Intensive Care Med (2006) 32:13921398DOI 10.1007/s00134-006-0252-0 PEDIATRIC ORIGINAL

Sina HeinrichHolger SchiffmannAlexander FrerichsAdelbert Klockgether-RadkeInz Frerichs

Body and head position effects on regionallung ventilation in infants: an electricalimpedance tomography study

Received: 17 June 2005Accepted: 24 May 2006Published online: 24 June 2006 Springer-Verlag 2006

This article is discussed in the editorialavailable at: http://dx.doi.org/10.1007/s00134-006-0253-z

Electronic supplementary materialThe electronic reference of this article ishttp://dx.doi.org/10.1007/s00134-006-0252-0. The online full-text version of thisarticle includes electronic supplementarymaterial. This material is available toauthorised users and can be accessed bymeans of the ESM button beneath theabstract or in the structured full-text article.To cite or link to this article you can use theabove reference.

I. Frerichs (!)University of Schleswig-Holstein,Department of Anaesthesiology andIntensive Care Medicine,Schwanenweg 21, 24105 Kiel, Germanye-mail: frerichs@anaesthesie.uni-kiel.deTel.: +49-431-5972998Fax: +49-431-5972230

S. Heinrich A. Frerichs A. Klockgether-Radke I. FrerichsUniversity of Gttingen, Centre forAnaesthesiology, Emergency and IntensiveCare Medicine,Gttingen, Germany

H. SchiffmannUniversity of Gttingen, Centre for Childand Adolescent Health,Gttingen, Germany

Abstract Objective: To determinethe effects of body and head positionson the spatial distribution of ventila-tion in nonintubated spontaneouslybreathing and mechanically ventilatedinfants using electrical impedancetomography (EIT). Design and set-ting: Prospective study in a neonatalintensive care unit. Patients: Tenspontaneously breathing (gestationalage 38 weeks, postnatal age 13 days)and ten mechanically ventilatedinfants (gestational age 35 weeks,postnatal age 58 days). Interven-tions: Supine and prone postureswith different head positions (mid-line and rotated to the left and rightside). Measurements and results:The distribution of ventilation in thechest cross-section was repeatedlydetermined from EIT data in eachbody/head position studied. Duringspontaneous breathing the tidal vol-umes in the left lung region were

reduced in the supine posture with thehead turned to the left as well as in theprone posture with the head rotated toeither side when compared with thesupine posture with the head in themidline position. During mechanicalventilation the tidal volumes in theleft lung region were unaffected bythe body and head position except forthe prone posture combined with theleftward head rotation which reducedthem. In both types of ventilationthe tidal volumes in the right lungregion were unaffected by the changein body/head position. Conclusion:The results indicate that the spatialdistribution of ventilation is influ-enced by the body and head positionin spontaneously breathing infants.Prone posture with the leftward headrotation has the most prominent ef-fect which is detectable even duringmechanical ventilation.

Keywords Intensive care, neonatal Critical care Electrical impedancetomography Electrical impedance Ventilation distribution Ventilationmonitoring

Introduction

Little is currently known about the regional characteristicsof lung ventilation in preterm and term neonates. Theeffects of anatomical and physiological factors on regionallung ventilation in this age group are difficult to study.

Computed or magnetic resonance tomography, whichis well established in studies on adult subjects, cannotbe used in small infants. Plain chest radiography canonly be used for diagnosis, and therefore radiographsare available only for infants suffering from lung diseaseor undergoing artificial ventilation therapy. Moreover,

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chest radiographic examinations are not able to assessthe functional aspects of regional lung ventilation. Theonly method available to indirectly study regional lungventilation in small infants free of lung disease is the inertgas washout technique [1, 2, 3]. This technique whichrequires the use of an endotracheal tube or a face maskcan detect inhomogeneities in lung ventilation but cannotexactly locate them. Consequently there are few studiesof unsedated spontaneously breathing infants with natural,unmodified respiratory mechanics.

In recent years electrical impedance tomography(EIT) has been identified as a possible new tool forstudying regional lung function in experimental andclinical studies [4, 5, 6, 7]. Its ability to determine regionallung volume changes has been validated [8, 9, 10, 11].EIT uses a radiation-free measuring principle and allowsexaminations to be performed during long periods oftime at scan rates up to about 40 scans per second.These characteristics make EIT attractive for monitoringapplications in a clinical setting, particularly in intensivecare patients [12, 13, 14].

We used EIT in a study of spontaneously breathingpreterm and term neonates shortly before their dischargefrom the neonatal intensive care unit (NICU) [15]. Westudied the effect of three different postures on the dis-tribution of lung ventilation in the chest cross-sectionduring rapid tidal breathing and sighs. The study revealedone unexpected finding: the prone position increased theasymmetry of the distribution of inspired air between theright and left lungs during tidal breathing by lowering theventilation in the left lung region.

There are a few indications that the head position mayinfluence respiratory mechanics in very small infants [16],and that it may have important clinical implications [17].The effect of head position was not followed in our pre-vious study, and its possible role in generating the asym-metric ventilation distribution during spontaneous breath-ing in the prone position could thus be neither excluded norconfirmed. We therefore carried out a new study with theaim of determining whether rotation of the infants headto right or left sides affects the ventilation distribution inthe two clinically relevant postures-supine and prone. Wealso studied an equally large group of mechanically venti-lated infants using the same protocol to establish whetherthere are differences between the ventilation distributionsin these two different types of ventilation.

MethodsPatients

Ten unsedated, nonintubated spontaneously breathing in-fants and ten mechanically ventilated infants were stud-ied in the NICU. The study was approved by the Univer-sity ethics committee, and informed written consent was

Table 1 Characteristics of the spontaneously breathing (SB) and me-chanically ventilated (MV) infants studiedPatient Gender Gestation- Birth Postnatal Weightno. al age weight (g) age (days) (g)

(weeks)SB1 M 40 3800 6 36202 F 35 1850 43 31853 M 36 2290 16 26004 F 40 2270 10 23505 M 38 3190 8 33806 F 38 3205 7 29507 F 35 1810 20 22808 F 39 3110 11 32509 F 40 2850 7 2830

10 M 36 2230 5 2150Mean 38 2 2661 664 13 11 2860 504 SD

MV1 F 33 1690 92 38002 M 24 780 128 29503 F 32 1055 67 23704 M 30 900 70 25005 M 41 3340 20 38206 M 40 3950 3 39307 F 35 2100 39 27008 M 40 3050 43 38309 F 34 2460 65 4300

10 M 38 3644 57 4580Mean 35 5 2297 1175 58 36 3478 782 SD

obtained from the parents. The measurements were con-ducted according to the Declaration of Helsinki.

Basic characteristics of the infants are presented inTable 1. All infants were free of respiratory disease and re-quired intensive care and mechanical ventilation for otherdiseases. In the spontaneously breathing group, the mostfrequent reason for admission to the NICU was suspectedintrauterine infection (see Electronic SupplementaryMaterial, ESM, S.T1). The most frequent diagnosis inthe second group was congenital hernia (see ESM, S.T2).Four of the spontaneously breathing infants and six of theventilated ones were prematurely born. Five infants fromthe former group and three from the latter were deliveredby cesarean section.

Electrical impedance tomography

EIT was used to determine the distribution of lung venti-lation. The EIT technique has frequently been described(e.g., [18, 19]). Briefly, the measuring principle of EIT isbased on rotating injection of very small electrical currentsand measurement of potential differences through a set ofelectrodes attached on the chest circumference. Each cy-cle of current injections and voltage measurements pro-duces one scan of the instantaneous distribution of elec-

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trical impedance in the chest. Relative values showing thechanges in local impedance with respect to a referencevalue (the average local impedance calculated over severalconsecutive breaths) are shown.

In our study EIT measurements were performed withthe 16-electrode Gttingen GoeMF II system (ViasysHealthcare, Hchberg, Germany) [20, 21]. Electricalcurrents of 5 mArms and 50 kHz were used. EIT data wererepeatedly acquired at 60-s intervals. The scan rate was13 scans/s with a scan resolution of 32 32 pixels.

Protocol

The spontaneously breathing infants were examinedapprox. 30 min postprandially on their last day in theNICU before their discharge from hospital. The ventilatedinfants were studied immediately after their transfer fromthe operating room to the NICU. They were intubatedvia the nasotracheal route and ventilated in the pressure-controlled continuous positive pressure ventilation mode(Babylog 8000, Drgerwerk, Lbeck, Germany).

Sixteen ECG electrodes (Blue Sensor BR-50-K,Ambu, Friedberg, Germany) were placed on the chestcircumference. (In the mechanically ventilated infants theelectrodes were attached in the operating room to mini-mize the handling time in the NICU.) The electrodes wereconnected to the EIT device. The infants were randomlyassigned to a supine/prone or prone/supine examinationsequence combined with different head positions. Thefollowing combinations were studied: supine with head inthe midline position (SM), supine with head turned to theright (SR), supine with head turned to the left (SL), pronewith head turned to the right (PR), and prone with headturned to the left (PL).

The examination lasted approx. 40 min in the spon-taneously breathing group and 20 min in the artificiallyventilated one. The spontaneously breathing infants wereunsedated; therefore occasional stretching or crawlingmovements occurred during the measurements. For thisreason a higher number of EIT measurements was per-formed in this group resulting in a longer total examinationtime. (The measurements were repeated between threeand five times in the spontaneously breathing and two orthree times in the mechanically ventilated infants.) Duringthe measurements no care procedures were allowed, andno adjustments of the ventilator settings were made.

Off-line data analysis

In each infant and body/head position studied six short EITdata sequences comprising four to six consecutive breathswere selected from the 60-s EIT recordings. The followingselection criteria were used during tidal breathing: (a) reg-ular breathing rate, (b) stable tidal and end-expiratory lung

volume, and (c) no body, head, or arm movement. Duringmechanical ventilation no special selection criteria had tobe used because the ventilatory pattern was stable and theinfants did not move. The data were low-pass filtered witha cutoff frequency of 2 Hz.

The short data sequences were analyzed as follows:first, the end-inspiratory maximum and the end-expiratoryminimum values of relative impedance change were identi-fied and the average differences between these values cal-culated in all image pixels (Fig. 1, right). These ventila-tion related impedance changes were depicted in the corre-sponding pixels in different gray tones depending on theirmagnitude (i.e., the largest values were shown in white andthe smallest in black). The light areas in such functionalscans show the ventilated lung regions (Fig. 1, left). Thenext data evaluation step summed the pixel values of ven-tilation related impedance changes in the right and left lungregions proportional to regional tidal volume. The regionswere defined using a procedure described elsewhere [22].The sum of ventilation related impedance changes in theright lung region divided by the sum of these values inboth lung regions gave the fractional ventilation of the rightlung in the chest cross-section studied. In each body/headposition all six short sequences of EIT data selected wereanalyzed in the described manner and average values de-termined.

Results in the text and figures are presented as means SD of ten infants. The data from the spontaneouslybreathing and mechanically ventilated groups were com-

Fig. 1 Functional EIT scan of regional lung ventilation (left) gen-erated from the EIT data obtained during six consecutive breaths ina mechanically ventilated infant (patient 4). The ventilator settingswere: tidal volume 13 ml, respiratory rate 25 breaths/min, positiveend-expiratory pressure 3 mbar, peak inspiratory pressure 24 mbar,inspiration/expiration time 1/3, fraction of O2 in inspired gas 0.3.The orientation of the ventilation scan is the following: anterior is atthe top and right side of the chest is on the left side of the image.The tracing of relative impedance change (right) shows a selected15-s data segment in one of a total of 912 image pixels (cross exactlocation of the pixel). Gray, white arrows End-inspiratory maximumand end-expiratory minimum values needed for the determination ofthe ventilation related tidal change in local electrical impedance. Thelarger the local air volume change the larger is the local ventilationrelated impedance change and the lighter appears the correspondingarea in the functional EIT ventilation scan

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Table 2 Length of the EIT data sequences analyzed, size of the rightand left lung regions in the EIT scans, and respiratory and heart ratesof the studied infants (means SD) (SM supine position with headin the neutral midline position, SR supine position with head turned

to the right, SL supine position with head turned to the left, PRprone position with head turned to the right, PL prone position withhead turned to the left, SB spontaneous breathing, MV mechanicalventilation)

SM SR SL PR PL

EIT data sequence (no. breaths)SB 5.4 1.6 5.4 1.3 5.3 1.7 5.7 1.7 5.3 1.4MV 4.3 0.8 4.5 0.8 4.5 0.7 4.5 0.7 4.4 0.6

Right lung region (no. pixels)SB 125 13 126 12 138 13 150 20 150 23MV 144 18 145 21 144 19 153 15 156 13

Left lung region (no. pixels)SB 119 14 113 18 112 12 111 19 108 20MV 114 21 117 22 117 19 122 17 110 18

Respiratory rate (breaths/min)SB 54 12 59 17 59 15 56 16 61 17MV 29 5 29 5 29 5 29 5 29 5

Heart rate (beats/min)SB 143 14 141 17 140 15 145 18 147 18MV 148 17 146 18 149 17 150 16 150 16

p< 0.05 vs. MV

pared using the paired Wilcoxon rank sum test. One-wayanalysis of variance and Students paried t test were usedfor comparisons within each group. Two-tailed p valuesless than 0.05 were considered statistically significant.

ResultsThe quantitative analysis was performed on data sequencesoriginating from several consecutive breaths. The number

Fig. 2 Sum of ventilation related impedance change in the right(a) and left lung region (b) in mechanically ventilated and spon-taneously breathing infants studied in different postures and headpositions (meansSD). SM supine position with the head in theneutral midline position, SR supine position with the head turnedto the right side, SL supine position with the head turned to the leftside, PR prone position with the head turned to the right side, PL

prone position with the head turned to the left side, Z electricalimpedance. p < 0.05, p < 0.01, p < 0.001 above means be-tween mechanically ventilated and spontaneously breathing infants; p < 0.05, p < 0.01, p < 0.001 upper, lower parts (b) withinthe mechanically ventilated and spontaneously breathing groups; p < 0.05, p < 0.01 higher values in the right than in the left lungregion

of breaths analyzed was comparable between the groups(Table 2). In the scans the right lung region was alwayslarger than the left one. The region area was unaffectedby the body/head position except for the right lung regionwhich was larger in the SL, PR, and PL positions than inthe SC during spontaneous breathing (Table 2). The spon-taneously breathing infants had a higher respiratory ratethan the ventilated ones (Table 2). No significant differ-ences between the respiratory rates in the five body/headpositions were observed. The mechanically ventilated

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Fig. 3 Fractional ventilation of the right lung in the chest cross-section in mechanically ventilated and spontaneously breathing in-fants studied in different postures and head positions (means SD). p < 0.05, p < 0.01 within the mechanically ventilated and sponta-neously breathing groups

infants were ventilated with the following settings: tidalvolume 29 13 ml, positive end-expiratory pressure3.2 1.2 mbar, peak inspiratory pressure 21.7 2.6 mbar,inspiration/expiration time 1/3.2 0.7 s, fraction of O2in inspired gas 0.28 0.04. There were no significantdifferences in the heart rates within or between the twogroups (Table 2).

The sums of ventilation related impedance change inthe right and left lung regions in spontaneously breathingand mechanically ventilated infants are given in Fig. 2.The tidal volumes in the right lung region (Fig. 2a)were significantly higher during mechanical than duringspontaneous tidal ventilation. They were unaffected bybody or head position. In prone infants the tidal volumesin the right lung region were significantly higher thanin the left one. The tidal volumes in the left lung region(Fig. 2b) were also higher during mechanical than duringspontaneous ventilation. However, in contrast with theright lung, their magnitude was influenced by the bodyand head position. During spontaneous breathing, thiseffect was more pronounced than during mechanicalventilation. Three combinations of body/head positions(SL, PR, PL) reduced the ventilation related changes inlung volume in the left lung region during spontaneousbreathing when compared with the SM position. Duringartificial ventilation only the PL position exhibited thiseffect. These changes in regional tidal volumes had animpact on the right-to-left distribution of air betweenthe two lung regions (Fig. 3) leading to an increase infractional ventilation of the right lung in the SL, PRand PL positions during tidal breathing and in the PLposition during mechanical ventilation. In both types ofventilation studied the largest effect was observed in thePL position.

Discussion

Our study demonstrates significant effects of head/bodyposition on the distribution of inspired air between the rightand left lung regions during spontaneous tidal breathing.The higher fractional ventilation of the right lung in thechest cross-section in the prone posture was also found inour previous study [15]. The current examinations con-firmed that the reduction in left lung tidal volumes oc-curred when the infants heads were turned both to theright and left sides whereby the leftward rotation had a sig-nificantly higher effect. The rotation of the head to the leftside reduced the tidal volumes in the left lung region andincreased the fractional ventilation of the right lung alsoin the supine posture, although to a lesser degree. We didnot expect the head position to have an influence on theright-to-left ventilation distribution during controlled me-chanical ventilation. However, the effect of the leftwardhead rotation was observed in the prone posture even dur-ing this type of ventilation. All positions other than PL hadno effect during artificial ventilation.

To our knowledge, such findings related to the distri-bution of regional ventilation in the lungs of neonates freeof respiratory disease have not been reported before. Be-cause of the methodological limitations addressed above,until recently almost no ethically justifiable methods ex-isted that could have been used in this population in studiesfocusing on regional lung function. Thus the introductionof EIT opens up new possibilities in visualizing and quan-tifying regional lung ventilation in infants. Nevertheless,the present study does not allow the identification of thecausative factors of this new phenomenon. We speculatethat the leftward rotation of the head leads to some mod-ification in the tissue and organ locations within the me-diastinum with possible reduction in the gas flow into theleft main and/or principal bronchi. The fact that rotation ofthe head to the left side affected the ventilation distributioneven during mechanical ventilation seems to be supportiveof such a mechanical, tractional effect. Nonetheless it isdifficult to totally exclude some artifactual changes in theEIT images when organs move within the thorax.

The larger angle of divergence of the left than the rightmain stem bronchus from the trachea [23] may influenceregional ventilation distribution. A postmortem studyperformed on intubated newborn infants revealed thatthe positioning of infants heads to the right facilitatedcatheterization of the left main bronchus. In the straighthead position and during leftward head rotation thecatheterization of the right main stem bronchus dom-inated [23]. These primarily anatomical results cannotbe directly compared with our dynamic functional data.Nevertheless, they provide a hint that the head positionhas an effect on the anatomical situation near the tracheabifurcation.

In spontaneously breathing infants the prone posturemay have had an additional effect on regional tidal

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volumes in the caudal regions of the left lung causedby the changed diaphragmatic movement. The humannewborn diaphragm is less effective in terms of its abilityto compress gastric content and expand lower thoraxbecause of its flatter configuration and narrower zone ofapposition [24]. The prone body position would thereforebe expected to affect the regional excursions of thediaphragm mainly near the stomach. This may explainwhy the ventilation redistribution was more pronouncedin the spontaneously than in the mechanically ventilatedneonates.

Because of the measuring principle of EIT, which isbased on using small alternating currents, the EIT scansrepresent a slice of the chest, not a single transverse plane.(Unlike ionizing radiation, which passes straight throughthe body, the passage of electrical current is not confined toa two-dimensional plane.) Therefore impedance changesoccurring out of the plane also contribute to the result-ing EIT scan, although to a lesser degree than those takingplace directly within the plane. This effect of the third di-mension on the EIT scans has previously been studied [25].Therefore the results of our study mainly reflect regionalinequalities in ventilation distribution in the caudal lungregions in a chest slice lying below the electrodes and notin the apical zones which also may have been affected bythe head/body position changes.

The EIT signal reflects all changes in electricalimpedance occurring in the chest. Therefore not only thelarge impedance changes associated with lung ventilationbut also the much smaller impedance changes associatedwith lung perfusion were detected. Several off-line dataevaluation steps ensured that the results reflected onlyventilation and not cardiac or perfusion related changes:(a) The EIT data were low-pass filtered; thus impedancechanges synchronous with heart rate were excluded fromanalysis. (b) The analysis was performed only within thelung regions (not within the cardiac and mediastinumregions). (c) The data were analyzed in terms of end-inspiratory to end-expiratory impedance differencesrepresentative of tidal gas volume changes.

The effects of head position on lung ventilation havehardly been studied in infants. Postural effects have beenfollowed more frequently, however, with partly conflictingfindings. In the prone position no effect of postural changeon the respiratory rate was found [26], there was reducedthoracoabdominal incoordination [26], fewer apneas, and

less periodic breathing [27]. Increased airway resistanceas well as lower peak flow rates and lung volumes werealso found in the prone posture [28]. In the latter studythe prone infants were only studied with their heads turnedto the left (i.e., in the position which mainly affected re-gional ventilation distribution in our study) and comparedwith the supine posture with straight head position. Thusthe study design did not allow the changes in lung me-chanics to be attributed solely to the change in posture be-cause the head position also may have had an effect. Rehanet al. [29] described significant differences between the di-aphragm resting length and shortening at the level of thezone of apposition between the supine and prone postures.Unfortunately, the measurements were only performed onthe right hemithorax. Thus they cannot provide informa-tion on any differences in the diaphragmatic excursionsbetween the right and left sides of the body which mighthave helped to elucidate the mechanisms leading to the re-gionally dissimilar ventilation found in various body/headpositions in our study.

Baird et al. [30] indirectly confirm the validity ofour findings. They used plain transthoracic electricalimpedance measurement to determine the breath ampli-tudes of the impedance signal in the supine and pronepostures. This technique, nowadays routinely used for therespiratory rate monitoring in a clinical setting, utilizes thesame basic measuring principle as EIT without providingany spatial information. Significantly lower breath ampli-tudes of transthoracic electrical impedance were foundin the prone than in the supine posture. Our results alsorevealed this reduced magnitude of the ventilation relatedimpedance change between inspiration and expiration inthe prone posture and found that these changes occurredmainly in the left lung.

Our study identified new physiological phenomena inregional lung ventilation in spontaneously breathing andmechanically ventilated infants with no pulmonary diseaseas a result of head and body position changes. The scien-tific discussion on the favorable or unfavorable body posi-tions in small infants is still going on. Because of the as-sociation between the prone sleeping position and suddeninfant death syndrome (e.g., [17, 31, 32]) with no clearlyidentified causative mechanism [33] this issue is still top-ical. Our study provides new input into this discussion byaddressing not only the effects of the body but also of thehead position.

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