FASCIA SCIENCE AND CLINANIMAL STUDY

Visceral massain a rat model

Susan L. Chapelle, RM

8-411, Dep

eived

KEYWORDSIntestinal intestinal motility, called postoperative ileus. Postoperative ileus extends hospital stays,

manipulation designed to emulate running of the bowel. Transabdominal massage was per-formed upon 10 operated and 10 control rats in the first 12 h following surgery. Ileus was as-

tions.

2012 Elsevier Ltd. All rights reserved.

* Corresponding author. Tel.: 1 207 602 2921, 1 207 294 7317, 1 207 590 8949; fax: 1 207 602 5931.E-mail address: gbove@une.edu (G.M. Bove).

1360-8592/$ - see front matter 2012 Elsevier Ltd. All rights reserved.doi:10.1016/j.jbmt.2012.05.004

Available online at www.sciencedirect.com

Journal of Bodywork & Movement Therapies (2013) 17, 83e88

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SCIENCEANDCLINICALAPPLICATIONSePOST-SURGICALVISCERALMASSAGE:ANIMALSTUDYResults: The surgery consistently caused ileus. Compared to the operated group with no treat-ment, the operated with treatment group showed increased gastrointestinal transit andreduced time to first fecal pellet discharge. Similar group comparisons revealed that the treat-ment decreased total intraperitoneal protein and numbers of intraperitoneal inflammatorycells.Conclusions: In this rat model, visceral massage reduced experimental postoperative ileus.The data suggest that the effect was through the attenuation of inflammation. A similar studycould be designed and performed in a hospital setting to assess the potential role of visceralmassage as part of the integrated care for postoperative ileus.sayed after 24 h using fecal pellet discharge and gastrointestinal transit. Intraperitonealinflammation was assayed using total intraperitoneal protein and inflammatory cell concentra-obstruction;Infertility;Postoperativecomplications

increases the costs of hospitalization, and may contribute to the formation of postoperativeadhesions. We designed experiments to determine if visceral massage affects postoperativeileus in a rat model.Material and methods: Forty female Long Evans rats were assigned to 4 groups in a 2(surgery) 2 (treatment) factorial design. Twenty rats were subjected to a small intestinala Squamish Therapeutics, 10bUniversity of New England

Received 9 March 2012; recICAL APPLICATIONS e POST-SURGICAL VISCERAL MASSAGE:

ge reduces postoperative ileus

T a, Geoffrey M. Bove, DC, PhD b,*

05 Tantalus Rd., Squamish, BC, Canadaartment of Biomedical Sciences, 11 Hills Beach Rd., Biddeford, ME 04005, USA

in revised form 2 May 2012; accepted 23 May 2012

Summary Objective: Abdominal surgery invariably causes a temporary reduction of normaljournal homepage: www.elsevier .com/jbmt

84 S.L. Chapelle, G.M. Bove

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SCIENCEANDCLINICALAPPLICATIONSePOST-SURGICALVISCERALMASSAGE:ANIMALSTUDY Introduction

Abdominal surgery invariably causes a temporary reductionof intestinal motility, called ileus. Ileus is characterized bya lack of coordinated intestinal activity and a substantialoverall reduction in peristalsis, and is an important cause ofpostoperative discomfort and prolonged hospital stays(Bauer, 2010; Mattei and Rombeau, 2006; Person andWexner, 2006). The increased number of days spent in thehospital places a huge financial burden on health caredelivery systems (estimated to be $0.75 billion per year inthe United States for colectomies alone) (Doorly andSenagore, 2012; Iyer et al., 2009; Johnson and Walsh,2009; Senagore, 2010). There remains no fully effectivetreatment for ileus (Bauer, 2010; Engel et al., 2010; Matteiand Rombeau, 2006; Zeinali et al., 2009), although recentadvances have been made by combining ileus-limitingapproaches such as laparoscopic surgery, epidural anes-thesia, pain management, and new drugs (Johnson andWalsh, 2009; Kraft, 2009; Person and Wexner, 2006).

The concept that visceral or abdominal massage andmobilization could attenuate ileus was first published morethan a century ago (Coe, 1899; Haberlin, 1899), but thetopic received little further consideration. More recently,abdominal massage using a mechanical device was shown toreduce ileus (Le Blanc-Louvry et al., 2002). A systematicrecords review supported that osteopathic manipulativetreatment reduced ileus (Crow and Gorodinsky, 2009),however, there were few details related to the treatmentmethods, and it cannot be gleaned whether the abdomenwas directly treated. Other supportive data include thatvisceral massage is effective for constipation (Ernst, 1999;Klauser et al., 1992; Lamas et al., 2009), and that itincreases bowel function in spinal cord injured patients(Ayas et al., 2006; Liu et al., 2005).

We recently described the effects of visceral massage onpostoperative adhesions in a rat model (Bove and Chapelle,2012). During these experiments, we observed that therats, who were fully accommodated to handling, consis-tently defecated during or soon after visceral massage,suggesting a prokinetic effect on the intestines. Wedesigned the current study to determine if visceral massagewould decrease ileus in a rodent model of postoperativeileus. Because inflammation has been shown to be the keyto postoperative ileus (Bauer, 2010; Mattei and Rombeau,2006; Tracey, 2002; Wehner et al., 2007), we also per-formed assays of intraperitoneal inflammation to deter-mine possible associations with visceral massage.

Materials and methods

Animals and surgery

All procedures were consistent with the Guide for the Careand Use of Laboratory Animals (National Research Council,USA), and were approved by the University of New EnglandInstitutional Animal Care and Use Committee. Forty adult,female Long Evans rats were obtained from Charles RiverLaboratories (USA), and weighed 225 g when used. Rats inthe surgery group were anesthetized with isoflurane in pureoxygen (4% for induction, 2% for maintenance), and theirabdominal walls were shaved and scrubbed with betadineand 70% isopropanol. The surgical field was draped andsurrounded with sterile saline-soaked gauze. A 3 cmvertical incision was made just lateral to the linea alba. Thesmall intestine from the distal duodenum to the distal ileumwas gently exteriorized using gloved fingers. Starting withthe distal duodenum and moving distally, the entire smallintestine was gently rolled between the thumbs and fore-fingers, enough to compress and move the luminalcontents, but not enough to fully occlude the lumen orcause bleeding. This process took 5 min. The small intestinewas then covered with saline-soaked gauze, left for 10 min,and then returned to the abdominal cavity. The incision wassutured in layers (4-0 Monoweb; Webster Veterinary, USA).The rats were injected subcutaneously with morphinesulphate (0.3 mg/kg s.c.), and wrapped in a soft pad forrecovery. To control for the effects of the morphine, all ratsnot subjected to surgery were also injected with morphinesulphate (0.3 mg/kg s.c.) at the onset of the experiment.The rats not subjected to the surgery were not anes-thetized, because inhaled anesthetic agents do not inter-fere with gastrointestinal function after their cessation(Condon et al., 1987).

Experimental design

Ten rats were randomly assigned to each of 4 experimentalgroups in a 2 2 design: Surgery/Treatment (ST), Surgery/No Treatment (SNT), No Surgery/Treatment (NST), and NoSurgery/No Treatment (NSNT). The start of the experimentwas defined as the time when the rats were injected withmorphine. Rats were placed in separate enclosures for theduration of the experiment to facilitate fecal pellet counts,with free access to food and water. The endpoint for all ratswas 24 h after the start of the experiment.

Treatment

Rats in the treated groups (ST and NST) were removed fromthe cage and turned supine. One massage therapist (SLC)performed all the treatments, which standardized theprocedures. SLC is a Registered Massage Therapist trainedin Canada, with 18 years experience, who has focused muchof her practice on postoperative care. The massage treat-ments consisted of gentle mobilization for 1 min. Treat-ments started with a side to side motion using the indexfinger and thumb placed lateral to the descending andascending colon, respectively, for approximately 15 s. Aftermobilization, treatment continued by massaging in smallcircles with the index finger over the ascending, transverse,and finishing with the descending colon in a clockwisepattern, starting from the bottom right abdominal quadrantto the bottom left abdominal quadrant, for approximately45 s. These maneuvers were intended to mobilize the smalland large intestines and encourage metabolite exchangewithin the intraperitoneal fluid. Treatments were per-formed at 15-min intervals for the first hour (4 treatments),at 30-min intervals for the next 2 h (4 treatments) andevery 2 h thereafter until 12 h postoperatively (4 treat-ments). Rats in the non-treated groups (SNT and NSNT)were picked up and handled for approximately 1 min to

control for possible non-specific effects of the treatment,on the same schedule that the rats in the other groups weretreated.

Outcome measurements

Outcome measurements included time to first fecal pelletdischarge; fecal pellet counts at 6, 12, and 24 h; gastroin-testinal transit time; intraperitoneal fluid total proteinconcentration; and numbers of intraperitoneal inflammatorycells. After counting fecal pellets at 24 h, rats were lightlyanesthetized and gavaged with w1 ml of a slurry of 10%charcoal and 1% arabic acid in water, to measure gastroin-testinal transit time. After 30 min, rats were anesthetizedwith isoflurane, followed by replacement of the gases withpure CO2 to cause death. A small incision was made in theproximal abdominal wall, and 2 ml sterile phosphate buff-ered saline was injected into the peritoneal cavity. The

by Tukeys HSD post-hoc tests when appropriate. Time tofirst fecal pellet discharge was measured in minutes andreported in hours. Fecal pellet discharge during the first15 min following anesthesia removal, or induced by themorphine injection procedure, was disregarded. If therewas no discharge after 12 h, it was recorded as 12 h (nZ 5).Alpha levels were set to 0.05.

Results

Although all rats in the treatment and non-treatmentgroups were initially given a low dose of morphine tosimulate postoperative ileus scenarios, no further drug orrestraint was necessary. None of the rats struggled, vocal-ized, or bit during any treatment, consistent with ourprevious experiences (Bove and Chapelle, 2012). Thetherapist reported that the abdomens of the rats that hadundergone surgery had a deeper resistance to movement

. Ventroutioarg

Visceral massage for postoperative ileus 85

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SCIENCEANDCLINICALAPPLICATIONSePOST-SURGICALVISCERALMASSAGE:ANIMALSTUDYabdominal contents were gently mobilized for 10 s, and theincision widened. Lavage fluid was collected with a gavageneedle, and placed in vacutainers coated with EDTA. Thesmall intestine was removed en bloc from the pylorus to theileocecal valve, and carefully placed along a tape measure.The length from the pylorus to the ileocecal valve wasmeasured and recorded. The distance from pylorus to themost distal visible charcoal was also measured, and used tocalculate the gastrointestinal transit over 30 min (expressedas percentage of total small intestine length). The collectedlavage fluid was then centrifuged, and the supernatantaspirated and used to assay total protein using a BCA proteinassay (Pierce-Thermo Scientific, USA). The pellet containingcells was washed and suspended in phosphate bufferedsaline, and the numbers of cells were quantified usinga standard hemocytometer. Trypan blue was added todifferentiate live from dead cells.

Data analysis

All data other than cumulative fecal pellet discharge wereanalyzed using 2 (surgery) 2 (visceral massage) ANOVAs(JMP 8.0 for Macintosh; USA). Cumulative fecal pelletdischarge data were analyzed using a multivariate ANOVA(surgery, visceral massage, time). Analyses were followed

Figure 1 Effect of visceral massage on postoperative ileus. ANST Z no surgery, treatment; NSNT Z no surgery, no treatmCumulative fecal pellet discharge was greater in the massaged grats (NORM), is depicted to demonstrate the probable contribumassage significantly reduced the time to first fecal pellet disch(see text for details). Data are presented as means SEM.than the unoperated rats.

Ileus model

Surgery significantly reduced gastrointestinal transit [maineffect of surgery; F (1, 33)Z 12.31, p < 0.001; Figure 1A],and reduced fecal pellet discharge [main effect of surgery;F (1, 34)Z 5.36; p < 0.05; Figure 1B]. There was no effectof surgery on the time to first fecal pellet discharge [F (1,33)Z 0.11; p > 0.10]. These data support that the surgicalprocedure consistently induced ileus. To determine if ileusremained after 24 h, the fecal pellet discharge of anothergroup of 10 normal rats was observed (these data were notincluded in the statistical analysis). The comparison sup-ported the presence of residual ileus after 24 h in all 4experimental groups (Figure 1B). This was likely to havebeen caused by the morphine.

Effect of treatment on gastrointestinal function

There was a main effect of visceral massage on gastroin-testinal transit [F (1, 33) Z 12.56, p < 0.001, Figure 1A].Post-hoc tests supported that visceral massage led tosignificant increases in small intestine transit in thesurgery and treatment (ST) group compared to the surgery

isceral massage significantly increased gastrointestinal transit.; ST Z surgery, treatment; SNT Z surgery, no treatment. B.ps (ST and NST). Fecal pellet discharge for a group of 10 normaln of morphine to ileus in all experimental groups. C. Viscerale. All noted differences were statistically significant by ANOVA

with no treatment (SNT) group (Tukeys HSD, p < 0.05,Figure 1A). Although there was no main effect of treat-ment on cumulative fecal pellet discharge, there weresignificant interactions between time and surgery (MAN-OVA, p < 0.005, Figure 1B), time and treatment(p < 0.01), and time, surgery, and treatment (p < 0.05),indicating that over time there was increased dischargedue to the treatment. Treatment reduced time to firstfecal pellet discharge [main effect; F (1, 33) Z 11.36:p < 0.01; Figure 1C], which was also independent ofwhether surgery had been performed (there was nointeraction between treatment and surgery; F (1,33) Z 1.24; p > 0.10). These data support that visceralmassage significantly increased gastrointestinal function,and reduced postoperative ileus.

86 S.L. Chapelle, G.M. Bove

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SCIENCEANDCLINICALAPPLICATIONSePOST-SURGICALVISCERALMASSAGE:ANIMALSTUDYTable 1 Effect of abdominal massage on total intraperi-toneal protein concentration and leukocyte numbers.

Group Protein (mg/ml) Cells/ml

NSNT 3.55 (0.63) 917 (249)NST 5.78 (0.47) 5673 (2293)SNT 11.82 (1.13) 12,192 (3190)ST 9.47 (1.01) 3708 (736)

All data are presented as mean (SEM). NSNTZ No Surgery, NoTreatment; NST Z No Surgery, Treatment; SNT Z Surgery, NoTreatment; ST Z Surgery; Treatment. Protein concentrationand cells/ml data are graphically depicted in Figure 2. See textfor details on Statistical analysis.Effect of treatment on total intraperitoneal proteinand leukocyte concentrations

To test the possibility that visceral massage may reduceileus through a suppressing effect on inflammation, weperformed peritoneal lavage on all rats just followingdeath, and assayed the concentrations of total proteinand numbers of inflammatory cells (leukocytes). Therewas a main effect of surgery on total intraperitonealprotein [F (1, 36) Z 49.08; p < 0.001; Table 1 andFigure 2A]. There was no main effect of treatment [F (1,36) Z 0.01, p > 0.10] but there was a significant inter-action between the surgery and treatment [F (1,36) Z 7.19; p < 0.01]. This highlighted that the effect ofthe treatment differed depending on whether surgery hadbeen performed or not performed. Post-hoc tests were notsignificant. The surgical procedure caused a large increasein the number of inflammatory cells compared to normalanimals [main effect; F (1, 36) Z 5.40; p < 0.05; Table 1and Figure 2B]. Although there was no main effect of thetreatment [F (1, 36) Z 0.87; p > 0.10], there was aninteraction between the surgery and treatment [F (1,36) Z 10.93; p < 0.005)], supporting that that the effectof the treatment differed in the surgical versus non-surgical groups. Post-hoc tests supported that visceralmassage led to a significant reduction in the number ofintraperitoneal cells in the ST group compared to the SNTgroup (Tukeys HSD, p < 0.05).Discussion

Our results indicated that visceral massage attenuatedpostoperative ileus in this rat model. Massage significantlyincreased gastrointestinal transit, augmented cumulativefecal pellet discharge, and shortened the time to first fecalpellet discharge. The comparison to a normal group of ratssuggested that ileus was maintained for 24 h. Because ofthe chosen endpoint, it is not known whether the treatmentaffected the time to complete ileus resolution; this couldbe addressed in a future study.

We considered that the effects of massage on post-operative ileus could be simply mechanical; in other words,did the treatment simply push the intestinal contentsalong? This is very unlikely: directional propulsion of theintestinal contents requires peristaltic waves, which arehighly coordinated. Mechanical effects of massage wouldnot likely be unidirectional, especially in the small intes-tine, where the contents are more liquid than solid andwhere we measured effects. Furthermore, the improve-ment 12 h past the time of treatment cessation indicateda lasting stimulatory effect of massage on postoperativeileus, arguing against simple mechanical effects. However,the possibility that the massage triggered effective peri-staltic activity of the large intestine is supported by a casereport of a patient with spastic paralysis of the bowel,where self-administered abdominal massage evoked tran-sient rectal peristaltic waves (Liu et al., 2005).

Intraperitoneal inflammation is currently held to be keyto prolonged postoperative ileus (Bauer, 2010; Mattei andRombeau, 2006; Wehner et al., 2007). Increased para-sympathetic activity decreases intraperitoneal inflamma-tion by inhibitory actions that have been collectively calledthe inflammatory reflex (for reviews, see Tracey, 2002,2007, and Van Der Zanden et al., 2009), and has been shownto ameliorate postoperative ileus (de Jonge et al., 2005;The et al., 2007). We show that intraperitoneal proteinconcentration and inflammatory cell numbers werereduced by visceral massage, indicating a dilution of theinflammatory milieu. Although the mechanisms of visceralmassages effects on intraperitoneal inflammation areunknown, it is proposed that the reduction we observedwas reflex-mediated, through the vagus nerve. Inflamma-tion sensitizes sensory receptors and axons to mechanicalstimuli (Beyak and Vanner, 2005; Bove et al., 2003; Hableret al., 1988; Koda and Mizumura, 2002), but ileus reducesmechanical stimuli to the gut sensory system. It is likelythat the mechanical stimuli of the massage increasedafferent input in this sensitized system. Reflexively,increased afferent drive in this pathway will result inincreased parasympathetic activity to the affected area(reviewed by Tracey, 2002). Interestingly, both totalprotein and leukocyte numbers increased in rats not sub-jected to surgery, suggesting that under normal conditions,the treatment is somewhat proinflammatory. This isconsistent with the fact that in the absence of pathology,intraperitoneal receptors are relatively insensitive, andthus would not be expected to initiate a substantialreflexive response from the parasympathetic system. Afuture study could be designed to investigate the role ofvagal reflexes in the effects of massage on ileus.

2006. The effect of abdominal massage on bowel function in

prevent peritoneal adhesions in a rat model. J. Bodywork Move.

amleu(see

Visceral massage for postoperative ileus 87

NICALAPPLICATIONSePOST-SURGICALVISCERALMASSAGE:ANIMALSTUDYIt has also been proposed that postoperative adhesions,a side effect of most abdominal surgery (Parker et al.,2007; Stanciu and Menzies, 2007), are fostered by ileus(Fu et al., 2005; Springall and Spitz, 1989). We havepreviously shown in a rat model that a visceral massageimmediately following surgery interfered with the forma-tion of postoperative adhesions (Bove and Chapelle, 2012).It follows that a reduction in postoperative ileus may limitadhesion formation by promoting normal peristaltic move-ments, although these beneficial effects could also be dueto passive motion of the intestines while normal peristalticmotions recover.

Assumptions could be made that in humans, post-operative abdominal pain and sensitivity will preclude suchtreatment; this assumption was also made regardingtreating the rats prior to performing these experiments.Our therapists experience with humans, and now with rats,support that visceral massage is welcomed. It has also beensuggested that such mechanical stimulation could disruptintestinal surgical repairs. This notion has no experimentalsupport, but our preliminary observations with an experi-mental endeend colonic anastomosis in rat support thatvigorous visceral massage does not disrupt even very deli-cate sutures. This should be addressed in a future study.With appropriate precautions, including clear communica-tion with the physician regarding the procedures per-formed, care to prevent infections, and maintainingconstant feedback from the conscious patient, gentlemobilization of the abdominal cavity immediately post-operatively should be safe.

The methods used in this study were scaled e down

Figure 2 Effect of visceral massage on intraperitoneal inflintraperitoneal protein (A) and the number of intraperitonealmeasures. Both effects were statistically significant by ANOVAversions of methods currently in routine use with humans,based on our therapists best estimation and broad expe-rience. Visceral massage, for constipation (Ernst, 1999;Lamas et al., 2010) and other complaints, is a standardpart of massage therapy education in North America(Kellogg, 1895; Salvo, 2009), and massage therapy isavailable at a growing number of integrated medicalhealth care facilities. The primary outcome measurementsof ileus in humans are non-invasive (increased bowelsounds, passing flatus) and are already monitored. There istherefore no reason why a prospective study similar to thisstudy cannot be performed in a hospital setting to deter-mine if postoperative visceral massage could complementexisting treatments for ileus. It is hoped that this reportwill catalyze such a study, which has the potential toTher., 76e82.Bove, G.M., Ransil, B.J., Lin, H.C., Leem, J.G., 2003. Inflammation

induces ectopic mechanical sensitivity in axons of nociceptorsinnervating deep tissues. J. Neurophysiol. 90, 1949e1955.patients with spinal cord injury. Am. J. Phys. Med. Rehabil. 85,951e955.

Bauer, A.J., 2010. Two immune arms to stop one gut. Nat. Med. 16,1378e1379.

Beyak, M.J., Vanner, S., 2005. Inflammation-induced hyperexcit-ability of nociceptive gastrointestinal DRG neurones: the role ofvoltage-gated ion channels. Neurogastroenterol. Motil. 17,175e186.

Bove, G.M., Chapelle, S.L., 2012. Visceral mobilization can lyse andreduce hospital stays, improve overall outcomes forabdominal and pelvic surgical patients, and reducehospitalization costs.

Acknowledgments

Disclosures: Financial assistance for this project wasprovided in part through a seed grant from the MassageTherapy Association of British Columbia to GMB and SLC.The authors acknowledge the generous assistance ofDr. Michael Burman, Dr. Ling Cao, and Ms. Jennifer Malon.

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Visceral massage reduces postoperative ileus in a rat model1. Introduction2. Materials and methods2.1. Animals and surgery2.2. Experimental design2.3. Treatment2.4. Outcome measurements2.5. Data analysis

3. Results3.1. Ileus model3.2. Effect of treatment on gastrointestinal function3.3. Effect of treatment on total intraperitoneal protein and leukocyte concentrations

4. DiscussionAcknowledgmentsReferences