Concepts of Tissue-Biomaterial Interactions E-Book

Rena Bizios

• Herausgeber: John Wiley & Sons
• Kategorie: Fachliteratur
• Sprache: Englisch

Veröffentlichungsjahr: 2024

Beschreibung

Biology and engineering meet in this groundbreaking and growing discipline

Biomedical engineering is an established interdisciplinary research and training area, combining various aspects of physiology, biology, materials science and engineering. Biomedical engineering programs and courses are integral parts of pertinent curricula, generating an urgent need for textbooks which can introduce this fundamental subject to new generations of students, researchers and practicing professionals.

The textbook Concepts of Tissue-Biomaterial Interactions meets this need with an introduction to the subject. Beginning with various, key, fundamental concepts of cellular biology and the physiology of tissue wound healing (required to understand interactions of tissues and implants) it offers essential information and insight regarding the design of successful biomaterial implants. Concluding with a look at the current forefront and future of the field, it is an indispensable introduction for fundamental and cutting-edge aspects of biomedical engineering applications.

Concepts of Tissue-Biomaterial Interactions readers will also find:

• Introduction to biological aspects such as cell-extracellular matrix interactions and cell-substrate interactions
• Details regarding various aspects of the process of normal tissue wound healing
• Current knowledge of tissue wound healing in the presence of implants
• Examples of pathological complications, including infection
• Design criteria for biocompatible implants
• The process of obtaining regulatory approval of new biomaterials and implantable medical devices by pertinent regulatory agencies
• Implant biomaterial and medical devices: past, present, and future

Concepts of Tissue-Biomaterial Interactions is recommended for advanced undergraduate and for graduate students interested in biomedical engineering, biomaterials, tissue engineering, and implantable biomaterials/medical devices, as well as a reference for practicing biomedical engineering professionals.

Leseprobe

Table of Contents

Cover

Table of Contents

Title Page

Copyright

Dedication

List of Figures

List of Tables

Preface

Acknowledgments

About the Companion Website

1 Materials for Prosthetic Devices and Implants Through the Ages

1.1 Traditional External Prosthetic Devices

1.2 Implantable Devices

1.3 Materials Used for Implants

References

2 Lessons Learned from Physiology

2.1 Tissue Wound Healing: Introduction

2.2 The Process of Normal Wound Healing in Injured Tissues

2.3 Blood Clotting (Thrombosis)

2.4 Fibrinolysis

2.5 Inflammation

2.6 The Proliferation/Repair Stage of the Tissue Wound Healing Process

2.7 Remodeling/Maturation Stage of the Tissue Wound Healing Process

References

3 Lessons Learned from Pathology

3.1 Blood-Coagulation-Related Clinical Complications

3.2 Prevention of Blood Clots: A Clinical Perspective

3.3 Fibrinolysis: Clinical Practice

3.4 Inflammation-Related Pathological Outcomes

3.5 Proliferation/Repair and Remodeling/Maturation-Related Pathological Outcomes

3.6 Other Undesirable Tissue Wound Healing Outcomes

3.7 Potential Lessons Learned from Malignant Tumor Pathology

3.8 Cancer and Implants

3.9 The Patient Factor

References

4 Lessons Learned from Biology

4.1 Mammalian Cells

4.2 The Extracellular Matrix

4.3 Brief Introduction to Proteins

4.4 Protein Adsorption on Substrates

4.5 Protein Interactions with Substrates: The “Substrate Prospective”

4.6 Adsorption of Proteins from Multicomponent Solutions. The Vroman Effect

4.7 Protein-Mediated Cell Interactions with Substrates

4.8 Protein and Cell Interactions with Materials: Applications

4.9 Select Chemical Modification of Substrate Surfaces

4.10 Select Mammalian Cell Adhesion on Chemically-modified, Peptide-Containing, Material Surfaces

4.11 Other Mammalian Cell Functions on Chemically-Modified, Peptide-Containing Material Surfaces

4.12 Closing Remarks

4.13 Protein and Cell Interactions with Nanostructured Materials

References

5 Tissue Wound Healing in the Presence of Implants

5.1 Introduction

5.2 Blood Coagulation and Fibrinolysis in the Presence of Implants

5.3 Inflammation in the Presence of Implants

5.4 Proliferation/Repair and Remodeling/Maturation in the Presence of Implants

5.5 Effects of the Biological/Physiological Milieu on Biomaterials

5.6 The Fate of Implants

References

6 Infection

6.1 Introduction

6.2 Clinical Treatments of Infection

6.3 Future Directions: Challenges and Opportunities

References

7 Sterile Conditions. Sterilization of Implants

7.1 Introduction

7.2 Determining Implant-Related Sterile Conditions

7.3 Methods for Implant Sterilization

7.4 Biomaterials: The Biomedical Engineering Connection

References

8 Evaluation of Biocompatibility

8.1 Mechanical Properties of Materials

8.2

In Vitro

Hemocompatibility (Blood Compatibility) Tests

8.3 Cultured Cell Models

8.4 Animal Tests

8.5 Clinical Trials

References

9 Lessons Learned from Implant Failure, Retrieval, and Evaluation

9.1 Complications Leading to Implant Failure Post Implantation

9.2 Examples of Vascular Implant Failure Post Implantation

9.3 Reasons for Failure of Orthopedic and Dental Implants Post Implantation

9.4 Examples of Orthopedic and Dental Implant Failure Post Implantation

9.5 Etiology of Implant Failure Post Implantation

9.6 Evaluation of Retrieved Failed Implants. Responsibilities of Biomedical Engineers

9.7 Closing Remarks

Reference

10 Hydrogels: Promising, Versatile Biomaterials for Implants

10.1 Introduction

References

11 Biocompatibility: Past, Present, and Future

References

Index

End User License Agreement

List of Tables

Chapter 1

Table 1.1 Types of materials used for implants.

Chapter 2

Table 2.1 Stages of the normal wound healing process following tissue injury...

Table 2.2 Composition of human blood plasma.

Table 2.3 Cells in human whole blood [1–3].

Table 2.4 Coagulation factors in human blood plasma.

Chapter 4

Table 4.1 List of amino acid components of the proteins in the human body.

List of Illustrations

Chapter 2

Figure 2.1 Schematic outline of tissue components affected by injury (left s...

Figure 2.2 The physiological tissue environment in the case of normal tissue...

Figure 2.3 Comparison of the major tissue components at the interface betwee...

Figure 2.4 Schematic illustrations (not to scale) of leukocyte morphology an...

Figure 2.5 Schematic illustration (not to scale) of platelet plug formation....

Figure 2.6 Flow chart of the plasma coagulation cascade. ADP, adenosine diph...

Figure 2.7 Flow chart of the conversion of plasminogen to plasmin.

Figure 2.8 Schematic illustration (not to scale) of the phagocytosis process...

Figure 2.9 Schematic illustration (not to scale) of activated monocyte funct...

Chapter 5

Figure 5.1 Schematic illustration (not to scale) of a cross-section of the a...

Figure 5.2 Schematic illustration (not to scale) of the mechanical forces in...

Chapter 6

Figure 6.1 Schematic illustration (not to scale) of biofilm formation. (A) P...

Guide

Cover

Table of Contents

Title Page

Copyright

Dedication

List of Figures

List of Tables

Preface

Acknowledgments

About the Companion Website

Begin Reading

Index

End User License Agreement

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Concepts of Tissue-Biomaterial Interactions

Fundamentals and New Directions

Rena Bizios

Lutcher Brown Endowed Distinguished University Chair Professor

Department of Biomedical Engineering

The University of Texas at San Antonio

One UTSA Circle

San Antonio, TX, USA

Marissa E. Wechsler

Assistant Professor

Department of Biomedical Engineering and Chemical Engineering

The University of Texas at San Antonio

One UTSA Circle

San Antonio, TX, USA

Copyright © 2025 by John Wiley & Sons, Inc. All rights reserved, including rights for text and data mining and training of artificial technologies or similar technologies.

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Library of Congress Cataloging-in-Publication Data applied for:

Hardback ISBN: 9781119841005

Cover Design: Wiley

Cover Image: © Tanvir Ibna Shafi/Getty Images

To all past, present, and future students and colleagues, our comrades () in the exploration of the interactions of cells and tissues with implantable biomaterials and medical devices. Our combined, continuous interest and contributions have placed this field in the mainstream of biomedical engineering.

List of Figures

Figure 2.1

Schematic outline of tissue components affected by injury (left side) and repaired during subsequent wound healing (right side).

Figure 2.2

The physiological tissue environment in the case of normal tissue injury.

Figure 2.3

Comparison of the major tissue components at the interface between injured tissues and implants.

Figure 2.4

Schematic illustrations (not to scale) of leukocyte morphology and content.

Figure 2.5

Schematic illustration (not to scale) of platelet plug formation. (A) Damage to endothelium activates platelets, evidenced by changes in their morphology. (B) Adhesion at the damaged endothelium site is followed by aggregation and formation of the platelet plug. (C) The fibrin network (end result of the plasma coagulation cascade) stabilizes the platelet plug and ensures the clot remains at the site of each formation in the dynamic environment of flowing blood.

Figure 2.6

Flow chart of the plasma coagulation cascade. ADP, adenosine diphosphate; HMWK, high molecular weight kininogen; Ca

2+

, calcium.

Figure 2.7

Flow chart of the conversion of plasminogen to plasmin.

Figure 2.8

Schematic illustration (not to scale) of the phagocytosis process resulting in elimination of a pathogen by an activated neutrophil.

Figure 2.9

Schematic illustration (not to scale) of activated monocyte function in the presence of a substrate. (A) Activated monocytes in flowing blood adhere to activated endothelium, transverse the vascular wall, and chemotactically migrate through tissues outside the vasculature to the site of implantation. In tissues, these cells are known as “macrophages”. (B) Macrophages adhere to the pre-adsorbed proteins at the implant surface and spread becoming further activated. (C) Several macrophages fuse and form

foreign body giant cells

characterized by their large size and presence of many nuclei.

Figure 5.1

Schematic illustration (not to scale) of a cross-section of the arterial wall tissue structure and composition.

Figure 5.2

Schematic illustration (not to scale) of the mechanical forces in the vasculature.

Figure 6.1

Schematic illustration (not to scale) of biofilm formation. (A) Planktonic bacteria (each with a characteristic flagellum) flow above a substrate. (B) Some motile bacteria interact with the substrate and then permanently adhere, each losing its flagellum. (C) Bacteria proliferation results in colony formation. Subsequent development of a biofilm encloses and protects the colony. (D) The bacteria colony inside the biofilm grows as a result of proliferation and entrapment of other cells and debris. (E) When the original colony grows too large to exist, parts may break off, flow downstream, adhere to another host site, and form a new pathogenic colony.

List of Tables

Table 1.1

Types of materials used for implants.

Table 2.1

Stages of the normal wound healing process following tissue injury.

Table 2.2

Composition of human blood plasma.

Table 2.3

Cells in human whole blood.

Table 2.4

Coagulation factors in human blood plasma.

Table 4.1

List of amino acid components of the proteins in the human body.

Preface

The original concept of Tissue-Biomaterial Interactions was developed into a new undergraduate course and was taught, for the first time, in 1989 at a time when biomedical engineering education was very young and needed everything, including new courses.

For that purpose, pioneering (for those times), interdisciplinary approaches judiciously chose and used fundamental concepts from physiology and biology and integrated them in a biomedical engineering course.

The aforementioned course was motivated by, and addressed, a need for pertinent textbooks in undergraduate biomedical engineering curricula. Judging by its subsequent appeal, acceptance, and use, the book An Introduction to Tissue-Biomaterial Interactions successfully met that need in academia.

In the interim, biomedical engineering has enjoyed remarkable growth and development. Thus, the current milieu needs an updated textbook which still addresses the process of wound healing and the latest developments regarding various interactions of the human body with implant biomaterials and medical devices. The present textbook is intended for a one-semester course during the third year of undergraduate curricula. By that time, students in a “typical biomedical engineering undergraduate curriculum” would have already taken introductory courses in biomaterials, cell biology, chemistry, and biomechanics; concepts of the aforementioned courses are the background needed to take a Tissue-Biomaterial Interactions course. In our opinion, a course using the present textbook is appropriate training for both undergraduate and first-year biomedical engineering graduate students focusing on biomaterials, cellular engineering, tissue engineering, and implantable medical devices.

This textbook summarizes our pertinent teaching experience with undergraduate and graduate courses to date. We are fully aware, however, of the future needs of biomedical engineering, a dynamic discipline which continuously expands into new scientific frontiers. For this reason, we consider this textbook only an introduction to a fascinating field of knowledge which provides fundamental training for students pertinent to their future careers. We encourage instructors, who use this textbook in teaching pertinent courses, to supplement the material presented in this textbook with appropriate updated information from the latest biomedical literature, as well as from their own research endeavors.

Acknowledgments

In writing this textbook, the result of teaching pertinent undergraduate and graduate courses, we benefited from the encouragement and support received from our students, colleagues, and families. We thank you all!

We wish, however, to especially acknowledge and thank Ms. Jordyn M. Wyse, for assistance with the figures of the textbook, and Ms. Leslie Sanchez, for assistance with various managerial aspects in finalizing this endeavor. All figures throughout this textbook were created with BioRender.com.

About the Companion Website

This book is accompanied by the companion website:

www.wiley.com/go/Concepts_of_Tissue-Biomaterial_Interaction_1e

The website includes:

Supplementary to script

1Materials for Prosthetic Devices and Implants Through the Ages

Through the ages, human medical needs have resulted from birth defects, trauma, age-related diseases, degenerative conditions, end-stage organ failure, etc. Several biological species have the capability for tissue/organ regeneration; for example, salamanders can regenerate lost limbs, tails, and even eyes [1]; deer regenerate antlers [2]; flatworms regenerate their bodies [3]; rabbits, domestic cats, and bats fill in ear holes [4]; zebrafish regenerate fins, etc. [5]. In contrast, humans have an extremely limited capacity to regenerate body tissues and organs.

In this respect, the Greek myth of Prometheus is pertinent. Long time ago, only the Gods of Olympus were privileged to have the comfort of fire. During those times, the mortal humans were doomed to live in a dark and cold world. Prometheus, a Titan and immortal, commiserated with the humans, stole the fire from Olympus, and, in direct opposition to the will of Zeus, the father of the Olympian Gods, gave it (and, thus, hope) to humans. This defiant act enraged Zeus, who severely punished Prometheus to be helplessly chained on the mountain Caucasus while a portion of his liver was eaten by a bird of prey every day. Because the liver regenerated overnight, this situation provided endless food supply to the bird of prey but subjected Prometheus to eternal torture. This Greek myth makes a great story but is also notable because it is part of the tradition of a civilization, which emphasized exclusively thinking approaches versus experimentation. Most remarkable is the “kernel” of truth, which the Prometheus myth contains. Organ and tissue regeneration in humans are extremely limited with the following very few exceptions: liver is the only human organ, which can regenerate completely from a minimum of 25% of its original mass [6]. As far as other tissues are concerned, bone fractures (but not nonunion bone defects) and small skin cuts heal through respective tissue regeneration processes.

1.1 Traditional External Prosthetic Devices

Through the millennia, medical responses to human loss of body parts (such as lower limbs and arms) were limited and involved exclusively external prostheses. Ancient treatments/solutions used “ordinary” materials such as wood, leather, string, etc., to assemble prostheses. An example is the replacement of the amputated right big toe of a 3000-year-old Egyptian mummy; this replaced appendage was composed of carved wood, attached to a piece of leather, and secured onto the foot of the recipient with string [7]. Undoubtedly, this is an anatomically correct and aesthetically acceptable prosthesis; its functional aspect, however, is questionable when one considers that the footwear of ancient Egyptians were sandals.

Prosthetic devices replacing lost parts of the body are also found in the literature. The legendary Captain Hook, in the children’s fictional story of Peter Pan, was infamous for his bad deeds but also scary because he had a metal hook replacement for his lost left arm. Although anatomically incorrect, and aesthetically unacceptable, this prosthesis was most functional because it gave Captain Hook a reliable way to hold on (indeed for dear life) when his ship encountered bad weather in the open seas and, thus, prevented him from being swept away in the stormy waters.

As recently as the beginning of the 20th century, prosthetic limbs available to patients who needed them were composed of “ordinary” materials (such as wood and metals) and were anthropomorphic (with stiff and nonfunctional parts such as fingers) renditions of human arms and hands [8]. Synthetic materials (such as plastics and metals) that had been developed for various other industrial and engineering applications were used for making prosthetic devices. Attempts to incorporate functionality into prosthetic hands led to the inclusion of cylindrical tubes one each for the four fingers. Later on, incorporation of mechanical features enabled such prototypes of human hands to have motor control of the finger motions required for actions such as playing the piano [8]. Further advancements in design addressed the sensor needs of prosthetic hands. These devices used various materials and electronic parts and added a “thumb part”, thus providing the hand prosthesis with the capability of grasp. During the 21st century, the needs of wounded soldiers promoted development of magnificent prosthetic arms and hands composed of “modern” materials (including various plastics, metals, and textiles); most importantly, these prostheses included sophisticated and advanced electronics attached to the muscles and neurons of the recipient amputee, thus allowing control of desirable movements and commands such as grasping, picking up objects, bringing a bottle to the mouth, and successfully drinking the contained water without any spills [9]. Another very important development of prosthetic hands was incorporation of mechanical and electronic parts that provided the recipient patients with the sensation of touch (i.e., recognizing hard and soft items) and pressure (e.g., while shaking hands) [10, 11].

During the aforementioned times, development of prosthetic legs paralleled that of arms and hands. Anthropomorphic but unyielding, one-piece (including monolithic wooden foot, calf, knee, and part of the thigh) legs were eventually replaced with devices which did not look like the human limbs but had unparalleled advantages. Such prostheses, composed of “modern” materials which are light and have the appropriate mechanical properties (such as strength in carrying mechanical loads during human locomotion, flexibility, etc.), provide needed support for several movements of the human body such as standing up and sitting down, walking (on various terrains including not only flat but also inclined surfaces and staircases) [12], jogging and running, swimming [13], and even surfing [14].

It should be noted that, in addition to humans, small (such as kittens) and big (such as elephants) animals need, and thus have received, prosthetic devices for missing or injured limbs [15]. Such prostheses are appropriately designed and scaled, either up or down, and are composed of similar materials as those used for applications to human patients. Veterinary care of pets, animals used in racing events, animals kept in zoos, and farm animals constitutes a sizable and major market for veterinary care and many biomedical applications including prosthetic devices.

1.2 Implantable Devices

External prosthetic devices have helped patients, but they neither addressed nor resolved medical needs requiring replacement, healing, and regeneration of mammalian tissues and organs; such needs require implantable devices. Both external and implantable prostheses are composed of materials and contain combinations of mechanical and electrical parts. In contrast to the temporary and intermittent use of the traditional, external prosthetic devices, implants are placed inside the bodies of patients (humans and/or animals) for various but mostly long-term time-periods, specifically the lifespan of the recipient.

Initially, synthetic materials developed for non-biomedical applications were chosen and used for biomedical implants; pertinent examples include elastic undergarment textiles to produce synthetic tubular substitutes for blood vessels, and titanium/titanium alloys (relatively light but strong materials) for load-carrying orthopedic implants (such as total hip prostheses). Because such cavalier, trial-and-error approaches resulted in dramatic failures (including implant malfunction and rejection), it became obvious that successful biomedical implant materials and devices require new specifications and must fulfill different criteria. Implant biomaterials (the components of implant devices) were eventually designed to be nontoxic, non-pyrogenic, nonallergenic, etc. Adherence to, and applications of, these requirements resulted in avoidance of implant rejection. For a while, attainment of a state of “tolerance” by the surrounding milieu inside the recipient patients’ bodies became an acceptable clinical outcome, despite the fact that those implants did not produce desirable and controlled interactions with surrounding tissues and did not trigger the normal tissue-healing process at the implant–tissue interface.

1.3 Materials Used for Implants

By definition, a “biomaterial” is either a natural or synthetic material used for biomedical applications to support, enhance, or replace damaged tissue or a biological function [16].

A summary of the types of materials which have been used for implants is given in Table 1.1.

Table 1.1 Types of materials used for implants.

Implant material

Polymers

Natural (e.g., collagen, fibrin, etc.)

Products of organic chemistry synthesis

Special formulation

: Biodegradable polymers

Ceramics

Natural (e.g., devitalized bone, coral, etc.)

Products of inorganic chemistry synthesis

Metals

Ores

Composites

Products of two or more the above materials

Products of various chemistry methods

Important Requirement: Approval by the Food and Drug Administration (FDA) in the United States of America and by pertinent regulatory agencies in other countries around the world is required for implant materials used in biomedical applications.

The historical development and progression of biomaterials were appropriately summarized by Dr. James A. Anderson, a pioneer, world-renowned pathologist, and biomaterials expert, who stated that the relative focus on the “bio” and “materials” components of the term “biomaterials” has changed over the years and can be classified into three historical eras of this field. Specifically, the materials aspect was the focus of pertinent research and development before 1975, followed by a period when both the “bio” and “materials” aspects attracted and received pertinent attention from researchers. Since 2000, however, the predominant focus of the biomaterials field has been on the “bio” component [17].

The most desirable outcome, and simultaneously the major biomedical need and challenge pertinent to implant materials and devices, is formation of normal and functional new tissue, eventually leading to timely and uncomplicated integration of synthetic implants into surrounding tissues in vivo. Such approaches depend on, and benefit from, continuous advances in several scientific and engineering fields including physiology, medicine, cellular and molecular biology, genetics, extracellular matrix biology, biochemistry, biomaterials science and engineering, cellular and tissue engineering, biomedical engineering, pathology, and regenerative medicine.

Presently, application of accumulated research-related experience is focusing on incorporating the latest knowledge from advances in several scientific and engineering fields regarding the design, formulation, and extensive testing of implantable materials and devices for specific clinical applications to meet biocompatibility requirements, leading to their approval by pertinent regulatory agencies (such as the Food and Drug Administration (FDA) in the United States and other pertinent regulatory agencies in other countries around the world) [18]. The process by which a material becomes a “biomaterial” for implants is continuously evolving and improving as it encompasses the latest developments from several pertinent scientific and engineering fields.

References

1

Joven A, Elewa A, Simon A. Model systems for regeneration: salamanders.

Development

[Internet]. 2019 Jul 1 [cited 2022 Jan 24]; 146(14). Available from:

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6679358/

.

2

Li C, Zhao H, Liu Z, McMahon C. Deer antler—a novel model for studying organ regeneration in mammals.

Int. J. Biochem. Cell Biol.

[Internet]. 2014; 56:111–22. Available from:

https://pubmed.ncbi.nlm.nih.gov/25046387/

.

3

Tanaka EM, Reddien PW. The cellular basis for animal regeneration.

Dev. Cell

2011 Jul 19; 21(1):172–85.

4

Metcalfe AD, Willis H, Beare A, Ferguson MWJ. Characterizing regeneration in the mammalian external ear.

J. Anat.

2006 Oct [cited 2022 Jan 24]; 209(4):439. Available from:

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2100363/

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5

Pfefferli C, Jaźwińska A. The art of fin regeneration in zebrafish.

Regeneration

2015 Apr [cited 2022 Jan 24]; 2(2):72. Available from: /pmc/articles/PMC4895310/.

6

Sheedfar F, Di Biase S, Koonen D, Vinciguerra M. Liver diseases and aging: friends or foes?

Aging Cell

[Internet]. 2013 Dec [cited 2022 Jan 24]; 12(6):950–4.

https://pubmed.ncbi.nlm.nih.gov/23815295/

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This 3,000-Year-Old Wooden Toe Shows Early Artistry of Prosthetics |Smart News | Smithsonian Magazine, 2017. [Internet]. [cited 2022 Jan 24]. Available from:

https://www.smithsonianmag.com/smart-news/study-reveals-secrets-ancient-cairo-toe-180963783/

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James R, Laurencin CT. Regenerative engineering and bionic limbs.

Rare Metals

. 2015 34(3):143–155.

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4429301/

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9

Vox. FDA Approves Robotic Prosthesis Controlled by Muscle Contractions – Vox [Internet]. [cited 2022 Jan 24]. Available from:

https://www.vox.com/2014/5/11/11626740/fda-approves-robotic-prosthesis-controlled-by-muscle-contractions

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Inhabitat. Shaking hands with the LifeHand 2 | Inhabitat – Green Design, Innovation, Architecture, Green Building [Internet]. [cited 2022 Jan 24]. Available from:

https://inhabitat.com/thought-controlled-robotic-arm-returns-the-sense-of-touch-to-amputees/lifehand2-1/

.

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Raspopovic S, Capogrosso M, Petrini FM, Bonizzato M, Rigosa J, Di Pino G, et al. Bioengineering: restoring natural sensory feedback in real-time bidirectional hand prostheses.

Sci. Transl. Med.

[Internet]. 2014 [cited 2022 Jan 24]; 6(222). Available from:

https://www.newscientist.com/article/dn25008-natural-sense-of-touch-restored-with-bionic-hand/

.

12

BBC (2014). Lesser-known things about prosthetic legs – BBC News [Internet]. [cited 2022 Oct 31]. Available from:

https://www.bbc.com/news/blogs-ouch-28225622

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13

Goldstein T, Oreste A, Hutnick G, Chory A, Chehata V, Seldin J, et al. A pilot study testing a novel 3D printed amphibious lower limb prosthesis in a recreational pool setting.

PM&R

[Internet]. 2020 [cited 2022 Jan 24]; 12(8):783. Available from: /pmc/articles/PMC7496828/.

14

The Nexus (2021). Designing a Prosthetic to Help Surfers Catch a Wave – The Nexus [Internet]. [cited 2022 Jan 24]. Available from:

https://nexus.jefferson.edu/design-and-style/designing-a-prosthetic-to-help-surfers-catch-a-wave/

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ABC News (2014). Double-Amputee Cat “Paw Stands” Down Stairs – ABC News [Internet]. [cited 2022 Oct 31]. Available from:

https://abcnews.go.com/Lifestyle/Pets/double-amputee-cat-paw-stands-stairs/story?id=23991141

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NIBIB (2017). Biomaterials [Internet]. [cited 2022 Jan 24]. Available from:

https://www.nibib.nih.gov/science-education/science-topics/biomaterials

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Anderson JM. The future of biomedical materials.

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2006; 17:1025–8.