Difficulty with oropharyngeal swallow requires careful diagnosis and treatment from a team of professionals including the patients' physicians and the speech-language pathologist specializing in dysphagia. The dentist can be a critical team member in prevention, early identification, and management of oropharyngeal dysphagia. This manuscript reviews the physiology of normal oropharyngeal swallow and the effects of normal aging on this physiology. Typical etiologies for oropharyngeal dysphagia are defined as is the most commonly used physiologic diagnostic procedure, the modified barium swallow (MBS). The critical role of the dentist in identifying risk of oropharyngeal dysphagia, making appropriate referrals, and improving oral hygiene to prevent aspiration pneumonia in the elderly is discussed.
The act of swallowing consists of a complex system of involuntary and voluntary muscle movements, neurologic pathways, and the triggering of sensate circuits of smell, taste, and sight. As the mouth ages, it affects these various biologic components. Some of these are visible such as facial muscles. Others are more functional but not visible, such as those involved in swallowing. Swallowing encompasses all of the biologic systems that are part of an oral exam and should be considered and recorded over time. There are over 22 muscles or structures utilized in swallow, which can be damaged individually or in combination, depending on the etiology of the patient's swallowing disorder (Logemann, 1998). Almost any neurologic damage or disease can affect the oropharyngeal swallow including but not limited to stroke, Parkinson's disease, amyotrophic lateral sclerosis, as can head and neck cancer and its treatment (Rademaker et al, 2003), and other types of structural damage such as spinal cord injury, head injury, or systemic diseases. The oropharyngeal swallow is comprised of three phases: the oral preparation, the oral phase, and the pharyngeal phase. A large number of muscles and structural movements of bone and cartilage are involved to prepare food in the mouth to be ready for the swallow, to propel food through the oral cavity, and, finally, through the pharynx into the esophagus (Logemann, 1998).
Aging causes a number of significant changes in the oropharyngeal swallow, although the swallow maintains a functional ability to propel food safely and efficiently from the mouth through the pharynx and into the esophagus. The changes created by age begin in the 50s and move through the 60s, 70s, 80s, and 90s (Daggett et al, 2006). Their general effect is to slow the swallow and to mildly but significantly reduce the efficiency of the swallow (Tracy et al, 1989; Robbins et al, 1999).
In oral preparation, the oral portion of the tongue is responsible for controlling food in the mouth during tasting, manipulation of food, and chewing. It is under cortical neural control by way of the 12th cranial nerve, the hypoglossal. The oral tongue places food on the teeth, picks food up from the teeth, mixes it with saliva, and places it back on the biting surfaces of the teeth. Unfortunately, there is often a misunderstanding that chewing is largely the responsibility of mandibular movement. In fact, the oral tongue is responsible for controlling the food throughout the masticatory process. As chewing is completed, oral tongue forms the food into a bolus of the correct volume in the context of its viscosities and sends information to sensory nerve endings in the oral tongue, which sends information regarding the thickness or viscosity of the food as well as the volume present in the mouth to the lower brainstem (medulla). As food becomes more viscous, each swallow is reduced in size from saliva (1–2 ml) to thin liquid such as water, which is usually swallowed in from 3 to 5, 10, or 17–20 ml. Thicker foods such as puree or pudding are swallowed in an average volume of 5–6 ml. The dimensions of the pharynx shift with the volume being swallowed such that the timing of movement of the base of tongue, airway closure, and the width and duration of upper esophageal sphincter (UES; the cricopharyngeal opening) are systematically changed (Kahrilas et al, 1988; Kahrilas and Logemann, 1993; Bisch et al, 1994). It is hypothesized that the sensory nerve endings in the oral tongue (taste, temperature, and pressure) send information on volume and viscosity as well as other food characteristics to the medulla or lower brainstem, which is the final swallowing center within the central nervous system. As the oral tongue propels food toward the posterior oral cavity, sensory nerve endings in the back of tongue and faucial arches send sensory information to the medulla, which triggers the pharyngeal stage of swallow.
The pharyngeal stage of swallow
The pharyngeal stage of swallow is no longer called a reflexive activity, but rather a programmed activity. Triggering of the pharyngeal swallow results in the function of a number of valves, which direct food through the pharynx and safely into the esophagus. It is at this point that the pharyngeal stage of swallow becomes invisible clinically, that is, by external observation (Logemann, 1993).
The normal pharyngeal stage of swallow involves function of valves to direct food through the mouth and pharynx into the esophagus and pressure to drive food efficiently through the pharynx and into the esophagus. Pressure is generated by the oral portion of the tongue in the oral stage of swallow and the tongue base (innervated by the medulla via the 10th cranial nerve, the vagus) in the pharyngeal stage of swallow in combination with the pharyngeal constrictors (Kahrilas et al, 1992, 1993).
As shown in Figure 1, the valves in the pharyngeal stage of swallow include the velopharyngeal valve to prevent food from entering the nose and the base of tongue moving backward to contact an anteriorly moving pharyngeal wall. As the base of tongue and pharyngeal walls move toward contact, the pharynx is reduced in size and increased pressure is created in the pharynx, propelling the bolus down to the lower pharynx and into the esophagus. The third valve involves closure of the airway to prevent food or liquid from entering. One of the most dangerous aspects of oropharyngeal swallow is when food enters the airway and is aspirated. There is a risk of developing pneumonia if the patient does not cough strongly enough to clear the aspirated material back into the pharynx and oral cavity. The airway closes at three levels, beginning with the true vocal folds, moving up to the false vocal folds, and, finally, the tilting forward of the arytenoid cartilage to meet the thickening base of epiglottis as the larynx elevates and the pharynx shortens. The vocal folds close as the larynx elevates to approximately 50% of its full elevation. If the food gets below that first level of laryngeal closure, it is quite likely that the patient will aspirate and be unable to clear the aspirated material efficiently.
The fourth and final valve at the top of the esophagus is known as the cricopharyngeal valve (the UES). It is comprised of the cricopharyngeus muscle and the cricoid cartilage of the larynx, the only full circle of cartilage in the larynx. For many years, it was thought that the UES was a muscular valve. It became clear from studies from three laboratories that, in fact, the UES was a musculoskeletal valve and its opening dependent on the upward forward movement of the hyoid bone and larynx during swallow. At rest, the muscular portion of the UES, the cricopharyngeus muscle, comprises the posterior and lateral portions of the UES. This muscle is at some level of contraction preventing air from being inhaled into the esophagus. As the pharyngeal stage of swallow begins, the cricopharyngeus muscle relaxes. This does not open the UES. Muscle relaxation in the cricopharyngeus allows the larynx to elevate and move forward by pull of the thyrohyoid and submandibular muscles. These muscles pull on the hyoid bone to move it up and forward. This then yanks the larynx up and forward. Thus, any damage to the thyrohyoid and/or submandibular muscles (mylohyoid, geniohyoid, or anterior belly of digastric) will damage hyolaryngeal upward and forward motion and thus affect the opening of the cricopharyngeal/upper esophageal sphincter (Kahrilas et al, 1995).
Role of aging in normal swallow
Among the changes that occur in the oropharyngeal swallow with normal aging is the increased frequency of using a dipper vs a tipper swallow (Dodds et al, 1989). The dipper swallow involves holding a liquid bolus on the floor of the mouth prior to initiating the swallow, and then sliding the oral tongue forward to pick up the bolus and bring it to the top of the tongue for initiation of the oral tongue movement to propel food backward and initiate the oral stage of swallow. In contrast, younger people use the tipper swallow more often, which involves holding the bolus on the top surface of the tongue as liquid is placed in the mouth. Then, the oral tongue immediately begins to propel the bolus backward to initiate the oral stage. While we know that the dipper pattern adds a slight but significant slowness to the oral stage of swallow, we do not know why this difference occurs. We do know that it does not relate to dental status, that is, the presence of a partial denture, absent teeth, or a full denture.
A second significant change in pharyngeal swallow with age is a slightly longer delay in triggering the pharyngeal stage. Increased slowness in movement is a general characteristic in aging. A third change with age is a loss of muscle reserve, especially in men (Logemann et al, 2002). A study of laryngeal and hyoid motion in 80-plus-year-old men vs 21- to 30-year-old men revealed that the movement of the hyoid and larynx to open the UES was identical to the point of upper sphincter opening for both the young and older men (Logemann et al, 2000). However, there was a significant difference between the hyoid and laryngeal movements after upper sphincter opening.
As shown in Figures 2a,b, the older and younger men pulled the hyoid anteriorly to the same level to produce opening of the UES. Younger men, however, continued the anterior motion of the hyoid until they achieved upper sphincter opening and went further by 8 mm. The difference between the amount of hyoid anterior movement needed to open the upper sphincter and the anterior amount of movement actually used in total is reserve. In older men, the hyoid anterior movement was just enough to get the UES open and only 1 to 2 mm more. While it may be said that the older men were more efficient in hyoid anterior movement in achieving UES opening, in fact, they exhibit no reserve. This difference in muscle control with age is also known as sarcopenia. Reserve is needed when someone becomes ill and loses muscle strength, particularly when they are in bed with the flu or some other infection. In the aging individual, having no reserve leaves them at risk of losing muscle strength to open the UES, thus damaging their oropharyngeal swallow and potentially causing an inefficient swallow with following aspiration. It has also been demonstrated that sarcopenia affects the oral aspect of the tongue, thus making it a less effective pressure generator during the oral stages of swallow.
Another normal change with age is an increase in frequency of laryngeal penetration of food during swallow (Robbins et al, 1992; Robbins et al, 1999). Penetration is the entry of food or liquid into the airway, but not below the true vocal folds. The frequency of penetration of thin liquid increases from the 20s through the 90s in normal subjects (Daggett et al, 2006). In these normal subjects, the penetration was not aspirated and no cough was needed to clear it from the airway. Airway clearance of penetrated material occurs in normal subjects of all ages as the larynx and hyoid continue to elevate and squeeze the penetrated material out of the airway (Daggett et al, 2006). Interestingly, the Daggett study found that at age 50, penetration began on pudding material and also increased slightly with age. These changes in penetration with age may again reflect the reduction in hyolaryngeal lifting because of reduced muscular reserve.
Abnormalities in the oropharyngeal swallow and their evaluation
Any of over 22 muscles or structures utilized in swallow can be damaged individually or in combination, depending on the etiology of the patient's swallowing disorder. Almost any neurologic damage or disease can affect the oropharyngeal swallow, as can head and neck cancer and its treatment and other types of structural damage such as spinal cord injury, head injury, or systemic diseases such as lupus or rheumatoid arthritis. The general management of oropharyngeal dysphagia begins with a clinical bedside assessment of the oral stage and pharyngeal stage of the swallow. At bedside and chair side, the patient is examined in the mouth and pharynx and a careful review of the patient's medical history is completed. Because the pharyngeal stage of swallow is complex, it is not visible clinically. Therefore, the bedside clinical evaluation is generally followed by a radiographic study, most often as the modified barium swallow (MBS) (Logemann, 1993). In this examination, the patient is given several swallows of measured volumes of thin liquids (1, 3, 5, 10 ml, and cup drinking) to define changes in physiology that occur with volume. Then, pudding or yogurt-textured barium is given in 3 ml amounts to look at the effect of the thicker viscosity. Finally, one-fourth of a Lorna Doone cookie coated with barium pudding is given, and the patient asked to chew and swallow it to assess the effect of mastication and of thicker viscosity on the swallow. If the patient exhibits a significant swallow disorder, strategies for treatment are introduced during the X-ray so that the optimal swallow conditions can be defined. The goal is to eliminate any aspiration and reduce the residue left behind after the swallow, thus improving the swallow safety and efficiency. The types of strategies include posture changes (Logemann et al, 1989; Welch et al, 1993; Logemann et al, 1994), heightening sensory input (Lazzara et al, 1986), teaching the patient a voluntary control during swallow (Kahrilas et al, 1991), and examining different food consistencies to identify the easiest for the patient to swallow. At the end of the MBS, a report is written that determines if the patient aspirates or has residue – that is, an inefficient swallow – and why or what causes these symptoms. Then, the successful or unsuccessful interventions to improve the swallow are defined. Thus, the goal for the patient during the MBS is to leave the test able to eat some foods safely and efficiently (Logemann, 1993).
The role of dentistry in the oropharyngeal swallow process and research needs
Status of dentition is a critical factor in the patient's ability to successfully chew in the presence of adequate oral tongue control. Having functional units – that is, maxillary and mandibular teeth, which match or make a functional unit – is critical to mastication. Maintaining some functional units is an important goal for the patient, particularly after treatment for head and neck cancer. Leaving the patient edentulous before treatment of head and neck cancer may make it difficult for the patient to wear a denture or any specially needed oral prosthesis. Maintaining several functional units is critical to facilitating mastication but also stabilizing a denture or other dental prosthesis.
The dentist should ask each patient, especially those 60 years and older and/or have any neurologic disease, damage to the head or neck, the following questions: Do you have any problems swallowing? Do you avoid any foods? Why? If yes, point to where you feel the problem is located? If the patient points to their mouth or their mid-neck, that is usually an oropharyngeal problem. If the patient points to their sternum or the bottom of their neck, it usually means an esophageal problem and the patient should be referred to a gastroenterologist.
Do you have any problem chewing? If yes, the dentist should examine oral tissues for any mucositis, xerostomia, or other oral tissues or dental diseases. Reporting these conditions to the patients' doctor(s) is critical. Xerostomia causes patients to feel they cannot swallow at all even though their swallow measures are normal on thin and nectar-thickened liquids and pureed foods. Much more research is needed on sensory changes resulting from dry mouth (Logemann et al, 2001, 2003; Rogus-Pulia and Logemann, 2011).
Maintaining oral health is also critical in the patient with dysphagia, particularly in those over age 60. Unfortunately, the speech-language pathologist, who is usually the clinician evaluating and treating the patient's dysphagia, often notes chronically poor oral care in patients in the healthcare system, whether the patient is in acute care, skilled nursing facilities, or other levels of care. The importance of this is emphasized by health care in Japan. That country's health insurance covers the cost of a dentist and/or dental hygienist going into nursing homes weekly to maintain good oral health. The US provisions of the federal Nursing Home Reform Act of 1987 (NHRA) acknowledged the importance of dentistry, declaring that long-term care (LTC) facilities ‘must provide (or arrange for the provision of) routine dental services and emergency dental services (that meet professional standards of quality) to meet the needs of each resident (42 U.S.C. §1396r(b)(4)(A)(vi))’. Despite this declaration, the Surgeon General's 2000 proclamation still holds true today: ‘By any standards in the United States, (residents in LTC facilities experience) a high degree of dental disease and dental care needs (US Surgeon General’s Report, 2000, p. 262 in U.S. Department of Health and Human Services, 2000; U.S. Department of Health and Human Services and National Center for Health Statistics, 2009)'. Studies conducted post-US Omnibus Budget Reconciliation Act (OBRA) 1987 show that elderly LTC residents continue to experience poor oral health status and have ‘substantial oral healthcare needs’ (Katz et al, 2010, p. 434).
While the NHRA 1987 dictates the minimum national standards for assessing dental care needs, it provides no minimum national intervention guidelines for the delivery of oral hygiene care (OHC) once such needs are identified. Current literature focuses on identifying and/or clarifying the Act's OHC assessment standards, or on refining the existing assessment guidelines (Katz et al, 2010). In contrast, little research has been carried out on the delivery of OHC services to elderly residents at any level of healthcare or on the daily intervention process itself vis-à-vis this population (Chalmers and Pearson, 2005; Coleman and Watson, 2006).
Perhaps most striking was the finding that of the eight (8) standards of OHC developed for the Coleman and Watson study by a panel of 10 geriatric experts, five (5) were never met. These included brushing teeth at least 2 min, flossing, oral assessment, rinsing with mouthwash, and wearing clean gloves during OHC (Coleman & Watson, 2006, p. 138). These investigators found that residents' teeth were brushed and mouths rinsed with water in only 16% of their observations, that is, 11 of the 67 residents. The overall average time spent on grooming the residents was 21:38 min. However, the average time spent by the certified nursing assistants (CNAs) on brushing a resident's teeth was 16.2 s, and the average time spent by the resident on brushing his/her teeth with cueing by a CNA was 39.3 s (2006, p. 140). In addition, Coleman and Watson found that for over two-thirds of the residents (68.7%), none of the basic OHC supplies (e.g., toothpaste, toothbrush, mouthwash, or toothette) were observed in either the residents' bathrooms, shower areas, or the washbasins used by the CNAs (2006, p. 141).
Critical questions still need to be answered regarding the role of oral bacteria in development of aspiration pneumonia (Garcia, 2005). There is a strong belief among dysphagia experts that poor oral care can lead to aspiration of oral bacteria resulting in aspiration pneumonia (Bassim et al, 2008). This is an important question to be answered by dentists in conjunction with caregivers, dysphagia experts, and pulmonologists. Many elderly patients with dysphagia are unable to keep their own mouth clean. Despite the fact that much of this research noted above was completed 6–10 years ago, little has changed. The importance of this problem places increased emphasis on the dental community, nursing, and dysphagia researchers to join together to study and define the optimal ways for caregivers in the home or healthcare situations to maintain optimal oral health for these patients.
G. Gensler – analyzed data; F.A. Curro – design of study and additional dental approach; B. Pauloski – collection of data; J.A. Logemann – design and collection of data.