Antibacterial ferroelectric materials: Advancements and future directions

https://doi.org/10.1016/j.jiec.2021.02.016Get rights and content

Abstract

Ferroelectric functional materials are known for a wide range of applications including sensors, actuators, energy harvesting devices. Very recent studies based on ferroelectric materials for environmental cleaning and bacterial remediation add a further up-and-coming field of application of these materials. They possess several advantages over conventional methods such as biocompatible range and sustainability. Although the research area is relatively new, some substantial experimental work has been done in the last couple of years. The rationale and underlying mechanisms of different published reports were compiled and explained to offer a better understanding of the subject. The three major mechanisms can be divided into catalysis via a change in surface potential, mediated catalysis by the formation of reactive oxide species on the ceramic surface due to piezoelectric or pyroelectric excitation, and enhanced photocatalysis due to internal electric fields. Our goal is to provide a comprehensive report on ferroelectric materials application in the prevention of bacterial infections and to give an outlook on further possible research strategies.

Introduction

We are exposed to a variety of microbial threats in our daily life ranging from water acquired infections to nosocomial infections. Biomaterials and medical implants are not devoid of microbial growth on their surface. More than 1 million people get infected every year due to biofilm growth over medical implants[1]. As per the world health organization (WHO), water-borne diarrheal infections alone account for more than 2 million deaths every year. Bacterial infections are still the second leading cause of human deaths across the world[2]. Bacterial contaminations are liable for 17 million deaths every year[3]. Major human organs that are at higher risk of bacterial infections are the skin, urinary tract, respiratory tract, vascular system, central nervous system, and gastrointestinal system. Blaak et al. reported the complete cycle of direct and indirect microbial exposure to human beings (Fig. 1)[4]. Constant efforts have been made in the treatment and prevention of microbial contaminations since the inception of penicillin[5]. However, drug-resistant bacteria introduce another daunting challenge in healthcare and sanitation. On average, drug resistance in bacteria is identified within two years of the introduction of a new antibiotic[6]. The only couple of novel classes of antibiotics have entered the market since 1962[7]. Because microbial cells possess the ability to utilize rich sources for growth and adaptive mutations, antimicrobial resistance (AMR) in bacterial colonies can arise due to a variety of reasons. AMR is a slow process in bacterial cells as a part of the evolutional process. However, the overuse and misuse of antimicrobial agents, especially in the farming industry, accelerate the resistance development in bacteria[8]. The farm animals are part of the food chain, and hence AMR bacteria can likely be transferred to humans. Thus, the bacteria can be found in animals, humans, food and the environment (water, soil, air) which can spread from one medium to another medium (Fig. 1). This breaches the mission of public health safeguard[9]. Poor sanitation conditions and prevention technologies further enhance the chance of bacterial and drug-resistant bacterial infections. The bacterial colonization on surfaces (by the formation of a biofilm) perturbs the functionality and performance of various interfaces like medical implants, aquatic flow systems, contact lenses, etc.[10]. Therefore, bacterial biofilm formation over the surfaces accounts for more than 64% of hospital-acquired infections around the globe[11]. The indoor and outdoor quality of air is also gets affected by contaminated surfaces[12]. Nevertheless, the exploration of new antimicrobial surfaces is part of the research for two decades now[13]. Most of the new strategies for microbial prevention are based on either contact killing of bacterial cells or antibiotic, inorganic metal ion release from the surface[14].

The schematic shown in Fig. 2 depicts primary mechanisms to repel/kill bacterial cells. These methods, however, possess some inherent risks like bacterial resistance against the antibiotics, high cytotoxicity of inorganic salts, and accumulation of the metal ions in the body[15], [16], [17], [18], [19]. Henceforth, it is obligatory to find new sustainable methods for the prevention of bacterial surface film formation. Very recently, scientists have started exploring new material surfaces like ferroelectric and piezoelectric surfaces against bacterial growth. The rationale is that ferroelectric materials carry remnant surface polarization after poling of the materials. These surface charges can directly influence the properties of the bacterial organisms or trigger micro electrolysis of water molecules and produce reactive oxygen species (ROS)[20], [21], [22], [23], [24], [25], [26]. These ROS then furthermore have a deleterious effect on bacterial cells. Additionally, photocatalytic processes in ferroelectric materials can be modified and optimized to induce electrochemical reactions with bacteria. Therefore, this review focuses on the mechanisms to induce or catalyze electrochemical reactions with the help of ferroelectric materials leading to bacterial degradation. Additionally, an outlook on possible strategies to optimize the performance of the materials is also discussed.

Ferroelectric materials are a subclass of pyroelectric materials, which are again a subclass of piezoelectric materials with the unique property of retaining an electric potential on its surface [27]. The net polarization in virgin ferroelectric material (unpoled) is zero in the absence of an external electric field due to the random orientation of ferroelectric domains. Polarization vectors of domains start aligning in the direction of a strong externally applied electric field (poling process). The polarization of a ferroelectric material increases with an increase in the external electric field strength and reaches a saturation polarization when there is an optimum of the domain orientation in the direction of the field. The reduction in polarization due to a decrease in the external electric field does not retrace the loop which results in remnant surface polarization when the external electric field is zero[28], [29]. The polarization can also be influenced by the application of mechanical stress. Thus, all ferroelectric materials are piezoelectric, as well. In a ferroelectric material polarization P is a nonlinear function of external electric field E. The typical characteristics of ferroelectric materials are 1. Spontaneous polarization 2. Ferroelectric hysteresis 3. Ferro-para transition temperature and 4. Reversible polarization. The remnant surface polarization enables ferroelectric materials to be used in a variety of essential applications[30]. There is a large amount of research dedicated to a variety of applications of ferroelectric and piezoelectric materials in energy harvesting, self-powered devices, optoelectronics, and further electromechanical applications[31], [32], [33], [34], [35], [36], [37], [38], [39]. In recent years, ferroelectric materials have also been employed in electrochemical reactions of organic and biological compounds[40], [41], [42]. The effect of remnant surface polarization on the degradation of organic molecules and biological molecules including lower organisms (bacteria) cells has been elucidated in the recent past.

There are three concepts with which electrochemical reactions can be induced or modified by ferroelectric materials as depicted by a schematic in Fig. 3. Due to the induced surface potential in poled ferroelectrics or deformed piezoelectric materials, surface reactions can be altered and catalyzed[21], [42], [43], [44], [45], [46], [47]. A cyclic mechanical activation can lead to a varying field facilitating redox reactions and adsorption or desorption of the surface species of interest[44], [45]. The research of the field-effect on bacteria has, nevertheless, focused mostly on externally applied electric fields[48], [49], [50]. Thus, an expansion of the research to ferroelectric and piezoelectric materials will be of high interest. The concept of mediated catalytic mechanisms is based on micro electrolysis of water molecules due to surface potential differences in ferroelectric materials [51]. The electrolysis of water molecules produces highly reactive oxygen species like hydrogen peroxide, superoxide, hydroxyl radicals, and singlet oxygen as a mediator which have the potential to catalyze a variety of molecules (Fig. 4). Fig. 4(a) is a schematic describing the possible mechanism of ROS production in aqueous media over the surface of potassium sodium niobate (KNN) ceramics[52]. The potential difference in the poled and unpoled surface of KNN has been displayed in Fig. 4 (b). The surface potential was recorded with help of scanning kelvin probe microscopy (SKPM) by Tan et.al. The third major process involves the enhancement of photo electrocatalytic reactions. An internal field or change in surface space charge can lead to exciton separation, and hence the longer lifetime of that exciton to facilitate enhanced redox reactions at the surface[42], [53], [54]. These mechanisms and their variations will be elucidated further concerning biological applications in the following sections.

Section snippets

Catalysis by electric fields/surface potential and mediated catalysis

A change in surface potential due to the poling of a ferroelectric material can have a direct effect on surface reactions[32], [44], [45], [47], [54]. Thus, making the surface more catalytically active. This is similar to the effect of an applied electric field during surface catalyzed reactions[55], [56]. A periodically varying field, for example by the mechanical stimulus of the ferroelectric material, could furthermore influence adsorption and desorption of reactants[44], [45]. The effect of

Bactericidal mechanism of reactive oxygen species

ROS are highly reactive oxygen species with reduced O2 due to the addition of electrons. Some of the commonly known ROS series are hydroxyl radical (°OH), Hydrogen peroxide (H2O2) Superoxide anions (°O2). All of them are produced regularly in the process of oxidative metabolism in every living cell. The organisms possess an integrated antioxidant system to counteract the ROS level inside and outside cells. The antioxidant systems include enzymatic and non-enzymatic modalities[121]. An increased

Remarks and future directions

Sterilization of surfaces and liquids with the help of ferroelectric and piezoelectric materials will be a very intriguing method to combat infections in the age of multi-drug resistant bacteria. The research involving ferroelectric materials for these purposes will furthermore be a challenging multi-disciplinary effort between medicine, biology, chemistry, physics and materials science. In this review, we illustrate the recent promising endeavours to use the polarized surfaces of

Declaration of interests

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgment

RV thanks to Biotechnology Industry Research Assistance Council (BIRAC), New Delhi for the project (BT/AMR0235/05/18).

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