| | Apnea associated with hypoxia in preterm infants: impact on cerebral blood volumeReceived 11 January 2002; received in revised form 12 June 2002; accepted 19 July 2002. Abstract The present study analyzed changes in cerebral blood volume (CBV) during apnea associated with hypoxia compared to apnea without hypoxia. Hypoxia was defined as pulsoxymetric oxygen saturation <80%>10 s. The employed technique was near infrared spectroscopy combined with electrocardiogram, electroocologram, pulsoxymetry, sidestream capnography and two respiratory effort sensors. In 24 preterm infants 44 incidences of apnea were analyzed. Two main patterns were observed: a significant decrease or a significant increase of CBV. In the ‘CBV decrease’ group ΔCBV was −55 μl/100 g brain in hypoxic apnea, and −62 μl/100 g brain in non-hypoxic apnea. In the ‘CBV increase’ group the rise of CBV above preapneic values was +50 μl/100 g brain in hypoxic apnea, and +47 μl/100 g brain in non-hypoxic apnea. Heart rate showed a significant decrease only in the ‘CBV decrease’ group. Endexpiratory CO2 increased significantly 1 min after apnea. In conclusion, this study observed significant changes of CBV during apnea in preterm infants, but no difference in CBV behavior regarding whether incidents of apnea were associated with hypoxia or not. It remains unclear which regulatory mechanisms are responsible for the two observed patterns of ΔCBV during apnea.
Abbreviations:
NIRS, near infrared spectroscopy,
Hbtot, total cerebral hemoglobin,
HbO2, oxygenated cerebral hemoglobin,
CBV, cerebral blood volume,
SaO2, pulsoxymetric oxygen saturation,
HR, heart rate,
etCO2, end tidal pCO2
1. Introduction  Apnea of prematurity is a very common phenomenon. Incidence varies from 59 to 78% with an inverse relationship between the proportion of infants having apneic events and gestational age [1]. The most common etiological factors contributing include immaturity of central respiratory control, impaired response to hypercapnic and/or hypoxic situations, and upper airway closure [2]. It is well known that apnea, especially if associated with hypoxia and/or bradycardia, may effect cerebral hemodynamics [3], [4], [5], [6]. In the literature, changes in cerebral hemodynamics have been measured using different methods; two of them are the Doppler technique and near infrared spectroscopy (NIRS). Using Doppler, Perlmann et al. found a decrease of cerebral blood flow velocity during episodes of apnea, especially when accompanied by severe bradycardia (heart rate, HR <80/min) [5]. Using NIRS, Jenni et al. described a decrease of cerebral blood volume (CBV), an increase of CBV, a combination of both, or no change of CBV during apnea [3]. Livera et al. demonstrated an increase of CBV during phases of moderate desaturation, and a decrease of CBV when apnea was accompanied by bradycardia [4]. Urlesberger et al. observed in 87% of cases a decrease of CBV during apnea in preterm infants [6]. There are thus different patterns of CBV behavior in association with apnea described in the literature. The reasons for changes in cerebral perfusion have not been thoroughly investigated. The HR may be of significant influence, as may changes in blood pressure. Changes in pCO2, or pO2 may have an influence, too. The global influence of pCO2 changes on CBV is well known and has been demonstrated [7], [8]. Since the cerebral pCO2 vasoreactivity is a matter of minutes, its influence during apnea seems to be limited. The influence of pO2 changes on CBV has not been that well demonstrated yet. Arterial hypoxia produces cerebral vasodilation and increases cerebral blood flow [9]. The aim of this study was to investigate whether there are significant differences in the course of total cerebral hemoglobin (cHbtot) and CBV during apnea with associated hypoxia in comparison to apnea of same length without associated hypoxia. 2. Methods 2.1. Patients The main criteria for study entry were recurrent apnea in premature infants. When such apnea had occurred, clinically polysomnography was done. Furthermore, apnea of a duration of >10 s with associated peripheral hypoxia was analyzed within this study. Hypoxia was defined as pulsoximetric SaO2 <80% lasting longer than 10 s. Exclusion criteria were the need for additional inspired oxygen, mechanical breathing support (e.g. mechanical ventilation, or nasal CPAP), or any impairment of cerebral function (e.g. history of perinatal asphyxia, intraventricular hemorrhage larger than Grade 1, or periventricular leukencephalomalacia). Poets et al. [10] showed that the behavior of SaO2 during periodic breathing differed significantly from behavior of SaO2 during apnea, and Urlesberger et al. [11] showed that there was cyclical desaturation and reoxygenation of cerebral blood during periodic breathing to a lesser degree compared to incidences where apnea lasted >15 s. Therefore, incidences of apnea that occurred during phases of periodic breathing were excluded from this analysis. Forty-four incidences of apnea in 24 preterm infants fulfilled the inclusion criteria. The infants’ median gestational age at birth had been 30.5 (range: 26–37) weeks, and at the time of our measurement 34.65 (range: 32–39) weeks. Their median weight at birth had been 1410 (range: 680–2666) g, and at the time of our measurement 1741 (range: 1100–2830) g. Fourteen infants had had treatment with euphyllin, 11 infants had suffered from IRDS, eight from sepsis, five from small subependymal hemorrhage and two from small for dateness. None of these infants showed any neurological deficits at the time of polysomnography. Informed consent was obtained from all parents. 2.2. Polygraphic monitoring All polygraphic tracings were done with a computer system (BEST, Multichannel System, B.E.S.T. Medical Systems, Austria). Polysomnography consisted of the following parameters: electroocolugram and electrocardiogram with a sampling rate of 64/s. HR and oxygen saturation were measured by pulsoximetry (CO2-SMO Novametrix Medical Systems Inc., Denmark), where SaO2 was measured by averaging a period of 2 s, HR by averaging a period of 8 s. Endexpiratory CO2 concentration (etCO2) was measured by side stream capnography (CO2SMO, Novametrix Medical Systems Inc., Denmark). For capnography an infant nasal CO2 sample cannula (Salter Labs, CA, USA) was placed with the tips into the infant's nostrils. Furthermore, breathing efforts were measured using two piezo respiratory effort sensors (Pro Tech, USA). The two belts were fastened at the level of the greatest in- and expiration of thorax and abdomen in such a way that separate measurements were able to be obtained. All parameters were stored within the multichannel computer system. 2.3. Near-infrared spectroscopy NIRS depends on the relative transparency of biological tissue (e.g. neonatal head) to light in the near-infrared region of the spectrum. The principles of NIRS were first described by Jöbsis [12]. NIRS enables the non-invasive continuous measurement of changes in concentration of oxygenated hemoglobin (ΔcHbO2), deoxygenated hemoglobin (ΔcHb) and cytochrom oxidase (ΔcCytO2). The sum of cHbO2 and cHb is calculated and described as total hemoglobin (cHbtot). Provided that hematocrit remains constant, cHbtot corresponds to the CBV. Changes in cerebral blood volume (ΔCBV) were calculated from ΔcHbtot using the formula: ΔCBV (ml/100 g brain)=0.89×ΔcHbtot/caHb, where caHb is the large vessel hemoglobin concentration in g/dl [13]. The NIRS measurements were carried out with the NIRO 300 and 500 (Hamamatsu Photonics, Japan). The optodes were fixed on the temporal skull, inter-optode distance was 4 cm in all measurements, and the sampling rate was 2/s. A differential path length factor of 3.85 was used [14]. Actually ΔcHbO2, ΔcHb, and ΔcCytO2 were measured, whereas ΔcHbtot and ΔCBV were calculated. 2.4. Protocol and data analysis Measurements were carried out under standardized conditions. The infants were lying in supine position in an incubator (Babytherm 8000, Dräger, Germany) during undisturbed daytime sleep of at least 2 h. When the infants had reached quiet sleep, the NIRS parameters were set to an arbitrary zero. Quiet sleep was defined by the absence of eye movements in electroocologram, absence of body movements, and regular quiet breathing. Two groups of apnea were defined whether they were associated with hypoxia or not. The hypoxia group included apnea with hypoxia, and the non-hypoxia group consisted of apnea of about the same length without hypoxia. The episodes of apnea with hypoxia were matched to episodes of apnea without associated hypoxia for duration of apnea (±25% length) and for postconceptional age. Hypoxia was defined as pulsoximetric SaO2 <80% lasting longer than 10 s. Beginning/end of cessation of breathing efforts of thorax and abdomen was taken as beginning/end of an incidence of apnea. The measurement period consisted of three phases: (a) 30 s prior to the apnea (baseline phase); (b) apnea (apnea phase); and (c) 1 min following apnea (postapnea-phase). The postapnea phase was divided into six periods, each lasting 10 s, in order to observe a dynamic course of parameter changes. In order to be included for analysis, infants had to show regular breathing during baseline and postapnea phase. If body movements or irregular breathing (e.g. short apnea, sighs) were observed, the data of the whole apnea were excluded from analysis. For all parameters mean values were calculated for each period, and for analysis of parameter changes data of apnea- and post-apnea phases 1–6 were compared to baseline phase. For SaO2 single minimum values were also calculated from stored data. The values of the HR were calculated from beat-to-beat analysis. Beneath the baseline period, the points for measurement were at the end of the apnea phase, and at 20, 40 and 60 s during postapnea phase. The time period for beat-to-beat analysis was 4 s (measurement points ±2 s), for further analysis the mean HR value over these 4 s was taken. Furthermore, behavior of etCO2 was analyzed during baseline phase, during postapnea phase 1 (first five breathing efforts after apnea) and at measurement points 20, 40 and 60 s (at each point five breathing efforts) during the postapnea phase. For analysis the mean value of five breathing efforts was taken. 2.5. Behavior of SaO2 According to the above criteria, SaO2 behavior of the two groups was ‘significantly different’, thus proving the efficacy of set criteria. In both groups SaO2 showed a significant decrease during the apnea phase and the postapnea phases 1–3. The mean SaO2 values of each phase are presented in Fig. 1. Comparing the hypoxia group to the non-hypoxia group there was a significant difference in SaO2 behavior during the apnea phase, and the postapnea phases 1 and 2 (Fig. 1). Minimum SaO2 was 74.2±1.1 (61–79)% in the hypoxia group, and 87.9±1.1 (78–97)% in the non-hypoxia group. 2.6. Data analysis All statistical analyzes of recorded data were performed using Statview 4.5® software. Values are given as mean±standard error of the mean (SEM) (range). The intergroup comparisons were made with analysis of variance for repeated measurements. The comparison of values with baseline measurements was done with the Wilcoxon ‘rank-sum’ Test. A P value of <0.05 was considered significant. 3. Results From January 1999 to June 2001 a total of 386 polysomnographic measurements were performed in preterm infants. A total number of 22 incidences of apnea fulfilled the inclusion criteria (hypoxia in association with apnea) and formed the hypoxia group. A number of 22 incidences of apnea without associated hypoxia were matched and formed the non-hypoxia group. The duration of apnea did not differ significantly: the length of apnea was 26.4±2.6 (11–53) s in the hypoxia group, and 22.8±2.6 (11–57) s in the non-hypoxia group. All polygraphic tracings of apnea that were entered in the study showed significant changes in ΔcHbtot during the apnea phase. Two patterns of cHbtot behavior were observed: a decrease during apnea (in 57%) or an increase during apnea (in 43%). Changes in cHbtot represent changes in CBV. Therefore, to enable further analysis, data were divided according to these two patterns of ΔcHbtot forming two groups, calling them ‘CBV increase’ and ‘CBV decrease’. The subdivision in the hypoxia group and the non-hypoxia group was maintained. Both increase and decrease in cHbtot were of statistical significance in the hypoxia group as well as in the non-hypoxia group. The decrease in the hypoxia group was −0.84 μmol/l (P=0.0007), and in the non-hypoxia group −1.16 μmol/l (P=0.005). The increase in the hypoxia group was +0.67 μmol/l (P=0.018), and in the non-hypoxia group +0.88 μmol/l (P=0.002). Regarding the changes in cHbtot, there was no significant difference between apnea with hypoxia and apnea without (Table 1). | | |  | | cHbtot increase (μmol/l) | cHbtot decrease (μmol/l) | |
|---|
| | Hypoxia | Non-hypoxia | Hypoxia | Non-hypoxia | |
|---|
| Apnea phase | 0.67 (±0.2) | 0.88 (±0.2) | −0.84 (±0.2) | −1.16 (±0.4) | |
| Postapnea phase 1 | 0.64 (±1.3) | 0.23 (±0.5) | −0.756 (±0.6) | −0.51 (±0.3) | |
| Postapnea phase 2 | 1.96 (±0.9) | 0.81 (±0.5) | 0.15 (±0.4) | 0.06 (±0.3) | |
| Postapnea phase 3 | 1.93 (±1.3) | 1.0 (±0.6) | 0.07 (±0.3) | 0.69 (±0.4) | |
| Postapnea phase 4 | 2.08 (±1.2) | 1.19 (±0.6) | 0.32 (±0.3) | 0.25 (±0.51) | |
| Postapnea phase 5 | 2.21 (±1.3) | 1.2 (±0.6) | 0.28 (±0.4) | 0.05 (±0.4) | |
| Postapnea phase 6 | 2.4 (±1.3) | 0.99 (±0.8) | 0.06 (±0.4) | −0.36 (±0.4) | | | | |
In the hypoxia group 15 incidences of apnea showed a decrease of CBV and seven incidences of apnea an increase of CBV. In the non-hypoxia group ten incidences of apnea showed a decrease of CBV and 12 incidences of apnea an increase of CBV. The Chi-Square Test did not show significant differences in the amount of apnea within these four different groups. Nor was there a significant difference between the four groups in regard to apnea length (Table 2). | | | | | CBV decrease | CBV increase | |
|---|
| | n | Length (s) | n | Length (s) | |
|---|
| Hypoxia | 15 | 23 | 7 | 29 | |
| Non-hypoxia | 10 | 20 | 12 | 18 | | | | |
Furthermore, we calculated ΔCBV (according to formula, see Section 2). ΔCBV in the ‘CBV increase’ group was +50 μl/100 g brain for the hypoxia group, and +47 μl/100 g brain for the non-hypoxia group. ΔCBV in the ‘CBV decrease’ group was −55 μl/100 g brain for the hypoxia group, and −62 μl/100 g brain for the non-hypoxia group. CBV showed a tendency to increase during the postapnea phase. There were not any significant differences between the hypoxia and non-hypoxia groups concerning the CBV behavior (Fig. 2). Analysis of the behavior of HR also did not show any significant difference between the hypoxia group and the non-hypoxia group. Only in the ‘CBV decrease’ group did the HR sink significantly during the apnea phase (in the hypoxia group (P=0.02) as well as in the non-hypoxia group (P=0.004)). In both groups of ‘CBV increase’ the HR showed a tendency to decrease, but the decrease was not significant (hypoxia group P=0.13, non-hypoxia group P=0.06) (see Fig. 3). The analysis of behavior of etCO2 did not show any significant differences between the hypoxia group and the non-hypoxia group. The etCO2 values showed a tendency to increase after the apnea phase; only during postapnea phase 6 was the increase significant in three of the four groups (Fig. 4). 4. Discussion In both groups there was a significant decrease of SaO2 during the apnea phase and postapnea phases 1–3. Following the set criteria, the SaO2 behavior between both groups (hypoxia/non-hypoxia) was significant different during the apnea phase and postapnea phases 1 and 2. In the hypoxia group the mean SaO2 of postapnea phase I was below 80%, although infants had already started breathing again. So the hypoxia in association with apnea criterion was met in the hypoxia group. Behavior of cHbtot during apnea always showed a significant change to baseline phase. Two patterns were observed: either an increase or a decrease of cHbtot during the apnea phase. As a consequence of this and for further analysis, two groups had to be introduced according to their pattern of cHbtot behavior (‘CBV increase’ and ‘CBV decrease’). There are several studies dealing with cHbtot behavior in association with apnea, using the NIRS technique. Livera et al. demonstrated that in most cases an arterial desaturation of a moderate degree was associated with an increase of cHbtot [4]. Because of the fact that in their study desaturation was induced to a large amount artificially by reducing the fraction of inspired oxygen, a comparison of their study to the present study is difficult. Jenni et al. described four different types of changes in cHbtot during apnea (lasting >10 s): (1) an isolated increase of cHbtot (in 12% of observed apnea); (2) an isolated decrease of cHbtot (35%); (3) no change in cHbtot (28%); and (4) a combination of an initial fall followed by an increase over the previous baseline of cHbtot (25%) (rebound-phenomenon) [3]. Urlesberger et al. described only two types of cHbtot changes in apnea lasting >15 s: they reported: (1) an increase of cHbtot (in 13% of observed apnea); and (2) an isolated decrease of cHbtot (87%) [6]. In the present study which investigates longer periods of apnea compared to Jenni et al., but apnea of similar length compared to Urlesberger et al., only two patterns of cHbtot changes were seen. However, compared to Urlesberger et al., the distribution of cHbtot behavior was more homogenous (57% decrease, 43% increase). Beneath the length of apnea, there were also methodological differences between the work of Jenni et al. and the present study. Jenni et al. [3] measured their children in prone body position whereas in the present study infants were measured in supine position. Using NIRS, Pichler et al. showed that there were body position-dependent changes in cerebral hemodynamics during apnea in preterm infants [15]. In addition, more than half of the patients of Jenni et al. received additional inspired oxygen during tracing [3], whereas in the present study additional oxygen was an exclusion criteria. The present study looked at mean values over a period, whereas Jenni et al. [3] (and Urlesberger et al. [6]) looked at minimum and maximum values using optical analysis. All these factors may have contributed to the different findings. Compared to Urlesberger et al. [6], there is definitely a difference in distribution of CBV increase and decrease. This difference might be due to the different methodological approach in parameter analysis (mean values of phases in the present study versus single data points in the study of Urlesberger et al.). Jenni et al. [3] observed a rebound phenomenon of cHbtot, the present study did not. Since Jenni et al. [3] observed this rebound phenomenon within median 46 s, it should have been observed during the postapnea phase within the present protocol. This difference is difficult to explain, but we speculate that the additional inspired oxygen in the study of Jenni et al. [3] might be a reason. In regard to the amount of cHbtot decrease, the fall of cHbtot was less in the present study. Jenni et al. [3] observed a maximum fall of cHbtot of median −4.88 μmol/l, Urlesberger et al. [6] observed a maximum fall of cHbtot of mean −2.1 μmol/l. Again, this difference should be due to the different methodological approach in parameter analysis (mean values of phases versus single data points). Arterial hypoxia produces cerebral vasodilation and increases cerebral blood flow [9]. In newborn lambs, Shadid et al. observed an increase of CBV and an increase of carotid artery flow during the first phase of hypoxia [16]. Therefore an increase of CBV during apnea with hypoxia was expected by us. But two different patterns of CBV behavior were observed, which were not correlated to hypoxia or non-hypoxia. Thus, the different pO2 behavior did not have any significant influence on behavior of CBV. Therefore, factors other than hypoxia have to be responsible for the different patterns of CBV behavior. Among these possible factors, changes in: (a) mean arterial blood pressure; (b) HR; and (c) pCO2 may have played an important role. To elucidate these factors the two groups ‘CBV increase’ and ‘CBV decrease’ had to be formed. Blood pressure has an important influence on cerebral perfusion pressure, but in healthy preterm infants blood pressure provides only limited information for evaluation of cerebral perfusion pressure due to cerebral autoregulatory mechanisms. Nevertheless, measurement of blood pressure would have been interesting in the present study. As none of the already healthy preterm infants was provided with an arterial line, only oscillometric blood pressure measurements would have been possible. But this technique was not feasible since it would have disturbed the infants’ sleep and woken them up very often, thus resulting in artifacts in the NIRS tracings. Nevertheless, Tsuji et al. demonstrated that a decrease in mean arterial blood pressure of >50% resulted only in a small, but non-significant decrease of cHbtot [17]. So, it seems unlikely that small changes of mean arterial blood pressure in healthy preterm infants had a significant impact on CBV, or even caused significantly different behavior of CBV. HR is known to have an significant influence on cerebral hemodynamics. In neonates the cardiac output depends very much on the HR, so a significant decrease in HR would be expected to cause a diminution in cerebral blood volume. Urlesberger et al. demonstrated a correlation between HR and changes in CBV during episodes of periodic breathing in preterm infants [11]. Livera et al. stated that CBV sank in association with bradycardia [4]. We saw a significant decrease of HR in the subgroup ‘CBV decrease’. In subgroup ‘CBV increase’ HR did not show a significant decrease, but a tendency to fall. We speculate that the significant drop in HR may have influenced the decrease in CBV, regardless of the presence of hypoxia. The study of Livera et al. [4] supports this speculation. Changes in pCO2 have been proved to have a strong influence on cerebral circulation [7], [8]. But since the cerebral blood circulation reactivity in response to pCO2 changes is a matter of minutes, pCO2 changes in association with apnea of a length of ∼25 s should theoretically have no influence on CBV during the apnea itself, but increased pCO2 levels may have an influence on cerebral circulation within a certain period after the apnea [8]. In accordance with this theory, pCO2 values only showed significant changes during the last periods of the postapnea phase. This may explain the tendency of CBV to increase during the postapnea phase in all groups. During apnea with hypoxia there is a very complex situation of partly counteracting mechanisms: (a) hypoxia potentially inducing an increase in CBV and cerebral blood flow; (b) a fall in HR inducing a decrease in CBV; (c) a pCO2 increase inducing an increase in CBV after some time; and (d) apnea with a consecutive rise of negative intrathoracic pressure to zero level with impairment of cerebral venous outflow inducing an increase in CBV. These complex and counteracting mechanisms may be responsible for: (a) the difficulties in interpretation of CBV behavior; and (b) for the small amount of changes in CBV. The change of about ±50 μl/100 g brain reflects a change in CBV of approximately ±2% (considering normal values of 2 ml/100 g brain in preterm infants [18]). Whether there is an increase or decrease of CBV in association with apnea cannot be predicted as long as the underlying mechanisms and their time course are still not completely understood. In conclusion, the present study observed significant changes of CBV in association with apnea, but there was no difference in CBV behavior with respect to whether apnea was associated with hypoxia (to the described extent), or not. Hypoxia in association with apnea alone was no trigger for different CBV behavior. In all groups the ΔCBV was within the range of ±2% of normal values. It remains unclear which regulatory mechanisms are responsible for the two observed patterns of ΔCBV during apnea. In the present study only HR showed a significantly different behavior in association with increase or decrease of CBV, but the significance was not very strong. Acknowledgements The authors thank Evelyn Ziehenberger for their support in the realization of this study. 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PII: S0387-7604(02)00121-3 doi:10.1016/s0387-7604(02)00121-3 © 2002 Elsevier Science B.V. All rights reserved. | |
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