Basic Science: The Foundation of Evidence-Based Voice Therapy Basic science research is part of the circle of translational research that provides the scientific underpinning for evidence-based practice. The translation from bench to bedside, however, is sometimes not obvious. This short review seeks to demonstrate ways in which basic science can inform our clinical practice as voice therapists. From ... Article
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Article  |   March 31, 2016
Basic Science: The Foundation of Evidence-Based Voice Therapy
Author Affiliations & Notes
  • Aaron M. Johnson
    Department of Speech and Hearing Science, University of Illinois at Urbana-Champaign, Champaign, IL
  • Disclosures: Financial: Aaron Johnson has no relevant financial interests to disclose.
    Disclosures: Financial: Aaron Johnson has no relevant financial interests to disclose.×
  • Nonfinancial: Aaron Johnson has no relevant nonfinancial interests to disclose.
    Nonfinancial: Aaron Johnson has no relevant nonfinancial interests to disclose.×
Article Information
Speech, Voice & Prosodic Disorders / Voice Disorders / Research Issues, Methods & Evidence-Based Practice / Speech, Voice & Prosody / Part 1
Article   |   March 31, 2016
Basic Science: The Foundation of Evidence-Based Voice Therapy
Perspectives of the ASHA Special Interest Groups, March 2016, Vol. 1, 7-13. doi:10.1044/persp1.SIG3.7
History: Received August 7, 2015 , Accepted August 31, 2015
Perspectives of the ASHA Special Interest Groups, March 2016, Vol. 1, 7-13. doi:10.1044/persp1.SIG3.7
History: Received August 7, 2015; Accepted August 31, 2015

Basic science research is part of the circle of translational research that provides the scientific underpinning for evidence-based practice. The translation from bench to bedside, however, is sometimes not obvious. This short review seeks to demonstrate ways in which basic science can inform our clinical practice as voice therapists. From in vitro molecular and cellular studies to in vivo animal models, basic science can investigate biological mechanisms of vocal health, such as vocal fold hydration, and voice use, such as voice rest and vocal exercise, in ways that are impossible in human clinical studies. Knowledge of these mechanisms inform and guide our clinical investigations and help provide evidence for behavioral voice therapy.

Introduction
Evidence-based practice is critical for providing effective and efficacious interventions for persons with communication disorders, including those with voice disorders, and has been a major focus of our field for over a decade (American Speech-Language-Hearing Association, 2005). Evidence-based medicine, from which evidence-based practice is derived, has provided frameworks for assessing the quality of individual research studies as well as levels of evidence to categorize and rank evidence (Guyatt et al., 1992; OCEBM Levels of Evidence Working Group, 2011). At the top of the levels of evidence hierarchy published by the Oxford Center for Evidence-Based Medicine sits the systematic review and randomized control trial that inform us of the efficacy and effectiveness of our interventions. At the bottom of the hierarchy sits “mechanism-based reasoning,” which includes basic science investigations. Due to its position in the levels of evidence, it may appear that basic science is less worthy or less applicable to our clinical practice than evidence at higher levels, such as randomized control trials. However, basic science allows us to investigate the biological mechanisms underlying functional improvements seen with our behavioral interventions in ways that are impossible with human clinical studies. Knowledge of these mechanisms is essential for understanding not just if our interventions work, but also why they work. This, in turn, allows us to improve and target our therapeutic interventions. Instead of considering basic science to be a lower level of evidence, think of it as the foundation of evidence-based medicine and practice. It is from basic science studies in the lab with highly-controlled systems and methodologies that we create the foundation of knowledge from which we are able to build our clinical investigations. The goal of this paper is to demonstrate why understanding these mechanisms is important and provide some examples of how basic science methods have been and are currently being used to investigate mechanisms underlying behavioral voice therapy.
What is Basic Science?
The classic definition of basic science is that it “is performed without thought of practical ends. It results in general knowledge and an understanding of nature and its laws” (Bush, 1945). This definition feeds the misconception that basic research has no applicability to clinical practice. While this definition still holds true in some disciplines, a more modern definition can help us understand how basic science can apply to our clinical practice as voice therapists. According to the American Cancer Society,

Basic science is a type of research that provides the knowledge and background required for later research into human health problems. It's not necessarily aimed directly at treating a specific disease or disorder, but it may be used later as part of the basis for a treatment. (American Cancer Society, n.d., “Basic Science”)

It is this type of basic science research that provides the underpinning for voice therapy.
Most basic science related to voice therapy is considered to be translational research. Translational research encompasses patient-oriented research, portions of both basic and population-based research, and the relationships between these three types of research (Rubio et al., 2010). Each component in this translational research model informs the other. Basic scientists provide new tools for use with patients and for assessment of their impact. Patient-oriented researchers make novel observations about the nature and progression of disease that often then stimulates basic science investigations. Population-based researchers contribute to the translational process by studying the epidemiology, public health implications, and cost-effectiveness of interventions (Rubio et al., 2010). There are many translational, basic research methods applicable to understanding and treating communication disorders, ranging from in vitro molecular and cellular studies to animal models (Bartlett, Jette, King, Schaser, & Thibeault, 2012). The primary goal of voice therapy is to improve vocal function by changing vocal behavior. The behavioral changes we ask of our patients can be broadly categorized as changes in either vocal hygiene or vocal use, including how and how much a patient uses his or her voice. Basic science methods have been and continue to be used to investigate both of these aspects of voice therapy.
Molecular and Cellular Investigations Into Vocal Fold Hydration
A common vocal hygiene recommendation is to stay hydrated by drinking plenty of water. Although it is generally agreed hydration is important for vocal health, there are many unanswered questions regarding hydration. For example, how much water should be consumed to ensure healthy vocal fold vibration? How does the water we drink impact hydration of the vocal fold surface (systemic vs. surface hydration)? Is there a relationship between systemic and surface hydration? Basic science has begun to answer some of the questions.
In 2001, Fisher and colleagues made an important discovery about the mechanism responsible for regulating vocal fold surface hydration (Fisher, Telser, Phillips, & Yeates, 2001). Using immunohistochemistry to examine cell types in canine vocal folds and using electrophysiology to measure membrane properties of the epithelium of the upper airway, they discovered an intrinsic sodium-potassium pump mechanism in the vocal fold epithelium that “provides the basis for the active volume regulation of vocal fold epithelium, important in this tissues' role as a tunable baffle for mechanical stress of phonation” (Fisher et al., 2001, p. 1409). In other words, the vocal fold epithelium plays an active role in regulating vocal fold surface liquid homeostasis and is not just a passive, protective cover.
Further basic research in this area led to the development of a model for the mechanism of water transport across the epithelium (for a review, see Leydon, Sivasankar, Falciglia, Atkins, & Fisher, 2009). This has provided a theoretical framework for understanding how behavioral and environmental challenges impact surface hydration. Additionally, this model provided the knowledge base to develop further in vitro studies using an animal model and clinical human in vivo studies investigating the effects of both superficial and systemic hydration on measures of phonatory efficiency; primarily on phonation threshold pressure and vocal quality. Without the foundational basic science work, the human work would not have been possible.
Voice Rest After Surgery
Debate continues about the use of voice rest post-surgery and when and how to resume voice use after vocal fold surgery (Behrman & Sulica, 2003; Coombs, Carswell, & Tierney, 2013). A review of the literature on this topic, including evidence from the orthopedic literature, concluded voice rest facilitates vocal fold wound healing better than uncontrolled phonation, especially in the early stages of healing, but that more biological, translational research investigations are needed to help understand the effects of voice rest and voice exercise on tissue remodeling (Ishikawa & Thibeault, 2010). The vocal folds are the only tissues in the human body subjected to high frequency vibratory impact forces; therefore, specific investigation of vocal fold wound healing is critical.
One way of examining the cellular response of the vocal folds to vibration is through the use of bioreactors. In vitro vocal fold bioreactors allow for systematic investigation of different degrees of both longitudinal strain and vibratory frequency on the cells of the vocal folds. While bioreactors have long been used to examine biomechanical properties of different tissues, bioreactors that mimic biologically realistic vibratory conditions are relatively new. There are several research groups working on vocal fold bioreactors. Although each group has its own design, they all essentially work by using a series of motors to stretch and vibrate strips of vocal fold cells (for a review, see Li, Heris, & Mongeau, 2013). Bioreactors can be used to measure many different aspects of the cellular response to vibration, including the genetic transcription and translation process underlying protein expression, stem cell proliferation, and changes in the extracellular matrix of the lamina propria (Gaston, Quinchia Rios, Bartlett, Berchtold, & Thibeault, 2012). Understanding the impact of vibration will provide the scientific underpinning for making recommendations of voice use and/or vocal rest after vocal fold surgery.
The previous in vitro examples of basic science research demonstrate how specific molecular and cellular aspects of the vocal fold can be isolated and investigated. Animal models provide an in vivo approach and assist with translation to human investigations. The anatomy and physiology of the vocal folds and the biomechanics of vocalization are quite similar across mammals (Alipour & Jaiswal, 2008; Titze, 2006). Although some aspects of the human voice are unique, animal models are useful for “modeling specific perturbations in an effort to understand the biology and assess potential therapies” (Institute of Medicine (US) Forum on Neuroscience and Nervous System Disorders, 2013, p. 68). For example, investigating voice rest after surgery using human participants presents many uncontrollable sources of variability, such as different sites and extents of surgical interventions and variable adherence to vocal rest recommendations. Animal models provide a higher level of control and greater access to cellular and molecular outcomes when investigating the impact of post-surgical voice use and phonotrauma on vocal fold tissue healing. For example, Dr. Rousseau's laboratory at Vanderbilt University uses an in vivo rabbit phonation model to stimulate phonation using electrical stimulation of the laryngeal muscles timed with a delivery of an artificial airflow via a tracheostomy (Mitchell, Kojima, Wu, Garrett, & Rousseau, 2014). The advantage of this model is the controlled amount of phonation, both in the amount and timing of phonation. Using this model, they have demonstrated modal phonation does not appear to increase or prolong the cellular inflammatory response in the vocal folds, possibly lending support for mobilizing tissue after acute inflammation has subsided and the process of active tissue remodeling has begun (Mitchell et al., 2014).
Vocal Use and Voice Exercise
Another area where animal models have proven useful is in the investigation of the effects of voice use and voice exercise on the laryngeal neuromuscular system. The clinical application of this work is to understand, prevent, and/or treat conditions related to muscle atrophy, such as age-related vocal decline (presbyphonia/presbylarynges). We know from studies of the limb musculature that exercise can preserve and/or restore muscular function in aging adults (Berger & Doherty, 2010). While effects of exercise on the limb muscles have been relatively well-studied, relatively little is known about the effects of vocal exercise on aging laryngeal muscles (Thomas, Harrison, & Stemple, 2008). This is likely due to the relative inaccessibility and small size of the laryngeal muscles, as well as a lack of an adequate animal model. However, two animal models, both using rats, have recently been introduced that show promise for studying the effects of vocal exercise on the laryngeal muscles: electrical stimulation of the laryngeal nerve, and behavioral training of rat ultrasonic vocalizations.
Direct in vivo electrical stimulation of the laryngeal nerves is different than the more common surface stimulation used to treat dysphagia (Clark, Lazarus, Arvedson, Schooling, & Frymark, 2009). In surface stimulation, an electrode is placed on the skin and an electrical pulse travels through all tissue layers until it reaches the muscle and stimulates a contraction (Ludlow et al., 2007). Although the muscle contracts, the neurophysiology of the contraction is quite different than voluntary contraction (Paillard, 2008). With direct nerve stimulation, however, an electrode cuff is implanted around a peripheral nerve (such as the recurrent laryngeal nerve) allowing electrical stimulation to be delivered directly to the intended nerve and, consequently, muscle or group of muscles innervated by that nerve. This mimics voluntary contraction and, therefore, is a more physiologically realistic model of voluntary exercise. Direct, in vivo stimulation of the recurrent laryngeal nerve in a rodent model was first developed to study the potential of nerve stimulation to treat laryngeal paralysis (Zealear et al., 2000). More recently at the University of Kentucky, McMullen and colleagues demonstrated the utility of direct stimulation of the recurrent laryngeal nerve to achieve supramaximal contraction of the thyroarytenoid muscle as a model of vocal exercise (McMullen et al., 2011). In this preliminary study, they found stimulation increased mitochondrial accumulations, decreased muscle fiber size, increased intracellular glycogen content, and increased the number of neuromuscular junctions in thyroarytenoid muscles. These findings may indicate a shift of the stimulated muscles to a more faster-contracting and fatigue-resistant fiber type, similar to what would be expected with exercise.
Behavioral Animal Model
The other in vivo rat model of vocal exercise is training rats to vocalize using operant conditioning. Training rats to produce ultrasonic vocalizations (USVs) is the model of vocal exercise I worked with at the University of Wisconsin and continue to develop at the University of Illinois (Johnson, Ciucci, & Connor, 2013; Johnson et al., 2011). Audible vocalizations of rats are typically in response to fear or pain, whereas USVs are used by rats to communicate with each other; rats use USVs to alarm one another of predators, to locate one another, and to indicate interest in mating (Brudzynski, 2009). The fundamental frequencies of adult rat USVs are typically centered on either 22 or 50 kHz. The 22-kHz USVs are considered to be alarm vocalizations and indicate a negative affect, whereas the 50-kHz USVs are produced in rewarding situations and indicate a positive affect (Brudzynski, 2009).
USVs and human vocalizations are produced using similar neuromuscular mechanisms and are a good model for studying laryngeal neuromuscular mechanisms for several reasons. The overall cartilaginous and muscular structure of the rat larynx and the central and peripheral laryngeal innervation are very similar to that of other mammals, including humans (Inagi, Schultz, & Ford, 1998; Van Daele & Cassell, 2009). There is strong support that a laryngeal constriction is the source of ultrasonic vocalizations, including evidence from acoustic studies using heliox, laryngeal denervation studies, and an excised larynx study (Johnson, Ciucci, Russell, Hammer, & Connor, 2010; Roberts, 1975). Additionally, the same laryngeal muscles (cricothyroid and thyroarytenoid) are used to modulate the frequency of both human and rat vocalizations (Riede, 2011). An important distinction between rat USVs and human vocalizations is that USVs are thought to be produced using a whistle mechanism, not vocal fold vibration (Roberts, 1975). Thus, rat USVs are a good model to study neuromuscular changes with vocal exercise, but not necessarily tissue changes with phonation.
To train rats to vocalize we use an operant conditioning mating paradigm (Johnson et al., 2011). First, male and female rats are placed together in a training chamber. The female rat is then removed from the chamber when the male rat expresses interest in her. This separation elicits vocalizations from the male rat, which then are rewarded with either a water or food reinforcement. After approximately 1–2 weeks, the female is no longer needed to elicit vocalizations and the male will begin vocalizing when placed in the training chamber. In addition to being a model of vocal exercise, this training model has been used to study the neural mechanisms underlying vocal deficits in Parkinson Disease (Ciucci, Ma, Kane, Ahrens, & Schallert, 2008).
Using this training paradigm, we have shown vocal exercise in rats impacts both vocal behavior (measured by USV acoustics) as well as underlying neuromuscular mechanisms; specifically, the morphology of neuromuscular junctions (NMJ) in the thyroarytenoid muscle. The NMJ is the where the peripheral motor nerve synapses onto the muscle fiber (Sanes & Lichtman, 1999). In the motor endplate on the post-synaptic muscle side of the NMJ, there are many tens of thousands of acetylcholine receptors (between 15,000–25,000 per μm2) tightly clustered together (Salpeter & Loring, 1985). In advanced age, these clusters begin to break apart and disperse, indicating possible deterioration of neuromuscular transmission reliability (Slater, 2008). We have demonstrated vocal training reduces this acetylcholine receptor dispersion in thyroarytenoid NMJs of aged rats relative to untrained controls (Johnson et al., 2013). This is the first evidence from a behavioral animal model that vocal exercise could possibly ameliorate age-related changes in laryngeal neuromuscular mechanisms.
Building on these promising first results, we are continuing to use this model at the University of Illinois to investigate neuromuscular changes with vocal exercise. We are currently determining the vocal exercise dose-response of laryngeal muscles by comparing different intensities and durations of vocal training. Our primary goal is to determine how different vocal exercise intensities impact muscle fiber size and type. We are also examining how vocal disuse interacts with aging to contribute to muscle atrophy in the vocal folds. Understanding the laryngeal neuromuscular mechanisms underlying functional changes resulting from voice therapy, vocal training, and vocal disuse is critical for understanding and treating atrophy-related disorders, such as presbyphonia.
Conclusion
Basic science makes crucial contributions to evidence-based practice, providing foundational scientific evidence to inform our therapies and guide our clinical investigations. The translational investigations done at the molecular, cellular, tissue, and animal model level, allow us to investigate the biological mechanisms that underlie our clinical recommendations.
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The 19 individual SIG Perspectives publications have been relaunched as the new, all-in-one Perspectives of the ASHA Special Interest Groups.