Regularity of center-of-pressure trajectories depends on the amount of attention invested in postural control The influence of attention on the dynamical structure of postural sway was examined in 30 healthy young adults by manipulating the focus of attention . In line with the proposed direct relation between the amount of attention invested in postural control and regularity of center-of-pressure -LRB- COP -RRB- time series , we hypothesized that : -LRB- 1 -RRB- increasing cognitive involvement in postural control -LRB- i.e. , creating an internal focus by increasing task difficulty through visual deprivation -RRB- increases COP regularity , and -LRB- 2 -RRB- withdrawing attention from postural control -LRB- i.e. , creating an external focus by performing a cognitive dual task -RRB- decreases COP regularity . We quantified COP dynamics in terms of sample entropy -LRB- regularity -RRB- , standard deviation -LRB- variability -RRB- , sway-path length of the normalized posturogram -LRB- curviness -RRB- , largest Lyapunov exponent -LRB- local stability -RRB- , correlation dimension -LRB- dimensionality -RRB- and scaling exponent -LRB- scaling behavior -RRB- . Consistent with hypothesis 1 , standing with eyes closed significantly increased COP regularity . Furthermore , variability increased and local stability decreased , implying ineffective postural control . Conversely , and in line with hypothesis 2 , performing a cognitive dual task while standing with eyes closed led to greater irregularity and smaller variability , suggesting an increase in the `` efficiency , or `` automaticity '' of postural control '' . In conclusion , these findings not only indicate that regularity of COP trajectories is positively related to the amount of attention invested in postural control , but also substantiate that in certain situations an increased internal focus may in fact be detrimental to postural control . Introduction By now , it is well established that maintaining and controlling an upright posture requires a certain amount of attention -LRB- for a review see Woollacott and Shumway-Cook 2002 -RRB- . The relation between attentional resources and the processing of information from somatosensory , visual , and vestibular systems is readily apparent in cases of reduced or conflicting sensory information -LRB- e.g. , Redfern et al. 2001 , 2004 ; Shumway-Cook and Woollacott 2000 ; Teasdale and Simoneau 2001 -RRB- . On the one hand , the degree of attention , or cognitive involvement , required for controlling posture increases with task difficulty . This has been -LRB- indirectly -RRB- illustrated by , for example , Lajoie et al. -LRB- 1993 -RRB- and Vuillerme and Nougier -LRB- 2004 -RRB- , who both found that the reaction time of a verbal response to an auditory stimulus increased with the difficulty of the postural task . On the other hand , the amount of attention required to perform a secondary suprapostural task is known to influence posture -LRB- e.g. , Balasubramaniam et al. 2000 ; Huxhold et al. 2006 ; Pellecchia 2003 ; Riley et al. 2003 -RRB- . The dependency of posture on attention is even more prominent in the presence of pathology or aging , when both peripheral and central changes occur that decrease the -LRB- physical -RRB- capability needed to maintain balance during standing or walking -LRB- e.g. , Brown et al. 1999 ; Lindenberger et al. 2000 ; Marchese et al. 2003 ; Rankin et al. 2000 ; Redfern et al. 2004 -RRB- . In balance-impaired elderly individuals , for example , the performance of a secondary cognitive task -LRB- i.e. , dual-task paradigm -RRB- may promote postural instability and even falls -LRB- Barra et al. 2006 ; Brauer et al. 2001 -RRB- . Hence , the amount of attention required for maintaining and controlling upright posture is indicative of the degree of `` automaticity '' of postural control and , for that reason , has been advocated and used as an important tool in clinically oriented studies -LRB- cf. , Geurts et al. 1991 ; Melzer et al. 2001 -RRB- . Center-of-pressure -LRB- COP -RRB- fluctuations measured while standing on a force platform provide a complex output signal of the postural control system in which various pertinent cognitive , perceptual , and motor processes are reflected . Recently , COP measures pertaining to the dynamical structure of COP fluctuations have helped to understand the inherent complexity of the postural control system and its constituent processes -LRB- e.g. , Baratto et al. 2002 ; Collins and De Luca 1993 ; Newell et al. 1993 ; Pascolo et al. 2005 ; Peterka 2000 ; Yamada 1995a ; cf. , Riley and Turvey 2002 for a review -RRB- . Inspired by this development in modern posturography , Roerdink et al. -LRB- 2006 -RRB- -- in a study on the functional recovery of posture in stroke patients -- proposed a direct relation between the amount of attention invested in postural control and the regularity of COP fluctuations . COP trajectories were more regular -LRB- as indexed by reduced sample entropy -RRB- in stroke patients than in healthy elderly and became less regular when performing a secondary cognitive task while standing . These results were interpreted to imply that postural sway regularity is positively correlated with the degree of cognitive involvement in postural control . Interestingly , the regularity of the COP fluctuations decreased with rehabilitation , whereas postural stability -LRB- as indexed by the largest Lyapunov exponent -RRB- increased , suggesting that the required degree of cognitive involvement in postural control decreased during the course of rehabilitation . Hence , these progressively more irregular COP fluctuations -LRB- as indexed by an increase in sample entropy -RRB- may be interpreted as an increase in the efficiency or `` automaticity '' of postural control . This interpretation is in line with physiological studies showing that a decrease in `` complexity '' or `` irregularity '' of a physiological time-series is indicative of a decrease in healthiness or effectiveness of the physiological control system -LRB- cf. , Goldberger et al. 2002 -RRB- , a phenomenon known as `` dynamical diseases '' -LRB- cf. Belair et al. 1995 -RRB- . In other words , increased COP regularity may be explained as an indication of an increasingly ineffective postural control strategy . The aim of the present study was to examine the role of attention in the regulation of posture . To this end , the amount of attention invested in postural control was manipulated experimentally in a large group of young healthy adults . In particular , we increased the difficulty of the postural task through visual deprivation under the assumption that an increase in task difficulty is associated with an increase in cognitive involvement in postural control , creating a so-called internal attentional focus -LRB- cf. , Andersson et al. 1998 ; Teasdale et al. 1993 ; Teasdale and Simoneau 2001 -RRB- . In contrast , we used a concurrent attention demanding cognitive task in order to withdraw attention from postural control , creating an external focus of attention -LRB- cf. , Huxhold et al. 2006 -RRB- . These manipulations of attention allowed us to examine the proposed direct relation between COP regularity and the amount of attention invested in postural control -LRB- Roerdink et al. 2006 -RRB- . In line with this relation , we hypothesized that : -LRB- 1 -RRB- increasing postural task difficulty -LRB- i.e. , by standing with eyes closed , creating an internal focus -RRB- increases the cognitive involvement in postural control and hence the regularity of COP fluctuations , and -LRB- 2 -RRB- reduced attention to postural control -LRB- i.e. , by performing a cognitive dual task , creating an external focus -RRB- decreases the regularity of COP fluctuations . In addition , based on the suggestion that posture is mainly controlled in the direction of the largest postural sway -LRB- Roerdink et al. 2006 -RRB- and the common finding that in healthy young adults postural sway is largest in the sagittal plane relative to the frontal plane -LRB- e.g. , Gatev et al. 1999 ; Winter et al. 1998 -RRB- , we expected COP regularity to be largest in the sagittal plane . Regularity of COP trajectories was quantified by the sample entropy -LRB- Richman and Moorman 2000 ; Roerdink et al. 2006 -RRB- . In order to examine the structure of COP fluctuations in more detail , we further used a combination of more traditional -LRB- i.e. , based on summary statistics -RRB- and dynamical measures that are all defined operationally in terms of readily interpretable features of motor control -LRB- see also Table 1 -RRB- : standard deviation of COP time-series -LRB- indexing variability or the amount of postural sway -RRB- , sway-path length of the normalized posturogram -LRB- indexing the amount of twisting and turning of the COP trajectory -RRB- , largest Lyapunov exponent -LRB- Rosenstein et al. 1993 ; indexing local stability -RRB- , correlation dimension -LRB- Grassberger and Procaccia 1983 ; indexing the number of active , dynamical degrees of freedom involved in postural control and hence its dimensionality , e.g. , Kay 1988 -RRB- and the scaling exponent -LRB- e.g. , Peng et al. 1995 ; indexing long-range correlations in COP time-series -RRB- . Based on previous research , we expected visual deprivation to decrease local stability and to increase variability of COP time-series -LRB- cf. , Roerdink et al. 2006 ; Woollacott and Shumway-Cook 2002 ; Yardley et al. 1999a -RRB- . Moreover , we anticipated the attention manipulations to induce adjustments in the dynamical structure of postural control leading to changes in scaling exponent , sway-path length and dimensionality of COP fluctuations . Table 1Abbreviations and meaning of interest of the calculated COP measuresVariableMeaning of interestSample entropy , SEnNegatively related with the regularity of COP trajectoryStandard deviation , σ -LRB- mm -RRB- Positively related with the variability of COP trajectorySway-path length , SPn -LRB- s − 1 -RRB- Positively related with the curviness of COP trajectoryLargest Lyapunov exponent , λmaxNegatively related with the local stability of COP trajectoryDimensionality , D2Positively related with the number of active control variablesScaling exponent , αLong-range correlations : α = 0.5 for uncorrelated data -LRB- i.e. , white noise -RRB- , α = 1.5 for `` Brown noise '' , the integration of white noise Methods Participants and procedures A total of 30 healthy young adults -LRB- 10 males , 20 females ; mean age = 24 years , range = 19 -- 30 years -RRB- , without known motor impairments or movement-related disorders , volunteered to participate in the experiment . Participants stood barefoot on a 1 × 1 m custom-made strain gauge force plate1 with their arms hanging relaxed alongside their body . The medial sides of the heels were separated by about 8 cm and each foot was placed with the toes outward at a 10 ° angle from the sagittal midline -LRB- i.e. , standard Romberg position -RRB- . In order to examine the role of attention in the regulation of posture we carried out two manipulations . On the one hand , we increased the postural task difficulty by inviting participants to stand with eyes closed , while on the other hand , we withdrew attention from postural control by inviting them to perform a cognitive dual task . In particular , the participants were invited to stand upright with -LRB- 1 -RRB- eyes open -LRB- EO-ST -RRB- , -LRB- 2 -RRB- eyes closed -LRB- EC-ST -RRB- , -LRB- 3 -RRB- eyes open while performing a dual task -LRB- EO-DT -RRB- and -LRB- 4 -RRB- eyes closed while performing a dual task -LRB- EC-DT -RRB- . The dual task consisted of uttering backwards names read out aloud by the investigator -LRB- e.g. , `` Simon '' had to be repeated as `` nomis '' -RRB- . The sole aim of this cognitive dual task was to withdraw attention from the postural task . Therefore , the participants were instructed to perform the task to the best of their ability . No feedback on the accuracy with which they performed this task was provided . Each participant performed the four task conditions in random order and once in reverse order , resulting in a total of eight recordings . COP trajectories were collected for 35 s at a sampling rate of 100 Hz . After the local ethics committee had approved the study , all participants gave their informed consent prior to their participation . Data analysis In order to examine whether posture is actively controlled in the direction of largest postural sway -LRB- Roerdink et al. 2006 -RRB- , we analyzed both the registered x -LRB- mediolateral ML -RRB- and y -LRB- anterioposterior AP -RRB- COP time-series . After omitting the first 5 s of each recording , leaving 30 s of data for further analyses -LRB- i.e. , 3,000 samples -RRB- , the time-series were bi-directionally filtered -LRB- second-order low-pass Butterworth filter , cut-off frequency of 12.5 Hz -RRB- to eliminate low amplitude measurement noise .2 First , we calculated the conventional standard deviation σ of x and y COP trajectories to quantify the variability , or amount , of postural sway . Subsequently , we normalized the x and y trajectories to unit variance -LRB- i.e. , by dividing the time-series in question by their respective standard deviation -RRB- and calculated the sway path defined as the length of the COP trajectory traveled per second . The applied normalization procedure enabled us to determine the sway path in the normalized posturogram , abbreviated as SPn , providing a scale-independent measure of the amount of twisting and turning of the COP trajectory . Apart from these summary statistics of postural sway -LRB- i.e. , SPn and σ -RRB- , which by definition ignore the temporal structure of the COP time-series , we assessed COP dynamics by means of sample entropy , largest Lyapunov exponent , correlation dimension and scaling exponent , which will be briefly explained in the following -LRB- for a more extensive description we refer to Roerdink et al. -LRB- 2006 -RRB- and references therein -RRB- . Table 1 presents the six different measures and their interpretation . Sample entropy , SEn Healthy physiological systems are often characterized by an irregular and complex type of variability , whereas disease or aging is often associated with greater regularity and less complexity -LRB- cf. , Goldberger 1996 ; Goldberger et al. 2002 ; Pincus et al. 1991 -RRB- . A method to quantify the regularity of time-series is the sample entropy analysis -LRB- Lake et al. 2002 ; Richman and Moorman 2000 -RRB- . Sample entropy indexes the regularity of a given time-series , and is used to analyze complex stochastic systems that -LRB- by definition -RRB- include both deterministic and random processes -LRB- Pincus 1991 -RRB- . Specifically , sample entropy calculates the probability that a sequence of data points , having repeated itself within a tolerance r for a window length M , will also repeat itself for M + 1 points , without allowing self-matches -LRB- see Lake et al. 2002 ; Richman and Moorman 2000 -RRB- .3 Smaller sample entropy values are associated with greater regularity . In the present study , a decrease in sample entropy -LRB- i.e. , more regular sway fluctuations -RRB- was interpreted as a decrease in the effectiveness of postural control . Largest Lyapunov exponent , λmax The largest Lyapunov exponent4 provides a measure of the local stability of a dynamical system -LRB- e.g. , Abarbanel et al. 1996 -RRB- , i.e. , the system 's sensitivity to initial conditions or its resistance to small internal perturbations , such as the natural fluctuations that occur while maintaining an upright stance . It quantifies the exponential divergence or convergence of initially nearby trajectories in state space as time progresses -LRB- e.g. , Rosenstein et al. 1993 -RRB- . If nearby points diverge , they produce instability . The exponent λmax indexes this instability : positive values of λmax indicate either the presence of deterministic chaos -LRB- i.e. , a form of variability that is brought about by an underlying lawful nonlinear dynamical structure -RRB- or complete randomness -LRB- i.e. , noise -RRB- , implying that nearby points diverge rapidly , reflecting local instability and lack of predictability . In order to distinguish a deterministic component from genuine randomness , it is necessary to validate results against surrogate data -LRB- cf. , Theiler et al. 1992 -RRB- . Dimensionality , D2 The dimensionality of all COP time-series was calculated using the correlation dimension algorithm of Grassberger and Procaccia -LRB- 1983 -RRB- .5 The correlation dimension provides an index of the number of independent degrees of freedom -LRB- equations of motion -RRB- that are required to reproduce the time evolutionary properties of the COP time-series . Note that this analysis of the dynamical degrees of freedom is different from the analysis of the -LRB- mechanical -RRB- degrees of freedom of the joints as commonly applied in the study of motor control , and that no straightforward or uniform relation exists between the number of component degrees of freedom in motion and the dimension of the organizational dynamic in controlling those components -LRB- Newell and Vaillancourt 2001 -RRB- . Scaling exponent , α In order to determine whether the measured COP time-series were characterized by the presence of long-range correlations , we applied a fractal analysis method for biological time-series called detrended fluctuation -LRB- DFA -RRB- analysis -LRB- Peng et al. 1995 -RRB- .6 The scaling exponent α as determined by this method indicates the presence or absence of -LRB- long-range -RRB- correlations in the COP trajectories , as defined by Peng et al. -LRB- 1995 -RRB- . For uncorrelated data , -LRB- e.g. white noise -RRB- α = 0.5 . An α greater than 0.5 and less than or equal to 1.0 indicates persistent long-range power-law correlations . In contrast , 0 < α < 0.5 indicates a different type of power-law correlation such that large and small values of the time series are likely to alternate . For α > 1 correlations exist but cease to be of a power-law form ; α = 1.5 indicates Brown noise , i.e. , integrated white noise . The scaling exponent α can also be viewed as an indicator that describes the roughness of the time series : the larger the value of α , the `` smoother '' the time series -LRB- Peng et al. 1995 -RRB- . Surrogate analysis To test for spurious effects and to distinguish between deterministic features and randomness , the scaling exponents , dimension estimates , Lyapunov exponents and entropy values were also computed for surrogate data -LRB- Theiler et al. 1992 -RRB- . In particular , we generated both time - and phase-randomized surrogate data of the filtered COP time-series -LRB- Fig. 1 -RRB- . In time-randomized surrogate data , the distribution of the original data is being preserved -LRB- i.e. , mean , variance , etc. are unaltered -RRB- , whereas the temporal correlations in the COP time-series are destroyed . The absence of temporal correlations will result in a scaling exponent α close to 0.5 and very large values for dimension and sample entropy . Phase-randomized surrogate data are obtained by randomizing the data 's Fourier phases . In contrast to time-randomization , this procedure does not alter the spectral power distribution and preserves the data 's auto-correlation function . Consequently , scaling exponents of phase-randomized and original data should match , whereas estimates of correlation dimension and sample entropy should be largely increased in the surrogate data.Fig . 1An example of the surrogate analysis , as applied to all time-series . Surrogate data of a measured COP trajectory -LRB- upper panel -RRB- were constructed by randomizing the Fourier phase -LRB- middle panel -RRB- and the temporal order -LRB- lower panel -RRB- Statistical analysis For all dependent variables , the first and second trials were averaged . To test for differences between AP and ML COP measures and to examine the effect of the different experimental tasks , we used a repeated measures analysis of variance -LRB- ANOVA -RRB- design with within-subject factors vision -LRB- 2 levels : standing with eyes open EO , and standing with eyes closed EC -RRB- , dual task -LRB- 2 levels : standing without cognitive dual task performance , i.e. , single task , ST , and standing with cognitive dual task performance , DT -RRB- , and plane -LRB- 2 levels : sagittal and frontal plane -RRB- .7 Subsequently , we tested for differences between surrogate and original data using a design involving a within-subject factor surrogate -LRB- 3 levels : original data and time - and phase-randomized surrogate data -RRB- . To assess the strength of the -LRB- main and interaction -RRB- effects , we determined the eta squared -LRB- η2 -RRB- , a commonly used measure of effect size in AVOVAs , reflecting the proportion of variance in the dependent variable that is attributable to each effect . Subsequently , η2 was converted into Cohen 's f according to : An effect size -LRB- f -RRB- of > 0.4 was considered to reflect a strong effect -LRB- Cohen 1988 -RRB- . The analyses were performed using SPSS -LRB- SPSS , Inc. , Chicago , IL , USA -RRB- . Results The result section is organized as follows . We first report possible differences in the dependent variables between the eyes open and eyes closed conditions -LRB- i.e. , main effect of vision , hypothesis 1 -RRB- . Second , we describe the effect of experimentally withdrawing attention from postural control by comparing single task and dual task conditions -LRB- i.e. , main effect of dual task , hypothesis 2 -RRB- . Third , we report whether significant vision × dual task interaction effects were present . Finally , we present the effects of plane , which may reveal possible directional differences in control . In this context , we also report the effects of randomization on the dependent variables to ensure that the observed changes in the dynamics of COP trajectories were genuine effects . Table 2 presents the results of the vision × dual task ANOVA for the six dependent posturographic measures -LRB- i.e. , interindividual means corresponding to the main effects of vision and dual task , collapsed over x and y time-series , as well as F , P and f values for main and interaction effects -RRB- . Significant vision × dual task interaction effects are presented in Fig. 2 . Table 2Main and interaction effects of vision and dual task -LRB- i.e. , collapsed over x and y time-series -RRB- of sample entropy -LRB- SEn -RRB- , standard deviation -LRB- σ -RRB- , sway-path length of the normalized -LRB- by the standard deviation -RRB- posturogram -LRB- SPn -RRB- , largest Lyapunov exponent -LRB- λmax -RRB- and scaling exponent -LRB- α -RRB- of COP time-series for 30 healthy individualsConditionMeanVision -LRB- EO vs. EC -RRB- ConditionMeanDual task -LRB- ST vs. DT -RRB- Vision × dual taskaF -LRB- 1 , 29 -RRB- PƒF -LRB- 1 , 29 -RRB- PƒF -LRB- 1 , 29 -RRB- PƒSEnEO0 .723.83 = 0.060 * 0.36 ST0 .701.45 ns0 .256.72 < 0.050.48 EC0 .70 DT0 .72 σEO3 .5211.82 < 0.0050.64 ST3 .892.45 ns0 .293.18 = 0.0850.33 EC4 .01 DT3 .64 SPnEO4 .275.28 < 0.050.43 ST4 .1313.57 < 0.0050.686.98 < 0.050.49 EC4 .52 DT4 .66 λmaxEO1 .5636.23 < 0.0011.12 ST1 .710.10 ns0 .064.26 < 0.050.38 EC1 .88 DT1 .73 D2EO2 .2323.58 < 0.0010.90 ST2 .2045.70 < 0.0011.266.15 < 0.050.46 EC2 .48 DT2 .51 αEO1 .3913.70 < 0.0010.69 ST1 .3924.57 < 0.0010.921.80 ns0 .25 EC1 .34 DT1 .35 * Significant vision × plane interaction -LRB- F -LRB- 1 , 29 -RRB- = 5.48 , P < 0.05 , ƒ = 0.44 -RRB- , which was caused by the fact that , in contrast to that in the frontal plane , the effect of vision was significant in the sagittal plane -LRB- F -LRB- 1 , 29 -RRB- = 6.47 , P < 0.05 , ƒ = 0.47 -RRB- a See Fig. 2 for mean values of the conditions EO-ST , EC-ST , EO-DT and EC-DTFig . 2Interindividual averages , collapsed over x and y time-series , of sample entropy -LRB- SEn -RRB- , standard deviation -LRB- σ -RRB- , sway-path length of the normalized -LRB- by the standard deviation -RRB- posturogram -LRB- SPn -RRB- , local stability -LRB- λmax -RRB- and dimensionality -LRB- D2 -RRB- for the four experimental conditions : standing with eyes open -LRB- EO-ST -RRB- , eyes closed -LRB- EC-ST -RRB- , eyes open while performing a cognitive dual task -LRB- EO-DT -RRB- and eyes closed while performing a cognitive dual task -LRB- EC-DT -RRB- . The asterisks indicate significant -LRB- P < 0.05 -RRB- differences between conditions Increased postural task difficulty -LRB- EO vs. EC -RRB- As is apparent from the significant main effects of vision in Table 2 , standing with eyes closed resulted in more regular sway fluctuations , as indexed by a decrease in SEn. In addition , sway variability -LRB- σ -RRB- , dimensionality -LRB- D2 -RRB- and sway-path length -LRB- SPn -RRB- were increased , whereas α and local stability -LRB- as indexed by an increase in λmax -RRB- decreased . Decreased attention to posture -LRB- ST vs. DT -RRB- Collapsed over x and y time-series and visual conditions , no significant main effects involving dual task were found for σ , SEn or local stability . In contrast , a main effect of dual task was found for both SPn and D2 in that performing a cognitive dual task brought about an increase in both variables as compared to the single task condition -LRB- Table 2 -RRB- . Moreover , as shown in Table 2 , performing a dual task resulted in a significant decrease of α indicating that dual task performance brought about changes in the time-varying structure of sway fluctuations . Vision × dual task interaction effects Significant dual task × vision interaction effects -LRB- Table 2 -RRB- revealed that the effects of visual deprivation on SEn , σ and SPn were different for single and dual task conditions -LRB- see Fig. 2 -RRB- . In particular , the observed effect of visual deprivation on σ and SEn was significant only for the single task condition , whereas the observed increase in SPn only existed for dual task performance -LRB- see Fig. 2 -RRB- . On the other hand , as can be appreciated from both Table 2 and Fig. 2 , the effects of introducing a cognitive dual task on SEn , σ and SPn depended on eye closure . Although no significant main effect of dual task was found for SEn , there was a significant dual task × vision interaction . This effect occurred because SEn increased significantly from 0.68 to 0.72 through the introduction of a dual task when standing with eyes closed , whereas such an increase was absent when standing with eyes open -LRB- 0.72 for both single and dual task conditions -RRB- . Similarly , when standing with eyes open , dual task performance had no significant effect on σ , whereas dual task performance resulted in a decrease in σ when standing with eyes closed -LRB- see Fig. 2 -RRB- . The observed significant dual task × vision interaction effects for λmax were brought about by the fact that the increase -LRB- i.e. , decrease in local stability -RRB- when standing with eyes closed was stronger for the single task condition than for the dual task condition . A similar asymmetric effect was found for D2 , in that the increase when standing with eyes closed was stronger for the dual task condition than for the single task condition . Moreover , as can be observed in Fig. 2 , the effect of performing a dual task -LRB- i.e. , increase in D2 -RRB- was larger when standing with eyes closed than with eyes open . Effects of plane and randomization Collapsed over conditions , significant differences between sagittal and frontal plane were found for all variables , except α . In particular , sway variability , σ , and local stability , λmax , were significantly larger in the sagittal than in the frontal plane -LRB- F -LRB- 1 , 29 -RRB- = 20.94 , P < 0.001 , f = 0.82 and F -LRB- 1 , 29 -RRB- = 15.19 , P < 0.005 , f = 0.72 , respectively -RRB- . In contrast , sample entropy , SEn , and dimensionality , D2 , were significantly lower in the sagittal than in the frontal plane -LRB- F -LRB- 1 , 29 -RRB- = 145.38 , P < 0.001 , f = 2.31 and F -LRB- 1 , 29 -RRB- = 16.01 , P < 0.001 , f = 0.74 , respectively -RRB- . A significant vision × plane interaction was found for SEn -LRB- F -LRB- 1 , 29 -RRB- = 5.48 , P < 0.05 , f = 0.44 -RRB- , which was caused by the fact that SEn was smaller when standing with eyes closed -LRB- EC-ST , see Fig. 2 -RRB- for COP fluctuations in the sagittal plane , whereas this was not the case for COP fluctuations in the frontal plane . Figure 3 shows the results of the interindividual means of the surrogate analyses . Sample entropy measures of both phase - and time-randomized surrogate data were significantly higher compared to the original COP time-series -LRB- F -LRB- 2 , 58 -RRB- = 10985.1 , P < 0.001 , f = 22.34 -RRB- . Whereas scaling exponents of phase-randomized surrogate data and original COP time-series did not differ , correlations were completely absent when the data were time-randomized as evidenced by α values around 0.5 -LRB- F -LRB- 2 , 58 -RRB- = 5436.7 , P < 0.001 , f = 14.12 -RRB- . As a result of very high-dimensional noise in the time-randomized data , no embedding dimension could be estimated and hence no dimensionality estimates and Lyapunov exponents could be determined for the time-randomized surrogate data .8 Randomizing the phases of original COP data significantly increased the dimensionality -LRB- F -LRB- 1 , 29 -RRB- = 50.07 , P < 0.001 , f = 1.31 -RRB- . In addition , the Lyapunov exponent of the phase-randomized surrogate data was significantly higher than that of the original time-series -LRB- F -LRB- 1 , 29 -RRB- = 53.44 , P < 0.001 , f = 1.36 -RRB- . Fig. 3Grand means , collapsed over all conditions , planes and participants , of sample entropy , scaling exponent , dimensionality and local stability for the original -LRB- OR -RRB- COP time-series and their phase-randomized -LRB- PHASE -RRB- and time-randomized -LRB- TIME -RRB- surrogate counterparts . The error bars represent the interindividual standard deviations . The asterisks represent significant -LRB- P < 0.05 -RRB- differences between the surrogate data and the original time-series Discussion The present experiment was conducted to investigate the role of attention in the regulation of posture . Specifically , we examined whether an increase in postural sway regularity -LRB- i.e. , as indexed by a decrease in SEn -RRB- is representative of an increase in cognitive investment in postural control . We hypothesized that COP trajectories become more regular -LRB- i.e. , SEn decreases -RRB- when task difficulty is increased -LRB- EC vs. EO -RRB- and , conversely , become less regular -LRB- i.e. , SEn increases -RRB- when an attention-demanding cognitive dual task is introduced -LRB- DT vs. ST -RRB- . We further expected that these changes in regularity of COP fluctuations would be accompanied by changes in variability , local stability , sway-path length , dimensionality and scaling exponent reflecting functional modifications of postural control . For the proper interpretation of the present findings , however , it was necessary to ascertain that the observed structure -LRB- and changes herein -RRB- of the COP fluctuations did not result from noise , but was indeed brought about by deterministic processes . Therefore , we will first discuss the results of the surrogate analyses before discussing the respective effects of vision , dual task and plane on the dynamical structure of postural sway . Surrogate analyses Although nonlinear estimates of dynamical structure are not readily interpretable in an absolute sense , they can be meaningfully interpreted by comparing them across conditions , -LRB- see e.g. , Newell et al. 1993 -RRB- , as well as with surrogate data . For example , entirely random data are characterized by large -LRB- theoretically infinite -RRB- dimensionality and large λmax values , whereas chaotic/deterministic data have smaller dimensionality and smaller λmax values . In the present analysis , the surrogate data had greater dimensionality and larger λmax values than the original data , implying that the latter had considerable deterministic structure -LRB- cf. , Theiler et al. 1992 -RRB- . Moreover , both phase - and time-randomized surrogate data showed increased sample entropy values . Hence , the original COP fluctuations clearly had a deterministic component , which was evidenced further by the fact that the scaling exponents became 0.5 after time-randomization -LRB- resulting from a loss of temporal correlations in the shuffled time-series -RRB- , but remained unaffected by phase-randomization -LRB- i.e. , preserving temporal correlations -RRB- . These findings are consistent with those of previous studies suggesting that COP fluctuations are -LRB- largely -RRB- of deterministic origin -LRB- e.g. , Doyle et al. 2004 ; Riley et al. 1999 ; Yamada 1995b -RRB- , and testify to the relevance and need of including dynamical measures in posturography . Increasing postural task difficulty -LRB- EO vs. EC -RRB- In the present study , standing with eyes closed brought about an increase of sway variability , which was accompanied by an increase in dimensionality and λmax , implying that local stability decreased . Possibly , the observed increase in dimensionality may serve as a mechanism to enrich information so as to facilitate the control of standing and to cope with the reduced -LRB- local -RRB- stability -LRB- cf. , Riley and Clark 2003 ; van Emmerik and van Wegen 2002 -RRB- . These observations are in line with the common notion that visual deprivation increases the task difficulty of postural control , and , consequently , requires cognitive monitoring of postural control . We expected that this increase in cognitive investment would be accompanied by a decrease in SEn -LRB- i.e. , an increase in regularity -RRB- , which was indeed the case -LRB- see Fig. 2 , compare EO-ST with EC-ST -RRB- , thus confirming hypothesis 1 . These findings are consistent with the results of other studies showing that COP variability tends to increase as experimental task conditions become increasingly difficult , whereas the temporal structure of postural sway tends to become increasingly regular -LRB- Riley and Clark 2003 ; Roerdink et al. 2006 ; Thurner et al. 2002 -RRB- . In the present study , visual deprivation resulted in qualitatively similar changes in the structure of COP trajectories as reported in the study of Roerdink et al. -LRB- 2006 -RRB- for stroke patients -LRB- i.e. , increased σ , λmax , D2 , and decreased SEn and α with respect to healthy elderly adults -RRB- . In healthy young adults , the qualitatively similar changes in COP dynamics with visual deprivation as compared to standing with eyes open may , likewise , be interpreted to indicate that postural control is performed less automatically and effectively . Whereas in stroke patients such modifications in postural control may be due to a defect or slowing down of the central processing of sensory information -LRB- cf. , Teasdale et al. 1991 ; Woollacott et al. 1986 -RRB- , in young healthy adults a more regular sway , resulting from standing with eyes closed , implies increased `` active '' monitoring of postural control with increasing task difficulty -LRB- cf. , Andersson et al. 1998 ; Nashner and McCollum 1985 ; Redfern et al. 2001 ; Teasdale et al. 1993 ; Teasdale and Simoneau 2001 -RRB- . If the proposed relation between cognitive investment in postural control and postural sway regularity does indeed exist , then the performance of a cognitive dual task should result in less regular COP trajectories . That this was indeed the case will be discussed in the next two subsections . Withdrawing attention from posture The performance of a concurrent dual task led to changes in scaling exponents and an increase in dimensionality , reflecting cognition-invoked adjustments of postural control . These changes under dual task performance may have served to enrich the information captured in sway fluctuations without increasing the amount of sway -LRB- i.e. , variability remained unaltered -RRB- . This interpretation is amplified by the observation that the sway-path length of the normalized posturogram increased , indicating more twisting and turning in the COP trajectories . Interestingly , despite the fact that attention was withdrawn experimentally from postural control , local stability remained unaltered . In contrast to what we expected , no main effect of dual task was found for SEn. However , this finding does not necessarily militate against the proposed relation between the regularity of COP fluctuations and the amount of attention directed to postural control , as will be argued in the following subsection . Vision × dual task interaction Especially noteworthy in this context and in view of our expectations is that while standing with eyes closed postural sway regularity decreased -LRB- i.e. , sample entropy increased -RRB- when performing a cognitive dual task -LRB- compare EC-DT and EC-ST in Table 2 and Fig. 2 -RRB- . This finding is consistent with hypothesis 2 and supports the proposed positive correlation between COP regularity and the degree of attention involved in postural control . Apparently , the fact that regularity remained unaltered -LRB- i.e. , 0.72 -RRB- when performing a dual task while standing with eyes open -LRB- EO-DT -RRB- implies that , for young healthy adults , standing with eyes open is not very attention demanding . Conversely , during the more challenging task of standing with eyes closed -LRB- EC-ST -RRB- COP fluctuations became more regular -LRB- i.e. , 0.68 ; Fig. 2 -RRB- . However , the finding that sample entropy again increased to its `` normal '' -LRB- EO-ST -RRB- level when withdrawing the focus of attention from the postural task -LRB- EC-DT -RRB- indicates that the increased cognitive monitoring of posture during EC-ST had a detrimental effect . Visual deprivation increased the awareness of the postural task -LRB- i.e. , creating an internal focus -RRB- , resulting in efforts to actively -LRB- consciously -RRB- control posture and , as such , preventing the postural control system to work in a relatively automatic and efficient manner -LRB- viz. , Andersson et al. 2002 ; Hunter and Hoffman 2001 ; McNevin and Wulf 2002 ; Milton et al. 2004 -RRB- . Similarly , when standing with eyes open the attention-demanding dual task had no significant effect on σ , whereas when standing with eyes closed the dual task did result in a decrease in σ -LRB- see Fig. 2 -RRB- , corroborating the findings of e.g. , Andersson et al. -LRB- 2002 -RRB- , McNevin and Wulf -LRB- 2002 -RRB- and Morioka et al. -LRB- 2005 -RRB- . In contrast , many authors have found an increase in postural sway variability when performing a cognitive dual task -LRB- see Shumway-Cook and Woollacott 2000 -RRB- . It has been suggested that this effect of dual task on the amount of sway may , in part , result from articulation -LRB- Dault et al. 2003 ; Yardley et al. 1999b -RRB- . In this context , it is important to note that the present finding that variability actually decreased with the introduction of a cognitive dual task indicates that articulation played no significant role in the present study . Sagittal versus frontal plane The increased variability of the COP trajectories in the sagittal plane -LRB- as compared to the frontal plane -RRB- was accompanied by reduced local stability and greater regularity -LRB- i.e. , a decrease in sample entropy -RRB- . These observations are consistent with the findings of Roerdink et al. -LRB- 2006 -RRB- , which showed that in healthy elderly adults local stability was reduced in the sagittal plane , whereas regularity and variability were elevated in this plane . Based on these results , they suggested that posture is mainly controlled in the direction of largest postural sway -LRB- i.e. , sagittal plane -RRB- , which required a certain amount of attention as reflected by the regularity findings . The present observation that during standing with eyes closed -LRB- EC-ST -RRB- regularity increased significantly in the sagittal plane , whereas no effect was found for the frontal plane , is in line with this suggestion : young healthy adults mainly control posture in the sagittal plane , which becomes particularly attention demanding when task difficulty is increased -LRB- see also Pellecchia 2003 ; Riley et al. 2003 -RRB- . Conclusion The present study showed that the amount of attention invested in postural control is positively correlated with sway regularity . Specifically , the present study showed that increasing postural task difficulty by means of visual deprivation -LRB- EC-ST -RRB- not only resulted in an increase of COP variability and a decrease in local stability , but also in more regular COP trajectories . These findings could be taken to imply that the participants actively monitored their posture in order to cope with the increased postural task difficulty . However , when the amount of attention invested in postural control was experimentally reduced by introducing a cognitive dual task -LRB- EC-DT -RRB- , both regularity and variability of sway fluctuations returned to values observed when standing with eyes open -LRB- EO-ST -RRB- . This finding suggests that during standing with eyes closed -LRB- EC-ST -RRB- the increase in monitoring posture was due to an increase in awareness of the postural task -LRB- i.e. , internal attentional focus -RRB- , preventing postural control from working in an automatic and efficient manner -LRB- e.g. , Hunter and Hoffman 2001 -RRB- . All in all , it is fair to conclude that the methodological and analytical approach adopted in the present study allows for disentangling whether or not there is an increase in cognitive involvement and to what extent an increase in cognitive involvement has a detrimental or beneficial effect .

B O O O O O O O O B O O B I O O O B O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O B O O B I O B O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O B O O O O O O B O B I O O O O O O O O O O O O O O O O B O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O B O O O O O O O O O O B O O B I O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O B I O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O B I O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O 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O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O 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O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O 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O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O 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O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O B O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O B I O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O B I O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O


What

is

new

in

otitis

media

The

wait

and

see

approach

in

acute

otitis

media

-LRB-

AOM

-RRB-

consisting

of

postponing

the

antibiotic

administration

for

a

few

days

has

been

advocated

mainly

to

counteract

the

increased

bacterial

resistance

in

respiratory

infections

This

approach

is

not

justified

in

children

less

than

years

of

age

and

this

for

several

reasons

First

AOM

is

an

acute

inflammation

of

the

middle

ear

caused

in

about

of

cases

by

bacteria

Redness

and

bulging

of

the

tympanic

membrane

are

characteristic

findings

in

bacterial

AOM

Second

AOM

is

associated

with

long-term

dysfunction

of

the

inflamed

eustachian

tube

-LRB-

ET

-RRB-

particularly

in

children

less

than

years

of

age

In

this

age

group

the

small

calibre

of

the

ET

together

with

its

horizontal

direction

result

in

impaired

clearance

ventilation

and

protection

of

the

middle

ear

Third

recent

prospective

studies

have

shown

poor

long-term

prognosis

of

AOM

in

children

below

years

with

at

least

of

recurrences

and

persisting

otitis

media

with

effusion

-LRB-

OME

-RRB-

in

about

months

after

AOM

Viruses

elicit

AOM

in

about

of

children

A

prolonged

course

of

AOM

has

been

observed

when

bacterial

and

viral

infections

are

combined

because

viral

infection

is

also

associated

with

ET

dysfunction

in

young

children

Bacterial

and

viral

testing

of

the

nasopharyngeal

aspirate

is

an

excellent

tool

both

for

initial

treatment

and

recurrence

of

AOM

Antibiotic

treatment

of

AOM

is

mandatory

in

children

less

than

years

of

age

to

decrease

inflammation

in

the

middle

ear

but

also

of

the

ET

particularly

during

the

first

episode

The

best

choice

is

amoxicillin

because

of

its

superior

penetration

in

the

middle

ear

Streptococci

pneumoniae

with

intermediary

bacterial

resistance

to

penicillin

are

particularly

associated

with

recurrent

AOM

Therefore

the

dosage

of

amoxicillin

should

be

mg/kg

per

day

in

three

doses

In

recurrent

AOM

with

β-lactamase-producing

bacilli

amoxicillin

should

be

associated

with

clavulanic

acid

at

a

dose

of

mg/kg

per

day

The

duration

of

the

treatment

is

not

established

yet

but

days

is

reasonable

for

a

first

episode

of

AOM

OME

may

be

a

precursor

initiating

AOM

but

also

a

complication

thereof

OME

needs

a

watchful

waiting

approach

When

associated

with

deafness

for

months

in

children

over

years

of

age

an

antibiotic

should

be

given

according

to

the

results

of

the

bacterial

resistance

in

the

nasopharyngeal

aspirate

The

high

rate

of

complications

of

tympanostomy

tube

insertion

outweighs

the

beneficial

effect

on

hearing

loss

The

poor

results

of

this

procedure

are

due

to

the

absence

of

effects

on

ET

dysfunction

Pneumococcal

vaccination

has

little

beneficial

effects

on

recurrent

AOM

and

its

use

in

infants

needs

further

studies

Treatment

with

amoxicillin

is

indicated

in

all

children

younger

than

years

with

a

first

episode

of

AOM

presenting

with

redness

and

bulging

of

the

tympanic

membrane

Combined

amoxicillin

and

clavulanic

acid

should

be

given

in

patients

with

β-lactamase-producing

bacteria

The

duration

of

treatment

is

estimated

to

be

at

least

days

depending

on

the

findings

by

pneumo-otoscopy

and

tympanometry

Bacterial

and

viral

testing

of

the

nasopharyngeal

aspirate

is

highly

recommended

particularly

in

children

in

day

care

centres

as

well

as

for

regular

follow-up

The

high

recurrence

rate

is

due

to

the

long-lasting

dysfunction

of

the

eustachian

tube

and

the

immune

immaturity

of

children

less

than

years

of

age

Introduction

The

number

of

publications

relating

to

acute

otitis

media

-LRB-

AOM

-RRB-

and

otitis

media

with

effusion

-LRB-

OME

-RRB-

has

been

increasing

markedly

within

the

last

years

-LSB-

-RSB-

It

points

to

the

difficulties

in

giving

generally

accepted

guidelines

for

treatment

The

confusion

can

be

partially

explained

by

the

absence

of

uniform

definitions

and

inhomogeneous

groups

of

patients

being

included

in

clinical

studies

AOM

is

an

acute

inflammation

of

the

middle

ear

frequently

elicited

by

viral

infections

and

characterized

by

redness

and

bulging

of

the

tympanum

Infections

with

bacteria

can

be

identified

in

at

least

of

the

cases

by

culture

of

the

middle

ear

purulent

fluid

containing

mainly

polymorphonuclear

cells

-LSB-

-RSB-

OME

is

an

effusion

of

the

middle

ear

without

symptoms

of

acute

inflammations

such

as

pain

and

fever

with

frequently

an

amber

or

opaque

aspect

of

the

tympanum

the

effusion

containing

mainly

macrophages

Retraction

of

the

tympanum

with

the

light

reflex

still

present

may

render

the

diagnosis

difficult

Cultures

for

bacteria

are

positive

in

about

of

cases

whereas

viruses

have

been

identified

in

about

-LSB-

-RSB-

OME

may

be

a

precursor

event

initiating

suppurate

AOM

but

it

can

be

the

continuum

of

AOM

as

well

OME

is

the

direct

consequence

of

impaired

middle

ear

ventilation

Tympanometry

-LRB-

Fig.

-RRB-

shows

a

flat

curve

type

b

in

both

AOM

and

OME

In

contrast

in

OME

associated

with

incomplete

obstruction

of

the

eustachian

tube

-LRB-

ET

-RRB-

a

curve

c

with

a

peak

in

the

negative

pressure

zone

is

observed

Moreover

lower

peak

height

and

greater

width

in

the

negative

pressure

zone

are

frequent

findings

in

OME

-LSB-

-RSB-

Fig.

three

main

types

of

tympanograms

showing

a

a

peak

near

atmospheric

pressure

expressed

in

daPa

with

stapedius

reflex

for

different

Hz

frequencies

b

a

flat

curve

without

stapedius

reflex

for

Hz

pointing

to

presence

of

middle

ear

exudate

AOM

or

OME

c

a

lower

peak

in

the

negative

pressure

zone

-LRB-

daPa

-RRB-

with

an

enlarged

width

pointing

to

OME

with

partial

permeability

of

ET

to

air

entrance

and

still

a

stapedius

reflex

This

overview

summarizes

the

main

new

findings

about

AOM

and

OME

which

are

in

accordance

with

some

basic

well-known

but

sometimes

forgotten

data

and

facts

with

particular

emphasis

on

the

vulnerability

of

young

children

below

the

age

of

years

Aetiopathogenesis

Role

of

the

eustachian

tube

The

great

importance

of

the

first

attack

of

AOM

in

young

children

lies

in

the

subsequent

long-lasting

dysfunction

of

the

ET

Indeed

the

main

functions

of

the

ET

are

ventilation

protection

and

clearance

of

the

middle

ears

-LRB-

Fig.

-RRB-

-LSB-

-RSB-

and

play

a

determining

role

in

the

recurrence

of

AOM

Ventilation

of

the

middle

ear

occurs

by

each

deglutition

by

action

of

the

tensor

velum

palatinum

muscle

leading

to

air

equilibration

with

the

atmospheric

pressure

By

obstruction

of

the

ET

a

negative

pressure

develops

inside

the

middle

ear

resulting

in

effusion

and

aspiration

of

nasopharyngeal

secretions

Poor

ventilation

leads

to

decreased

which

results

in

decreased

bactericide

power

of

polymorphonuclear

cells

Impaired

clearance

results

in

proliferation

not

only

of

aerobic

but

also

anaerobic

bacteria

in

the

middle

ear

Conversely

reflux

otitis

occurs

with

decreased

compliance

of

the

ET

due

to

abnormal

flaccidity

Fig.

physiologic

functions

of

the

eustachian

tube

in

relation

to

the

middle

ear

NP

nasopharynx

ET

eustachian

tube

TVP

tensor

velum

palatinum

muscle

ME

middle

ear

MAST

mastoid

TM

tympanic

membrane

EC

external

canal

ET

dysfunction

is

a

major

problem

in

the

young

child

the

small

calibre

of

the

ET

as

well

as

its

horizontal

direction

-LSB-

-RSB-

-LRB-

Figs.

and

-RRB-

are

responsible

for

both

the

high

incidence

of

AOM

and

the

frequent

relapses

by

each

viral

infection

This

explains

the

poor

long-term

prognosis

evidenced

in

a

prospective

study

comprising

AOM

patients

of

less

than

years

of

age

by

Damoiseaux

et

al.

-LSB-

-RSB-

At

least

of

the

patients

had

recurrences

of

AOM

and

persistence

of

OME

was

observed

in

of

them

after

months

and

in

after

months

Yet

only

of

these

patients

were

treated

with

amoxicillin

Unfortunately

the

authors

do

not

mention

either

the

delay

of

treatment

or

the

dosage

of

the

antibiotic

Fig.

difference

in

the

angle

of

the

eustachian

tube

between

infants

and

adults

-LSB-

-RSB-

Fig.

tympanic

membrane

forms

the

lateral

wall

of

the

box-shaped

middle

ear

The

function

of

the

eustachian

tube

is

to

equilibrate

middle

ear

pressure

with

that

in

the

nasopharynx

Bacteria

and

viruses

resident

in

the

nasopharynx

may

reach

the

middle

ear

during

pressure

equilibration

One-third

of

the

middle

ear

mucosa

and

the

entire

eustachian

tube

are

lined

with

mucociliary

epithelium

to

transport

bacteria

from

the

middle

ear

back

to

the

nasopharynx

Air

from

the

middle

ear

enters

the

mastoid

air

cells

by

way

of

the

aditus

In

other

words

the

first

episode

of

AOM

determines

the

evolution

and

the

recurrences

because

of

the

associated

acute

inflammation

involving

also

the

ET

Role

of

viruses

and

bacteria

Viruses

Most

children

are

infected

with

respiratory

syncytial

virus

-LRB-

RSV

-RRB-

in

their

first

year

of

life

A

prospective

study

-LSB-

-RSB-

in

children

aged

months

with

bronchiolitis

showed

that

of

them

had

AOM

at

entry

or

within

days

and

an

additional

developed

OME

only

patients

remained

free

of

both

AOM

and

OME

during

a

observation

period

These

findings

were

confirmed

in

a

recent

study

showing

that

in

patients

with

persistent

RSV

antigen

in

the

middle

ear

effusion

relapsed

despite

a

favourable

outcome

of

the

first

AOM

episode

-LSB-

-RSB-

The

association

of

AOM

with

several

viral

infections

has

been

largely

documented

The

prevalence

of

respiratory

viruses

in

the

middle

ear

fluid

of

children

aged

months

to

years

with

AOM

was

-LSB-

-RSB-

RSV

was

the

most

frequent

virus

isolated

followed

by

parainfluenza

influenza

enteroviruses

and

adenoviruses

These

findings

have

been

confirmed

by

others

-LSB-

-RSB-

and

rhinovirus

coronavirus

and

metapneumovirus

should

be

added

to

the

above-mentioned

list

-LSB-

-RSB-

Even

the

measles

virus

has

recently

been

isolated

from

the

middle

ear

fluid

in

two

patients

-LSB-

-RSB-

Bacteria

In

of

patients

with

AOM

bacteria

can

be

found

by

culturing

the

middle

ear

fluid

-LSB-

-RSB-

The

most

frequent

species

isolated

are

Haemophilus

influenzae

and

Streptococcus

pneumoniae

-LSB-

-RSB-

Nasopharyngeal

aspirate

culture

may

give

valuable

information

on

the

bacteria

involved

in

AOM

-LSB-

-RSB-

The

presence

of

conjunctivitis

points

to

Haemophilus

influenzae

infection

-LSB-

-RSB-

Heikkinen

et

al.

found

Streptococcus

pneumoniae

in

of

their

patients

Haemophilus

influenzae

in

and

Moraxella

catarrhalis

in

-LSB-

-RSB-

It

has

been

demonstrated

that

recurrences

of

AOM

are

associated

with

positive

bacterial

culture

in

the

nasopharynx

-LSB-

-RSB-

even

at

the

end

of

the

antibiotic

treatment

-LSB-

-RSB-

and

in

most

cases

the

pathogen

was

Streptococcus

pneumoniae

-LSB-

-RSB-

However

recurrence

more

than

days

after

an

initial

AOM

episode

is

mostly

due

to

a

new

infection

i.e.

not

a

true

relapse

-LSB-

-RSB-

In

a

most

recent

prospective

study

on

purulent

meningitis

-LSB-

-RSB-

the

association

of

AOM

was

found

in

half

of

the

patients

-LSB-

-RSB-

Bacteria

and

viruses

Bulut

et

al.

performed

both

bacterial

and

viral

testing

in

children

with

AOM

-LSB-

-RSB-

These

patients

aged

between

months

and

years

did

not

receive

an

antibiotic

for

weeks

prior

to

the

study

A

positive

bacterial

culture

was

obtained

in

of

the

children

and

respiratory

viruses

were

identified

in

of

them

combined

viral

and

bacterial

infection

was

demonstrated

in

of

the

samples

Persistent

otitis

was

documented

in

about

of

the

children

with

combined

viral

and

bacterial

infection

in

a

prospective

study

of

children

because

viral

infections

contribute

to

the

ET

dysfunction

-LSB-

-RSB-

Other

risk

factors

The

immaturity

of

the

immune

system

of

young

children

makes

them

incapable

of

killing

encapsulated

bacteria

This

along

with

the

ET

dysfunction

explains

the

long-lasting

course

of

AOM

as

well

as

the

high

recurrence

rate

This

is

particularly

important

for

infants

attending

day

care

centres

-LSB-

-RSB-

It

is

sometimes

necessary

to

withdraw

these

infants

from

these

institutions

during

the

winter

to

avoid

recurrences

Additional

risk

factors

are

passive

smoking

young

siblings

going

to

school

and

siblings

with

previous

AOM

episodes

These

factors

were

identified

in

a

prospective

study

on

children

aged

months

to

years

published

in

-LSB-

-RSB-

The

proportion

of

patients

developing

at

least

one

episode

of

OME

was

at

months

and

at

months

Breast

feeding

and

exposure

to

tobacco

smoke

contributed

little

to

the

outcome

but

a

lower

socioeconomic

status

and

repeated

exposure

to

other

children

at

home

or

in

day

care

centres

were

the

most

important

risk

factors

Children

with

cleft

palate

are

particularly

prone

to

otitis

and

should

be

treated

by

early

tympanostomy

tube

insertion

-LSB-

-RSB-

Complications

mastoiditis

Mastoiditis

should

be

treated

by

antibiotics

according

to

the

bacterial

resistance

and

by

temporarily

inserting

tympanostomy

tubes

to

improve

drainage

-LSB-

-RSB-

because

of

the

narrow

calibre

of

the

aditus

ad

antrum

-LSB-

-RSB-

-LRB-

Fig.

-RRB-

Treatment

General

considerations

A

wait

and

see

approach

has

been

advocated

in

the

treatment

of

AOM

in

children

mainly

because

of

the

increased

antimicrobial

resistance

of

bacteria

causing

respiratory

infections

-LSB-

-RSB-

Indeed

a

meta-analysis

of

children

aged

months

to

years

and

collected

from

randomized

trials

concluded

that

there

was

a

significant

but

modest

impact

of

antibiotics

on

the

primary

control

of

AOM

-LSB-

-RSB-

Similar

results

emerged

from

a

subsequent

study

published

by

Damoiseaux

et

al.

in

-LSB-

-RSB-

This

randomized

double-blind

prospective

trial

carried

out

by

general

practitioners

in

children

aged

months

to

years

showed

that

only

and

maybe

of

them

needed

antibiotics

Both

studies

however

suffer

from

major

flaws

the

absence

of

long-term

data

in

particular

the

recurrence

rate

of

AOM

and

OME

not

being

considered

an

end

point

Moreover

the

former

study

included

patients

with

a

very

large

age

range

and

therefore

blunted

the

effect

of

the

critical

age

group

of

the

patients

below

the

age

of

years

Indeed

over

of

AOM

patients

present

their

first

attack

during

the

first

year

of

life

and

over

within

years

of

age

-LSB-

-RSB-

The

visualisation

of

the

tympanum

in

this

age

group

is

not

always

easy

especially

when

cerumen

obstructs

the

narrow

external

ear

channel

Yet

as

already

mentioned

above

bulging

and

redness

of

the

tympanic

membrane

are

important

diagnostic

signs

of

bacterial

AOM

-LSB-

-RSB-

Treatment

of

AOM

The

crucial

role

of

the

first

attack

of

AOM

makes

the

immediate

administration

of

antibiotics

mandatory

in

all

patients

with

AOM

with

redness

and

a

bulging

tympanum

-LRB-

Table

-RRB-

-LSB-

-RSB-

A

wait

and

see

approach

can

only

increase

the

inflammation

and

hence

the

ET

dysfunction

The

choice

of

the

antibiotic

must

take

into

account

the

penetration

in

the

middle

ear

and

the

type

of

bacteria

involved

The

penetration

for

amoxicillin

about

of

the

blood

concentration

is

much

higher

than

for

cephalosporins

-LRB-

about

-RRB-

and

macrolides

-LRB-

about

-RRB-

but

lower

than

for

cotrimoxazole

-LRB-

-RRB-

-LSB-

-RSB-

The

penetration

of

amoxicillin

is

not

changed

by

the

addition

of

clavulanate

to

amoxicillin

-LSB-

-RSB-

Table

for

treatment

of

AOMEpisodeSigns

or

symptomsTreatment

or

approachChildren

years

of

ageFirst

episodeAmoxicillin

mg/kg

per

day

for

at

least

days

according

to

the

bacterial

resistanceWeekly

follow-up

by

tympanometry

and

pneumo-otoscopyRecurrent

episodeWith

redness

and

bulging

tympanumAmoxicillin

or

amoxicillin

mg/kg

per

day

clavulanic

acid

mg/kg

per

day

according

to

bacterial

resistanceWithout

bulging

Wait

and

see

approachChildren

years

of

ageWith

redness

and

bulging

tympanum

or

otorrhoeaSame

treatment

as

recurrent

episode

Without

evident

bulging

tympanum

Wait

and

see

approach

Because

of

the

increased

incidence

of

Streptococcus

pneumoniae

with

intermediary

resistance

-LSB-

-RSB-

the

dosage

of

amoxicillin

should

be

doubled

i.e.

mg/kg

per

day

given

in

three

administrations

as

recommended

by

the

Centers

for

Disease

Control

and

Prevention

-LSB-

-RSB-

Haemophilus

influenzae

is

more

likely

to

become

β-lactamase

positive

after

previous

antibiotic

administration

-LSB-

-RSB-

Therefore

the

addition

of

clavulanate

at

a

dose

of

mg/kg

per

day

to

amoxicillin

makes

sense

Most

Moraxella

catarrhalis

strains

are

nowadays

also

β-lactamase

positive

-LSB-

-RSB-

The

duration

of

the

antibiotic

treatment

is

a

matter

of

discussion

For

children

less

than

years

of

age

a

course

is

reasonable

Pneumo-otoscopy

and

tympanometry

can

help

to

appreciate

the

permeability

of

the

ET

Careful

follow-up

is

necessary

Nasopharyngeal

aspirate

cultures

may

give

valuable

results

and

are

highly

recommended

in

children

remaining

in

day

care

centres

or

with

a

history

of

previous

AOM

episodes

-LSB-

-RSB-

For

children

more

than

years

of

age

the

previously

watchful

guidelines

can

be

maintained

but

some

flexibility

is

recommended

-LSB-

-RSB-

Treatment

of

OME

tympanostomy

tubes

The

approach

to

OME

must

take

into

account

the

natural

history

of

spontaneous

healing

and

the

main

complication

which

is

temporary

hearing

impairment

-LSB-

-RSB-

The

absence

of

spontaneous

healing

after

weeks

to

months

in

children

over

years

of

age

is

an

indication

for

a

antibiotic

course

according

to

the

results

of

the

nasopharyngeal

aspirate

cultures

It

is

our

experience

that

this

approach

has

several

advantages

First

the

effect

even

temporarily

on

the

hearing

defect

is

frequently

successful

Second

it

decreases

the

recurrence

of

AOM

by

improving

the

ET

functions

and

third

it

allows

postponement

or

avoidance

of

tympanostomy

tube

insertion

because

improved

hearing

points

to

improved

permeability

of

the

ET

The

delay

of

weeks

or

months

before

treatment

of

OME

-LRB-

Table

-RRB-

is

based

on

the

duration

of

OME

Indeed

in

a

prospective

study

by

Renko

et

al.

-LSB-

-RSB-

of

children

with

AOM

years

of

age

treated

with

amoxicillin

or

cefuroxime

axetil

for

days

the

mean

duration

of

OME

was

days

-LRB-

range

days

-RRB-

only

of

still

had

OME

after

days

Table

for

treatment

of

OME

SMZ

sulfamethoxazole

TMP

trimethoprimIndicationApproachTreatmentWithout

deafness

Watchful

waiting

approachWith

deafnessAfter

months

in

children

yearsAmoxicillin

mg/kg

per

day

or

amoxicillin

mg/kg

per

day

clavulanic

acid

mg/kg

per

day

for

days

according

to

the

results

of

the

bacterial

resistanceNo

swimmingRecurrent

OME

or

OME

of

long

durationAzithromycin

mg/kg

per

day

days/week

for

weeksCotrimoxazole

mg

SMZ

mg

TMP/kg

per

day

according

to

the

results

of

the

bacterial

resistanceAdenoidectomy

in

children

years

of

age

with

nasopharyngeal

obstruction

and

recurrent

adenoiditisNo

swimming

In

a

long-term

prospective

study

in

healthy

infants

treated

according

to

specified

guidelines

Paradise

et

al.

-LSB-

-RSB-

observed

bilateral

OME

in

only

of

the

children

who

had

not

received

tympanostomy

tubes

at

the

age

of

The

indication

to

insert

tubes

is

equivocal

The

large

prospective

studies

on

infants

and

young

children

by

the

Paradise

group

have

shown

the

absence

of

or

negligible

effects

of

tympanostomies

on

developmental

outcomes

at

years

-LSB-

-RSB-

On

the

other

hand

insertion

of

tympanostomy

tubes

during

the

first

years

of

life

is

associated

with

complications

in

at

least

of

the

patients

-LSB-

-RSB-

Tympanostomy

can

be

a

source

of

bacterial

infections

-LSB-

-RSB-

and

of

tympanosclerosis

Extensive

reviews

by

Kubba

et

al.

-LSB-

-RSB-

Rosenfeld

et

al.

-LSB-

-RSB-

Rovers

et

al.

-LSB-

-RSB-

and

the

recent

Cochrane

Database

by

Lous

et

al.

-LSB-

-RSB-

concluded

that

there

was

only

a

small

benefit

of

the

conventional

ventilation

tube

The

main

reason

for

the

poor

results

of

tympanostomy

tubes

is

the

absence

of

effects

on

the

ET

dysfunction

It

has

never

been

demonstrated

that

tympanostomy

tubes

improve

the

functions

of

the

ET

The

recommendations

by

the

American

Academy

of

Pediatrics

-LSB-

-RSB-

are

to

insert

tubes

in

conditions

with

persisting

hearing

loss

of

more

than

dB

particularly

with

posterosuperior

retraction

pockets

ossicular

erosions

and

adhesive

atelectasis

because

of

the

increase

of

structural

damage

with

effusion

duration

Watchful

waiting

for

months

in

the

winter

period

seems

advisable

in

children

with

mild

hearing

deficit

Adenoidectomy

should

be

considered

in

children

years

of

age

with

nasopharyngeal

obstruction

and

recurrent

adenoiditis

-LSB-

-RSB-

Vaccination

The

effects

of

pneumococcal

vaccination

on

recurrent

AOM

have

been

studied

extensively

In

a

randomized

controlled

trial

by

Brouwer

et

al.

-LSB-

-RSB-

in

children

aged

years

with

recurrent

AOM

the

effects

in

children

treated

with

heptavalent

pneumococcal

vaccine

were

compared

with

children

receiving

hepatitis

A

or

B

vaccines

The

study

concluded

that

there

was

no

beneficial

effect

A

similar

conclusion

was

drawn

from

a

study

by

Van

Kempen

et

al.

-LSB-

-RSB-

in

children

aged

years

and

in

the

Cochrane

Database

by

Straetemans

et

al.

-LSB-

-RSB-

A

shift

of

the

causative

pathogen

has

been

observed

from

Streptococcus

pneumoniae

to

Haemophilus

influenzae

or

to

other

strains

of

pneumococci

than

the

ones

included

in

the

vaccine

-LSB-

-RSB-

A

slight

reduction

of

the

incidence

of

AOM

of

was

observed

in

the

USA

-LSB-

-RSB-

Infants

and

prematures

A

high

incidence

of

OME

has

been

observed

in

neonatal

intensive

care

units

due

to

the

nasally

placed

tubes

for

ventilatory

assistance

It

has

been

suggested

that

immune

immaturity

with

impaired

neuromotor

function

predisposes

to

this

complication

-LSB-

-RSB-

Vaccination

with

the

heptavalent

pneumococcal

vaccine

has

been

advocated

in

premature

babies

and

neonates

-LSB-

-RSB-

but

this

study

does

not

provide

information

on

the

actual

AOM

prevalence

in

a

control

group

receiving

only

hepatitis

B

vaccine

It

should

be

remembered

that

meconium

aspiration

into

the

entry

of

the

middle

ear

is

associated

with

increased

risk

of

AOM

and

therefore

early

nasopharyngeal

suction

is

mandatory

-LSB-

-RSB-

O O O O O O O O O O O O O O O B I I O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O B I I I O B O O O O O O O O B O O O B O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O B O O O O O B O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I I O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I I O B O O B I I I O B O O O O O O O O O O O O O O O O O O O O O O O O O B I I O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O B O O O O O O O B O O O B O O O O O O O O O O O O O O O O O O O O O O O B O B O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O B O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O B O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O B O O O O O O O O B O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I I O O O O O O B B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O B O O O O O O O O B O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O B I I O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O B O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O B O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O

acute otitis media
otitis media with effusion
vaccination
tympanostomy tube insertion
mastoiditis
aom
ome
guidelines for treatment

eustachian tube dysfunction
otitis media in infants