Deglutition is one of the most important bodily functions, allowing the intake of required nutrients and hydration. Safe deglutition is crucial, since the consequences of unsafe swallowing (dysphagia) can affect and threaten individuals’ wellbeing. The highest incidence rates for oropharyngeal dysphagia are observed following central or peripheral lesions (i.e. traumatic brain injury, stroke, cancerous lesion in the oropharynx and oesophagus) and during the course of neurodegenerative diseases.
Deglutition and its stages was described as early as 1816 by the pioneer experimental physiologist Magendie.1 Literature and case studies for the diagnosis and treatment of oropharyngeal dysphagic symptoms appeared a bit later. A case study by Horne in 19132 is amongst the earliest. Since then, the therapeutic procedures for oropharyngeal dysphagia have changed dramatically mainly due to advances in medical and experimental imaging and the increase of our knowledge. But, how and why?
What are we currently using in our clinical practise?
The aim of rehabilitation for oropharyngeal dysphagia is to allow for safer and greater nutrient intake. Most of the work on the behavioural strategies for oropharyngeal dysphagia, was performed by Logemann and colleagues.3 The procedures proposed then, and still employed, include several step-wise approaches to diet modification and compensatory postures with the focus on protecting the airway and preventing aspiration during swallowing. Most of the manoeuvres (chin tuck etc) are classified as compensatory therapies. The evidence for the beneficial changes on patients’ swallowing performance was gathered early.3,4 Research laboratories continue the investigation for the effects following these techniques.5
Exercise-based approaches were also introduced early.3 These included lingual strength programs and isometric exercises,6,7,8 isometric head lifts9 etc. Rigorous research investigations on the effects of exercise-based approaches are still taking place, but trials investigating the ‘net-effect’ of the combination of such strategies in the clinics show promising results.10 The main issue delaying the conduct of large randomised controlled trials is that clinical researchers attempt to find a single ‘fit-all’ regime for all the patients (exact number of repetitions, duration, etc).
The reality in the clinics and hospital wards is that:
- there is high heterogeneity of dysphagia symptoms within specific disease populations with oropharyngeal dysphagia, and
- there are specific individual characteristics such as patient’s compliance and/or cognitive load/capacity that may affect the ability to follow instructions during the rehabilitation programme with exercises.
Consequently, in some cases the therapeutic programme is not introduced. For other patients, the therapeutic programme is introduced later in the recovery phase, i.e. from a stroke lesion. However, the timely introduction of the therapeutic approaches is of the essence. For dysphagia, delay in recovery may result in nutritional compromise. We already know that following brain injuries both adaptive and maladaptive processes take place.11 Maladaptive processes may stand in the way of full recovery, especially if one relies only on compensation.11 Therefore, in some patients with peripheral and central lesions, delayed introduction of therapy and on-going dependence on compensation may reinforce maladaptive behaviour.
Plasticity: The turning-point
The turning point in the field of rehabilitation was the introduction of the principles of neuroplasticity. Understanding how and why long lasting changes in the brain evolve (in neural pathways and synapses) is very important for the rationale behind rehabilitation. Early work by Kaas, Merzenich and colleagues12 showed changes of the topography of musculature representations on the cortex following peripheral lesions, and inspired the work by many in the field of neurorehabilitation.
As a result, the surge in the number of new techniques and new outcome measures in the field of deglutology was unavoidable.13 The introduction of neuroplasticity principles and neurorehabilitation approaches in deglutology is proved to be a bigger challenge. Swallowing is ‘multidimensional in nature’;14 the output of a very precise interplay between different brain areas. This translates into a well-tuned coordinated muscle activity during a swallow. The patterned response of swallowing, with elements of subconscious programming overridden voluntarily, differs from limb musculature control. Thus, some of the principles of rehabilitation for the limb muscles might not directly apply to swallowing.
Increase in the number of neurorehabilitation techniques
In the literature we now observe different neurostimulation approaches: peripheral electrical neurostimulation, central (cortical) stimulation (transcranial magnetic stimulation (TMS) and direct current stimulation) and many others. The number of research studies is increasing and the results so far have shown beneficial effects on swallowing. Most of these neurorehabilitation approaches were developed on previous knowledge coming from earlier work with animals (find examples here 15).
However the question is: what are we seeking with the use of the neurostimulation approaches? Are we becoming neurorehabilitationists? Are we trying to boost adaptive and beneficial neurophysiological processes? Are we trying to boost and complement our current therapeutic modalities and accelerate recovery?
Some neurostimulation approaches16,17 with TMS (‘virtual’ lesions) allow us to examine the effects of neurorehabilitation18 in healthy individuals before we apply techniques to our patients.
Other techniques allow us to find the ‘ceiling’ and the effect size of the change in healthy swallowing and in disease.19
With neurostimulation, we can also objectively and transiently modify the chemistry in specific brain areas (by provoking changes in neurotransmitters, which are important for the communication between neurons). We now understand that the changes in specific neurotransmitters in the brain are important for recovery of function.20 Therefore, our treatments for oropharyngeal dysphagia should provoke these changes in the brain while benefiting behaviour.
Yes, there will be. However, translating some of the more experimental neurorehabilitation approaches in clinical practice might take longer for the field of deglutology.20 There are numbers of reasons. As a point of fact:
- our understanding for the swallowing network continues to evolve
- we are catching up with the work in the other fields and we are adopting different methods to measure change in swallowing (functional magnetic resonance imaging fMRI etc)
- we still investigate the heterogeneity within disease models and the underlying mechanisms for the manifestation of dysphagia, i.e. Parkinson’s disease21-25 and lastly
- we still investigate the mechanisms for swallowing recovery following disease and lesions.
Understanding how and why we should use any future developments in the field of rehabilitation for oropharyngeal dysphagia is of paramount importance. Chances are that this way we will get a firm rationale behind our rehabilitation approaches and we will advance our evidence-based practice further.
- Magendie, F. Précis élémentaire de physiologie. France, Paris, Méquignon-Marvis, 1816
- Horne WJ. Dysphagia presenting Unusual Features rapidly remedied by Treatment. Proc R Soc Med. 1913;6 (Laryngol Sect):73-4.
- Logemann J. Evaluation and Treatment of Swallowing Disorders / Edition 1 (College-Hill Press, 1983)/ 2(Pro-Ed 1998)
- Logemann JA, Kahrilas PJ, Kobara M, Vakil NB. The benefit of head rotation on pharyngoesophageal dysphagia. Arch Phys Med Rehabil. 1989 Oct;70(10):767-71.
- Ra JY, Hyun JK, Ko KR, Lee SJ. Chin tuck for prevention of aspiration: effectiveness and appropriate posture. Dysphagia. 2014 Oct;29(5):603-9.
- Jordan K. Rehabilitation of the patients with dysphagia. Ear, Nose, and Throat Journal 1979, 58, 86-87.
- Robinovitch SN, Hershler C, Romilly DP. A tongue force measurement system for the assessment of oral-phase swallowing disorders. Arch Phys Med Rehabil. 1991 Jan;72(1):38-42.
- Lazarus CL, Logemann JA, Pauloski BR, Rademaker AW, Larson CR, Mittal BB, Pierce M. Swallowing and tongue function following treatment for oral and oropharyngeal cancer. J Speech Lang Hear Res. 2000 Aug;43(4):1011-23.
- Shaker R, Easterling C, Kern M, Nitschke T, Massey B, Daniels S, Grande B, Kazandjian M, Dikeman K. Rehabilitation of swallowing by exercise in tube-fed patients with pharyngeal dysphagia secondary to abnormal UES opening. Gastroenterology. 2002 May;122(5):1314-21.
- Carnaby G, Hankey GJ, Pizzi J. Behavioural intervention for dysphagia in acute stroke: a randomised controlled trial. Lancet Neurol. 2006 Jan;5(1):31-7.
- Nudo RJ. Recovery after damage to motor cortical areas. Cur Opinion in Neurobiology 1999, 9:740-747.
- Kaas JH, Merzenich MM, Killackey HP. The reorganization of somatosensory cortex following peripheral nerve damage in adult and developing mammals. Annu Rev Neurosci. 1983;6:325-56.
- Martin RE. Neuroplasticity and swallowing. Dysphagia. 2009 Jun;24(2):218-29
- Martin RE, Sessle BJ. The role of the cerebral cortex in swallowing. Dysphagia. 1993;8(3):195-202.
- Michou E. Hamdy S. Neurostimulation as an Approach to Dysphagia Rehabilitation: Current Evidence. Current Physical Medicine and Rehabilitation Reports. December 2013, Volume 1, Issue 4, pp 257-266.
- Mistry S, Verin E, Singh S, Jefferson S, Rothwell JC, Thompson DG, Hamdy S. Unilateral suppression of pharyngeal motor cortex to repetitive transcranial magnetic stimulation reveals functional asymmetry in the hemispheric projections to human swallowing. J Physiol. 2007 Dec 1;585(Pt 2):525-38.
- Verin E, Michou E, Leroi AM, Hamdy S, Marie JP. “Virtual” lesioning of the human oropharyngeal motor cortex: a videofluoroscopic study. Arch Phys Med Rehabil. 2012 Nov;93(11):1987-90.
- Michou E, Mistry S, Jefferson S, Singh S, Rothwell J, Hamdy S. Targeting unlesioned pharyngeal motor cortex improves swallowing in healthy individuals and after dysphagic stroke. Gastroenterology. 2012 Jan;142(1):29-38.
- Michou E, Mistry S, Rothwell J, Hamdy S. Priming pharyngeal motor cortex by repeated paired associative stimulation: implications for dysphagia neurorehabilitation. Neurorehabil Neural Repair. 2013 May;27(4):355-62.
- Kim YK, Yang EJ, Cho K, Lim JY, Paik NJ. Functional Recovery After Ischemic Stroke Is Associated With Reduced GABAergic Inhibition in the Cerebral Cortex: A GABA PET Study. Neurorehabil Neural Repair. 2014 Jan 24;28(6):576-583.
- Doeltgen SH, Huckabee ML. Swallowing neurorehabilitation: from the research laboratory to routine clinical application. Arch Phys Med Rehabil. 2012 Feb;93(2):207-13.
- Ciucci MR, Grant LM, Rajamanickam ES, Hilby BL, Blue KV, Jones CA, Kelm-Nelson CA. Early identification and treatment of communication and swallowing deficits in Parkinson disease. Semin Speech Lang. 2013 Aug;34(3):185-202.
- van Hooren MR, Baijens LW, Voskuilen S, Oosterloo M, Kremer B. Treatment effects for dysphagia in Parkinson’s disease: a systematic review. Parkinsonism Relat Disord. 2014 Aug;20(8):800-7.
- Kikuchi A, Baba T, Hasegawa T, Kobayashi M, Sugeno N, Konno M, Miura E, Hosokai Y, Ishioka T, Nishio Y, Hirayama K, Suzuki K, Aoki M, Takahashi S, Fukuda H, Itoyama Y, Mori E, Takeda A. Hypometabolism in the supplementary and anterior cingulate cortices is related to dysphagia inParkinson’s disease: a cross-sectional and 3-year longitudinal cohort study. BMJ Open. 2013 Mar 1;3(3).
- Suntrup S, Teismann I, Bejer J, Suttrup I, Winkels M, Mehler D, Pantev C, Dziewas R, Warnecke T. Evidence for adaptive cortical changes in swallowing in Parkinson’s disease. 2013 Mar;136(Pt 3):726-38.
- Michou E, Hamdy S, Harris M, Vania A, Dick J, Kellett M, Rothwell J. Characterization of corticobulbar pharyngeal neurophysiology in dysphagic patients with Parkinson’s disease. Clin Gastroenterol Hepatol. 2014 Dec;12(12):2037-2045.