Review on low- and high-frequency sonolytic, sonophotolytic and sonophotochemical processes for inactivating pathogenic microorganisms in aqueous media

Highlights

• High-frequency sono- and sonophotolytic processes for water disinfection are reviewed.

• 0.2–2 MHz ultrasound is effective against pathogenic microorganisms in aqueous media.

• Sonophotochemical processes are scarcely studied and represent a future research area.

• Key mechanisms of inactivation are comprehensively discussed.

Abstract

Ultraviolet and ultrasound-based advanced oxidation processes (AOPs) are gaining considerable research attention for water treatment and disinfection. Compared to low-frequency ultrasound (LFUS, <100 kHz), high-frequency ultrasound (HFUS, >100 kHz and MHz range) for water disinfection remains much less investigated. The present review aims at surveying and discussing literature data on microbial inactivation in non-food aqueous media using HFUS alone and with AOPs. More specifically, the review covers sonophotolytic (US/UV) processes under sequential and simultaneous modes as well as sonophotochemical processes, where both low and high frequencies were applied. Addressing a state-of-the-art biomedical research, we have attempted to provide more insight into mechanical and sonochemical mechanisms of inactivation under ultrasonic exposure. Sonoporation, intracellular generation of reactive oxygen species (ROS), energy stimulation of aquaporins to deliver ROS, and injection of extracellular ROS into sonoporated cells have all been identified as primary ways of inactivation. Application of ultrasound in the 0.2–2 MHz range and mercury-free light sources to support the Minamata Convention on Mercury is an ongoing challenge for effective elimination of microbial pathogens from water and wastewater through sonophotolytic and sonophotochemical AOPs.

Introduction

Ultrasound and ultraviolet (UV) irradiation have been known as some of the most effective reagent-free methods for inactivating pathogenic microorganisms in aqueous media. To date, UV treatment has become a widely used technology for water and wastewater disinfection. However, UV disinfection is easily affected by water quality and has other limitations, which are noncritical for ultrasound disinfection. Therefore, ultrasonication can be considered as an alternative individual method or in combination with UV radiation for improving its performance. Upon sonication, the acoustic cavitation produces collapsing micro-bubbles in water, leading to extremely high local temperatures and pressures in supercritical regions (hot spots). After collapsing, the microbubbles generate H₂O₂ and reactive oxygen species (ROS) such as OH•, HO₂• and O•, which are responsible for oxidation processes (Mark et al., 1998; Furuta et al., 2004; Sathishkumar et al., 2016), and capable of inactivating enzymes and damaging membranes, DNA, RNA, proteins and lipids (Riesz and Kondo, 1992; Cabiscol et al., 2000). Ultrasound cavitation also induces physical or mechanical effects such as shock waves, shear forces, and micro-jets, which lead to mechanical disruption of the cell membrane and lysis (Jyoti and Pandit, 2001; Ananta et al., 2005; Gao et al., 2014a). Historically, the influence of frequency on the chemical (oxidation by ROS) and mechanical effects has been intensively studied since the 1990s for the degradation of chemical compounds (Petrier et al., 1992; Mason et al., 1994; Portenlänger and Heusinger, 1997). It is generally accepted that on increasing frequency, the mechanical effects decrease and the chemical effects increase. Mason et al. (2011) observed the inverse dependence of mechanical and chemical effects on the frequency (20–1142 kHz) with respect to the surface modification of a plastic material. Later, Tran et al. (2014) quantified the mechanical effects in the frequency range from 20 kHz to 1 MHz and confirmed that their slowing down with an increasing frequency above 100 kHz. It is believed that the microbial inactivation by high-frequency ultrasound (HFUS, >100 kHz and MHz range) is mainly via the generation of ROS and subsequent chemical reactions, while under lower frequencies the inactivation occurs primarily due to direct mechanical effects (Wu et al., 2012; Gao et al., 2014a, b). Low-frequency ultrasound (LFUS, <100 kHz, typically 20–48 kHz) has been widely used in inactivation studies both individually and in combination with UV light, oxidants or catalysts in sono-based advanced oxidation processes (AOPs). Compared to LFUS, the potential of HFUS for inactivating microorganisms in aqueous media remains much less investigated. Meanwhile, in view of ROS production and intensification of inactivation processes, HFUS appears to be an attractive alternative to the commonly-employed LFUS. The low- and high-frequency sono-based AOPs (especially, sonophotocatalysis) for organic chemical degradation in water have been extensively studied and comprehensively reviewed (Ince et al., 2001; Pang et al., 2011; Rayaroth et al., 2016; Sathishkumar et al., 2016; Chu et al., 2017; Panda and Manickam, 2017; Yap et al., 2019). A literature analysis showed that little research on microbial inactivation, which is an equally important field for water treatment applications, has been conducted using sono-based AOPs. To our knowledge, this is the first review that aims at surveying and discussing literature data on the inactivation of pathogenic microorganisms in aqueous media using HFUS and selected AOPs, namely, sonophotolytic (US/UV) and sonophotochemical processes (US/UV + oxidant/catalyst). Mechanisms of inactivation are discussed addressing a state-of-the-art biomedical research. Research gaps and future research directions are also identified.