ORIGINAL CONTRIBUTION

Effect of Cranial Osteopathic Manipulative Medicine on Cerebral Tissue Oxygenation Xiangrong Shi, PhD; Seth Rehrer, OMS IV; Parna Prajapati, MBBS, MPH; Scott T. Stoll, DO, PhD; Russell G. Gamber, DO, MPH; and H. Fred Downey, PhD Context: The use of cranial osteopathic manipulative medicine (OMM) to alter cerebral tissue oxygen saturation could play a role in the maintenance of cerebral homeostasis. Objective: To examine the effects of cranial OMM on cerebral tissue oxygen saturation (SCTO2) and cardiac autonomic function in healthy adults. Methods: Cranial OMM augmentation and suppression techniques and sham therapy were randomly applied to healthy adults. During cranial OMM and sham therapy, SCTO2 of the prefrontal cortex was determined bilaterally by using nearinfrared spectroscopy. Heart rate, blood pressure, and systemic arterial blood oxygen saturation (SaO2) were also measured. Power spectral analysis was applied to continuous 4-minute R-R intervals. Measurements were made during 2-minute baseline periods, during 4-minute applications of the techniques, and during 5-minute recovery periods. Results: Twenty-one adults (age range, 23-32 y) participated in the present study. Differences in mean baseline measurements for the augmentation technique, suppression technique, and sham therapy were not statistically significant for heart rate, blood pressure, SaO2, left SCTO2, or right SCTO2. During the suppression technique, there was a statistically significant decrease in both left (slope [standard deviation]= -0.33 [0.08] %/min, R2=0.85, P=.026) and right (slope [standard

From the departments of integrative physiology (Drs Shi and Downey and Mr Prajapati) and osteopathic manipulative medicine (Drs Rehrer, Stoll, and Gamber), the Cardiovascular Research Institute (Drs Shi and Downey), and The Osteopathic Research Center (Drs Shi, Gamber, and Downey) at the University of North Texas Health Science Center in Fort Worth. Financial Disclosure: This study was supported in part by AOA grant #0911-594. Address correspondence to Xiangrong Shi, PhD, 3500 Camp Bowie Blvd, Department of Integrative Physiology, University of North Texas Health Science Center, Fort Worth, TX 76107-2644. E-mail: [email protected] Submitted December 22, 2010; final revision received July 15, 2011; accepted August 22, 2011. 660 • JAOA • Vol 111 • No 12 • December 2011

deviation]=-0.37 [0.06] %/min, R2=0.94, P=.007) SCTO2 with increased cranial OMM time. However, neither the augmentation technique nor the sham therapy had a statistically significant effect on SCTO2. Decreases in normalized low-frequency power of R-R interval variability and enhancements of its high-frequency power were statistically significant (P=.05) during cranial OMM and sham therapy, indicating a decrease in cardiac sympathetic influence and an enhanced parasympathetic modulation. Conclusion: The cranial OMM suppression technique effectively and progressively reduced SCTO2 in both prefrontal lobes with the treatment time. J Am Osteopath Assoc. 2011;111(12):660-666

he efficacy of cranial osteopathic manipulative medicine (OMM) has been reported in the treatment of tension-type headache.1 To our knowledge, however, the mechanisms of action for cranial OMM have not been explored and are poorly understood. It has been hypothesized that these mechanisms, at least in part, involve improved cerebral homeostasis associated with changes in cerebral blood flow and cerebral tissue oxygenation (SCTO2). Cranial OMM is an area of study based on the postulation that intracranial structures exhibit interdependent movements during the process of internal respiration, or the primary respiratory mechanism.2 Brain tissues, including the parenchyma, arteries, and cerebrospinal fluid, show rhythmic motion.3-5 Human lambdoid sutures, which join the occipital and parietal bones, maintain the patency that allows small amounts of movement.6 Although the cranial bones and the dura mater do not generate rhythmic movement, their compliance allows limited movement7,8 and they can, thus, respond to cranial OMM. During flexion movement, the sphenoid and occipital bones rotate about their transverse axes anteriorly; during extension movement, these bones move in reverse. Therefore, we postulated that use of cranial OMM to enhance flexion and extension of the cranial sphenobasilar synchondrosis at the occipital and posterior parietal bones could augment the primary respiratory mechanism (ie, augmentation technique) and that the use of cranial OMM to prohibit flexion and enhance extension of the movement of the cranial base and the petrous portions of the temporal bones could suppress the

T

Shi et al • Original Contribution

ORIGINAL CONTRIBUTION

primary respiratory mechanism (ie, suppression technique). The purpose of the present study was to examine whether SCTO2 and cardiac autonomic modulation would be responsive to cranial OMM augmentation and suppression techniques. We hypothesized that the use of cranial OMM to alter the primary respiratory mechanism or to cause movement at the occipital and posterior parietal bones could elicit responses or changes in SCTO2 and cerebral blood flow or volume. In other words, we believed that the augmentation technique would increase SCTO2, and the suppression technique would decrease SCTO2. Furthermore, we hypothesized that cranial OMM would help balance the cardiac autonomic nervous function, as reflected by change in heart rate or R-R interval variability.

Methods The present study took place October 12, 2009, through December 10, 2009, at the research laboratory of the Department of Integrative Physiology, University of North Texas Health Science Center in Fort Worth. The study was approved by the institutional review board of the University of North Texas Health Science Center.

Participants Participants were recruited by means of advertisement, personal contact, and e-mail during September 2009 through November 2009. Participants were included in the study if they were 18 to 75 years old, healthy, and normotensive. Exclusion criteria included the use of antihypertensive medication. Volunteers who met the study criteria gave their consent to participate in the study and completed a physical examination within 2 weeks of recruitment. Cranial OMM appointments were scheduled on a rolling basis according to the availability of the participant and the physician.

Procedure After approximately 15 minutes of supine rest after instrumentation (ie, placing instruments on the participant), the participant underwent 2 cranial OMM techniques and sham therapy (Table 1). The order of the cranial OMM techniques and sham therapy was randomly assigned. The procedures followed a single-blind protocol; participants were blinded to the order of therapy. In a previous study,9 we found that 5 minutes of recovery time between treatments was sufficient for return to baseline. Each of the steps was completed with either “hands on” or “hands off.” For hands-on steps, the physician’s hands were placed directly behind the back of the participant’s head. For hands-off steps, the physician’s hands were removed from the back of the participant’s head. The cranial OMM techniques and sham therapy comprised 2 minutes of baseline with hands on, 4 minutes of therapy, Shi et al • Original Contribution

and 5 minutes of recovery with hands off. All procedures were performed by the same AOA board-certified osteopathic physician (S.T.S.). These cranial OMM techniques were selected based on the findings of a pilot study9; they caused no substantial head movement and no interference with continuous measurement of SCTO2 from the prefrontal lobes of the cortex. The cranial OMM used in the procedure comprised an augmentation technique and a suppression technique. The augmentation technique involved enhancing flexion and extension movement of the cranial sphenobasilar synchondrosis at the occipital and posterior parietal bones to augment the primary respiratory mechanism. This technique was performed using the standard vault hold.2 With the participant lying supine on a table, the operator (S.T.S.) sat 8 to 10 inches away from the head of the table. With forearms resting comfortably on the head of the table, he then lightly contacted the sides of the participant’s head with both hands, using the palmar surface of all his fingers and palms but not the thumbs. The index and middle fingers were placed bilaterally on the greater wings of the sphenoid bones, while the ring and little fingers were placed on the lateral angles of the occiput. The operator encouraged both flexion and extension by enhancing the motion of the sphenoid and occiput bones with his own hands. The suppression technique involved prohibiting flexion movement and enhancing extension movement of the cranial Table 1. Effect of Cranial Osteopathic Manipulative Medicine Techniques and Sham Therapy on Cerebral Tissue Oxygenation: Experimental Protocol* Protocol Step

Duration, min

䡲 Baseline 䡲 Augmentation ▫ Baseline with hands on ▫ Augmentation technique ▫ Recovery with hands off 䡲 Suppression ▫ Baseline with hands on ▫ Suppression technique ▫ Recovery with hands off 䡲 Sham Therapy ▫ Baseline with hands on ▫ Sham therapy ▫ Recovery with hands off

5 2 4 5 2 4 5 2 4 5

* The order of the manipulative techniques and sham therapy was randomized in a single-blind fashion; however, all patients began with baseline. “Hands on” means the physician’s hands were placed directly behind the back of the patient’s head; “hands off” means the physician’s hands were removed from the back of the patient’s head.

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ORIGINAL CONTRIBUTION base and the petrous portions of the temporal bones to suppress the primary respiratory mechanism.2 To perform this technique, the operator applied compression of the fourth ventricle (CV-4) technique. With the participant resting in the supine position on the table, the operator placed 1 of his hands in the palm of the other, so that his thenar eminences laid parallel to one another. The operator then slipped his hands under the participant’s head, with the lateral angles of the occiput medial to the occipitomastoid suture resting on the thenar eminences. The operator’s fingers were free and not pressing on the neck. The weight of the head rested on the thenar eminences, which gently compressed the lateral angles. The operator suppressed the cranial rhythm by enhancing cranial extension and discouraging cranial flexion. During extension, the occiput moved in a superior direction. The operator enhanced this motion by adding superior traction to the occiput during that phase of the cycle. He then discouraged flexion movement by maintaining that superior traction. The sham therapy was uniform for each participant and mimicked the suppression technique (ie, CV-4 technique) by using a random manual maneuver. Neither augmentation nor suppression was performed during the sham therapy.

Measurements During the study, heart rate, blood pressure, SCTO2, and systemic arterial oxygen saturation (SaO2) were continuously monitored. Heart rate was determined using electrocardiography. Systemic arterial blood oxygen saturation was continuously measured using an arterial pulse oximeter (OXY100C; BIOPAC Systems Inc; Goleta, California). Beat-tobeat radial systolic blood pressure and diastolic blood pressure were noninvasively monitored with blood pressure tonometry (Colin CBM-7000, San Antonio, Texas). In a previous study,9 we validated that radial blood pressure carefully measured with the tonometry method is highly correlated with the blood pressure monitored with an intraradial arterial catheter. In addition, R-R interval variability was assessed as an indication of cardiac autonomic modulation.10,11 Regional SCTO2 of the prefrontal lobes was determined with near-infrared spectroscopy by using 2 sensors (4100 INVOS Cerebral Oximeter; Somanetics; Troy, Michigan) placed bilaterally on the forehead with outputting analog samples at 1 Hz. In each of these sensors, 2 light diodes generated low-intensity, near-infrared light at 730-nm and 805nm wavelengths that were emitted into the participant’s forehead. The light penetrated the skull, dura mater, and cerebrospinal fluid and passed through the cerebral cortex (⩽ approximately 2 cm in depth; ie, approximately half the distance between the near-infrared light source and the detector). The spectral absorption of blood in the region of the prefrontal cerebral cortex targeted by the light was determined by measuring the amount of light returned to 2 detectors positioned at distances of 3 cm and 4 cm from the light 662 • JAOA • Vol 111 • No 12 • December 2011

source.12,13 A strong correlation (slope=0.98, R2=0.96) between changes in SCTO2 and jugular venous blood oxygen saturation has been demonstrated previously.14 This technique and measurement have been successfully applied in our previous studies.15-17

Data Analysis We converted a section of 4-minute continuous beat-to-beat R-R interval data with minimum variance into power spectral data by using a fast Fourier transform algorithm. Both low-frequency (0.05-0.15 Hz) and high-frequency (0.20-0.30 Hz) power spectra of R-R interval variability were extracted and were normalized by the ratios of low frequency/(low frequency + high frequency) and high frequency/(low frequency + high frequency), respectively.11 These low frequency and high frequency ranges include the rhythms for the Mayer wave (approximately 0.1 Hz) and normal breathing frequency (approximately 15 cycles/min), respectively. Analysis of variance was applied to test the effect of different procedures on the cardiovascular and oxygenation variables. Linear regression was applied to test the changes in these variables with the time of the procedures. P values less than or equal to .05 were considered to indicate a statistically significant difference. The data were reported as group mean and standard error of the mean (SEM). Statistical Analysis System (SAS, Cary, North Carolina) and DADiSP (DSP Development Corporation, Cambridge, Massachusetts) software programs were applied for statistical analysis and power spectral analysis, respectively.

Results Twenty-one healthy volunteers (8 women, 13 men) aged 23 to 32 years (mean [SEM] body mass index, 24 [3.7]) gave written consent and participated in the present study. No volunteers were excluded from the study. Differences in baseline measurements (group mean [SEM]) for the augmentation technique, suppression technique, and sham therapy were not statistically significant for heart rate (69 [15], 71 [23], 66 [9] beats/min), mean blood pressure (79 [2], 77 [3], 76 [3] mm Hg), SaO2 (98 [1], 97 [1], 97 [1]%), left SCTO2 (65 [9], 66 [10], 66 [10] %), or right SCTO2 (66 [11], 67 [10], 67 [10] %) (Table 2). Heart rate, blood pressure, and SaO2, remained constant during the cranial OMM techniques and sham therapy (Figure 1). Neither augmentation (left: 0.10 [0.05] %/min, R2=0.56, P=.144; right: 0.06 [0.05] %/min, R2 = 0.33, P=.314) nor sham therapy (left: -0.06 [0.02 ]%/min, R2=0.68, P=.084; right: -0.10 [0.05] %/min, R2=0.54, P=.156) affected cerebral tissue oxygenation. Cerebral tissue oxygenation was decreased in left (-0.33 [0.08] %/min, R2=0.85, P=.026) and right (-0.37 [0.06] %/min, R2=0.94, P=.007) prefrontal lobes by the suppression technique (Figure 2). The group mean (SEM) low-frequency power of R-R interval variability for the baseline condition, augmentation Shi et al • Original Contribution

ORIGINAL CONTRIBUTION

deficiency (Figure 2). However, the suppression technique, or CV-4 technique, elicited a response in SCTO2, which was progressively decreased in both the left and right sides of the prefrontal lobes Manipulative Technique, Group Mean (SEM)* with the increasing application time Augmentation Suppression Sham (Figure 2). This response could not be a Characteristic Technique Technique Therapy result of the placebo factor because there ◾ SaO2, % 97.6 (0.18) 97.3 (0.17) 97.5 (0.18) was no response to sham therapy. Also, ◾ Heart Rate, beats/min 67 (2) 66 (2) 62 (2) the order of the techniques was random ◾ Blood Pressure, mm Hg and patients were blinded. ▫ Systolic 115 (3) 112 (4) 111 (3) Changes in heart rate, blood pres▫ Diastolic 61 (2) 60 (2) 59 (3) sure, and SaO 2 during the augmenta◾ SCTO2, % tion technique, suppression technique, ◽ Left side 65.3 (1.9) 66.0 (2.1) 65.6 (2.1) ◽ Right side 66.8 (2.1) 67.5 (2.1) 67.2 (2.2) and sham therapy were not statistically significant (Figure 1). Furthermore, neither cranial OMM nor sham therapy *No differences were statistically significant. seemed to increase the oxygen extracAbbreviations: SaO2, systemic arterial oxygen saturation; SCTO2, cerebral tissue oxygen saturation; SEM, tion rate in the cerebral tissue as indistandard error of the mean. cated by SCTO2. On the basis of these findings, we may assume that the partechnique, suppression technique, and sham therapy was ticipant’s overall systemic and cerebral metabolic rate 461.7 (90.3), 460.3 (152.2), 396.7 (96.0), and 426.0 (89.0) mil- remained constant during the experiment and that the liseconds2, respectively. The group mean (SEM) high-fre- decrease in SCTO2 we observed during the suppression techquency power of R-R interval variability was 383.6 (248.0), nique was most likely due to reduced oxygen delivery 555.3 (374.7), 395.6 (182.2), and 535.8 (301.2) milliseconds2 for resulting from depression of cerebral blood flow. This notion the baseline condition, augmentation technique, suppression is supported by findings from Formes et al,16 which revealed technique, and sham therapy, respectively. The differences that decreases in middle cerebral blood flow velocity, deterof these variables were not statistically significant between mined with transcranial Doppler ultrasonography, closely baseline and therapies. However, the normalized low-fre- paralleled decreases in SCTO2 during central hypovolemia quency power was statistically significantly lower and the or simulated hemorrhage. In another study, Zhang et al17 normalized high-frequency power was statistically signifi- observed increases in SCTO2 during CO2 stimulated cerebral cantly higher during the augmentation maneuver (P=.032), the vasodilation, which appeared to be independent of oxygen suppression maneuver (P=.035), and the sham therapy content. (P=.013) than during the baseline condition. This finding indiCollectively, findings of the present study suggest that cates a diminished sympathetic influence and an enhanced the cranial OMM suppression technique could be effectively parasympathetic modulation on the heart (Figure 3). applied to alleviate excessive intracranial pressure by reducing cerebral blood flow or volume. Although the mechanism by Comment which the suppression technique was able to elicit SCTO2 The present study provides 2 novel findings. First, cranial responses was not clear, we postulated that suppression of the OMM with suppression technique can effectively and pro- cranial rhythmic impulses as a result of enhancing cranial gressively elicit cerebral hemodynamic response by decreasing extension and discouraging cranial flexion could more effeccerebral tissue oxygenation in the left and right prefrontal tively create intracranial force to facilitate venous outflow cortex with the treatment time.3 Second, cranial OMM and from the dural sinuses into the internal jugular vein and to sham therapy to the cranium relax cardiac sympathetic mod- resist internal carotid arterial blood flow. This impact of the ulation and enhance cardiac vagal modulation as reflected by suppression technique may be even greater if the technique power spectral analysis of R-R interval variability. is applied on patients with excessive intracranial pressure We did not observe a statistically significant increase in or volume. In addition, the effect could be further enhanced SCTO2 during cranial OMM with the augmentation techwith repeated therapy bouts or multiple therapy sessions. nique, which was contrary to our original hypothesis. This Thus, these findings support application of cranial OMM finding suggests that the augmentation technique is ineffecfor conditions in which cerebral blood flow or pressure is tive in altering the cerebral hemodynamic response in healthy excessive, such as migraine headaches. In any case, findings young participants when there is no cerebral tissue oxygen from the present study suggest that the decrease in SCTO2 Table 2. Baseline Characteristics of Healthy Participants Receiving Cranial Osteopathic Manipulative Medicine and Sham Therapy (N=21)

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Figure 1. Group heart rate, mean blood pressure, and arterial oxygen saturation during cranial osteopathic manipulative medicine augmentation technique, suppression technique, and sham therapy. No statistically significant differences from baseline were noted for any variables during any therapy.

produced by the suppression technique of cranial OMM is benign in a group of healthy, young adults. Although heart rate was not statistically significantly affected by cranial OMM or sham therapy, the normalized R-R interval variability was decreased in the low-frequency power spectrum and increased in the high-frequency power spectrum (Figure 3). This outcome is consistent with a study by Henley et al18 that determined that both cervical OMM and its sham therapy statistically significantly improved heart rate variability. It is well recognized that low frequency of the R-R interval variability power spectrum is modulated by sympathetic nerve activity, and high frequency is influenced by parasympathetic modulation.10 Improved cardiac vagal dominance and reduced sympathetic nervous activity are 664 • JAOA • Vol 111 • No 12 • December 2011

protective against cardiac attack and arrhythmia.10,19,20 In the present study, cardiac autonomic function improved during sham therapy as well as during the cranial OMM augmentation and suppression techniques. Although there was an apparent placebo effect on the normalized R-R interval variability during the cranial OMM, these results demonstrate positive effects of manually touching the patient in accordance with osteopathic principles.21 This outcome suggests that the autonomic nervous system could be more readily affected by psychological influence than other physiologic responses (eg, cerebral tissue oxygenation). A limitation of this study is that the present interventional observation is unable to pinpoint the physiologic mechanism for the responses of SCTO2 that were correlated with Shi et al • Original Contribution

ORIGINAL CONTRIBUTION

Figure 2. Cerebral tissue oxygen saturation during cranial osteopathic manipulative medicine augmentation technique, suppression technique, and sham therapy.

Side of Prefrontal Cortex Left

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Slope = 0.10 R 2 = 0.56 P = .144

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the time of the suppression technique but not with the augmentation technique. In addition, the inclusion of only healthy, young volunteer participants may limit the implications of the present study’s findings regarding the efficacy of cranial OMM. More obvious responses to cranial OMM (either the suppression or augmentation techniques) might be elicited in patients with excessive intracranial pressure or with autonomic dysfunction. This possibility merits further investigation.

Conclusion The present study examines the systemic and cerebral hemodynamic response to augmentation and suppression cranial OMM techniques in healthy adults. Our data suggest that the suppression technique elicits a mild but statistically signifiShi et al • Original Contribution

3

4

cant reduction in the cerebral blood flow as manifested by SCTO2 (an index of cerebral blood flow) that correlated with the treatment time. Thus, this technique could be applied to alleviate conditions associated with intracranial hypertension or excessive volume. Future studies should be conducted in patients with these types of chronic clinical conditions to further assess the effect of multiple sessions of cranial OMM with suppression technique on cerebral homeostasis, as well as on autonomic nervous balance. We believe that the physiologic response, or the efficacy of cranial OMM, will be more substantial in patients with intracranial hypertension or excessive volume than in healthy adults.

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2. Nicholas A, Nicholas E. Osteopathy in the cranial field. In: Nicholas AS, Nicholas EA, eds. Atlas of Osteopathic Techniques. Philadelphia, PA: Lippincott Williams & Wilkins; 2008:475-495. 3. Greitz D, Wirestam R, Franck A, et al. Pulsatile brain movement and associated hydrodynamics studied by magnetic resonance phase imaging: the Monro-Kellie doctrine revisited. Neuroradiology. 1992;34(5):370-380. 4. Poncelet BP, Wedeen VJ, Weisskoff RM, Cohen MS. Brain parenchyma motion: measurement with cine echo-planar MR imaging. Radiology. 1992; 185(3):645-651. 5. Enzmann DR, Pelc NJ. Brain motion: measurement with phase-contrast MR imaging. Radiology. 1992;185(3):653-660. 6. Sabini RC, Elkowitz DE. Significance of differences in patency among cranial sutures [published correction appears in J Am Osteopath Assoc. 2006;106 (12):688]. J Am Osteopath Assoc. 2006;106(10):600-604. 7. Ferguson A. A review of the physiology of cranial osteopathy. J Osteopath Med. 2003;6(2):74-88. http://faculty.une.edu/com/jnorton/PDFfilesCranial /CranialPhysiology.pdf. Accessed June 2, 2011. 8. Frymann VM. A study of the rhythmic motions of the living cranium. J Am Osteopath Assoc. 1971;70(9):928-945.

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Normalized Power of R-R Interval Variability, Hz

1.0

Low Frequency High Frequency

0.8

0.6

Figure 3. Normalized low-frequency and highfrequency power of R-R interval variability. Compared to the baseline, the low frequency power was lower and the high frequency power was higher during cranial osteopathic manipulative medicine augmentation technique, suppression technique, and sham therapy (P⬍.05). No statistically significant differences were found between therapies.

0.4

0.2

0

saturation from cerebral oximetry or arterial O2 saturation during isocapnic hypoxia. J Clin Monit Comput. 2000;16(2): 191-199. Baseline

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Sham Therapy

15. Guo H, Tierney N, Schaller F, et al. Cerebral autoregulation is preserved during orthostatic stress superimposed with systemic hypotension. J Appl Physiol. 2006;100(6):1785-1792.

9. Wray DW, Formes KJ, Weiss MS, et al. Vagal cardiac function and arterial blood pressure stability. Am J Physiol Heart Circ Physiol. 2001;281(5):H1870H1880.

16. Formes K, Zhang P, Tierney N, Schaller F, Shi X. Chronic physical activity mitigates cerebral hypoperfusion during central hypovolemia in elderly humans. Am J Physiol Heart Circ Physiol. 2010;298(3):H1029-H1037.

10. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. Heart rate variability: standards of measurement, physiological interpretation and clinical use. Circulation. 1996;93(5):1043-1065.

17. Zhang P, Huang G, Shi X. Cerebral vasoreactivity during hypercapnia is reset by augmented sympathetic influence. J Appl Physiol. 2011;110(2):352-358.

11. Smith M, Clark K, Shi X. Manual medicine and the autonomic nervous system: assessing autonomic function in humans. In: King H, Janig W, Patterson M, eds. The Science and Clinical Application of Manual Therapy. Edinburgh, United Kingdom: Churchill Livingstone Elsevier; 2010:85-92. 12. Hongo K, Kobayashi S, Okudera H, Hokama M, Nakagawa F. Noninvasive cerebral optical spectroscopy: depth-resolved measurements of cerebral haemodynamics using indocyanine green. Neurol Res. 1995;17(2):89-93. 13. Firbank M, Okada E, Delpy DT. Investigation of the effect of discrete absorbers upon the measurement of blood volume with near-infrared spectroscopy. Phys Med Biol. 1997;42(3):465-477.

18. Henley CE, Ivins D, Mills M, Wen FK, Benjamin BA. Osteopathic manipulative treatment and its relationship to autonomic nervous system activity as demonstrated by heart rate variability: a repeated measures study. Osteopath Med Prim Care. 2008;2:7. doi:10.1186/1750-4732-2-7. 19. Barron HV, Viskin S. Autonomic markers and prediction of cardiac death after myocardial infarction. Lancet. 1998;351(9101):461-462. 20. Hohnloser SH, Klingenheben T, Zabel M, Li YG. Heart rate variability used as an arrhythmia risk stratifier after myocardial infarction. Pacing Clin Electrophysiol. 1997;20(10 pt 2):2594-2601. 21. Palpation: the art and practice of feeling. In: Liem T. Cranial Osteopathy: A Practical Textbook. Seattle, WA: Eastland Press; 2009.

14. Kim MB, Ward DS, Cartwright CR, et al. Estimation of jugular venous O2

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Shi et al • Original Contribution