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INTERNATIONAL JOURNAL OF HUMAN–COMPUTER INTERACTION, 15(3), 469–486 Copyright © 2003, Lawrence Erlbaum Associates, Inc.

Immersive Virtual Reality for Reducing Experimental Ischemic Pain Hunter G. Hoffman Human Interface Technology Laboratory Department of Psychology University of Washington

Azucena Garcia-Palacios Human Interface Technology Laboratory University of Washington Universidad Jaume I, Castellon Spain

Veronica Kapa Jennifer Beecher Human Interface Technology Laboratory Department of Psychology University of Washington

Sam R. Sharar Department of Anesthesiology University of Washington School of Medicine

This study explored the novel use of immersive virtual environments as a nonpharmacologic pain control technique and whether it works for both men and women. Fourteen female and 8 male students underwent pain induced via a blood pressure cuff ischemia lasting 10 min or less. Pain ratings increased significantly every 2 min during the no distraction phase (0 to 8 min) and dropped dramatically during the last 2 min period when participants were in the virtual environment (a 59% drop for women and a 41% drop for men). Five visual analog pain scores for each treatment condition served as the primary dependent variables. All 22 participants reported a drop in pain in the virtual environment, and the magnitude of pain reduction from the virtual environment was large (a 52% drop) and statistically significant. This is the first study to show

This study was supported by NIH grant GM42725-07, NIH grant HD37683-02, NIDRR grant H133A970014, and the Paul Allen Foundation for Medical Research. Thanks to Professor Thomas Furness III for valuable comments and generous hardware support, and for lending us Konrad Schroder. Special thanks to the participating undergraduate Psychology students, to Ross Chambers for fundraising and Ian Dillon from SGI for an equipment loan. Requests for reprints should be sent to Hunter G. Hoffman, Box 352142, University of Washington, Seattle, WA 98195. E-mail: [email protected]

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immersive virtual environment distraction is also effective for women. The results show that virtual environments can function as a strong nonpharmacologic pain reduction technique, showing the same pattern of results obtained from recent clinical studies using virtual environments with burn patients during physical therapy. Practical applications of virtual environment pain reduction, and the value of a multidisciplinary approach to studying pain are discussed.

1. INTRODUCTION Morphine-related drugs (i.e., opioids) are effective for treating the pain of burn patients resting in bed. In sharp contrast, although opioids are essential, they are usually inadequate for procedural pain of severe burn patients. The majority of burn patients receiving standard analgesic pharmacologies rate their pain during burn wound care procedures as severe to excruciating (Carrougher et al., 2003; Perry, Heidrich, & Ramos, 1981; see also Melzack, 1990). Managing pain from severe burns is particularly difficult because of the high frequency and intensity of painful procedures. Dressings are changed and wounds cleaned daily to prevent infection. Extreme pain increases the time and effort required to complete wound care, and is difficult for both patients and nurses. In addition, patients must undergo aggressive physical therapy (skin stretching and muscle building) to counteract contraction of the injured or newly grafted skin, and muscle atrophy from inactivity during the healing process. Intense pain during physical therapy can discourage patients from completing their exercises (Ehde, Patterson, & Fordyce, 1998). Opioids have common side effects such as constipation, nausea, delirium, reduced respiration, and the less common but ever-present possibility of respiration failure. These factors complicate pain management based solely on pharmacologies. This fact has important medical implications because the amount of pain reported during hospitalization has been associated with postdischarge physical and psychologic recovery (Ptacek, Patterson, Montgomery, & Heimbach, 1995). For example, noncompliance with physical therapy can make additional surgery necessary, and/or can limit the final post-healing maximal range of limb motion, exaggerating burn-related physical disability (see Ward, 1998). New pain control techniques are needed that can be used in addition to traditional pharmacologies. This study explores the use of immersive virtual environments to help reduce pain. There is a strong psychological component to pain perception, and nonpharmacological psychological pain control treatments used adjunctively (in addition to) opioid analgesics can be effective (Everett, Patterson, & Chen, 1990; Patterson, 1992, 1995; Patterson, Everett, Burns, & Marvin, 1992). Such results are often interpreted within the context of a gate control mechanism. According to the gate-control mechanism proposed by Melzack and Wall (1965), an incoming pain signal of a given neurological intensity can be interpreted as more painful or less painful, depending on what the patient is thinking and/or attending to at the time. Previous experience, expectation, culture, focus of attention, and anxiety are psychological factors that can contribute strongly to the subjective experience of pain (Melzack, 1998). Such psychological influences are thought to modulate, inhibit, or

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modify the nociceptive signals at the spinal cord, which serves as a gate to control the intensity of pain signals ever reaching the higher cortex. At a less theoretical level, regardless of the mechanism, the effectiveness of cognitive interventions involving distraction for pain reduction is already supported in the literature. In a meta-analysis of adjunctive treatments, Fernandez and Turk (1989) found that cognitive–behavioral strategies significantly reduced ratings of pain in 85% of the 47 studies analyzed, and studies that involved distraction were among the most effective. A growing number of recent laboratory and field studies from several disciplines are consistent with this conclusion (see Tan, 1982, for a review). Pain tolerance to laboratory-induced pain increased significantly for participants viewing humorous or repulsive movies (Weisenberg, Tepper, & Schwarzwald, 1995). Kozarek et al. (1997) found that distraction with movies improved pain tolerance to gastrointestinal procedures in 82% of patients. Cartoon distraction paired with coaching reduced children’s distress during immunizations (Cohen, Blout, & Panopoulos, 1997) and a program combining behavioral training with a video cartoon/movie distraction technique allowed 9 of 11 child patients to avoid traditional sedation for daily cancer radiation treatments (Slifer, 1996). Most relevant to this project, Miller, Hickman, and Lemasters (1992) found that burn patients shown scenic movies and music during burn wound dressing changes rated their pain 13% lower than a “no distraction” control group. Further controlled evaluations of pain distraction during burn wound care are needed, and a technology capable of creating a more dramatic reduction in pain than videos might be more widely adopted in hospital practice. Immersive virtual environments (i.e., involving a head mounted display that occludes viewing the real world) is state-of-the-art technology for capturing attention. A virtual reality (VR) computer system sends video output to two miniature computer screens inside a wide field-of-view VR helmet. Position sensors attached to the head and hand keep track of the user’s head and hand position and orientation and feed this information into the virtual environment (VE) computer. When patients move their heads (e.g., look up toward the ceiling), the computer quickly updates the visual images in the artificial environment accordingly. These real time changes in sensory input, in response to their actions in the VE, give patients the illusion that they are inside the computer-generated environment, a sensation referred to as “presence.” Presence is the essence of virtual environments (Laurel, 1995). In our preliminary case report (Hoffman, Doctor, Patterson, Carrougher, & Furness, 2000) patients saw a virtual kitchen complete with kitchen countertops, a window overlooking a partly cloudy sky, as well as three-dimensional cabinets, and doors that could be opened and shut. Patients could pick up a teapot, plate, toaster, plant, or frying pan by inserting their cyberhand into the virtual object, and clicking a grasp button on their three-dimensional mouse. Each patient also physically picked up a virtual plate possessing solidity and weight, using a mixed-reality force feedback technique (Carlin, Hoffman, & Weghorst, 1997; Hoffman, 1998). The multi-sensory, highly interactive, verbal, spatial, visual, auditory, and tactile nature of VEs makes the experience difficult for the brain to ignore, since it draws upon multiple attentional resources (e.g., Wickens, 1992) each of which has a limited capacity. Distractions can draw attention away from patients’ mental process-

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ing, thereby decreasing the amount of pain consciously experienced by the patient (Farthing, Venturino, & Brown, 1984; McCaul & Malott, 1984). VEs may prove to be an exceptionally attention-grabbing experience. The cognitive–attentional state of the participant could be changed by drawing their minds inside a three-dimensional, immersive, computer-simulated VE. Although case reports are inherently inconclusive (Campbell & Stanley, 1963), they can sometimes be revealing. Hoffman, Doctor, et al., (2000) measured pain levels of two pre-adult patients undergoing burn wound dressing changes, wound cleansing, and staple removal from skin grafts while adjunctively being distracted by a VE and by Nintendo64 (order counterbalanced) during a single wound care session. VE distraction was dramatically more effective as an analgesic than the Nintendo64 video game. Interestingly, that study also suggests why the VE works better; presence in the Nintendo games was much lower than the illusion of presence in the VE. More recently, Hoffman, Patterson, and Carrougher (2000) found a statistically significant reduction in pain while in a VE in a controlled within-subject clinical study of severe burn pain during physical therapy (VE vs. no distraction). While in the VE, patients reported a 47% drop in the amount of the physical therapy session they spent thinking about their pain and wound care, a 33% drop in pain unpleasantness (an emotional component of pain), and a 22% drop in pain intensity. In this analog study, Experiment 1 is a conceptual replication of Hoffman, Patterson, et al. (2000) in a controlled laboratory environment testing healthy uninjured undergraduates. Pain was induced by placing a tourniquet (blood pressure measuring cuff) on the participants’ arm for up to 10 min. Every 2 min the participants made pain ratings. Pain studies using the tourniquet technique consistently show a steady increase in pain over a 10 min ischemia (Hamalainen & Kemppainen, 1990; Lorenz & Bromm, 1997; Maixner & Humphrey, 1993; Segendahl, Ekblom, & Sollevi, 1994). For example, Hamalainen and Kemppainen (1990) reported average subjective assessments of ischemic pain on 100 mm visual analog scales (VAS) ratings of 5 mm pain at 2 min, 10 mm pain at 4 min, 25 mm pain at 6 min, 45 mm pain at 8 min, and 62 mm pain after 10 min of ischemia. Using a within-subjects design, pain reported during a no distraction condition (conventional treatment) was compared to the pain experienced while the participant was in the VE. After 8 min of wearing the tourniquet with no distraction, participants went into an immersive VE, interacted with a virtual spider and ate a virtual candy bar (Hoffman, Hollander, Schroder, Rousseau, & Furness, 1998). Participants rated pain on five 100 mm VAS and one rating of anxiety for each condition with the blood pressure cuff still on. “A VAS is a line, usually l00 mm in length … with anchors at each end to indicate the extremes of the sensation under study” (Gift, 1989). The participant makes a mark on the line to indicate the amount of sensation experienced, and the experimenter measures the number of mm from the low end of the scale to the participants mark (Gift, 1989). Based on the 10 min ischemic pain literature consistently showing a steady increase in pain the longer the ischemia lasts, with no distraction, the last 2 min period of the 10 min ischemia would be the most painful segment of the study. Yet a drop in pain during the last 2 min when participants went into virtual reality was predicted in this study.

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Prior to this study, only one female burn patient had been treated with a VE for pain control. One goal of this study is to determine whether VE pain control is also effective for women. Another goal was to replicate a finding by Hoffman, Hollander, et al., (1998) that allowing participants to physically touch and physically eat mixed reality virtual objects (using tactile augmentation) increases the user’s sense of presence in the virtual world.

2. EXPERIMENT 1 2.2. Method Participants. Twenty-two healthy undergraduate Psychology students from the University of Washington participated individually for extra credit. Fourteen of the participants were women, eight were men. Studies were conducted under both written and verbal informed consent using protocols reviewed and approved by the University of Washington’s Committee on the Rights of Human Subjects. Students with a history of extreme susceptibility to motion sickness were excluded, and students were fully informed prior to volunteering/signing up that the experiment was designed to study pain, and involved a 10 min pressure cuff induced ischemia.

Procedure. Ischemic arm pain was induced using a tourniquet (e.g., Fillingim et al., 1997; Hamalainen & Kemppainen, 1990; Maixner, Gracely, Zuniga, Humphrey, & Bloodworth, 1990). The participant elevated his/her left forearm for 60 sec, after which a standard blood pressure measuring cuff was inflated (by the participant) to 250 mmHg on the lower bicept, (200 mmHg for women) and the forearm was returned to the horizontal position, resting on a table. This signaled the official beginning of the ischemia. No muscle exercises were performed. Participants were told that it was important to let the experimenters know if they needed to take off the pressure cuff prior to the 10 min completion (e.g., if it became too painful), and experimenters would immediately begin slowly deflating and removing the pressure cuff. Participants gave pain ratings every 2 min during the ischemia. The experimenter also verbally asked the participant if they were alright after each 2 min period. Participants did not wear the VR helmet during the no distraction phase. Participants able to tolerate 8 min of the ischemia with no distraction were put into the VE for the last 2 min of the ischemia, and afterwards asked to rate how much pain they had been in during the last 2 min (when they were in the VE). To minimize the occurrence of excessively high pain levels, the duration of the ischemia was reduced for any participant whose “average pain” measure for the most recent 2 min period with no distraction reached 50 mm or higher on a 100 mm VAS subjective pain rating at any pain rating prior to the 8 min mark. Such participants were immediately placed into the VE for the next 2 min period, participants filled out current pain ratings for that 2 min segment in the VE, and the pressure cuff was removed. After answering their last pain ratings while

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wearing the cuff, the pressure cuff was slowly deflated for each participant, and the participant placed their left hand in their lap, and filled out the post-experimental questionnaire (e.g., simulator sickness and presence ratings). They were then engaged in conversation until 6 min had passed since the end of their ischemia, at which point they filled out pain ratings once more, to make sure their pain was back to zero, or very near zero. Most (n = 16) participants had returned to near zero pain within 6 min of ending the ischemia and all other participants (n = 6) had returned to near zero pain after 12 min. It was interesting to measure how quickly pain subsided, and the experimenters were obligated to monitor the participants’ full recovery. Furthermore, participants went on to participate in Experiment 2, which required that participants were no longer in pain. A Silicon Graphics Octane MXE with Octane Channel Option1 coupled with a VR helmet was used to create an immersive, three-dimensional, interactive, computer-simulated environment. A Polhemus FastrakTM motion sensing system with 6 degrees of freedom sensors was used to measure the position of the user’s head and hand position. Participants experienced SpiderWorld, a modified version of Division LTD’s DVS-3.1.2 KitchenWorld2 complete with countertops, a window, a sink, a stove, and three-dimensional cabinets. Participants were randomly assigned to one of two groups: ordinary VE or VE with tactile augmentation. No sounds were used in either condition. Participants in both groups were placed in the middle of the virtual kitchen, and did not have a navigation device. Instead, they stood in the virtual kitchen and could “pick up” virtual objects (e.g., a spider and a candy bar) with their cyberhand. Using tactile augmentation (Carlin, Hoffman, & Weghorst, 1997; Garcia-Palacios, Hoffman, Carlin, Furness, & Botella-Arbona, in press; Hoffman, 1998; Hoffman, Doctor, et al., 2000; Hoffman, Garcia-Palacios, Carlin, Furness, & Botella-Arbona, in press; Hoffman et al., 1996), a real world toy twin of the virtual brown spider made it possible for participants to “physically touch” the virtual spider. Apalm-sized toy replica of a Guyana bird-eating tarantula was attached to a position sensor held by the experimenter. As the participant reached out with their cyberhand to touch the virtual spider, their real hand explored the position-tracked toy spider. The objective was to provide the subjective experience of a virtual spider that felt furry, had weight (cyberheft), and solidity. Any movement of the toy spider led to a similar movement by the virtual spider. Similarly, participants in the tactile augmentation group could physically eat a virtual candy bar linked via a position sensor attached to its real world twin. They saw a Hershey’s chocolate bar in their cyberhand in the virtual kitchen. When they held the virtual candy bar up to their mouths, they took a bite out of the real position tracked candy bar. The experimenter pushed a button changing the graphics such that when the participant pulled the virtual candy bar away from their mouth, there was a bite missing in the virtual candy bar. This led them to have the illusion of physically eating the virtual candy bar as they stood in the virtual kitchen. Participants in the ordinary VE condition were handed an ordinary virtual spider (a position sensor with no toy spider attached), 1Silicon Graphics, Inc., 13810 S. E. Eastgate Way, Suite 300, Bellevue, WA 98105; (425) 746–7563; http://www.sgi.com/ 2Division Incorporated; http://www.division.com/

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and imagined taking a bite from a virtual candy bar with no real candy bar attached (their position tracked hand lifted their cyberhand and virtual candy bar up to their mouth). The experimenter pushed the button to make the candy bar show a bite mark when participants imagined taking a bite. This software was chosen by Hoffman and colleagues for treating burn patients during physical therapy (Hoffman, Patterson, & Carrougher, 2000) because it had been shown to consistently give users a relatively high sense of presence. Pain, the primary dependent variable, was measured immediately after each experimental condition (ischemic pain with no distraction, and ischemic pain during VR). Participants completed five retrospective subjective pain ratings using 100 mm (Gift, 1989; Huskisson, 1974). The VAS has concurrent validity and test–retest reliable (Gift, 1989). Such self-report scales provide valid reflections of pain experience across patient populations (see review by Jensen, 1997). Self-report is the most valid method for assessing pain experience (cf. Hilgard & Hilgard, 1994; Jensen, 1997). With respect to the most recent 2 min of the ischemia, participants rated (a) how much time they spent thinking about their pain and/or their arm (endpoints labeled zero min, the entire time), (b) their worst pain (no pain, worst pain), (c) their average pain (no pain, worst pain), (d) how much their arm bothered them (not at all bothersome, the most bothersome), (e) how unpleasant they found the ischemia (not at all unpleasant, the most unpleasant), and (f) their anxiety (no anxiety, highest anxiety). These measures are designed to assess the sensory component of pain (worst pain and average pain in this study) and the affective component (unpleasant and bothersome in this study). Sensory and affective are two separately measurable and sometimes differentially influenced components of the pain experience (Gracely, McGrath, & Dubner, 1978; Melzack & Wall, 1965). Time spent thinking about pain is a new measures of procedural pain recently introduced by Hoffman, Doctor, et al. (2000). After the ischemia, participants were asked the following ratings using visual analog scales: (a) To what extent (if at all) did you feel nausea as a result of experiencing the virtual environment? (none, very much); (b) While experiencing the virtual environment, to what extent did you feel like you went into the virtual world? (I did not feel like I went into the virtual world at all, I went completely into the virtual world); (c) How real did the objects in the virtual world seem to you (completely fake, indistinguishable from a real object). Hendrix and Barfield (1995) describe several studies showing the reliability of a similar subjective measure of presence.

2.2. Results First, results were analyzed with men and women combined. Alpha is set at .05 for F tests. For t tests, a Bonferroni (Keppel, 1982) correction factor (dividing alpha by the number of t tests) was used (.05/6 = .008). According to 100 mm VAS pain ratings (see Figure 1), mean pain ratings increased significantly every 2 min during the no-distraction phase (0 to 8 min). There was a significant rise in pain from 2 min to 4 min, F(1, 21) = 9.42, p = .006, MSe = 49.02, from 4 to 6 min, F(1, 21)

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FIGURE 1

Mean pain ratings of men and women, taken every 2 minutes.

= 10.60, p = .004, MSe = 32.92, from 6 to 8 min (the control condition), F(1, 21) = 10.91, p = .003, MSe = 80.95, and a significant and large (53%) drop in pain between 8 and 10 min, when participants went into virtual reality, F(1, 21) = 29.16, p < .001, MSe = 293.41.3 As shown in Figure 2, comparing all participants in the control condition (6–8 min period, or the next to the last 2 min session) to the VE condition (8–10 min or the last 2 min session), pain while in the VE dropped significantly for each of the five VAS pain ratings, time spent thinking about their pain, t(21) = 4.79, p < .001, SE = 7.43; unpleasant, t(21) = 5.02, p < .001, SE = 5.44; bothersome, t(21) = 5.48, p < .001, SE = 5.28; worst pain, t(21) = 4.93, p < .001, SE = 5.10; average pain, t(21) = 4.41, p