Deglutition and Respiration: Development, Coordination, and Practical Implications

ABSTRACT

Temporal coordination of deglutition and respiration is essential for survival because both functions share the pharynx as a common pathway. Disruptions in this interface in young infants may result in dysphagia that may lead to aspiration and injury to the developing lung. Likewise, respiratory problems may contribute to the development of swallowing problems.

This article focuses on the coordination between swallowing and breathing in infants and children, aspiration during periods of postnatal lung development and airway protective mechanisms. Identification of infants and children at increased risk for oropharyngeal dysphagia and respiratory disease is critical for optimal intervention. Assessment and management considerations are described.

KEYWORDS

Deglutition - aspiration - pediatric - swallowing - breathing - lung injury

REFERENCES

• 1 Loughlin G M, Lefton-Greif M A. Dysfunctional swallowing and respiratory disease in children.  Adv Pediatr. 1994;  41 135-162
• 2 Wolff P H. The serial organization of sucking in the young infant.  Pediatrics. 1968;  42(6) 943-956
• 3 Bamford W, Taciak V, Gewolb I H. The relationship between rhythmic swallowing and breathing during suckle feeding in term neonates.  Pediatr Res. 1992;  31(6) 619-624
• 4 Gewolb I H, Vice F L. Maturational changes in the rhythms, patterning, and coordination of respiration and swallow during feeding in preterm and term infants.  Dev Med Child Neurol. 2006;  48(7) 589-594
• 5 Kelly B N, Huckabee M L, Jones R D, Frampton C M. The first year of human life: coordinating respiration and nutritive swallowing.  Dysphagia. 2007;  22(1) 37-43
• 6 Timms B J, DiFiore J M, Martin R J, Miller M J. Increased respiratory drive as an inhibitor of oral feeding of preterm infants.  J Pediatr. 1993;  123(1) 127-131
• 7 Miller M J, Kiatchoosakun P. Relationship between respiratory control and feeding in the developing infant.  Semin Neonatol. 2004;  9(3) 221-227
• 8 Perlman A L, Ettema S L, Barkmeier J. Respiratory and acoustic signals associated with bolus passage during swallowing.  Dysphagia. 2000;  15(2) 89-94
• 9 Martin-Harris B, Brodsky M B, Price C C, Michel Y, Walters B. Temporal coordination of pharyngeal and laryngeal dynamics with breathing during swallowing: single liquid swallows.  J Appl Physiol. 2003;  94(5) 1735-1743
• 10 Hanlon M B, Tripp J H, Ellis R E, Flack F C, Selley W G, Shoesmith H J. Deglutition apnoea as indicator of maturation of suckle feeding in bottle-fed preterm infants.  Dev Med Child Neurol. 1997;  39(8) 534-542
• 11 Kelly B N, Huckabee M L, Jones R D, Frampton C M. Nutritive and non-nutritive swallowing apnea duration in term infants: Implications for neural control mechanisms.  Respir Physiolo Neurobiol. 2006;  154(3) 372-378
• 12 Hadjikoutis S, Pickersgill T P, Dawson K, Wiles C M. Abnormal patterns of breathing during swallowing in neurological disorders.  Brain. 2000;  123(Pt 9) 1863-1873
• 13 Klahn M S, Perlman A L. Temporal and durational patterns associating respiration and swallowing.  Dysphagia. 1999;  14(3) 131-138
• 14 Preiksaitis H G, Mayrand S, Robins K, Diamant N E. Coordination of respiration and swallowing: effect of bolus volume in normal adults.  Am J Physiol. 1992;  263(3 Pt 2) R624-R630
• 15 Shaker R, Li Q, Ren J et al.. Coordination of deglutition and phases of respiration: effect of aging, tachypnea, bolus volume, and chronic obstructive pulmonary disease.  Am J Physiol. 1992;  263(5 Pt 1) G750-G755
• 16 Preiksaitis H G, Mills C A. Coordination of breathing and swallowing: effects of bolus consistency and presentation in normal adults.  J Appl Physiol. 1996;  81(4) 1707-1714
• 17 Smith J, Wolkove N, Colacone A, Kreisman H. Coordination of eating, drinking, and breathing in adults.  Chest. 1989;  96(3) 578-582
• 18 Martin B J, Logemann J A, Shaker R, Dodds D W. Coordination between respiration and swallowing: Respiratory phase relationships and temporal integration.  J Appl Physiol. 1994;  76(2) 714-723
• 19 Paydarfar D, Gilbert R J, Poppel C S, Nassab P F. Respiratory phase resetting and airflow changes induced by swallowing in humans.  J Physiol. 1995;  483(Pt 1) 273-288
• 20 Morton R, Minford J, Ellis R, Pinnington L. Aspiration with dysphagia: the interaction between oropharyngeal and respiratory impairments.  Dysphagia. 2002;  17(3) 192-196
• 21 Perlman A L, He X, Barkmeier J, Van Leer E. Bolus location associated with videofluoroscopic and respirodeglutometric events.  J Speech Lang Hear Res. 2005;  48(1) 21-33
• 22 Hiss S G, Treole K, Stuart A. Effect of age, gender, and repeated measures on intraoral air pressure in normal adults.  J Voice. 2001;  15(2) 159-164
• 23 Hirst L J, Ford G A, Gibson G J, Wilson J A. Swallow-induced alterations in breathing in normal older people.  Dysphagia. 2002;  17(2) 152-161
• 24 Hiss S G, Strauss M, Treole K, Stuart A, Boutilier S. Effects of age, gender, bolus volume, bolus viscosity, and gustation on swallowing apnea onset relative to lingual bolus propulsion onset in normal adults.  J Speech Lang Hear Res. 2004;  47(3) 572-583
• 25 Rempel G, Moussavi Z. The effect of viscosity on the breath-swallow pattern of young people with cerebral palsy.  Dysphagia. 2005;  20(2) 108-112
• 26 Selley W G, Flack F C, Ellis R E, Brooks W A. The Exeter dysphagia assessment technique.  Dysphagia. 1990;  4(4) 227-235
• 27 Selley W G, Parrot L C, Lethbridge P C et al.. Non-invasive technique for assessment and management planning of oral-pharyngeal dysphagia in children with cerebral palsy.  Dev Med Child Neurol. 2000;  42(9) 617-623
• 28 Selley W G, Flack F C, Ellis R E, Brooks W A. Respiratory patterns associated with swallowing: Part 2. Neurologically impaired dysphagic patients.  Age Ageing. 1989;  18(3) 173-176
• 29 Pinnington L L, Muhiddin K A, Ellis R E, Playford E D. Non-invasive assessment of swallowing and respiration in Parkinson's disease.  J Neurol. 2000;  247(10) 773-777
• 30 Thurlbeck W M. Postnatal human lung growth.  Thorax. 1982;  37(8) 564-571
• 31 Jeffrey P K. The development of large and small airways.  Am J Respir Crit Care Med. 1998;  157(5 Pt 2) S174-S180
• 32 Von Mutius E. Paediatric origins of adult lung disease.  Thorax. 2001;  56(2) 153-157
• 33 Eber E, Zach M S. Long term sequelae of bronchopulmonary dysplasia (chronic lung disease of infancy).  Thorax. 2001;  56(4) 317-323
• 34 Jobe A J. The new BPD: an arrest of lung development.  Pediatr Res. 1999;  46(6) 641-643
• 35 Colombo J L, Hallberg T K. Airway reactivity following repeated milk aspiration in rabbits.  Pediatr Pulmonol. 2000;  29(2) 113-119
• 36 Gelfand A S, Larsen G L, Loader J E, Graves J P, Fan L L, Colasurdo G N. Effect of aspiration of milk on mechanisms of neural control in the airways of developing rabbits.  Pediatr Pulmonol. 1997;  23(3) 198-204
• 37 Janahi I A, Elidemir O, Shardonofsky F R et al.. Recurrent milk aspiration produces changes in airway mechanics, lung eosinophilia, and goblet cell hyperplasia in a murine model.  Pediatr Res. 2000;  48(6) 776-781
• 38 Toder D S. Respiratory problems in the adolescent with developmental delay.  Adolesc Med. 2000;  11(3) 617-631
• 39 Chiu C Y, Wong K S, Tsai M H. Massive aspiration of barium sulfate during an upper gastrointestinal examination in a child with dysphagia.  Int J Pediatr Otorhinolaryngol. 2005;  69(4) 541-544
• 40 Seddon P C, Khan Y. Respiratory problems in children with neurological impairment.  Arch Dis Child. 2003;  88(1) 75-78
• 41 Warner M A, Warner M E, Warner D O, Warner L O, Warner E J. Perioperative pulmonary aspiration in infants and children.  Anesthesiology. 1999;  90(1) 66-71
• 42 Karakoc F, Karadag B, Akbenlioglu C et al.. Foreign body aspiration: what is the outcome?.  Pediatr Pulmonol. 2002;  34(1) 30-36
• 43 Lear C S, Flanagran Jr J B, Moorrees C F. The frequency of deglutition in man.  Arch Oral Biol. 1965;  10 83-100
• 44 Huxley E J, Viroslav J, Gray W R, Pierce A K. Pharyngeal aspiration in normal adults and patients with depressed consciousness.  Am J Med. 1978;  64(4) 564-568
• 45 Gleeson K, Eggli D F, Maxwell S L. Quantitative aspiration during sleep in normal subjects.  Chest. 1997;  111(5) 1266-1272
• 46 Eigen H, Laughlin J J, Homrighausen J. Recurrent pneumonia in children and its relationship to bronchial hyperreactivity.  Pediatrics. 1982;  70(5) 698-704
• 47 Ahrens P, Weimer B, Hofmann D. Severe interstitial lung disease from pathologic gastroesophageal reflux in children [In French.]  Pneumologie. 1999;  53(7) 369-372
• 48 Matsuse T, Teramoto S, Matsui H, Ouchi Y, Fukuchi Y. Widespread occurrence of diffuse aspiration bronchiolitis in patients with dysphagia, irrespective of age.  Chest. 1998;  114(1) 350-351
• 49 Taniguchi M H, Moyer R S. Assessment of risk factors for pneumonia in dysphagic children: significance of videofluoroscopic swallowing evaluation.  Dev Med Child Neurol. 1994;  36 495-502
• 50 Thach B T. Maturation and transformation of reflexes that protect the laryngeal airway from liquid aspiration from fetal to adult life.  Am J Med. 2001;  111(Suppl 8A) 69S-77S
• 51 Rogers B, Arvedson J, Buck G, Smart M. Characteristics of dysphagia in children with cerebral palsy.  Dysphagia. 1994;  9(1) 69-73
• 52 Cass H, Wallis C, Ryan M, Reilly S, McHugh K. Assessing pulmonary consequences of dysphagia in children with neurological disabilities: when to intervene?.  Dev Med Child Neurol. 2005;  47(5) 347-352
• 53 Lefton-Greif M A, Crawford T O, Winkelstein J A et al.. Oropharyngeal dysphagia and aspiration in patients with ataxia- telangiectasia.  J Pediatr. 2000;  136(2) 225-231
• 54 Arvedson J, Rogers B, Buck G, Smart P, Msall M. Silent aspiration prominent in children with dysphagia.  Int J Pediatr Otorhinolaryngol. 1994;  28 173-181
• 55 Lefton-Greif M A, Carroll J L, Loughlin G M. Long-term follow-up of oropharyngeal dysphagia in children without apparent risk factors.  Pediatr Pulmonol. 2006;  41(11) 1040-1048
• 56 Chang A B, Widdicombe J G. Cough throughout life: Children, adults and the senile.  Pulm Pharmacol Ther. 2007;  20(4) 371-382
• 57 Brumbaugh D E, Accurso F J. Persistent silent aspiration in a child with trisomy 21.  Curr Opin Pediatr. 2002;  14(2) 231-233
• 58 Frazier J B, Friedman B. Swallow function in children with Down syndrome: a retrospective study.  Dev Med Child Neurol. 1996;  38(8) 695-703
• 59 Newman L A, Keckley C, Petersen M C, Hamner A. Swallowing function and medical diagnoses in infants suspected of Dysphagia.  Pediatrics. 2001;  108(6) E106
• 60 Sheikh S, Allen E, Shell R et al.. Chronic aspiration without gastroesophageal reflux as a cause of chronic respiratory symptoms in neurologically normal infants.  Chest. 2001;  120(4) 1190-1195
• 61 Mercado-Deane M G, Burton E M, Harlow S A et al.. Swallowing dysfunction in infants less than 1 year of age.  Pediatr Radiol. 2001;  31(6) 423-428
• 62 Radford P J, Stillwell P C, Blue B, Hertel G. Aspiration complicating bronchopulmonary dysplasia.  Chest. 1995;  107(1) 185-188
• 63 Khoshoo V, Edell D. Previously healthy infants may have increased risk of aspiration during respiratory syncytial viral bronchiolitis.  Pediatrics. 1999;  104(6) 1389-1390
• 64 Heuschkel R B, Fletcher K, Hill A, Buonomo C, Bousvaros A, Nurko S. Isolated neonatal swallowing dysfunction: a case series and review of the literature.  Dig Dis Sci. 2003;  48(1) 30-35
• 65 Singh A M, Moore P E, Gern J E, Lemanske Jr R F, Hartert T V. Bronchiolitis to asthma: a review and call for studies of gene-virus interactions in asthma causation.  Am J Respir Crit Care Med. 2007;  175(2) 108-119
• 66 Tawfik R, Dickson A, Clarke M, Thomas A G. Caregivers' perceptions following gastrostomy in severely disabled children with feeding problems.  Dev Med Child Neurol. 1997;  39(11) 746-751
• 67 Burklow K A, Phelps A N, Schultz J R, McConnell K, Rudolph C. Classifying complex pediatric feeding disorders.  J Pediatr Gastroenterol Nutr. 1998;  27(2) 143-147
• 68 Nair R H, Kesavachandran C, Shashidhar S. Spirometric impairments in undernourished children.  Indian J Physiol Pharmacol. 1999;  43(4) 467-473
• 69 Loughlin G M. Respiratory consequences of dysfunctional swallowing and aspiration.  Dysphagia. 1989;  3(3) 126-130
• 70 Abrams S A. Chronic pulmonary insufficiency in children and its effects on growth and development.  J Nutr. 2001;  131(3) 938S-941S
• 71 Biniwale M A, Ehrenkranz R A. The role of nutrition in the prevention and management of bronchopulmonary dysplasia.  Semin Perinatol. 2006;  30(4) 200-208
• 72 Frank L, Sosenko I R. Undernutrition as a major contributing factor in the pathogenesis of bronchopulmonary dysplasia.  Am Rev Respir Dis. 1988;  138(3) 725-729
• 73 Knudsen E I. Sensitive periods in the development of the brain and behavior.  J Cogn Neurosci. 2004;  16(8) 1412-1425
• 74 Kalenga M. Lung growth and development during experimental malnutrition.  Pediatr Pulmonol Suppl. 1997;  16 165-166
• 75 Burklow K A, McGrath A M, Valerius K S, Rudolph C. Relationship between feeding difficulties, medical complexity, and gestational age.  Nutr Clin Pract. 2002;  17(6) 373-378
• 76 Kallapur S G, Jobe A H. Contribution of inflammation to lung injury and development.  Arch Dis Child Fetal Neonatal Ed. 2006;  91(2) F132-F135
• 77 de Kleine M J, den Ouden A L, Kollee L A et al.. Lower mortality but higher neonatal morbidity over a decade in very preterm infants.  Paediatr Perinat Epidemiol. 2007;  21(1) 15-25
• 78 Gewolb I H, Vice F L. Abnormalities in the coordination of respiration and swallow in preterm infants with bronchopulmonary dysplasia.  Dev Med Child Neurol. 2006;  48(7) 595-599
• 79 Lau C, Smith E O, Schanler R J. Coordination of suck-swallow and swallow respiration in preterm infants.  Acta Paediatr. 2003;  92(6) 721-727
• 80 Northway Jr W H, Moss R B, Carlisle K B et al.. Late pulmonary sequelae of bronchopulmonary dysplasia.  N Engl J Med. 1990;  323(26) 1793-1799
• 81 Bier J B, Ferguson A, Cho C, Oh W, Vohr B R. The oral motor development of low-birth-weight infants who underwent orotracheal intubation during the neonatal period.  Am J Dis Child. 1993;  147 858-862
• 82 Jolley S G, Halpern C T, Sterling C E, Feldman B H. The relationship of respiratory complications from gastroesophageal reflux to prematurity in infants.  J Pediatr Surg. 1990;  25(7) 755-757
• 83 Akinola E, Rosenkrantz T S, Pappagallo M, McKay K, Hussain N. Gastroesophageal reflux in infants < 32 weeks gestational age at birth: lack of relationship to chronic lung disease.  Am J Perinatol. 2004;  21(2) 57-62
• 84 Ravelli A M, Panarotto M B, Verdoni L, Consolati V, Bolognini S. Pulmonary aspiration shown by scintigraphy in gastroesophageal reflux-related respiratory disease.  Chest. 2006;  130(5) 1520-1526
• 85 Suskind D L, Thompson D M, Gulati M, Huddleston P, Liu D C, Baroody F M. Improved infant swallowing after gastroesophageal reflux disease treatment: a function of improved laryngeal sensation?.  Laryngoscope. 2006;  116(8) 1397-1403
• 86 Kurzner S I, Garg M, Bautista D B, Sargent C W, Bowman C M, Keens T G. Growth failure in bronchopulmonary dysplasia: elevated metabolic rates and pulmonary mechanics.  J Pediatr. 1988;  112(1) 73-80
• 87 Khoshoo V, Ross G, Kelly B, Edell D, Brown S. Benefits of thickened feeds in previously healthy infants with respiratory syncytial viral bronchiolitis.  Pediatr Pulmonol. 2001;  31(4) 301-302
• 88 Rogers B, Msall M, Shucard D. Hypoxemia during oral feedings in adults with dysphagia and severe neurological disabilities.  Dysphagia. 1993;  8(1) 43-48
• 89 Mikkola K, Ritari N, Tommiska V et al.. Neurodevelopmental outcome at 5 years of age of a national cohort of extremely low birth weight infants who were born in 1996-1997.  Pediatrics. 2005;  116(6) 1391-1400
• 90 Mirrett P L, Riski J E, Glascott J, Johnson V. Videofluoroscopic assessment of dysphagia in children with severe spastic cerebral palsy.  Dysphagia. 1994;  9(3) 174-179
• 91 Spiroglou K, Xinias I, Karatzas N, Karatza E, Arsos G, Panteliadis C. Gastric emptying in children with cerebral palsy and gastroesophageal reflux.  Pediatr Neurol. 2004;  31(3) 177-182
• 92 Kohda E, Hisazumi H, Hiramatsu K. Swallowing dysfunction and aspiration in neonates and infants.  Acta Otolaryngol Suppl. 1994;  517 11-16
• 93 Griggs C A, Jones P M, Lee R E. Videofluoroscopic investigation of feeding disorders of children with multiple handicap.  Dev Med Child Neurol. 1989;  31(3) 303-308
• 94 Guilleminault C, Coons S. Apnea and bradycardia during feeding in infants weighing > 2000 gm.  J Pediatr. 1984;  104(6) 932-935
• 95 Thach B T. Can we breathe and swallow at the same time?.  J Appl Physiol. 2005;  99(5) 1633
• 96 Plaxico D T, Loughlin G M. Nasopharyngeal reflux and neonatal apnea.  Am J Dis Child. 1981;  135(9) 793-794
• 97 Steinschneider A, Weinstein S L, Diamond E. The sudden infant death syndrome and apnea/obstruction during neonatal sleep and feeding.  Pediatrics. 1982;  70(6) 858-863
• 98 Hay A D, Wilson A, Fahey T, Peters T J. The duration of acute cough in pre-school children presenting to primary care: a prospective cohort study.  Fam Pract. 2003;  20(6) 696-705
• 99 Hay A D, Wilson A D. The natural history of acute cough in children aged 0 to 4 years in primary care: a systematic review.  Br J Gen Pract. 2002;  52(478) 401-409
• 100 Willging J P, Miller C K, Hogan M J, Rudolph C D. Fiberoptic evaluation of swallowing in children: Preliminary report of 100 procedures.  Dysphagia. 1995;  11(2) 162
• 101 Lefton-Greif M A, Loughlin G M. Specialized studies in pediatric dysphagia.  Semin Speech Lang. 1996;  17(4) 311-329
• 102 Arvedson J C, Lefton-Greif M A. Pediatric Videofluoroscopic Swallow Studies: A Professional Manual with Caregiver Handouts. San Antonio, TX; Communication Skill Builders 1998
• 103 Willging J P. Benefit of feeding assessment before pediatric airway reconstruction.  Laryngoscope. 2000;  110(5) 825-834
• 104 Noel R J, Delaney A L, Beecher R B, Arvedson J C, Rudolph C. Feeding of children with impaired airway protection - screening for pulmonary disease with CT scanning of the chest.  J Pediatr Gastroenterol Nutr. 2005;  41(4) 517-518
• 105 Boesch R P, Daines C, Willging J P et al.. Advances in the diagnosis and management of chronic pulmonary aspiration in children.  Eur Respir J. 2006;  28(4) 847-861
• 106 Perlman A L, Luschei E S, DuMond C E. Electrical activity from the superior pharyngeal constrictor during reflexive and nonreflexive tasks.  J Speech Hearing Res. 1989;  32(4) 749-754
• 107 Weir K, McMahon S, Chang A, Weir K. Restriction of oral intake of water for aspiration lung disease in children.  Cochrane Database Syst Rev. 2005 Oct 19;  (4) CD005303
• 108 Langmore S E, Terpenning M S, Schork A et al.. Predictors of aspiration pneumonia: how important is dysphagia?.  Dysphagia. 1998;  13(2) 69-81
• 109 Hafidh M A, Young O, Russell J D. Intractable pulmonary aspiration in children: Which operation?.  Int J Pediatr Otorhinolaryngol. 2006;  70(1) 19-25
• 110 Manrique D, Settanni F A. Campones do Brasil OO. Surgery for aspiration: analysis of laryngotracheal separation in 23 children.  Dysphagia. 2006;  21(4) 254-258
• 111 Yamana T, Kitano H, Hanamitsu M, Kitajima K. Clinical outcome of laryngotracheal separation for intractable aspiration pneumonia.  ORL J Otorhinolaryngol Relat Spec. 2001;  63(5) 321-324