VISCERAL RESPONSES TO SPINAL MANIPULATION
 
   

Visceral Responses to Spinal Manipulation

This section was compiled by Frank M. Painter, D.C.
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FROM:   J Electromyogr Kinesiol. 2012 (Oct); 22 (5): 777–784 ~ FULL TEXT

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Philip Bolton, Brian Budgell

School of Biomedical Sciences & Pharmacy,
Faculty of Health,
University of Newcastle,
Callaghan NSW 2308, Australia.
Philip.Bolton@newcastle.edu.au


While spinal manipulation is widely seen as a reasonable treatment option for biomechanical disorders of the spine, such as neck pain and low back pain, the use of spinal manipulation to treat non-musculoskeletal complaints remains controversial. This controversy is due in part to the perception that there is no robust neurobiological rationale to justify using a biomechanical treatment of the spine to address a disorder of visceral function. This paper therefore looks at the physiological evidence that spinal manipulation can impact visceral function. A structured search was conducted, using PubMed and the Index to Chiropractic Literature, to construct of corpus of primary data studies in healthy human subjects of the effects of spinal manipulation on visceral function. The corpus of literature is not large, and the greatest number of papers concerns cardiovascular function. Authors often attribute visceral effects of spinal manipulation to somato-autonomic reflexes. While this is not unreasonable, little attention is paid to alternative mechanisms such as somato-humoural pathways. Thus, while the literature confirms that mechanical stimulation of the spine modulates some organ functions in some cohorts, a comprehensive neurobiological rationale for this general phenomenon has yet to appear.



From the FULL TEXT Article:

Introduction

Spinal manipulation is generally accepted as one reasonable treatment option in the management of musculoskeletal disorders such as low back pain and neck pain. Some evidence also exists that certain visceral disorders benefit from spinal manipulation (for example, see Bakris et al., 2007). However, the mechanisms by which spinal manipulation might alter visceral function, and so impact visceral disease, remain unclear. Therefore, in this paper, we review the currently available literature concerning visceral responses to the application of mechanical stimuli to the spine and paraspinal tissues. We specifically draw from human studies using high velocity, low amplitude manipulations, and also from research using biomechanically similar manoeuvres. Therefore, in this paper, the term ‘spinal manipulation’ may be interpreted liberally to include a range of related procedures.

To provide some clinical context for this review, it is to be noted that only a relatively small percentage of patients receive spinal manipulation specifically for the management of a non-musculoskeletal complaint. Numbers vary somewhat from survey to survey, but in Denmark, for example, the proportion of all patients presenting to chiropractors with non-musculoskeletal complaints apparently fell from 7% in 1966 to 3% in 1999 (Hartvigsen et al., 2003). Furthermore, the range of non-musculoskeletal complaints reported to be treated with spinal manipulation is quite limited. In fact, a previous review found that approximately half of the case reports and case series dealing with manipulative management of non-musculoskeletal complaints pertained to only a handful of disorders including gynecological complaints, visual deficits, asthma and enuresis (Budgell, 1999). Clinical trials of spinal manipulation in the treatment of non-musculoskeletal disorders are similarly restricted with the bulk of studies focused on cardiovascular disease, gynecological complaints, infantile colic and asthma (Hawk et al., 2007; Nakayama and Budgell, 2009). Given the restricted interests of clinical reports and controlled studies, as described above, we will therefore review basic physiological studies of what appear to be the most clinically relevant phenomena: cardiovascular, respiratory, gastrointestinal and female reproductive function.



Methods

Between April 25 and April 29, 2011, the PubMed and Index to Chiropractic Literature databases were searched, without date limitations, for the terms spinal manipulation or spinal manipulative therapy in combination with the terms somatovisceral, cardiovascular, respiratory, gastrointestinal, and gynecological. Thus, a representative search string would appear as: (‘‘manipulation, spinal’’ [MeSH Terms] or (‘‘manipulation’’ [All Fields] and ‘‘spinal’’ [All Fields]) or ‘‘spinal manipulation’’ [All Fields] or (‘‘spinal’’ [All Fields] and ‘‘manipulation’’ [All Fields])) or (‘‘spinal’’ [All Fields] and (‘‘musculoskeletal manipulations’’ [MeSH Terms] or (‘‘musculoskeletal’’ [All Fields] and ‘‘manipulations’’ [All Fields]) or ‘‘musculoskeletal manipulations’’ [All Fields] or (‘‘manipulative’’ [All Fields] and ‘‘therapy’’ [All Fields]) or ‘‘manipulative therapy’’ [All Fields])) and somatovisceral [All Fields].

Figure 1

Titles of identified articles were reviewed to eliminate studies which were either clearly off-topic, not published in English or which did not appear to report original data (reviews, commentaries etc.). The abstracts were then reviewed for the articles which passed the first filtering process. The abstracts were further reviewed for the additional criteria that the articles reported original studies in healthy humans of physiological responses to manual treatment (spinal manipulation or mobilization) of the spine. Articles which satisfied these criteria (Figure 1) were obtained as full text for data extraction and synthesis in this review.

Additionally, articles held in the authors’ own collections but which were not identified by the electronic searches were included in this review if they satisfied the inclusion criteria. These have been marked with an asterisk in their respective tables and included nine articles pertaining to humoural or neurological responses to manipulation, 15 articles pertaining to cardiovascular responses, and one article each pertaining to respiratory and gastrointestinal function. On reading the full texts, some articles were excluded because it became apparent that the subjects were symptomatic patients. The sum of the numbers of articles located with each of the five searches does not equal the total number of articles subsequently analyzed since there was some duplication of results. That is to say that some studies investigated outcomes from more than one system, for example both cardiovascular and respiratory.



Results

      Studies of cardiovascular function

Table 1A

Table 1B

Table 1C

Perhaps because of the limitations of available technology to record other physiological parameters and due to clinical relevance, the largest number of experimental studies of spinal manipulation and somato-visceral effects in humans has examined outcomes in cardiovascular function. A total of 18 articles which satisfied our inclusion criteria were retrieved (Table 1). The cardiovascular measures commonly reported were heart rate (HR), blood pressure (BP) and heart rate variability (HRV), from which changes in autonomic output to the heart may be implied. Earlier studies of effects of spinal manipulation on heart rate and blood pressure have employed less reliable technology. For example, in studies of effects of SMT on blood pressure in healthy young cohorts, McKnight and DeBoer (1988) and Tran and Kirby (1977a,b) employed single before and after measures obtained by auscultatory sphygmomanometry, whereas Nansel et al., using a similar cohort, did not describe their methods of measuring heart rate or blood pressure (Nansel et al., 1991). Automated methods of monitoring blood pressure and heart rate are demonstrably more reliable than manual methods (for example, see Pastellides, 2009). Earlier studies may also have eschewed statistical analysis of results in favor of the authors’ subjective opinion of what constituted an important effect (for example, see Tran and Kirby, 1977a,b). Therefore, this review only considers in detail those studies that define both the outcome measure and statistical analysis used.

A few studies have employed arterial tonometry, a method which uses a force transducer placed over an artery to continuously measure blood pressure and, from the frequency of the pulse waves, heart rate. The tonometry equipment is costly but technically simple to apply and is a conventional method for monitoring blood pressure during surgery. The first pilot study using arterial tonometry to measure responses to spinal manipulation reported no significant changes or slight decreases in heart rate and blood pressure in alert healthy subjects (n = 11) receiving a series of mechanical cervical stimuli: direct pressure to cervical muscles, slow passive rotations of the neck and high velocity low amplitude manipulations, all of which were characterized as innocuous by the subjects (Fujimoto et al., 1999). Of these stimuli, cervical spinal manipulation produced the largest effects: decreases in systolic and diastolic pressures of 6.8 (S.D. ±1.9) mmHg and 6.6 (S.D. ±2.1) mmHg, respectively. While the authors of this study speculated that the cardiovascular changes seen were mediated primarily via the autonomic nervous system, they did not perform calculations in the time or frequency domains, for example power spectrum analysis, on their blood pressure and heart rate data which would have given some quantitative measure of changes in autonomic output to the cardiovascular system. Using a more complex design, four treatment paradigms over four successive days with measures of blood pressure pre-treatment and at 5, 15 and 30 min post treatment, Pastellides (2009) consistently showed decreases in systolic blood pressure in response to upper cervical manipulation, thoracic manipulation, and combined cervical and thoracic manipulation. Interestingly, McGuiness et al. (1997) referred to an increase in heart rate, and systolic and diastolic blood pressure following a ‘grade III posteroanterior mobilization’, although their paper does not report the actual data on heart rate and blood pressure.

While heart rate is a commonly used outcome measure, it is not constant even in a resting subject, but varies over a narrow range largely in response to changes in autonomic output to the cardiovascular system. Consequently analysis of heart rate variability has been used to indirectly assess relative autonomic drive to the heart (Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology, 1996). To explain the physiological mechanisms in brief, in humans relatively fast oscillations in heart rate, in the range of 0.25 Hz, are driven by the respiratory cycle (Grossman et al., 2004): as we inhale, thoracic pressure decreases, drawing blood pressure down slightly, in response to which baroreflexes attenuate vagal output to the heart somewhat, thereby permitting a slight rise in heart rate. The reverse process occurs as we exhale. Thus the relatively fast oscillations in heart rate reflect parasympathetic (vagal) output to the heart. Slower oscillations in heart rate, in the range of 0.15 Hz and lower, reflect a systemic ebbing and flowing of sympathetic output to the blood vessel walls creating low amplitude oscillations in blood pressure which again feed through the barore- flexes to modulate vagal tone. Thus, the slower oscillations in heart rate are ultimately driven by sympathetic tone but are dependent upon the integrity of the parasympathetic nervous system (Grasso et al., 1997). Nonetheless, computer algorithms can discriminate between fast and slow oscillations in R–R interval and generate numerical values which are broadly representative of sympathetic and parasympathetic cardiac tone.

Hence, based on HRV calculated from ECG recordings in healthy, pain-free young adults, it was reported that both cervical (Budgell and Hirano, 2001) and thoracic (Budgell and Polus, 2006) spinal manipulation were associated with increases in sympathetic output to the heart, even as heart rate decreased somewhat. Changes in HRV, and so autonomic output to the heart, have also been reported with lumbar manipulation (Roy et al., 2009). However, the small increases reported in parasympathetic tone in subjects without low back pain barely achieved the level of statistical significance.

Hence, while the numbers of studies and the sizes of their cohorts have been modest, there is some evidence that, in healthy subjects, high-velocity low-amplitude manipulation of the cervical, thoracic or lumbar spine modulates autonomic output to the heart. Cervical and thoracic manipulation have been associated with no changes or a shift in favor of sympathetic output to the heart in healthy young adults. Lumbar manipulation was associated with a small increase in cardiac parasympathetic output. Both cervical and thoracic manipulation have been associated with changes in heart rate and blood pressure. The actual magnitudes of changes in heart rate and blood pressure in the reports cited thus far have been modest – single digit decreases in HR (bpm), and systolic and diastolic blood pressures (mmHg) – and, in the healthy subjects employed, of course, of no clinical significance (but see Koch et al., 2002).

A number of authors have also reported effects of spinal manipulation on peripheral vascular physiology. Outcome measures have included such parameters as

peripheral blood flow velocity and volume (Licht et al., 1998, 1999),

skin temperature and skin blood flux (Harris and Wagnon, 1987; Chiu and Wright, 1996; Vicenzino et al., 1998; Karason and Drysdale, 2003; Roy et al., 2008).

No statistically significant effects have been observed in the functions of the larger vessels; however, skin temperature and skin blood flow changes of various sorts have been reported in the

upper limb (Harris and Wagnon, 1987; Chiu and Wright, 1996; Vicenzino et al., 1998),

lower limb (Karason and Drysdale, 2003) and

paraspinal region (Roy et al., 2008).

Cervical mobilization has been associated with no (Chiu and Wright, 1996) or small (Vicenzino et al., 1998) decreases in skin temperature and blood flux (Vicenzino et al., 1998). Interestingly, Harris and Wagnon (1987) reported increases in hand skin temperature using what was likely a higher velocity manipulation (vs. Chiu and Wright’s and Vicenzino’s mobilization) of the cervical spine. Karason and Drysdale (2003) showed mixed results, with lumbar manipulation resulting in decreased blood flow in the dorsum of the foot in non-smoking subjects.

In earlier studies, effects of manipulation on skin temperature have been interpreted based on the assumption that an increase in skin temperature reflected vasodilation driven by decreased sympathetic output to dermal blood vessels. This assumption is now known to be overly simplistic (see Hodges and Johnson, 2009), so that skin temperature and skin blood flow measurements cannot be regarded as surrogates for direct measurement of autonomic output. Hence, while it may be said with some confidence that spinal manipulation can affect peripheral cutaneous blood flow in certain cohorts, the underlying mechanisms remain to be resolved and there is no obvious explanation for why different studies should report changes of the opposite polarity (see Harris and Wagnon, 1987 vs. Vicenzino et al., 1998).

One published study used single photon emission computed tomography to examine the effects of spinal manipulation on central nervous system blood flow (Cagnie et al., 2005). No raw data were presented, but the authors stated that in a cohort of 15 subjects it was possible to identify one region of the cerebellum where blood flow decreased when recorded 30 min after a cervical spinal manipulation. The physiological significance of this finding is not clear, and no correlation could be drawn with symptomatology in what was, after all, a healthy cohort. The authors suggest, however, that cerebellar hypoperfusion could be one source of subjective side effects following spinal manipulation (Cagnie et al., 2005).

      Studies of respiratory function

Table 2

In comparison to the number of studies of cardiovascular function, investigations of the effects of spinal manipulation on respiratory function are rather sparse; only three papers were found which satisfied the inclusion criteria (Table 2). McGuiness et al. referred to an increase in respiratory rate following a ‘grade III posteroanterior mobilization’ (McGuiness et al., 1997), although their paper did not report the actual pre- and post-treatment respiratory rates. A study of an apparently well cohort of adults demonstrated that a 2 week course of upper cervical manipulation was associated with statistically significant increases in forced vital capacity of approximately 6% and forced expiratory volume of approximately 5%, although this study also had no control cohort (Kessinger, 1997). A small study with only five subjects in the intervention group also referred to increases in FVC and FEV-1 with manipulation (Engel and Vemulpad, 2007), but did not report the data on which these results were apparently based. The existing literature therefore is essentially phenomenological and provides little meaningful data about the effects of spinal manipulation on respiratory function in humans (but see, for example, Koch et al., 1998).

      Studies of gastrointestinal function

Table 3

Notwithstanding the interest by practitioners in the effects of spinal manipulation on gastrointestinal function, basic physiological studies are all but absent (Table 3). One small study (13 trials in four subjects) reported that gastric tone, as determined by electrogastrogram wave amplitude, increased in response to upper cervical manipulation (6 trials) and in comparison to trials in which subjects (7 trials) did not receive spinal manipulation (Wiles, 1980). Raw data and the statistical methods for pre- vs. postSMT comparisons were not described in detail.

      Studies of female reproductive function

Table 4

Our systematic searches of PubMed and the Index to Chiropractic Literature revealed only one study of spinal manipulation in humans with implications for female reproductive function (Table 4). Nogueira de Almeida et al. (2010) examined the effects of sacral manipulation on intravaginal and basal perineal tonus. In this uncontrolled, single cohort trial, manipulation was associated with increased phasic perineal contraction amplitude.

      Human studies of somato-autonomic reflexes

Table 5

Somato-autonomic reflexes are often invoked as the mechanisms underlying somato-visceral phenomena associated with spinal manipulative therapy. Therefore, to do justice to the topic of spino-visceral phenomena, it is also appropriate to review studies of changes in autonomic function, and changes in organ or tissue function which are reflective of autonomic activity but which do not yet have any clear clinical implications. Five papers which satisfied the inclusion criteria were identified (Table 5).

Examples of autonomically-mediated responses to spinal manipulation include:

sweating, which has been measured indirectly by skin conductance (see for example, Moulson and Watson, 2006; Jowsey and Perry, 2010),

static pupil diameter (Briggs and Boone, 1988) and

edge light pupil cycle time (Gibbons et al., 2000).

The studies of skin conductance suggest that a sympathoexcitatory effect can be induced in the lower limbs with lumbar spinal manipulation (Perry et al., 2011), and perhaps in the hands following mobilization of the thoracic region (Jowsey and Perry, 2010). The study by Perry et al. (2011) compared two interventions, a ‘high-velocity low amplitude grade V manipulation’ of the lumbar spine, and a set of lumbar extension exercises (25 subjects per cohort). Both interventions produced a transient and statistically significant increase in skin conductance, with the response to manipulation being significantly larger than the response to exercise. The study by Jowsey and Perry (2010) compared the effects of a ‘grade III postero-anterior rotator joint mobilization technique applied to the T4 vertebra’ with the effects of sustained pressure to the same region (18 subjects per cohort). The sustained pressure resulted in no changes in hand skin conductance whereas the mobilization was accompanied by a slight increase in skin conductance in one hand (p = 0.034 per one way ANOVA) but not the other; these calculations based on percentage change from baseline.

Studies of the effects of spinal manipulation on the regulation of pupil diameter report mixed results. Upper cervical manipulation produced either increases or decreases in static pupil diameter in individuals within a cohort of eight subjects who received spinal manipulation, but no statistically significant change for the cohort as a whole, a control cohort of seven subjects who did not receive spinal manipulation also showed no change in pupillary diameter over the 4-day course of the study. (Briggs and Boone, 1988). On the other hand, in an uncontrolled study of a cohort of 13 young men, upper cervical manipulation was also associated with a decrease in edge light pupil cycle time (p = 0.002 per paired t-test); i.e. the time it takes for the pupil to constrict and dilate following a brief exposure to light. Thus, the manipulative procedure appeared to accelerate the reflex response of the pupil, but it was not possible to resolve specific effects on the parasympathetic vs. sympathetic contributions to the reflex (Gibbons et al., 2000). While these are intriguing human studies involving direct measures of autonomically mediated responses to spinal manipulation, they provide little physiological insight into the therapeutic impact of spinal manipulation on visceral conditions.

      Somato-humoural studies

Table 6

The discussion so far has focused on studies of responses which are most often presumed to be mediated by the autonomic nervous system. However, responses to spinal manipulation may also be mediated by other mechanisms, and a few studies have specifically examined humoural and cellular mechanisms. Seven articles were identified which measured such responses to spinal manipulation in healthy cohorts (Table 6).

A controlled trial demonstrated that in a cohort (n = 27) of healthy young males cervical manipulation was associated with a statistically significant increase in plasma levels of the endogenous analgesic beta-endorphin at 5 min post-treatment when measured by radioimmune assay (Vernon et al., 1986). On the other hand, a study of the effects of lumbar manipulation with a cohort of asymptomatic subjects (n = 20) found no changes in beta-endorphin levels at 5 and 30 min following treatment, nor changes in serum cortisol (Christian et al., 1988). Whelan et al. (2002) also reported no changes in salivary cortisol levels attributable to cervical manipulation.

Early controlled studies also report that thoracic spinal manipulation was associated with increased immune function, as measured by zymosan-stimulated chemiluminescence, in neutrophils and monocytes, and increased production of substance P and tumor necrosis factor (TNF-a) at 15 min post treatment (Brennan et al., 1991, 1992). On the other hand, a later and larger (n = 64) controlled study using different methods of assay and a longer time frame (up to 2 h) found that in healthy adults thoracic manipulation was associated with a decrease in synthesis of TNF-a and interleukin (IL-1b), and no change in levels of substance P (Teodorczyk-Injeyan et al., 2006). The latter authors suggested that such down regulation of inflammatory cytokines as they observed was likely not mediated by substance P, but might have been the result of activation of the parasympathetic nervous system. Using a comparable design, they also demonstrated increased synthesis of immunoglobulin G and immunoglobulin M at 20 min and 2 h, respectively, following thoracic manipulation (Teodorczyk-Injeyan et al., 2010). Collectively, these results do not paint a cohesive picture of the effects of spinal manipulation on the complex interactions within the immune system. Nonetheless, they do demonstrate the phenomenon of immunological response to manual therapy in the cohorts described.



Conclusions

Notwithstanding substantial interest by manual medicine practitioners in somato-visceral disorders, there are relatively few basic physiological studies in humans to guide clinical practice. The corpus of somato-visceral studies is characterized by small cohorts of subjects, uncontrolled trials and one time pilot exercises with no subsequent follow-up. The field has been slow to adopt new technologies. Only recently have teams of researchers appeared with the sustained interest, expertise and resources to pursue meaningful programmes of research. The greatest number of physiological studies has focused on cardiovascular function, with few investigations of other organ systems. There is a justifiable interest in autonomically-mediated phenomena. However, somato-humoural and non-autonomic neural mechanisms of spino-visceral interactions remain largely unexplored.


Acknowledgements

P.S. Bolton’s research is supported by Grants from the National Health and Medical Research Council of Australia and the Australian Spinal Research Foundation.




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