Cross-System Integration of Respiration and Deglutition: Function, Treatment, and Future Directions.

Swallowing occurs preferentially in the expiratory phase of the quiet breathing cycle and at mid-to-low tidal volume. This coordinative pattern imparts important biomechanical advantages to swallowing and airway protection and facilitate laryngeal elevation, laryngeal vestibular and vocal fold closure, and cricopharyngeal sphincter opening. This preferred coordinative relationship between breathing and swallowing is impaired in a variety of patient populations, including head and neck cancer survivors with dysphagia. We developed a training protocol to re-establish more optimal phasing of swallowing with breathing in these patients with striking outcomes, including reduced swallowing physiological impairments and improved airway protection. This motivated us to continue to refine and expand this training protocol and develop new assistive technologies for swallowing monitoring outside of the lab. In this review, we highlight the origins of our optimal respiratory-swallowing coordination hypothesis, describe the biomechanical advantages it provides, carefully describe our training protocol and findings, and chart a course for the next phase of this work. Our overall goal is to harness technology combined with carefully constructed learning paradigms to improve the lives of patients with impaired respiratory-swallowing coordination consequent to a variety of pathologies including head and neck cancer and degenerative neurological conditions such as Parkinson's disease.

Physiological measures of mother-infant interactional synchrony.

Mother-infant interactional synchrony has been hypothesized to be crucial for the development of many key neurodevelopmental behaviors in infants, including speech and language. Assessing synchrony is challenging because many interactive behaviors may be subtlety, if at all, observable in overt behaviors. Physiological measures, therefore, may provide valuable physiological/biological markers of mother-infant synchrony. We have developed a multilevel measurement platform to assess physiological synchrony, attention, and vocal congruency during dynamic face-to-face mother-infant interactions. The present investigation was designed to provide preliminary data on its application in a group of 10 mother-infant dyads (20 subjects) ranging in age from 7 to 8.5 months at the time of the experimentation. Respiratory kinematics, heart rate, and vocalization were recorded simultaneously from mothers and infants during nonstructured, face-to-face interactions. Novel statistical methods were used to identify reliable moments of synchrony from cross-correlated, mother-infant respiration and to tag infant attention from heart rate deceleration. Results revealed that attention, vocal contingency, and respiratory synchrony are temporally clustered within the dyad interaction. This temporal alignment is consistent with the notion that biological synchrony provides a supportive platform for infant attention and mother-infant contingent vocalization.

Effect of Single-Use, Laser-Cut, Slow-Flow Nipples on Respiration and Milk Ingestion in Preterm Infants.

PURPOSE: Single-use, laser-cut, slow-flow nipples were evaluated for their effect on respiration and milk ingestion in 13 healthy preterm infants (32.7-37.1 weeks postmenstrual age) under nonlaboratory, clinical conditions. METHOD: The primary outcomes of minute ventilation and overall milk transfer were measured by using integrated nasal airflow and volume-calibrated bottles during suck bursts and suck burst breaks during slow-flow and standard-flow nipple bottle feedings. Wilcoxon signed-ranks tests were used to test the effect of nipple type on both outcomes. RESULTS: Prefeeding minute ventilation decreased significantly during suck bursts and returned to baseline values during suck burst breaks across both slow-flow and standard-flow nipples. No differences were found in minute ventilation (p > .40) or overall milk transfer (p = .58) between slow-flow and standard-flow nipples. CONCLUSIONS: The lack of difference in primary outcomes between the single-use slow-flow and standard-flow nipples may reflect variability in nipple properties among nipples produced by the same manufacturer. Future investigations examining the effect of both single-use and reusable nipple products are warranted to better guide nipple selection during clinical care.

Prior History of Feeding-Swallowing Difficulties in Children With Language Impairment.

PURPOSE: This study updated and extended our previous investigation (Malas et al., 2015) of feeding-swallowing difficulties and concerns (FSCs) in children with language impairments (LI) by using more stringent inclusion criteria and targeting children earlier in the care delivery pathway. METHOD: Retrospective analyses were performed on the clinical files of 29 children (average age: 60 months, SD = 9.0) diagnosed as having LI using standardized testing, nonstandardized testing and final speech-language pathologist judgment. The files of children born prematurely or with a history of anatomical, structural, neurodevelopmental, cognitive, sensory, motor, or speech disorders were excluded. Literature-based indicators were used to determine the prevalence of difficulties in sucking, food transition, food selectivity, and salivary control. Values were compared with the general population estimate of Lindberg et al. (1992). RESULTS: A significantly higher percentage of histories of FSCs (48%) were found in the files of children with LI when compared with the population estimate (χ2 = 13.741, df = 1, p < .001). Difficulties in food transition (31%) and food selectivity (14%) were the most frequent. Data confirm and extend our previous findings and suggest that a previous history of FSCs may characterize children with LI early in their care delivery pathway.

Feeding-swallowing difficulties in children later diagnosed with language impairment.

AIM: The aim of this retrospective study was to assess the relationship between feeding-swallowing difficulties (FSDs) and later language impairments in children. METHOD: Retrospective analyses were carried out using the clinical files of 82 children with language impairments from a large urban rehabilitation center. Two subgroups of these children were established: children with motor impairments, referred to as the language impairment with motor impairment ('LI+MI') subgroup (n=23, mean age 4y 6mo, SD 8.7mo), and children without motor impairments, referred to as the language impairment without motor impairment ('LI-MI') subgroup (n=59, mean age 5y, SD 8mo). The prevalence of food selectivity, difficulties in sucking, salivary control issues, and food transition difficulties was extracted. Data were compared with a general population estimate of FSDs. RESULTS: FSDs were documented in 62% of the clinical files; 87% of these files were from the LI+MI subgroup and 53% were from the LI-MI subgroup. Among each subgroup of children with language impairments, the prevalence of FSDs was significantly higher than the general population estimate of 20% (LI+MI:χ(2) =55.965, df=1, p<0.001; LI-MI: χ(2) =32.807, df=1, p<0.001). Furthermore, the prevalence of FSDs was significantly higher in children with language impairments and motor impairments than in those with language impairments but without motor impairments (χ(2) =6.936, df=1, p<0.01). Both food transition difficulties (χ(2) =14.99, df=1, p<0.001) and salivary control issues (χ(2) =5.02, df=1, p=0.02) were more frequent in the LI+MI subgroup than in the LI-MI subgroup. Combinations of two or more FSDs were also more frequent in the LI+MI subgroup than in the LI-MI subgroup (χ(2) =4.19, df=1, p=0.04). INTERPRETATIONS: These findings suggest that early FSDs may be used as a potential marker for language impairment. However, larger prospective studies are needed to confirm this.

Innovative technology for the assisted delivery of intensive voice treatment (LSVT®LOUD) for Parkinson disease.

PURPOSE: To assess the feasibility and effectiveness of a newly developed assistive technology system, Lee Silverman Voice Treatment Companion (LSVT(®) Companion™, hereafter referred to as "Companion"), to support the delivery of LSVT(®)LOUD, an efficacious speech intervention for individuals with Parkinson disease (PD). METHOD: Sixteen individuals with PD were randomized to an immediate (n = 8) or a delayed (n = 8) treatment group. They participated in 9 LSVT LOUD sessions and 7 Companion sessions, independently administered at home. Acoustic, listener perception, and voice and speech rating data were obtained immediately before (pre), immediately after (post), and at 6 months post treatment (follow-up). System usability ratings were collected immediately post treatment. Changes in vocal sound pressure level were compared to data from a historical treatment group of individuals with PD treated with standard, in-person LSVT LOUD. RESULTS: All 16 participants were able to independently use the Companion. These individuals had therapeutic gains in sound pressure level, pre to post and pre to follow-up, similar to those of the historical treatment group. CONCLUSIONS: This study supports the use of the Companion as an aid in treatment of hypokinetic dysarthria in individuals with PD. Advantages and disadvantages of the Companion, as well as limitations of the present study and directions for future studies, are discussed.

Oral and nonoral sensorimotor interventions facilitate suck-swallow-respiration functions and their coordination in preterm infants.

BACKGROUND: Preterm infants are at high risk of encountering oral feeding difficulties. Early sensorimotor interventions may improve oral feeding skills in preterm infants. AIM: To further explore the effects of an oral (O), tactile/kinesthetic (T/K), and combined (O+T/K) sensorimotor intervention on preterm infants' nutritive sucking, swallowing and their coordination with respiration. STUDY DESIGN: Seventy-five infants (29 [0.3, standard error of mean, SEM] weeks gestation, 49 males/26 females) were randomly assigned to an O group involving sensorimotor input to the oral structures; a T/K group involving sensorimotor input to the trunk and limbs; a combined (O+T/K) group; and a control group. OUTCOME MEASURES: Stage of sucking, suction and expression amplitudes (mmHg), suck-swallow ratio, stability of suck-swallow interval, and swallow-respiration patterns. RESULTS: The O group had significantly more advanced sucking stages, and greater suction and expression amplitudes than controls [p≤0.035, effect size (ES) >0.6]. The suck-swallow ratio and stability of suck-swallow intervals did not significantly differ among groups (p≥0.181, ES≤0.3). The three interventions led to fewer swallows bracketed by prolonged respiratory pauses compared to controls (pause-swallow-pause, p≤0.044, ES≥0.7). The T/K and combined (O+T/K) groups had greater occurrence of swallows bracketed by expiration than the control and O groups (expiration-swallow-expiration, p≤0.039, ES≥0.3). CONCLUSION: The O intervention enhanced specific components of nutritive sucking. All three interventions resulted in improved swallow-respiration coordination. Sensorimotor interventions have distributed beneficial effects that go beyond the specific target of input.

Significance of nonrespiratory airflow during swallowing.

This study was designed to further our understanding of a potentially significant clinical event of negative nasal airflow near the end of the respiratory pause (inhibition) to accommodate swallowing. This negative flow, referred to as "SNIF," or swallow noninspiratory flow, occurs at the onset of airway reestablishment at the conclusion of the oropharyngeal swallow. Using simultaneous digital video fluoroscopic and nasal respiratory airflow recordings on 82 healthy adults (21-97 years old), the objectives of this study were to determine (1) the frequency of occurrence of SNIF during a 5-ml natural cup-drinking task, (2) differences in SNIF occurrence by age group, and (3) the temporal relationship between SNIF and other swallowing events. Results revealed that for most participants SNIF was observed in both swallowing trials. There was a statistically significant difference in SNIF occurrence by age category, with SNIF observed less frequently in the oldest participants. The peak onset of SNIF is closely related to the first release of contact between the soft palate and tongue base with the posterior pharyngeal wall and opening of the laryngeal vestibule. Based on this, and in agreement with previous investigators, we suggest that this negative flow may be related to a partial vacuum established by the relaxation of pharyngeal contraction near the conclusion of the pharyngeal swallow. The more frequent occurrence of SNIF in younger adults and less in older adults suggests a reduction in pharyngeal pressure associated with healthy aging.

Oral and non-oral sensorimotor interventions enhance oral feeding performance in preterm infants.

AIM: The aim of this study was to determine whether oral, tactile/kinaesthetic (T/K), or combined (oral+T/K) interventions enhance oral feeding performance and whether combined interventions have an additive/synergistic effect. METHOD: Seventy-five preterm infants (mean gestational age 29 wk; standard error of the mean [SEM] 0.3 wk; mean birthweight 1340.3g; SEM 52.5 g; 49 males and 26 females) were randomly assigned to one of three intervention groups or a control group. The oral group received sensorimotor input to the oral structures, the T/K group received sensorimotor input to the trunk and limbs, and the combined group received both. The outcomes were time from introduction of nipple feeding to independent oral feeding (d), proficiency (intake in the first 5 min, %), volume transfer (%), rate of transfer (mL/min), volume loss (%), and length of hospital stay (d). RESULTS: Infants in the three intervention groups achieved independent oral feeding 9-10 days earlier than those in the control group (p<0.001; effect size 1.9-2.1). Proficiency (p ≤ 0.002; effect size 0.7-1.4) at the time of one to two and three to five oral feedings per day, volume transfer (p ≤ 0.001; effect size 0.8-1.1) at one to two, three to five, and six to eight oral feedings per day, and overall rate of transfer (p ≤ 0.018; effect size 0.8-1.1) were greater, and overall volume losses were less (p ≤ 0.007; effect size 0.9-1.1), than in the control group (p ≤ 0.042). The combined group attained independent oral feeding at a significantly younger postmenstrual age than controls (p=0.020) and had clinically greater proficiency than the T/K group (p=0.020; effect size 0.7) and oral group (p=0.109; effect size 0.5). Length of hospital stay was not significantly different between groups (p=0.792; effect size 0.02-0.3). INTERPRETATION: Oral and T/K interventions accelerated the transition from introduction to independent oral feeding and enhanced oral feeding skills. T/K has beneficial effects beyond the specific targeted system. The combined sensorimotor intervention led to an additive/synergistic effect for proficiency, further benefiting this population.

Articulatory and acoustic adaptation to palatal perturbation.

Previous work has established that speakers have difficulty making rapid compensatory adjustments in consonant production (especially in fricatives) for structural perturbations of the vocal tract induced by artificial palates with thicker-than-normal alveolar regions. The present study used electromagnetic articulography and simultaneous acoustic recordings to estimate tongue configurations during production of [s s t k] in the presence of a thin and a thick palate, before and after a practice period. Ten native speakers of English participated in the study. In keeping with previous acoustic studies, fricatives were more affected by the palate than were the stops. The thick palate lowered the center of gravity and the jaw was lower and the tongue moved further backwards and downwards. Center of gravity measures revealed complete adaptation after training, and with practice, subjects' decreased interlabial distance. The fact that adaptation effects were found for [k], which are produced with an articulatory gesture not directly impeded by the palatal perturbation, suggests a more global sensorimotor recalibration that extends beyond the specific articulatory target.

Respiratory-swallow phase patterns and their relationship to swallowing impairment in patients treated for oropharyngeal cancer.

BACKGROUND: Unstable respiratory-swallowing coordination has been associated with disorders and disease. The goals of this study were (1) to describe respiratory-swallow patterns in patients with dysphagia consequent to treatments for cancers of the oropharynx and (2) to determine the association between respiratory-swallow patterns, airway invasion, and overall severity of swallowing impairment. METHODS: This prospective, cross-sectional design compared respiratory-swallow patterns in 20 patients treated for oropharyngeal cancer and 20 healthy, age-matched control participants. Nasal airflow direction was synchronously recorded with videofluoroscopic imaging in participants who swallowed 5-mL thin liquid barium boluses. RESULTS: Respiratory-swallow patterns differed between groups. Most control participants initiated and completed swallowing bracketed by expiratory airflow. Swallowing in patients often interrupted inspiratory flow and was associated with penetration or aspiration of the bolus. CONCLUSIONS: We suggest nonexpiratory bracketed respiratory-swallowing phase patterns in patients with oropharyngeal cancer may place patients at greater risk of airway penetration or aspiration during swallowing.

Respiratory-swallowing interactions during sleep in premature infants at term.

Non-nutritive swallowing occurs frequently during sleep in infants and is vital for fluid clearance and airway protection. Swallowing has also been shown to be associated with prolonged apnea in some clinical populations. What is not known is whether swallowing contributes to apnea or may instead help resolve these clinically significant events. We studied the temporal relationships between swallowing, respiratory pauses and arousal in six preterm infants at term using multi-channel polysomnography and a pharyngeal pressure transducer. Results revealed that swallows occurred more frequently during respiratory pauses and arousal than during control periods. They did not trigger the respiratory pause, however, as most swallows (66%) occurred after respiratory pause onset and were often tightly linked to arousal from sleep. Swallows not associated with respiratory pauses (other than the respiratory inhibition to accommodate swallowing) and arousal occurred consistently during the expiratory phase of the breathing cycle. Results suggest that swallowing and associated arousal serve an airway protective role during sleep and medically stable preterm infants exhibit the mature pattern of respiratory-swallowing coordination by the time they reach term.

Swallowing function and upper airway sensation in obstructive sleep apnea.

The objective of this study was to determine whether impaired upper airway (UA) mucosal sensation contributes to altered swallowing function in obstructive sleep apnea (OSA). We determined UA two-point discrimination threshold (2PDT) and vibratory sensation threshold (VST) in 15 men with untreated OSA and 9 nonapneic controls (CL). We then assessed swallowing responses to oropharyngeal fluid boluses delivered via a catheter. The threshold volume required to provoke swallowing and the mean latency to swallowing were determined, as was the phase of the respiratory cycle in which swallowing occurred [expressed as percentage of control cycle duration (%CCD)] and the extent of prolongation of the respiratory cycle after swallowing [inspiratory suppression time (IST)]. 2PDT and VST were significantly impaired in OSA patients compared with CL subjects. 2PDT was positively correlated with swallowing latency and threshold volume in CL subjects, but not in OSA patients. Threshold volume did not differ between the groups [median value = 0.1 ml (95% confidence interval = 0.1-0.2) for OSA and 0.15 ml (95% confidence interval = 0.1-0.16) for CL], whereas swallowing latency was shorter for OSA patients [3.3 (SD 0.7) vs. 3.9 (SD 0.8) s, P = 0.04]. %CCD and IST were similar for OSA patients and CL subjects. However, among OSA patients there was a significant inverse relation between VST and IST. These findings suggest that oropharyngeal sensory impairment in OSA is associated with an attenuation of inhibitory modulating inputs to reflex and central control of UA swallowing function.

The science and practice of LSVT/LOUD: neural plasticity-principled approach to treating individuals with Parkinson disease and other neurological disorders.

Our 15 years of research have generated the first short- and long-term efficacy data for speech treatment (Lee Silverman Voice Treatment; LSVT/LOUD) in Parkinson's disease. We have learned that training the single motor control parameter amplitude (vocal loudness) and recalibration of self-perception of vocal loudness are fundamental elements underlying treatment success. This training requires intensive, high-effort exercise combined with a single, functionally relevant target (loudness) taught across simple to complex speech tasks. We have documented that training vocal loudness results in distributed effects of improved articulation, facial expression, and swallowing. Furthermore, positive effects of LSVT/LOUD have been documented in disorders other than Parkinson's disease (stroke, cerebral palsy). The purpose of this article is to elucidate the potential of a single target in treatment to encourage cross-system improvements across seemingly diverse motor systems and to discuss key elements in mode of delivery of treatment that are consistent with principles of neural plasticity.

Clinical implications of cross-system interactions.

In this review, we briefly highlight potential cross-system interactions between swallowing and speech production, using data from recent neuroimaging studies, common clinical impairments, cross-system treatment effects, and developmental considerations as supporting evidence. Our overall hypothesis is that speech and swallowing (and other motor behaviors) are regulated through a shared network of brain regions and other neural processes that are modulated on the basis of specific task demands. We emphasize the clinical utility of viewing speech and swallowing as being closely linked from both a diagnostic and treatment perspective. We stress the importance of continuing research to explore the common and perhaps distinct neural circuitry underlying speech and swallowing and the clinical intervention strategies that attempt to capitalize on potential cross-system therapeutic benefits.

Electropalatographic, acoustic, and perceptual data on adaptation to a palatal perturbation.

Exploring the compensatory responses of the speech production system to perturbation has provided valuable insights into speech motor control. The present experiment was conducted to examine compensation for one such perturbation-a palatal perturbation in the production of the fricative /s/. Subjects wore a specially designed electropalatographic (EPG) appliance with a buildup of acrylic over the alveolar ridge as well as a normal EPG palate. In this way, compensatory tongue positioning could be assessed during a period of target specific and intense practice and compared to nonperturbed conditions. Electropalatographic, acoustic, and perceptual analyses of productions of /asa/ elicited from nine speakers over the course of a one-hour practice period were conducted. Acoustic and perceptual results confirmed earlier findings, which showed improvement in production with a thick artificial palate in place over the practice period; the EPG data showed overall increased maximum contact as well as increased medial and posterior contact for speakers with the thick palate in place, but little change over time. Negative aftereffects were observed in the productions with the thin palate, indicating recalibration of sensorimotor processes in the face of the oral-articulatory perturbation. Findings are discussed with regard to the nature of adaptive articulatory skills.

Persistence of respiratory-swallowing coordination after laryngectomy.

The present study was designed to provide additional insights into the neural mechanisms underlying respiratory-swallowing coupling by studying potential alterations in movement coordination when upper airway protection is no longer necessary. Twelve laryngectomized participants, all at least 3 years postsurgery, were compared to age- and sex-matched controls. Respiration and swallowing were monitored before, during, and after mastication. No significant differences were found between the laryngectomized and normal control participants in the distribution of the respiratory phase in which swallowing occurs, our primary measure of respiratory-swallowing stability. Data suggest that the coupling between the swallowing and respiratory pattern generators is highly stable. Pronounced masticatory-related apnea was observed in 3 of the laryngectomized participants but in none of the controls, suggesting that masticatory/respiratory interactions may become abnormal in these patients.