Furgała, Agata

Gościński, Igor

Kolasińska-Kloch, Władysława

Mądroszkiewicz, Dorota

Mądroszkiewicz, Ewa

Thor, Piotr

Medical Science Monitor

English

Jagiellonian Univeristy Repository

WWW.MEDSCI MONIT.COMClinical ResearchSignature: Med Sci Monit, 2003; 9(9): CR392-395PMID: 12960928CR392Gastric myoelectric activity in patients with closedhead brain injuryPiotr J. Thor1adefg, Igor Gościński2adefg, Władysława Kolasińska-Kloch3defg,Dorota Mądroszkiewicz4bcdef, Ewa Mądroszkiewicz2bcdef, Agata Furgała1bcdef1 Department of Pathophysiology, Collegium Medicum, Jagiellonian University, Cracow, Poland2 Department of Neurotraumatology, Collegium Medicum, Jagiellonian University, Cracow, Poland3 2nd Clinic of Cardiology the Institute of Cardiology, Collegium Medicum, Jagiellonian University, Cracow, Poland4 Department of Gastroenterology, Collegium Medicum, Jagiellonian University, Cracow, PolandSource of support: This study was supported by grant no. 501/P/79/L from the State Committee for ScientificResearch (KBN), Warsaw, Poland.SummaryBackground: Traumatic brain injury (TBI) constitutes a major public health problem. Most of the acute dis-turbances of autonomic nervous system activity seen in clinical practice resulting from headinjury are due to increased intracranial pressure (ICP), which precipitates a complex set ofchanges causing lack of food tolerance. The aim of our study was to evaluate the effects ofTBI on gastric myoelectric activity in coma patients.Material/Methods: 24 patients (23 male, 1 female; mean age 43.6±7 yr.) hospitalized for TBI in the Departmentof Neurotraumatology were included in the study. Gastric myoelectric activity was recordedusing the Synectics system (Sweden) on the 1st and 2nd day after injury. The control groupconsisted of healthy volunteers matched for age and gender.Results: In the control group, electrogastrography (EGG) showed the percentage of time with brady-gastria, normogastria and tachygastria to be 9.7±6.4, 88.3±7.6 and 2.0±3.5 respectively. Theamplitude of the signal was 181±11.5 [µV2]. In TBI patients, the percentage of time withbradygastria and tachygastria increased to 46.5±21.8 (p=0.03) and 5.5±11.8 (p=0.001)respectively, while the duration of normogastria decreased to 47.2±20.4 (p=0.001). Highlysignificant changes were observed in signal amplitude, which increased to 766±550 [µV2](p=0.0007). There was positive correlation between GCS and normogastria (r=0.66,p<0.001) and negative correlation between GCS and bradygastria (r=–0.77, p<0.001).Conclusions: In patients with brain trauma and coma, the functional brain-gut link is altered, causing gas-tric dysrrhythmias and intolerance to feeding. Prokinetics during enteral feeding are recom-mended.key words: traumatic brain injury • increased intracranial pressure • gastric myoelectric activityFull-text PDF: http://www.MedSciMonit.com/pub/vol_9/no_9/3180.pdfWord count: 1424Tables: 1Figures: 4References: 20Received: 2002.10.03Accepted: 2003.07.14Published: 2003.09.08Author’s address: Professor Piotr J. Thor, Department of Pathophysiology, Medical College, Jagiellonian University,ul. Czysta 18, 31-121 Cracow, Poland, email: mfthor@cyf-kr.edu.plAuthors’ Contribution:A Study DesignB Data CollectionC Statistical AnalysisD Data InterpretationE Manuscript PreparationF Literature SearchG Funds CollectionCR393Med Sci Monit, 2003; 9(9): CR392-395 Thor JP et al – Electrogastrography in closed head brain injuryCRBACKGROUNDGastric motility and emptying is governed not only byperipheral myogenic activity (pacesetter activity), butalso remains under the control of autonomic innervationlocated centrally in the autonomic brain centers.Traumatic brain injuries (TBIs) vary considerably intheir etiology, pathophysiology and clinical presentation.For classification purposes, TBIs are usually divided intofocal and diffuse. Focal brain injuries include contusions,brain lacerations, and hemorrhage leading to the forma-tion of hematoma in the extradural subarachnoid, sub-dural or intracerebral compartments [1]. Diffuse braininjuries involve cerebral contusion, edema, diffuse axon-al injury, and prolonged posttraumatic coma. Trauma ofthe brain involves neural or vascular elements, whichresults in axonal damage of the Ranvier nodes, ischemia,cerebral edema and increased intracranial pressure(ICP) [2,3]. However, the effects of TBI on gastric motili-ty and the lack of food tolerance is described in the liter-ature in conflicting terms. For example, Livingston [4]found that increased ICP stimulated gastric contractility,but the opposite effect was observed by Garrick [5].It is well known that gastric myoelectrical activity is high-ly correlated with gastric motility [6,7]. The non-invasiverecording of gastric myoelectric activity using skin elec-trodes has become lately a very popular research andclinical tool in humans. The summary of recorded gas-tric myoelectrical activity is called an electrogastrogram(EGG). The frequency of gastric contractions is con-trolled by the gastric slow wave, and the amplitude ofgastric contractions is associated with higher cholinergicdrive [7]. Central damage to the autonomic system cau-sed by TBI, resulting in autonomic dysfunction, shouldbe expected to affect gastric myoelectric activity.The aim of our study was to evaluate the effects of trau-matic brain injury on gastric myoelectric activity incomatose patients.MATERIAL AND METHODSWe studied 24 patients, 23 male and 1 female (meanage 43.6±7yrs), in coma after a closed head injury, onthe first or second day after trauma. Six of them haddiffuse brain damage, six had extradural and six sub-dural hematoma, and six patients had intracerebralhematoma. Their clinical status on the Glasgow ComaScale (GCS) was between 4 and 7 points. Fasted antralmyoelectric activity was captured in all patients withstandard cutaneous electrodes (Synectics, Sweden) andthe data stored on the hard disc of a computer. The col-lected data were analyzed and presented graphically(software from Synectics Medical AB, Stockholm,Sweden). The patterns of gastric myoelectric activitywere analyzed with regard to the percentage time ofbradygastria (frequency 0.5–2.0 cycles per minute,cpm), normogastria (2–4 cpm), and tachygastria (4–10cpm). The following parameters were also calculated:• PDF – Period Dominant Frequency, the dominant fre-quency (highest peak) of the mean or average FFT(Fast Fourier Transform) line;• PDP – Period Dominant Power, the power or ampli-tude of the PDF peak;• DFIC – Dominant Frequency Instability Coefficient,also based on the dominant frequencies of the FFTlines that make up a given period. The DFIC indicatesdominant frequency changes over the course of theperiod. It is computed by first calculating the meanand standard deviation of the individual dominantfrequencies for the period in question. The standarddeviation of the dominant frequencies is then dividedby the mean of the dominant frequencies to give theDFIC, which is reported as a percentage;• DPIC – Dominant Power Instability Coefficient, basedon the powers of the dominant frequencies over thegiven period. The DPIC is a measure of how muchthe power of the dominant frequency changes overthe course of the period.24 healthy volunteers without neurological symptomsmatched for age and gender served as a control group.Patients with obesity, hypertension, diabetes mellitus orvalvular heart disease were excluded from the study. Nosubjects had a prior history of gastrointestinal tract diseases.The research was performed between January 1999 andJanuary 2001 in the Neurotraumatology Clinic at theJagiellonian University College of Medicine. The pro-ject was approved by the Jagiellonian University’s ethi-cal review committee, and was performed in accordancewith the Helsinki Declaration.Statistical analysisFor statistical analysis we used Statistica software (Stat-soft, USA). Data are presented as mean values (SD) A Pvalue <0.05 was considered significant.RESULTSIn the control group, the percentage of recorded timewith bradygastria, normogastria and tachygastria was9.7±6.4%, 88.3±7.6% and 2.0±3.5% respectively. Thefasting amplitude of signal was 181±11.5 [µV2]. In theTBI patients, the percentage of time in bradygastria andtachygastria increased to 46.5±21.8% (p=0.03) and5.5±11.8% (p=0.001) respectively, at the cost of normo-gastria, which was reduced to 47.2±20.4% (p=0.001)(Figure 1). The amplitude of signal was higher in the TBIpatients (766±55 [µV2], p=0.0007) than in the controlgroup (Figure 2). Amplitude increased about 200% in thecontrol group after a meal, to 366±38.4 [µV2]. The PDF,PDP, DPIC, DFIC values are presented in Table 1.There was positive correlation between the GlasgowComa Scale score and normal frequency timing (Spear-man’s rank correlation r=0.66; p<0.001) (Figure 3),and negative correlation between bradygastria timingand GCS (r=–0.77; p<0.001) (Figure 4).DISCUSSIONIn the functional division of the stomach the proximaland distal parts are differentiated. The distal stomach isCR394Med Sci Monit, 2003; 9(9): CR392-395Clinical Researchgoverned by a basic electrical rhythm (slow waves) gen-erated by a gastric pacesetter localized 2/3 of the wayalong the gastric curvature. The proximal part isresponsible for the active reception of the meal and pro-duces tonic contractions responsible for liquid gastricemptying. The distal part, by its peristaltic activity dri-ven by the pacesetter-dependent rhythm (2–4 cycle permin, cpm), is responsible for gastric emptying of solids.Both parts are under well-balanced stimulatory/inhibitory control from the autonomic central nervoussystem (ACNS). Gastric myoelectric activity reflects gas-tric motility, recorded by measuring gastric slow wavefrequency and the amplitude of the EGG signal [6].From the theoretical point of view, gastric motility andemptying disturbances in TBI patients may be causedby the head injury itself (axon damage in the ACNS) ortransmitted peripherally by nerves to the viscera or/andchemical mediators, which are released locally fromnerve terminals in these patients [3,8,9]. Studies on ani-mals have recently demonstrated that releases of excita-tory amino acids play a major role in neuronal damageafter brain injury and ischemia [10]. Trauma victimsdemonstrate severely decreased bowel sound, gastro-paresis, and lack of cardiac response to tracheal stimula-tion and high gastric retention. These symptoms ofperipheral autonomic dysfunction related to lesions ofthe dorsal vagus nucleus suggest vagal dysfunction [11].Garrick found that peripheral cholinergic stimulationwith betanechol reversed the inhibition of gastric andduodenal motility in response to increased ICP only fora short period of time. These short-lasting effects ofbetanechol confirmed mainly failure of the cholinergicsystem [5]. Kacker also claimed that intracranial hyper-tension is responsible for suppression of vagal activity0102030405060708090%PatientsControl0.5–2cpm 2–4cpm 4–10cpmp=0.03p=0.001p=0.001Figure 1. EGG changes in frequency timing in TBI patients and controls.0100200300400500600700800µV2AmplitudePatients Controlp=0.0007Figure 2. Signal amplitude recorded in TBI patients and controls.0.020.040.060.080.0100.0120.00 1 2 3 4 5 6 7 8Glasgow Coma Scale (in points)Slowe waves frequency 0.5–2 cpmSpearman's rank correlation r=–0.7Figure 3. Correlation between Glasgow Coma Scale score and percent-age of time recording slow wave frequency of 0.5–2 cpm.Figure 4. Correlation between Glasgow Coma Scale score and percent-age of time recording slow waves frequency of 2–4 cpm.PDFPDP (µV2)DPIC (%)DFIC (%)2.7±0.8403±23034.2±1865±332.07±1.291711±42061±35120±530.020.0020.00230.0006Parameters Controls Patients p*Table 1. EGG parameters in TBI patients and controls.Level of statistical significance: p<0.050.010.020.030.040.050.060.070.080.090.00 2 4 6 8Glasgow Coma Scale (in points)Slow waves frequency 2–4 cpmSpearman's rank correlation r=0.66CR395Med Sci Monit, 2003; 9(9): CR392-395 Thor JP et al – Electrogastrography in closed head brain injuryand inhibition of gastric emptying [12]. We found thatgastric dysrrhythmias are related to GCS: a low GCSscore is associated with a higher percentage of dysr-rhythmias and vice versa, a higher GCS score correlateswith normal frequency timing. This is important,because both types of dysrrhythmias of the gastric pace-setter cause delay in gastric emptying. The autonomicdysfunction induced by trauma could be the main rea-son for the observed gastroparesis [13]. Wood et al. alsoobserved prolongation of gastric emptying for bothphases of meal and antral hypomotility, with activityfronts appearing simultaneously in the proximal smallintestine [14]. In our data the increase in dysrrhythmiatime was associated with an increase in the amplitude ofthe slow waves, indicating stronger antral contractileactivity, which contradicts Wood’s observations in TBIpatients. The underlying mechanisms of this observa-tion are unclear [15,16]. Van Miert and De La Parrasuggest that released endotoxins and liposaccharidesafter trauma are strong inhibitors of gastric emptying inrats [17]. It has been found that in patients with headinjury the levels of interleukin-1 in the cerebrospinalfluid (CSF) are significantly elevated when compared tothe level in lumbar CSF from patients undergoing rou-tine myelograms [18]. Studies done by Tache [19] sug-gest that intracisternal corticotropin–releasing factorprobably acts centrally to delay gastric emptyingthrough brain sites that have not yet been determined.Other investigators have found a feedback loop betweencytokines and CRF levels [17,20]. The issue of the mech-anisms of the gastric motility changes in TBI patientsremains open. It is probably the result of both directneuronal damage and functional changes resulting fromthe release of inflammatory mediators, which in concertdelay food transit in the gastrointestinal tract. Thus theuse of prokinetics in these patients seems reasonable.CONCLUSIONSOur results provide evidence that in patients with braintrauma and coma, the functional brain-gut link isaltered, causing gastric dysrrhythmias and intoleranceto feeding. This suggests the use of prokinetics inunconscious patients on enteral feeding. The mecha-nisms of these disturbances remain unclear. Thehypotheses that they are the result of neuronal damageor of functional changes due to release of inflammatorymediators require further studies.REFERENCES:1. MacQueen BD: Imagining the brain. Med Sci Monit, 2001; 7(4):716-7242. Clifton GL, Robertson CS, Grossman RG et al: The metabolicresponse to severe head injury. J Neurosurg, 1984; 60: 687-6963. Valadka AB, Gopinath SP, Robertson CS: Midline shift after severehead injury; pathophysiologic implication. J Trauma 2000; 49 (1): 1-84. Livingstone EH, Passaro EP, Garrick T: Elevated intracranial pres-sure stimulates gastric contractility in the rat. J Surg Res, 1999;50(2): 106-1105. Garrick T, Mulvihill S, Buack M et al: Intracerebroventricular pres-sure inhibits gastric antral and duodenal contractility but not acidsecretion in conscious rabbits. Gastroenterology, 1988; 95: 26-316. Chen J, McCallum RW, Richards R: Frequency components of theelectrogastrogram and their correlations with gastrointestinal con-tractions in humans. Med Biol Eng Comput, 1993; 31: 60–677. Chen JD, Lin Z, Pan J, McCallum RW: Abnormal gastric myoelectri-cal activity and delayed gastric emptying in patients with symptomssuggestive of gastroparesis. Dig Dis Sci, 1996; 41(8): 1538-15458. Ott l, Young B, Ohillips R et al: Altered gastric emptying in thehead injured patient: relationship to feeding intolerance. JNeurosurg, 1991; 74: 738-7429. Armstead W: NOC/oFQ activates PKC and generates superoxide toimpair hypotensive cerebrovasodilation after hypoxia/ischemia.Med Sci Monit, 2002; 8(4): 31-3810. Bullock R, Zauner A, Woodward JJ et al: Factors affecting excitato-ry amino acid release following severe human head injury. JNeurosurg, 1998; 89(4): 507-51811. Haig AJ, Ho KC, Ludwig G: Clinical, physiologic, and pathologicevidence for vagus dysfunction in a case of traumatic brain injury. JTrauma Injury Inf Critical Care, 1996; 40(3): 441–44412. Kacker V, Mehta VS, Gupta YK: Acute intracranial hypertension-induced inhibition of gastric emptying: evaluation in conscious rats.Eur J Pharmacol, 1999; 369: 65-7213. Altmayer T, O’Dell MW, Jones M et al: Cisapride as a treatment forgastroparesis in traumatic brain injury. Arch. Physical Med Rehab,1996; 77(10): 1093-109414. McArthur CJ, Gin T, McLin IM et al: Gastric emptying after braininjury: effects of choice of sedation and intracranial pressure.Intensive Care Medicine, 1995; 21(7): 573-57615. Norton JA, Ott LG, McClain C et al: Intolerance to enteral feedingin brain-injured patients. J Neurosurg, 1988; 68: 62-6616. Wood JR, Camilleri M, Low PA, Malagelada JR: Brainstem tumorpresenting as an upper gut motility disorder. Gastroenterology,1985; 89: 1411-141417. Nompleggi D, Teo TC, Blackburn GL: Human recombinant inter-leukin-1 decreases gastric emptying in the rat. Gastroenterology,1988; 94: 326 (Abstract)18. Van Miert ASJ, De La Parra: Inhibition of gastric emptying byendotoxin in conscious rats and modification of this response bydrugs affecting the autonomic nervous system. Arch IntPharmacodyn Ther, 1970; 184: 27-3319. Tache Y, Maeda-Hagiwara M, Turkelson CM: Central nervous sys-tem action of corticotropin-releasing factor inhibits gastric empty-ing in rats. Am J Physiol, 1987; 253: 241-24520. Young AB, Ott LG, Beard D et al: The acute phase response of thebrain-injured patient. J Neurosurg, 1988; 69: 375-380CR

Gastric myoelectric activity in patients with closed head brain injury

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Gastric myoelectric activity in patients with closed head brain injury

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