A Systematic Review of Physiological Changes in Swallowing in the Oldest Old

Abstract

Age-related swallowing changes are well-researched in deglutology, usually distinguishing those over 60 years as older aged. World-wide, older adults are healthier and forecast to live longer: many over 85 years. It is necessary for clinicians to understand healthy swallowing changes in this ‘oldest old’ in order to appropriately manage swallowing complaints in older patients. This systematic review collated and critically appraised studies investigating swallowing changes in adults over 85 years using instrumental assessment. Criteria for inclusion were healthy subjects over 85 years. Exclusion criteria included studies focused on anatomy and oral processing. Studies published until December 2018 were retrieved from BIOSIS, CINAHL, Embase, Medline, and Scopus, totaling 2125 articles. During data screening, 64% of studies investigating age-related swallowing changes were excluded, as the oldest old were not recruited. After PRISMA screening, 44 articles met criteria. These were further reviewed for data extraction, bias and quality. Main quantitative age-related changes in swallowing included increases in delay in swallow onset, bolus transit times, duration of UES opening, pressure above the UES and UES relaxation pressure, and reduction in pressure at the UES. Few studies detected increased residue or airway compromise in the form of aspiration. Results were not easily comparable due to differences in age ranges, methods for deeming participants ‘healthy’, measures used to define swallowing physiology, and swallowing tasks. Age-related swallowing changes are identified that do not compromise safety. The oldest old are underrepresented in normative deglutition research. It is essential future studies plan accordingly to recruit those over 85 years.

Appendices

Appendix 1: Details of Included Studies

Study (in chronological order)	Age range	Participant groups (n)	Oldest group (mean, SD)	How deemed ‘healthy’?	Medications?	Instrumental assessment	Swallow tasks (bolus size, texture)	Study aim
Khan et al. [47]	20–89 years	20–39 years (43) 60–89 years (49)	Not stated	Interview: ‘carefully questioned’	Not stated	LRM	5 ml boluses of water, total unclear	Effect of age on esophageal motility
Dejaeger et al. [31]	Not stated	Healthy volunteers (20) Elderly (16)	80 years, 5 years	No relevant history	Not stated	VFS LRM	At least 3 × 10 ml liquid barium	Effect of age on quantitative and qualitative swallowing measures
Nishimura et al. [48]	23–89 years	< 49 years (11) 50–59 years (15) 60–69 years (11) > 70 years (10)	Not stated	No relevant history	Screened	LRM	10 × 3–5 ml tap water	Effect of age on esophageal motility
Dejaeger et al. [46]	Not stated	Young (18) Elderly (25)	80 years, 7 years	No relevant history	Screened	VFS LRM	3 × 10 ml liquid barium	Quantitative differences in swallowing between swallows with and without pharyngeal residue
Rademaker et al. [19]	20–89 years	20–39 years (61) 40–59 years (45) 60–79 years (38) 80–89 years (23)	Not stated	No relevant history	Screened	VFS	2 × 1, 3, 5 and 10 ml liquid barium	Effect of age and bolus size on healthy swallowing function
Kern et al. [40]	24–90 years	Young (14) Elderly (14)	75 years, 2.8 years	Not stated: ‘without any swallowing difficulties’	Not stated	VFS LRM	3 × 5 and 10 ml liquid barium	Effect of age on timing, width and pressure of UES opening, and associated biomechanical events
Logemann et al. [20]	21–94 years	21–29 years (8) 80–94 years (8)	Not stated	No relevant history	Screened	VFS	2 × 1 and 10 ml liquid barium	Effect of age on swallowing timing and biomechanics
Yokoyama et al. [32]	21–89 years	21–31 years (32) 61–74 years (12) 75–89 years (12)	Not stated	Not stated: ‘nondysphagic’	Not stated	LRM VFS	10 ml liquid barium	Effect of age on swallowing pressure and function
Logemann et al. [21]	21–93 years	21–29 years (8) 80–93 years (8)	Not stated	No relevant history	Screened	VFS	2 × 1 and 10 ml liquid barium	Effect of age on swallowing function
Van Herwaarden et al. [44]	18–91 years	< 60 years (61) > 60 years (23)	71.3 years	No relevant history	Screened	LRM	3 × at least 4 swallows of 5 ml water, 5 ml pudding and ¼ cookie	Effect of age and gender on UES and pharyngeal manometric parameters
Kendall et al. [57]	18–88 years	Young (60) Old (63)	Not stated	Self–reported, no relevant history	Not stated	VFS	1 and 20 ml liquid barium	Coordination between structural movements relative to bolus movements before UES opening
Kendall et al. [58]	65–88 years	No medical problems (23) Medical conditions (63)	Not stated	No relevant history, head and neck exam	Screened: taken for chronic older conditions	VFS	1 and 20 ml liquid barium	Effect of medical conditions on swallowing in older adults
Leonard et al. [33]	18–88 years	Nonelderly (84) Elderly (88)	Median 70 years	Interview, HEENT exam, dietary questionnaire	Screened: taken for chronic older conditions	VFS	Lateral: 1 and 3 ml paste, 20 ml liquid bolus. Anterior–posterior: 20 ml liquid bolus	Effect of age on UES opening. Relationship between UES opening and swallowing events
Kim et al. [22]	21–87 years	Younger (20) Older (20)	Not stated	Questionnaire, cranial nerve exam	Not stated	VFS	2 × 5 and 10 ml thin liquid. Puree and solid not analyzed	Effect of age and gender on swallowing timing
Martin-Harris et al. [34]	Not stated	All healthy (76)	Not stated ≥ 81 years	Interview, questionnaire	Screened	VFS	2 × 5 ml liquid barium	Normative respiratory patterns and temporal coordination of breathing and swallowing
Martin-Harris et al. [35]	21–97 years	21–40 years (21) 41–59 years (21) 61–80 years (19) 81–97 years (21)	86 years	Interview, questionnaire	Screened	VFS	2 × 5 ml liquid barium	Effect of age on swallowing and interdependence of temporal onsets of swallowing events
Yoshikawa et al. [23]	24–87 years	Young (14) Elderly (19)	81.2 years	Questionnaire, interview, repetitive saliva swallowing test	Not stated	VFS	3 ml barium solution, 3 × 10 ml barium solution	Effect of age on swallowing
Daggett et al. [50]	20–94 years	< 30 years (13) 30–39 years (14) 40–49 years (13) 50–59yrs (13) 60–69 years (15) 70–79 years (13) 80–89 years (13) 90+ years (4)	Not stated	No relevant history	Screened	VFS	2 × thin liquid (1, 3, 5, 10 ml, own sip from cup), 3 ml pudding, ¼ cookie, bite of apple	Effect of age, bolus type and volume on severity of penetration
Dozier et al. [59]	23–91 years	All healthy (70)	Not stated	Interview, questionnaire	Screened	VFS	50 ml of liquid barium	Comparison of respiratory patterns during sequential swallowing to single liquid swallows
Leonard and McKenzie [60]	18–88 years	Nonelderly (63) Elderly (88)	Median 70 years	No relevant history	Screened: taken for chronic older conditions	VFS	Lateral: 1 and 3 ml paste, 20 ml liquid bolus. Anterior–posterior: 20 ml liquid bolus	Relationship between bolus transit and hyoid displacement
Martin–Harris et al. [24]	21–97 years	All healthy (76)	Not stated	Interview, questionnaire	Screened	VFS	2 × 5 ml liquid barium	Effect of age on bolus head location and temporal measures
McCullough et al. [25]	21–103 years	21–39 years (20) 40–59 years (20) 60–79 years (20) 80+ years (20)	Not stated	Questionnaire, cranial nerve, oral motor and structural exam	Not stated	VFS	3 × 5 and 10 ml thin, 2 × 20 ml thin, 2 × 5 ml puree, 2 × cookie, 3 oz thin liquid sequential	Effect of age, gender and bolus on swallowing function, residue, penetration and aspiration
Mendell and Logemann [61]	22–92 years	20–29 years (20) 40–49 years (20) 60–69 years (20) 70–79 years (20) 80+ years (20)	Not stated	No relevant history from database	Screened	VFS	2 × 3 and 10 ml liquid barium, 1x 3 ml paste barium	Description of swallowing event sequencing
Kelly et al. [51]	23–88 years	Young (21) Elderly (30)	75 years	No relevant history	Screened	FEES	5, 10 ml and large mouthful liquid, 10 ml yogurt, 10 ml chopped banana, 3x3 cm sandwich	Effect of age on amount and location of pharyngeal residue from unmodified boluses
Kim and McCullough [41]	21–87 years	Young (20) Old (20)	77.2 years, 6.85 years	Questionnaire, cranial nerve exam, oral motor/structural exam	Not stated	VFS	2 × 5 and 10 ml thin liquid barium	Effect of age on hyoid movement
Butler et al. [52]	69–87 years	Healthy older adults (20)	78.9 years	Questionnaire	Screened	FEES LRM	Catheter in vs out (5 ml water and 10 ml milk); 10 ml water vs milk vs barium; cup vs syringe (5 and 10 ml milk); 5 ml milk vs pudding vs 2 g cracker	Effect of catheter, bolus (type, volume, viscosity), delivery method or gender on penetration and aspiration in healthy older adults
Ayala and Logemann [26]	20–90 years	20–30 years (10) 60–70 years (10) 80–90 years (10)	83.7 years	Self–reported	Not stated	VFS	45 total swallows, including cold, thin, paste, sour, sweet, cold and sour, water	Effect of sensory bolus characteristics (temperature, taste, viscosity) and continuous use on swallowing
Butler et al. [53]	61–90 years	61–70 years (18) 71–80 years (28) 81–90 years (30)	83.8 years, 2.3 years	Self-reported	Not stated	FEES	5, 10, 15 and 20 ml × water, skim milk, 2% milk, whole milk via straw and cup	Effect of age, sex, liquid type, delivery method and volume on penetration and aspiration
Kurosu and Logemann [42]	22–94 years	Young (20) Middle-aged (20) Older (20)	84.5 years	Questionnaire	Screened	VFS	2 × 1, 3, 5, 10 ml and self-selected sip liquid barium, 2 × 3 ml barium paste, ¼ cookie with paste	Effect of age and gender on airway closure and UES opening
Butler et al. [27]	61–90 years	61–70 years (18) 71–80 years (26) 81–90 years (33)	83.6 years, 2.4 years	Self-reported	Not stated	FEES	5, 10, 15 and 20 ml × water, skim milk, 2% milk, whole milk via straw and cup; soy milk (5, 10, 15 and 20 ml straw); puree (5, 10 ml applesauce and pudding); 2 g cracker	Effect of age, sex, liquid type, delivery method and viscosity on bolus dwell times
Butler et al. [54]	69–87 years	Healthy older adults (19)	79.2 years	Questionnaire	Screened	FEES LRM	Catheter in: 5 and 10 ml water and milk Catheter out: 5 and 10 ml water and milk via syringe; 5, 10, 15 ml water and milk via cup	Effect of aspiration status, sensor location, liquid type and volume on pharyngeal and UES pressures
Brodsky et al. [62]	21–97 years	21–40 years (21) 41–60 years (21) 61–80 years (19) > 81 years (21)	Not stated	Interview, questionnaire	Screened	VFS	2 × 5-ml liquid barium	Relationship between swallow non-inspiratory flow and swallowing events, and effect of age
Im et al. [36]	21–89 years	Younger (20) Older (20)	77.25 years, 8.4 years	Cranial nerve exam, questionnaire	Not stated	VFS	2 × 5 ml thin liquid, thick liquid, puree	Effects of age, gender and bolus consistency on swallowing
Omari et al. [28]	20–91 years	20–39 years (15) 40–59 years (15) 60–79 years (18) 80+ years (20)	84 years	Self-reported, questionnaire	Screened	HRIM	5 × 5 ml and 10 ml saline, 5 ml and 10 ml viscous bolus	Effect of age on automated impedance manometry (AIM) analysis and the swallow risk index
Veiga et al. [37]	62–87 years	Elderly (30)	72.8 years, 7 years	No relevant history	Not stated	FEES	100 ml water via cup and via straw	Effect of cup or straw during sequential swallowing by healthy elderly
Kagaya et al. [63]	25–89 years	Younger < 60 years (28) Older ≥ 60 years (25)	Median 70 years	No relevant history	Not stated	VFS	10 ml liquid barium, 8 g corned beef, 5 ml liquid barium with 4 g corned beef	Effect of age and bolus type on occurrence of isolated pharyngeal swallow
Cock et al. [45]	20–93 years	Younger (30) Older (15)	85 years, 4 years	No relevant history, questionnaire	Screened	HRIM	5 × 5 and 10 ml liquid and viscous bolus	Effect of age on bolus clearance and esophageal propulsive physiology
Cock et al. [29]	20–91 years	Younger (50) Older healthy (16) Patients (27)	85 years, 4 years	Interview, questionnaire	Screened	HRIM	5 × 5 ml liquid and viscous boluses	Comparison of UES function in patients (with restricted UES opening) to healthy controls across ages
Miles et al. [38]	20–98 years	< 40 years (36) 40–59 years (27) 60–79 years (32) 80+ years (13)	Not stated	Questionnaire	Not stated	VFS	20 ml fluid bolus, barium tablet, 5 ml paste	Esophageal bolus transit times in healthy adults for a normative database
Cock et al. [49]	20–93 years	Younger (30) Older (15)	85 years, 4 years	No relevant history, questionnaire	Screened	HRIM	5 × 5 and 10 ml liquid and viscous bolus	Evaluation of esophagogastric junction function and effect of age
Butler et al. [55]	20–90 years	20–30 years (27) 31–40 years (29) 41–50 years (30) 51–60 years (27) 61–70 years (28) 71–80 years (31) 81–90 years (31)	84 years, 2.2 years	Self-reported	Not stated	FEES	4 liquid types (water, skim milk, 2% milk and whole milk) with 4 bolus volumes (5, 10, 15, and 20 ml) using 2 delivery methods (straw vs cup)	Effect of age, sex, liquid type, bolus volume and bolus delivery on penetration and aspiration
Herzberg et al. [64]	22–90 years	Young (20) Older (23)	74.7 years	No relevant history	Not stated	VFS	3 × 5 and 20 ml thin liquid barium, 5 ml nectar thick barium	Effect of age on swallowing event sequencing
Jardine et al. [39]	20–99 years	Younger (45) Older > 70 years (59) Patients (55)	81.2 years, 8.18 years	Questionnaire	Not stated	VFS	Lateral view: 1, 3, 20, 100 ml liquid barium, 3 ml barium paste. A-P view: 20 ml liquid barium, 3 ml paste, pill	Comparison of quantitative swallowing measures in healthy adults vs older patients with new onset dysphagia
Molfenter et al. [56]a	> 65 years	Healthy seniors (44)	76.9 years, 7.1 years	Interview, oral motor sensory exam, questionnaire	Not stated	VFS	12 self-administered, uncued barium boluses. 9 for this study: 3 × 5 ml and 20 ml thin liquid, nectar thick liquid	Effect of pharyngeal volume on pharyngeal swallowing biomechanics and residue in healthy aging

1. ^aIn December 2018 this article was accessible early online

Appendix 2: Adapted checklist from the Critical Appraisal Skills Programme

• 1. Was the cohort recruited in an acceptable way?

• 2. Was the outcome accurately measured to minimize bias?

• 3. Have the authors identified all important confounding factors, and included these in the design and/or analysis?

• 4. Do the results include quantitative measures of swallowing or swallowing parameters?

• 5. Are the results plausible?

• 6. Does the study include participants over 85 years old?

• 7. Do the results develop our understanding of swallowing in advanced age?

• 8. Does the study report clinical implications?