Fetal Breathing Movements Research Articles

Scaling analysis of paces of fetal breathing, gross-body and extremity movements

Using detrended fluctuation analysis (DFA), we studied the scaling properties of the time instances (occurrence) of the fetal breathing, gross-body, and extremity movements scored on a second by second basis from the recorded ultrasound measurements of 49 fetuses. The DFA exponent α of all the three movements of the fetuses varied between 0.63 and 1.1. We found an increase in α obtained for the movement due to breathing as a function of the gestational age while this trend was not observed for gross-body and extremity movements. This trend was argued as the indication of the maturation of lung and functional development of respiratory aspect of the fetal central nervous system. This result may be useful in discriminating normal fetuses from high-risk fetuses.

Maternal Breath-Holding and the Valsalva Maneuver: Methods to Overcome Fetal Breathing Movements During Doppler Sonography

Fetal breathing movements (FBM) hinder Doppler measurements in the fetus. The aim of the present study was to establish whether FBM are overcome by the mother holding her breath for a few seconds or performing the Valsalva maneuver (VM). This prospective study included a group of 120 consecutive patients showing FBM. In 78 patients (65%), FBM were observed only at the beginning of the examination and then stopped spontaneously. In the other 42 patients, FBM were still present during and at the end of the general examination. These patients were considered for the evaluation. In a first step, the mother was asked to hold her breath for 5 s. If FBM continued, the procedure was repeated. If this also failed, the Valsalva maneuver was performed. In the presence of fetal apnea, flow velocity measurements were taken from the umbilical artery. Nine patients (21%) halted FBM with the first attempt at maternal breath-holding, four patients (10%) with the second attempt and 22 patients (52%) on using the VM. FBM was arrested within a maximum of 94 s after breath-holding or the VM. No reaction to any of the procedures was observed in seven patients (17%). Breath-holding alone or in combination with the Valsalva maneuver has been shown to be effective in overcoming the problem of FBM during prenatal Doppler examination in most cases. (E-mail: gabriele.meyberg-solomayer@med.uni-tuebingen.de)

Movimentos respiratórios fetais em gestações com diabetes mellitus pré-gestacional

OBJETIVO: analisar o padrao dos movimentos respiratorios fetais (MRF) em gestantes diabeticas no terceiro trimestre de gestacao. METODOS: foram avaliadas 16 gestantes com diabetes mellitus pre-gestacional e 16 gestantes normais (grupo controle), com os seguintes criterios de inclusao: gestacao unica entre a 36a e a 40a semana, ausencia de outras doencas maternas e ausencia de anomalias fetais. No perfil biofisico fetal (PBF), foram avaliados os parâmetros: frequencia cardiaca fetal, MRF, movimentos corporeos fetais, tonus fetal e indice de liquido amniotico. Os MRF foram avaliados por 30 minutos, periodo em que o exame foi integralmente gravado em fita de video VHS para posterior analise do numero de episodios de MRF, do tempo de duracao dos episodios e do indice de movimentos respiratorios fetais (IMR). O IMR foi calculado pela formula: (intervalo de tempo com MRF/tempo de observacao) x 100. No inicio e no final do PBF foi dosada a glicemia capilar materna. Os resultados foram analisados pelo teste de Mann-Whitney U e teste exato de Fisher, adotando-se nivel de significância de 5%. RESULTADOS: as glicemias demonstraram media significativamente superior nas diabeticas (113,3±35,3 g/dL) em relacao as gestantes normais (78,2±14,8 g/dL, p<0,001). A media do indice de liquido amniotico mostrou-se maior no grupo das gestantes diabeticas (15,5±6,4 cm) quando comparado aos controles (10,6±2,0 cm; p=0,01). A media do numero de episodios de MRF foi superior nas diabeticas (22,6±4,4) em relacao aos controles (14,8±2,3; p<0,0001). A media do IMR nas diabeticas (54,6±14,8%) foi significativamente maior do que no grupo controle (30,5±7,4%; p<0,0001). CONCLUSOES: os maiores valores glicemicos podem estar associados a diferente padrao nos movimentos respiratorios de fetos de maes diabeticas. A utilizacao deste parâmetro do PBF, na pratica clinica, deve ser considerada de forma criteriosa nas gestantes diabeticas.

Automatic detection of ultrasonic Doppler signal episodes resulting from fetal breathing movements

A method for automatic detection of fetal breathing movements has been proposed, based on the time-frequency structure of the corresponding continuous wave ultrasonic Doppler signals. The method uses spectral analysis of the envelope of the directional Doppler signal and cross-correlation analysis of both directional envelopes. Detection rule comprises the following criteria: presence of the peak in the envelope spectrum and of the adequate signal level in the frequency range corresponding to the fetal breathing rhythm, the peak value and the position limits of the peak of the cross-correlation coefficient of the both directional envelopes. The effect of the criteria setting on the rule performance and the tradeoff between the specificity and sensitivity was investigated. The rule is most sensitive to the threshold value of the cross-correlation coefficient of the envelopes. The limits of the position of this peak are crucial for the distinction between the breathing episodes and hiccups. The optimal settings of the criteria, resulting in average sensitivity and specificity exceeding, respectively, 0.70 and 0.80, are proposed.

Prediction and Prevention of Abnormal Antenatal Lung Growth

Pulmonary hypoplasia, the result of abnormal antenatal lung growth, occurs as a primary anomaly or more usually the consequence of disorders resulting in reduction of amniotic fluid volume, intra-thoracic space or fetal breathing movements. Two dimensional (2D) ultrasound examination yields useful information on amniotic fluid volume and the presence of congenital abnormalities associated with pulmonary hypoplasia. Assessment of the thoracic or lung size by 2D ultrasound examination, is insufficiently specific, but a very low lung to head ratio predicts a fatal outcome in fetuses with congenital diaphragmatic hernia (CDH). Three-D ultrasound examination provides information on fetal lung volume prior to 34 weeks of gestation but can be inaccurate if there is oligohydramnios. Magnetic resonance imaging is expensive and has limited patient acceptability. Antenatal interventions attempted to prevent pulmonary hypoplasia include amnioinfusion, which can facilitate ultrasound examination, but only temporarily relieves oligohydramnios. Thoraco-amniotic shunting results in effective drainage of pleural effusions, facilitating resuscitation, but is usually performed too late in pregnancy to influence lung growth. In utero surgical repair of CDH has been attempted, but a more promising technique is obstruction of the normal egress of fetal lung fluid by placing a balloon in the trachea. Keywords: Pulmonary hypoplasia, lung growth, congenital diaphragmatic hernia, oligohydramnios, ultrasound, magnetic resonance imaging

Quantification of fetal heart rate regularity using symbolic dynamics

Fetal heart rate complexity was examined on the basis of RR interval time series obtained in the second and third trimester of pregnancy. In each fetal RR interval time series, short term beat-to-beat heart rate changes were coded in 8 bit binary sequences. Redundancies of the 2(8) different binary patterns were reduced by two different procedures. The complexity of these sequences was quantified using the approximate entropy (ApEn), resulting in discrete ApEn values which were used for classifying the sequences into 17 pattern sets. Also, the sequences were grouped into 20 pattern classes with respect to identity after rotation or inversion of the binary value. There was a specific, nonuniform distribution of the sequences in the pattern sets and this differed from the distribution found in surrogate data. In the course of gestation, the number of sequences increased in seven pattern sets, decreased in four and remained unchanged in six. Sequences that occurred less often over time, both regular and irregular, were characterized by patterns reflecting frequent beat-to-beat reversals in heart rate. They were also predominant in the surrogate data, suggesting that these patterns are associated with stochastic heart beat trains. Sequences that occurred more frequently over time were relatively rare in the surrogate data. Some of these sequences had a high degree of regularity and corresponded to prolonged heart rate accelerations or decelerations which may be associated with directed fetal activity or movement or baroreflex activity. Application of the pattern classes revealed that those sequences with a high degree of irregularity correspond to heart rate patterns resulting from complex physiological activity such as fetal breathing movements. The results suggest that the development of the autonomic nervous system and the emergence of fetal behavioral states lead to increases in not only irregular but also regular heart rate patterns. Using symbolic dynamics to examine the cardiovascular system may thus lead to new insight with respect to fetal development.

The Actifetus System: A Multidoppler Sensor System for Monitoring Fetal Movements

Fetal heart rate (FHR) monitoring is a crucial part of monitoring at-risk pregnancies and labor. Its aim is to detect any abnormalities that might indicate acute fetal distress and a need for rapid treatment to avoid death or serious sequelae, including cerebral handicap. The use of fetal biophysical profiles in high-risk pregnancies (gravidic hypertension, in utero infection, etc.) helps to distinguish healthy fetuses from those with chronic conditions. Fetal biophysical profile scores have been developed that integrate five biophysical parameters, one of which is derived from the FHR. The major parameters detected are the rate of fetal movements, fetal tone, fetal breathing movement and amniotic fluid volume. All of those parameters except FHR are obtained by prolonged echographic observation and cannot be used routinely. We developed in this study a new multigate multitransducer pulsed Doppler system for survey of fetal behavior. Fast Fourier transform and autocorrelation function have been used for processing and analyzing ultrasonic Doppler signals generated by fetal movements. Several parameters are analyzed in each of the 12 × 5 = 60 Doppler gates: amplitude of signals reflected by moving fetal structures, velocity, direction and amplitude of displacement of fetal structure (heart, chest, limbs). From these parameters it is possible to calculate FHR and characterize fetal activity. Preliminary in vivo results obtained in 15 pregnant women (30 to 36 wk) are very encouraging but they have yet to be confirmed in future studies. These results also demonstrate the advantages of transducers designed for improved fetal movement detection. The algorithms needs to be precise enough to allow the Actifetus system to function in real time. We now have at our disposal some algorithms that succeed in quantifying FHR and fetal movements with a signal from a given sensor at a given depth. This study confirms the feasibility of monitoring fetal movements by the Actifetus system and demonstrates the importance of the characterization of fetal rhythms (and fetal behavior). The Actifetus system will serve as a new mean for studying fetal response to environment and detecting anomalies related to fetal suffering. (E-mail: ali.kribeche@med.univ-tours.fr)

16th World Congress on Ultrasound in Obstetrics and Gynecology, 3–7 September 2006, London, UK: presentations and awards

16^th World Congress on Ultrasound in Obstetrics and Gynecology, 3–7 September 2006, London, UK: presentations and awards

BIOPHYSICAL SCORE

A pregnancy is defined as high risk when there is a likelihood of anadverse outcome to the woman and or her baby that is greater than the incidence of that outcome in the generalpregnant population. Objectives: To determine the efficacy and predictive value of biophysical profile in detectingperinatal outcome. Design: Observational study. Setting: Obstetrics and Gynaecology department, PNS SHIFA KarachiPeriod: From February 2003 to October 2003. Patients and Methods: The study was carried on 100 randomlyselected high risk pregnant patients who reported to gynae OPD or were referred from different armed forces hospitalsfrom all over sindh . Manning’s biophysical profile excluding nonstress test and including only ultrasound basedparameters were employed for fetal screening ( BPS 8/8). These parameters include four variables i.e fetal breathingmovement, fetal tone, fetal movements, and amniotic fluid volume. Nonstress test and Doppler studies were used asbackup tests where biophysical profile was abnormal. All cases selected were admitted in the hospital and each hadan admission biophysical profile followed by subsequent monitoring. Parameters for abnormal perinatal outcome includefetal distress in labour, five minute apgar score less than 7/10, admission of newborn to intensive care unit and stillbirthor neonatal death. The result of last biophysical profile is compared with perinatal outcome. For statistical analysis thepredictive value, specificity and sensitivity are used to determine the ability of biophysical profile to predict an abnormalperinatal outcome. Results: Out of 100 cases 92 had a normal biophysical profile in the last scan of 8/8. 90 cases hada normal perinatal outcome with A/S &gt; 7/10. In two cases A/S at 1 and 5 minute is &lt; 7/10 with one baby shifted tonursery for delayed cry. 08 cases had an abnormal biophysical profile with scores of 4/8 and 2/8. There was one falsepositive who showed abnormal biophysical profile but baby was born with an A/S of 8/10 at 05 minutes. There was noneonatal death in this study group. The sensitivity of biophysical profile was 77.7%, specificity 98.90%. predictive valuefor a positive test was 87.5%, predictive value for a negative test was 97.8%. Conclusion: Biophysical profile is highlyaccurate and reliable test of diagnosing fetal status.

CFTR gene therapy, a method to rescue lung hypoplasia in congenital diaphragmatic hernia?

despite progress in neonatal care and despite changing concepts in treatment in the recent years, the mortality rate of infants with congenital diaphragmatic hernia (CDH) remains high ([20][1]). Pulmonary hypoplasia and vascular alterations associated with CDH have tremendous postnatal functional

Increases in lung expansion alter pulmonary hemodynamics in fetal sheep

Prolonged increases in fetal lung expansion stimulate fetal lung growth and development, but the effects on pulmonary hemodynamics are unknown. Our aim was to determine the effect of increased fetal lung expansion, induced by tracheal obstruction (TO), on pulmonary blood flow (PBF) and vascular resistance (PVR). Chronically catheterized fetal sheep (n = 6) underwent TO from 120 to 127 days of gestational age (term approximately 147 days); tracheas were not obstructed in control fetuses (n = 6). PBF, PVR, and changes to the PBF waveform were determined. TO significantly increased lung wet weight compared with control (166.3 +/- 20.2 vs. 102.0 +/- 18.8 g; P < 0.05). Despite the increase in intraluminal pressure caused by TO (5.0 +/- 0.9 vs. 2.4 +/- 1.0 mmHg; P < 0.001), PBF and PVR were similar between groups after 7 days (TO 28.1 +/- 3.2 vs. control 34.1 +/- 10.0 ml.min(-1).100 g lung wt(-1)). However, TO markedly altered pulmonary hemodynamics associated with accentuated fetal breathing movements, causing a reduction rather than an increase in PBF at 7 days of TO. To account for the increase in intraluminal pressure, the pressure was equalized by draining the lungs of liquid on day 7 of TO. Pressure equalization increased PBF from 36.8 +/- 5.2 to 112.4 +/- 22.8 ml/min (P = 0.01) and markedly altered the PBF waveform. These studies provide further evidence to indicate that intraluminal pressure is an important determinant of PBF and PVR in the fetus. We suggest that the increase in PBF associated with pressure equalization following TO reflects an increase in growth of the pulmonary vascular bed, leading to an increase in its cross-sectional area.

Factors Influencing Adenovirus-Mediated Airway Transduction in Fetal Mice

Intra-amniotic injection of adenovirus allows transduction of the fetal airways following natural fetal breathing movements. This administration method is promising for use in gene therapy for cystic fibrosis and other diseases for which the main target for exogenous gene expression is the lung. Here we have investigated factors that may affect the efficacy of gene transfer to the murine fetal lung. We examined marker compound distribution and transgene expression (from a first-generation adenoviral vector) at different stages of development. This demonstrated that fetal breathing movements at 15-16 days of gestation are of sufficient intensity to carry marker/vector into the fetal lungs. These movements can be significantly stimulated by the combination of intra-amniotic theophylline administration and postoperative exposure of the dam to elevated CO(2) levels. However, the most important factor for efficient and consistent pulmonary transgene delivery is the dose of adenoviral vector used, as both the degree of transduction and the percentage of lungs transduced increases with escalating viral dose.

Maternal Fluoxetine Infusion Does Not Alter Fetal Endocrine and Biophysical Circadian Rhythms in Pregnant Sheep

Depression during pregnancy is frequently treated with the selective serotonin reuptake inhibitor (SSRI), fluoxetine (FX), commonly known as Prozac (Eli Lilly & Co, Indianapolis, IN). FX potentiates serotoninergic neurotransmission and serotonin has been implicated in the regulation of circadian rhythms. We have therefore investigated the effect of chronic administration of FX on maternal and fetal circadian rhythms in sheep. Following an initial bolus dose of 70 mg FX, an 8-day continuous infusion of FX (n = 11, 98.5 microg/kg x d) was performed. Controls (n = 13) were treated with sterile water vehicle only. Maternal and fetal plasma melatonin and prolactin concentrations were determined every 3 hours for 24 hours and then every 6 hours for 24 hours beginning on the fourth day of infusion. FX treatment did not alter either the basal or circadian rhythms of either maternal or fetal plasma melatonin and prolactin concentrations. Fetal cardiovascular and behavioral state parameters were measured continuously. While the incidence of low-voltage (LV) electrocortical (ECOG) activity was significantly reduced in fetuses in the FX group, there was no effect of FX on the diurnal rhythms in fetal arterial pressure, heart rate, breathing movements, or behavioral state. These results show that maternal FX treatment does not result in significant alterations in maternal and fetal hormonal and behavioral circadian rhythms.

Congenital diaphragmatic hernia: A retinoid‐signaling pathway disruption during lung development?

Congenital diaphragmatic hernia (CDH) usually occurs sporadically. The prognosis remains poor, with a 50% perinatal mortality rate. Most deaths result from hypoxemia due to lung hypoplasia and abnormal development of pulmonary vasculature that results in persistent pulmonary hypertension. Our current understanding of the pathogenesis of CDH is based on an assumption linking herniation of abdominal viscera into the thorax with compression of the developing lung. Pulmonary hypoplasia, however, can also result from reduced distension of the developing lung secondary to impaired fetal breathing movements. Moreover, a nitrofen-induced CDH model shows that lung hypoplasia precedes the diaphragmatic defect, leading to a "dual-hit hypothesis." Recent data reveal the role of a retinoid-signaling pathway disruption in the pathogenesis of CDH. We describe the clinical and epidemiological aspects of human CDH, the metabolic and molecular aspects of the retinoid-signaling pathway, and the implications of retinoids in the development of the diaphragm and the lung. Finally, we highlight the existing links between CDH and disruption of the retinoid-signaling pathway, which may suggest an eventual use of retinoids in the treatment of CDH.

Perinatal development of respiratory motoneurons

Breathing movements require the coordinated recruitment of cranial and spinal motoneurons innervating muscles of the upper airway and ribcage. A significant part of respiratory motoneuron development and maturation occurs prenatally to support the generation of fetal breathing movements in utero and sustained breathing at birth. Postnatally, motoneuron properties are further refined and match changes in the maturing respiratory musculoskeletal system. In this review, we outline developmental changes in key respiratory motoneuronal populations occurring from the time of motoneuron birth in the embryo through the postnatal period. We will also bring attention to major deficiencies in the current knowledge of perinatal respiratory motoneuron development. To date, our understanding of processes occurring during the prenatal period comes primarily from analysis of phrenic motoneurons (PMNs), whereas information about postnatal development derives largely from studies of PMN and hypoglossal motoneuron properties.

Transient Loss of the Diurnal Rhythms of Fetal Movements, Heart Rate, and Its Variation after Maternal Betamethasone Administration

Antenatal betamethasone administration to enhance fetal lung maturation is associated with transient reductions in fetal heart rate (FHR) variation, breathing, and body movements 2 d after the first dose (d 2). This study examines whether steroid administration affects the natural diurnal rhythms of fetal variables. Sixteen women at 27-32 wk of gestation received two doses of betamethasone 24 h apart. One-hour recordings of FHR, breathing, and body movements were made in the morning, afternoon, and evening of d 2, and again in the morning of d 3. Repeat recordings were obtained at 4-6 d later from 9/16 women. Maternal blood samples were obtained with each recording to determine ACTH and cortisol. No diurnal rhythm was present for FHR, FHR variation, breathing, and body movements on d 2. This resulted from suppression of the expected natural rise in body and breathing movements, and heart rate variation in the course of the day. Suppression of the diurnal rhythm of body movements depended on gestation (R = -0.89; p < 0.01). All variables showed diurnal rhythms 4-6 d later. Maternal ACTH and cortisol diurnal rhythms were completely suppressed on d 2. Four to six days later, the normal diurnal pattern was resumed, although absolute levels of ACTH and cortisol were still suppressed. We conclude that maternal betamethasone administration transiently abolishes the fetal diurnal rhythms of heart rate and its variation, breathing, and body movements.

Perinatal maturation of the respiratory rhythm generator in mammals: from experimental results to computational simulation

The survival of neonatal mammals requires a correct function of the respiratory rhythm generator (RRG), and therefore, the processes that control its prenatal maturation are of vital importance. In humans, lambs and rodents, foetal breathing movements (FBMs) occur early during gestation, are episodic, sensitive to bioamines, central hypoxia and inputs from CNS upper structures, and evolve with developmental age. In vitro, the foetal rodent RRG studied in preparations where the upper CNS structures are lacking continuously produces a rhythmic command, which is sensitive to hypoxia and bioaminergic inputs. The rhythm is slow with variable periods 4 days before birth. It becomes faster 2 days before birth, similar to the postnatal rhythm. Compelling evidence suggests that a region of the RRG called the preBötzinger complex (PBC) contains respiratory pacemaker neurones which play a primary role in perinatal rhythmogenesis. Although the RRG functions during early gestation, no pacemakers are found in the putative PBC area and its electrical stimulation and lesion do not affect the early foetal rhythm. To know whether the early foetal and perinatal rhythms originate from either pacemaker neurones or network connection properties, and to know which maturational processes might explain the appearance of PBC pacemakers and the rhythm increase during perinatal development, we computationally modelled maturing RRG. Our model shows that both network noise and persistent sodium conductance are crucial for rhythmogenesis and that a slight increase in the persistent sodium conductance can solve the pacemaker versus network dilemma in a noisy network.

Analysis of fetal breathing movements at 30–38 weeks of gestation

This study reports the changes in patterns of fetal breathing movements recorded with a photogrammetric method in three successive periods of gestation. Respiratory movements were studied in fetuses of 28 healthy women with uncomplicated pregnancies of 30-38 weeks of gestation. Women were divided into three groups according to gestational age of the fetus: 30-32 weeks, 7 fetuses; 33-36 weeks, 9 fetuses; and 37-38 weeks, 12 fetuses. Sonographic images of the fetuses were recorded on videotape, digitized (1 image per 0.12 s) and analyzed with specially developed software. The proportion of fetuses in each age group for which movements were detectable was similar in all three groups, as was the frequency of movements. Duration of a complete respiratory cycle, the inspiratory phase and the expiratory phase tended to be shorter at 33-36 weeks of gestation than in younger and older fetuses. Fetuses in the 30-32-week group had slower breathing rates than fetuses in the two older groups. The photogrammetric technique revealed differences in some patterns of fetal breathing movements between weeks 30-32, 33-36 and 37-38 of gestation. The data provide a sound basis for relating changes in fetal breathing movements with physiological and anatomical changes that occur as the respiratory system matures.

Undesired effects of steroids during pregnancy

Antenatal corticosteroid administration for enhancing fetal lung maturity can be expected to induce negative maternal and fetal side-effects. Maternal short-term effects after multiple courses of corticosteroids are an increase of infections and a higher incidence of endometritis and chorionamnionitis in patients with premature rupture of membranes. A single dose of corticosteroid induces an increase in the count of maternal white blood cells and metabolic effects such as the augmentation of amino acid concentration and of fasting glucose levels in maternal plasma. Negative fetal effects of antenatal corticosteroids are a reduction of fetal body and breathing movements and a reduction of fetal heart rate variation, without any changes in Doppler waveform patterns of fetoplacental vessels. It has been suggested that a multiple course of corticosteroids antenatally might induce negative effects on fetal intrauterine growth and on neonatal birth weight. In addition, multiple courses are associated with an increased risk of early-onset neonatal sepsis.

Influence of fetal breathing movements on pulmonary hemodynamics in fetal sheep.

During fetal development, pulmonary vascular resistance (PVR) is high, and, as a result, blood flow through the fetal lungs is low. Although PVR markedly decreases at the time of birth, the factors that regulate pulmonary blood flow (PBF) and PVR before and immediately after birth are not clear. Our aim was to examine the relationship between episodes of fetal breathing movements (FBM) and pulmonary hemodynamics during late gestation to further understand the relationship among lung luminal volume, phasic changes in intrapulmonary pressure, and PVR before birth. In chronically catheterized fetal sheep (120-128 d gestation; n = 5; term approximately 147 d), PBF and PVR were measured during periods of FBM and apnea. Episodes of FBM were divided into periods of accentuated (amplitude of >3.5 mm Hg change in tracheal pressure) and nonaccentuated periods of FBM. During accentuated episodes of FBM, mean PBF was increased to 159.5 +/- 23.4% (p < 0.0025) of the preceding apneic period and was associated with a 19.1 +/- 5.2% reduction in PVR. In addition, during accentuated episodes of FBM, the retrograde flow of blood through the left pulmonary artery was reduced to 90.1 +/- 1.0% of the preceding apneic period, which most likely contributed to the increase in mean PBF at this time. Although a change in PBF and PVR could not be detected during nonaccentuated FBM, compared with the preceding apneic period, PBF was linearly and positively correlated with the amplitude (change in pressure) of FBM. We conclude that PVR is decreased and PBF is increased during accentuated episodes of FBM, possibly as a result of phasic reductions in intrapulmonary pressures.