later due to a sudden change in the amplitude of the pacemaker, the stimulus was decreased as a result of a fracture of the stainless steel lead. After analyzing the reason for failure many researchers have made an attempt by replacing the lead with different materials including alloys of cobalt, chromium, and nickel to the stainless steel. The lead-related issues were finally solved by the use of materials such as silicone or polyurethane-insulated noble metal coils of platinum and iridium or titanium [61]). The most common metal used in cardiac pacemakers is titanium and it was developed in the year 1970. The effective biocompatible materials for pacemaker application other than titanium include noble metals and their alloys, biograde stainless steels, some cobalt-based alloys, tantalum, niobium, titanium niobium alloys, Nitinol, MP35N (a nickel cobalt molybdenum alloy), alumina, zirconia, quartz, fused silica, biograde glass, silicon, and some biocompatible polymers [62 67]. Implantable cardioverter defibrillators (ICDs) were introduced in the 1980s and were later approved by the United States Food and Drug Administration (FDA) in 1985 [68]. The implantation of pacemakers and ICD involves primary allergic reactions including localized pain within 2 days to 24 months after implantation and in some cases generalized pruritus was observed and it will be resolved with the removal of the pacemaker [69]. 13.5 Future perspective A rapid technological advance was observed in the field of stent technology for treating the patients with coronary artery disease. The application of biodegradable metals as implants will be revolutionized as the potential materials for the next generation treatment of cardiovascular system are developed. In the future the development of advanced biodegradable materials in fusion between metal, polymer, and 294 Fundamental Biomaterials: Metals ceramic materials shall overcome the limitations such as thrombosis and restenosis and improve the applications of biodegradable metals in cardiovascular systems. Clinical trials based on metallic implantations were investigated to a greater extent in both in vitro and in vivo studies to gain a better knowledge. On considering the fatal consequences of metallic implants, the focus should be maintained on the eradication, rather than the minimization of this serious complication. The optimal design of the metal scaffold and its degradation rate should be further studied using different combination of alloys to find a perfect metal implant with greater superiority in the near future. 13.6 Conclusion In recent years, the application of biodegradable metallic implants has gained significant clinical attention in the field of cardiovascular system. 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