Biofeedback Volume 35, Issue 2, pp. 54-61 ©Association for Applied Psychophysiology & Biofeedback www.aapb.org SPECIAL TOPICS Is There More to Blood Volume Pulse Than Heart Rate Variability, Respiratory Sinus Arrhythmia, and Cardiorespiratory Synchrony? Erik Peper, PhD,1 Rick Harvey, PhD,1 I-Mei Lin, MA,2 Hana Tylova,1 and Donald Moss, PhD3 1 San Francisco State University, San Francisco, CA; 2National Chung Cheng University, Taiwan; 3Saybrook Graduate School, San Francisco, CA Keywords: blood volume pulse, heart rate variability, respiratory sinus arrhythmia, cardiorespiratory synchrony Summer 2007 Ô Biofeedback A growing body of research reports the health benefits of training heart rate variability (HRV), and the clinical use of HRV training protocols has increased dramatically in recent years. Many of the home training devices and many of the sophisticated biofeedback instrumentation systems rely on the blood volume pulse (BVP) sensor, or photoplethysmograph, because it is more user friendly than the electrocardiogram used in medical settings. However, the BVP signal is valuable in its own right, not merely as a convenient measure of HRV. This article explores the methodology of BVP recording, the underlying physiology, and the potential benefits from BVP treatment and training protocols. For example, the shape of the BVP waveform reflects arterial changes correlated with hypertension. In addition, BVP training offers promise for the treatment of migraine and the monitoring of human sexual arousal. 54 Studies of methods for training improvement in heart rate variability (HRV), respiratory sinus arrhythmia (RSA), and cardiorespiratory synchrony (CRS) are promising areas of current research, expanding our knowledge of new clinical applications and training procedures for improving sympathetic-parasympathetic balance (see Table for the expansion of the abbrevations in text). For example, research by Lehrer and colleagues (Lehrer et al., 2006; Lehrer et al., 2004) has demonstrated that HRV training in patients with asthma reduces their asthma severity. Similarly, research by Del Pozo and colleagues (Del Pozo, Del Pozo Scher, & Guarneri, 2004) has shown that cardiac patients can improve their HRV. In addition, Giardino, Chan, and Borson (2004) reported a benefit for patients with chronic obstructive pulmonary disease using HRV training and an exercise protocol. It appears that learning to increase HRV results in strengthening sympathetic-parasympathetic balance and offers hope for many chronic illnesses (Gevirtz, 2003). Whereas clinical applications and feedback training of RSA or CRS have been used to address illness affected by the sympathetic-parasympathetic imbalance, new HRV training protocols could be employed as well. Measuring HRV, the beat-to-beat variability in the sinus rhythm over a given period of time, is usually done by calculating the standard deviation of the average of normalto-normal heart beats (SDNN or SDANN). This statistical index has health implications, predicting morbidity and mortality. We will elaborate later on this relationship between HRV and health (Kleiger, Miller, Bigger, & Moss, 1987). There are many technologies that can estimate the beatto-beat variability in the sinus rhythm over a given period Table. Alphabet soup of abbreviations BVA Blood volume amplitude BVP Blood volume pulse CRS Cardiorespiratory synchrony EKG Electrocardiography ECG Electrocardiography FFT Fast Fourier transform HR Heart rate HRV Heart rate variability NN Normal-to-normal beat (interbeat interval) PPG Photoplethysmography PTT Pulse transit time RSA Respiratory sinus arrhythmia SDANN Standard deviation of average normal-to-normal beat (also known as SDNN: standard deviation of the normal-to-normal beat) SDAHR Standard deviation of average heart rate Peper, Harvey, Lin, Tylova, Moss Figure 1. Blood volume pulse, blood volume amplitude, heart rate, and respiration before training. breaths per minute with a corresponding heart rate of 73 beats per minute (SD = 10.1 beats). Whereas designing training protocols for improving HRV or RSA/CRS is possible using BVP technologies, the BVP signal holds even greater promise as a tool for use in improving other clinical applications and training protocols. The remainder of this article explores various components of the BVP technology. Background The BVP signal is derived with a PPG sensor that measures changes in blood volume in arteries and capillaries by shining an infrared light (a light-emitting diode) through the tissues. This infrared light is selectively transmitted, backscattered, reflected, and absorbed. The amount of light that returns to a PPG sensor’s photodetector is proportional to the volume of blood in the tissue. The PPG signal represents an average of all blood volume in the arteries, capillaries, and any other tissue through which the light passed. The PPG signal depends on the thickness and composition of the tissue beneath the sensor and the position of the source and receiver of the infrared light. Most PPG sensors can be placed anywhere on the body, from the earlobe to the vaginal wall, with the finger as the most common location for recording a BVP signal. The PPG sensor measures relative changes in the perfusion of the blood through the tissue underneath the sensor. For example, changes in the BVP signal can indicate relative changes in the vascular bed due to vasodilation or vasoconstriction (increase or decrease in blood perfusion) as well as changes in the elasticity of the vascular walls, reflecting changes in blood pressure. Because the blood volume in the arteries and Biofeedback Ô Summer 2007 of time using measures of the volume of blood that passes over a photoplethysmographic (PPG) sensor with each pulse, also called blood volume pulse (BVP). Recently, HRV training using BVP measurements has escaped out of the laboratory and into the marketplace. BVP training devices are commercially available as portable units such as the StressEraser and the emWave or as units built for use with computers such as the FreezeFramer or the Journey to Wild Divine. By using these BVP training devices, individuals can become aware of factors that increase or decrease their HRV. For example, excessive sensory arousal; shallow, rapid breathing; and excessive emotions of fear, worry, anger, or panic will decrease HRV. On the other hand, reducing sensory arousal, breathing slowly at approximately five to seven breaths per minute, and experiencing emotions of appreciation and love will increase HRV. In clinical settings, practitioners use sophisticated multichannel biofeedback systems to train clients to increase HRV and CRS. In most clinical settings, heart rate information is derived from a BVP signal rather than from an electrocardiography (ECG) signal. Whereas the ECG signal is more precise (e.g., with fewer movement artifacts), applying an ECG sensor is also more cumbersome and obtrusive compared to applying a BVP sensor (e.g., without gel or tape or placement on a chest). Using PPG feedback devices alone and/or in conjunction with respiratory feedback devices such as respiratory strain gauges, clients can learn to increase HRV/RSA, as shown in Figures 1 and 2. The participant data from Figure 1 represent an average respiration rate of 14 breaths per minute, with a corresponding heart rate of 68 beats per minute (SD = 5.0 beats). The data from Figure 2 represent an average respiration rate of 7 Figure 2. Blood volume pulse, blood volume amplitude, heart rate, and respiration during training designed to increase cardiorespiratory synchrony. 55 Blood Volume Pulse Figure 3. Heart rate is derived from measures of blood volume pulse by measuring the interbeat interval and then transforming this information into beats per minute. For example, the interbeat interval of 0.80 seconds is equal to a heart rate of 75 beats per minute, whereas the interbeat interval of 0.93 seconds is equal to a heart rate of 64.5. capillary bed increases with each arterial pulsation, heart rate can be estimated from the BVP signal. Heart rate, or the number of heartbeats per minute, is calculated by estimating the time interval between the heartbeats, called the interbeat interval. The time in seconds of the interbeat interval is divided into 60 seconds to calculate the beat-by-beat heart rate, as shown in Figure 3. The time between each beat can vary; therefore, the estimated beat-by-beat heart rate can also vary. There are two estimates of the variability of the heart rate: variability estimated by the SDANN or variability estimated by the standard deviation of the average beat-by-beat heart rate (SDAHR). A methodological issue includes the fact that the raw BVP signal must be artifact free before meaning is assigned to the SDANN and SDAHR measures of variability in the heart rate data. The next section address artifacts in the BVP signal. Inspecting the Raw BVP Signal for Artifacts Summer 2007 Ô Biofeedback When analyzing average heart rates, it is important to eliminate artifacts before calculating estimates of HRV. Heart rate averages calculated from the data may not be reliable if artifacts exist, as illustrated in the following vignette: 56 What happened? He reported increased arousal during the stressful imagery, yet his heart rate was higher during the initial baseline condition. It was only when I included the raw blood volume pulse (BVP) signal from which the heart rate was calculated that I realized the average signal was incorrect. Figure 4. Recording of the heart rate derived from the raw blood volume pulse during the baseline period. The average heart rate included a segment of very rapid heart beat reflecting movement artifact rather than a true increase in average heart rate. Figure 5. When movement artifact is excluded from the signal shown in Figure 4, the actual heart rate is estimated at 61.05 beats per minute. This dialogue illustrates issues related to artifacts in the BVP data. The data included movement artifacts, as shown in Figure 4. After eliminating the movement artifact as shown in Figure 5, the heart rate information was nearly five beats lower. Note also that in this participant, there was a slight increase in heart rate during the stressful imagery rehearsal once the segments of data affected by artifact were removed. Once movement artifacts are removed from BVP estimates of heart rate, the BVP measure of HRV becomes an easy-to-administer technology for use in clinical settings. HRV is usually a sign of cardiac health, as it suggests that the heart has flexibility in response to the demands of the body. HRV reflects cardiovascular health as a sign of sympathetic Peper, Harvey, Lin, Tylova, Moss Figure 6. Example of blood volume pulse signal with amplitude and timing markers. Time t1 (between markers 1 and 5) indicates the interbeat interval and is used to calculate the heart rate. Pulse measure P1 (marker 1) is a measure of pulse amplitude. Volume at V (marker 3) is the indicator of the blood volume influenced by the dicrotic notch. Reprinted with permission from Hlimonenko, Meigas, and Vahisalu (2003). and parasympathetic nervous system balance. When HRV is absent or reduced, it may signal pathology (Del Pozo et al., 2004; Kleiger et al., 1987). Namely, when HRV is low, as indicated by an SDANN <50 milliseconds and an SDAHR <2.5 beats, there is a fourfold increase in relative risk of death after myocardial infarction compared to those who have a high HRV (SDANN >100 milliseconds and SDAHR >5 beats; Kleiger et al., 1987). Whereas artifact-free BVP signals can be used for training of HRV, BVP measures may also be used for estimating cardiovascular health in terms of blood pressure because the BVP signal also reflects changes in the elasticity of the vascular walls (Asada, Shaltis, Reisner, Rhee, & Hutchinson, 2003; Babchenko et al., 2001; Speckenbach & Gerber, 1999; Weng, Matz, Gehring, & Konecny, 2002). Changes in BVP Waveform Shape Reflect Other Types of Cardiovascular Health Changes in BVP Amplitude May Reflect Moment-by-Moment Sympathetic/Parasympathetic and Cognitive/Emotional Activity The BVP amplitude displays moment-by-moment HRV and may offer significant insight into individual emotional responses, as illustrated in Figure 8. Figure 8 shows psychophysiological responses during a standardized stress protocol. The participant’s responsiveness to internal and Biofeedback Ô Summer 2007 The shape of the BVP waveform may be an indicator of cardiovascular variables such as blood pressure because stiffer arterial walls are associated with higher blood pressure (Speckenbach & Gerber, 1999). The raw BVP signal is the product of many factors that influence blood flow through the vascular bed. The raw BVP wave pattern is the result of the recording location, the heart’s left ventricular ejection, and the elasticity/stiffness of the aorta and arteries. The shape of BVP signal can be used for deriving interbeat interval (t1), which in turn can be transformed into an estimate of heart rate as well as the pulse amplitude (P1), both of which represent the relative increase in blood volume caused by the heart contracting, as shown in Figure 6. The elasticity in the arterial vasculature is partially reflected in the magnitude of the dicrotic notch signal, shown as marker 3 in Figure 6. The dicrotic notch signal depends on the interaction of the initial pressure wave when the heart contracts, arterial stiffness that decreases the pulse transit time, and the reflected pressure wave from the peripheral arterial bed. The loss of arterial wall elasticity is usually an indicator of aging and suggests an increased risk of cardiovascular disease, especially hypertension (Izzo & Shykoff, 2001). Increasing arterial stiffness decreases the pulse transit time (PTT). PTT can be time referenced to the R-wave of the ECG signal corresponding time between P1 and V of the BVP signal graph in Figure 6. The stiffer the arterial walls, the faster the PTT, with the effect most pronounced in the periphery of the toes compared to the fingers and ears (Allen & Murray, 2002). Decreases in PTT have been significantly correlated with an increase in blood pressure and age. The decrease in PTT affects the BVP waveform by appearing as a diminution of the dicrotic notch as the initial and reflected pressure waves come closer together. The relationship between the PTT and BVP waveforms is illustrated by the BVP and the blood pressure recordings of parents and children of varying ages, as illustrated in Figure 7. Even though HRV training offers great clinical potential, it is important to remember that many factors affect blood circulation and thereby the BVP signal. These include sympathetic arousal, which induces vasoconstriction; decreased sympathetic arousal and increased parasympathetic arousal, which induce vasodilation especially as the person relaxes; low external temperature, which induces vasoconstriction; recreational and prescription drugs (e.g., alcohol increases vasodilation, whereas nicotine increases vasoconstriction); and illnesses such as Raynaud’s disease, which is characterized by arteriole vasoconstriction and reduced blood flow in the fingers. Changes in the BVP signal can be very rapid and thereby may reflect sudden shifts in arousal or cognitions. Because arousal and cognitions change rapidly, the BVP signal may also be used as an indicator of transient processes. 57 Blood Volume Pulse Figure 7. Comparison of finger blood volume pulse recording of parents (62year-old father and 52-year-old mother) and child (17-year-old daughter). The mother has borderline hypertension. The absence of the dicrotic notch in the borderline hypertensive (top) tracing suggests a stiffening of the arteries, indicating increased blood pressure. Figure 8. Example blood volume pulse amplitude analysis by measuring the percentage change for each condition [(maximum – minimum)/maximum × 100]. Summer 2007 Ô Biofeedback This exploration of emotions and BVP training could include some of the following: 58 external physical and emotional stressors is vividly depicted in the variations of BVP amplitude presented Figure 8. The pattern portrays decreases in amplitude in the BVP signal in response to prompts such as sighs and claps that triggered sympathetic activation. In this participant, eye closure during the protocol evoked an unanticipated and large decrease in the BVP amplitude compared to any of the physical or imagined stress conditions. This unanticipated decrease in BVP may be interpreted as a kind of anticipatory anxiety. Initially, the eye closure was only an instruction before asking the person to think about a stressful experience. The idiosyncratic BVP amplitude changes are a window into her psychological processes. The large response (vasoconstriction) to the instruction “close your eyes” indicates the participant’s general ongoing arousal and vigilance. Instead of relaxing to the “close your eyes” instruction, she reported later that she started to think, “What will happen now?” She was continuously checking if her experience of the world was safe. This cognitive reaction is often found in people who are anxious, fearful, or want to please others. The BVP amplitude can also indicate the extent to which the person has been captured by his or her emotions; the more captured, the longer it takes for the BVP signal to return to some baseline level. In the example above of anticipatory anxiety, the BVP signal returned rapidly to baseline, reflecting a state of vigilance rather than the activation of a memory of an emotional trauma. By observing her response pattern during the training session, the participant could explore strategies that would enable her to feel safe and to prevent a decrease in her BVP amplitude when she closes her eyes. • Identification of the thoughts, feelings, and emotions associated with the responses • Exploration of past and present patterns that let the person interpret the world as unsafe • Exploration of how to reframe the experience so that the vigilance response is not evoked • Practice of physiological desensitization so that the response is extinguished The BVP signal may also be interpreted in terms of peripheral temperature changes because the signal reflects changes in vasoconstriction and vasodilation. The Use of BVP Amplitude as an Indicator of Changes in Peripheral Temperature Changes in BVP represent changes in the blood volume. If BVP amplitude increases, it reflects an increase in vasodilation, which leads to an increase in peripheral temperature; if the BVP amplitude decreases, it reflects a decrease in peripheral circulation and a decrease in peripheral temperature. BVP amplitude changes are very rapid and precede changes in temperature, as temperature is a slow-averaging signal, as shown in Figure 9. When BVP is monitored simultaneously with temperature, the rapid BVP amplitude changes can facilitate peripheral warming. For example, when the BVP amplitude started to increase, even though the peripheral temperature was still decreasing, it may help the clinician and participant to identify emotional and cognitive images and sensations Peper, Harvey, Lin, Tylova, Moss Figure 9. Simultaneous recording of right and left blood volume pulse (BVP), temperature, and electromyography signals. Temperature changes lag behind the BVP amplitude changes. Even as BVP amplitude is increasing, the temperature is still decreasing. From Zoe Talbot and Sarah Langensiepen, personal communication. that facilitate peripheral warming. Among these strategies are slower and diaphragmatic breathing, autogenic phrases, relaxation instructions, and imagery to increase peripheral warmth. In addition to BVP signals being used as indicators of peripheral temperature, the BVP signal may also be used for treating headaches as well as for monitoring sexual arousal. Overlooked BVP Applications: Treatment of Migraine and Monitoring Human Sexual Arousal and temporal BVP reduction biofeedback in the treatment of migraine. Results showed that temporal constriction and finger temperature biofeedback were equally effective in controlling migraine headaches and produced greater benefits than the waiting list condition. Nestoriuc and Martin (2007) performed a meta-analysis examining the efficacy of biofeedback training in treating migraine. Results showed that biofeedback training was more effective than control conditions. The strongest improvements were in the frequency of migraine attacks and perceived self-efficacy. BVP feedback yielded higher effect sizes than peripheral skin temperature feedback and electromyography feedback. Moderator analyses revealed biofeedback training in combination with home training to be more effective than therapies without home training. BVP has also been used as an indicator of sexual arousal. For example, PPG sensors measure tissue engorgement by blood from any location ranging from the nasal septum to measure cerebral blood flow to the vaginal wall to measure sexual arousal. As early as 1967, Palti and Bercovici used a PPG sensor to measure vasoengorgement of the vaginal wall as an indicator of sexual arousal to erotic stimuli, as shown in Figure 10 (Brotto, Basson, & Gorzalka, 2004; Palti & Berovici, 1967). Other applications of BVP measurement and feedback have yet to be fully explored Exploring Other Uses of the BVP Signal The biofeedback applications of BVP are expanding rapidly with the availability of the new economic HRV/CRS home trainers. These portable and relatively inexpensive devices allow people to become aware of factors that affect the BVP signal. Through HRV training, participants can develop Biofeedback Ô Summer 2007 Using BVP feedback to encourage vasomotor control offers numerous clinical applications such as the treatment for migraine by recording the BVP from the temporal artery (Feuerstein & Adams, 1977). Allen and Mills (1982) used photoelectric plethysmograph feedback to train to selfregulate BVP amplitude in eight female migraine sufferers. Participants learned to increase and decrease BVP amplitude on the scalp at superficial temporal artery (STA) and finger locations. The results of the research showed a significant relationship between voluntary pulse amplitude changes in the BVP amplitude measured at the STA and corresponding pain reports during a migraine. Hoelscher and Lichstein (1983) used a temporal BVP biofeedback protocol in treating chronic cluster headache patients. The result shows a 70% reduction in daily headache frequency and a 45% decrease in headache severity. Improvement was maintained at 1, 3, 6, 12, and 21 months of follow-up. Large decreases in the consumption of migraine abortives, narcotic analgesics, and antiemetics were also observed. Gauthier, Lacroix, Coté, Doyon, and Drolet (1985) reported using finger warming Figure 10. The vaginal blood volume and pulse amplitude of a woman who is shown a neutral stimulus and an erotic stimulus. The genital response occurs within seconds of the presentation of an erotic stimulus in sexually healthy women, regardless of age or menopausal status. Reprinted with permission from Brotto and Gorzalka (2006). 59 Blood Volume Pulse sympathetic/parasympathetic balance and master strategies to prevent and reverse illness. In addition, easily available computerized monitoring providing the corresponding digital analysis such as power spectrum analysis (fast Fourier transform) and feedback may allow new areas of biofeedback BVP applications to emerge. Among those are the following: • Analysis and training of specific components of the BVP signal, such as increasing the dicrotic notch to improve cardiovascular flexibility or reducing high blood pressure. • Correlating BVP waveforms recorded from multiple locations on the body with Chinese pulse used as a diagnostic tool in traditional Chinese medicine (TCM). In TCM, for more than 2000 years, a stiff pulse has been an indicator of aging and/or pathology. • Exploring the changes in blood flow as indicators of illness or health by recording the BVP response patterns simultaneously from multiple locations such as from different sympathetically enervated dermatomes. • Ongoing analysis and treatment of male and female sexual dysfunctions as well as development of strategies to enhance orgasmic quality. This could possibly include correlations of penile and vaginal wall engorgement with peripheral blood flow changes in other areas of the body that may contribute to sexual arousal. • Combining BVP monitoring with psychotherapy, as the rapid changes in BVP amplitude may indicate cognitive and emotional responses. • Teaching increasing BVP amplitude to improve circulation and thus regeneration in cases of diabetic ulcers and frostbites (Rice & Schindler, 1992; Graul, Stanculescu, Peper, Johansen, & Doyle, 2004). The goal of this article was to raise awareness of the use of BVP technologies beyond the calculation of HRV or RSA/CRS indicators. Whereas other uses of the PPG/BVP technology will emerge in the future, those described here offer a good start for stimulating new areas of research. Summer 2007 Ô Biofeedback Acknowledgments 60 This article was adapted from E. Peper, H. Tylova, K. H. Gibney, and R. 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