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.

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Funding

This study was funded by the Health Research Council of New Zealand and the HOPE Foundation.

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Correspondence to Marie Jardine.

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The authors declare that they have no conflicts of interest.

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Marie Jardine has received scholarships for her PhD from the Health Research Council of New Zealand and the HOPE Foundation.

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. 1.

    Was the cohort recruited in an acceptable way?

  2. 2.

    Was the outcome accurately measured to minimize bias?

  3. 3.

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

  4. 4.

    Do the results include quantitative measures of swallowing or swallowing parameters?

  5. 5.

    Are the results plausible?

  6. 6.

    Does the study include participants over 85 years old?

  7. 7.

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

  8. 8.

    Does the study report clinical implications?

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Jardine, M., Miles, A. & Allen, J. A Systematic Review of Physiological Changes in Swallowing in the Oldest Old. Dysphagia 35, 509–532 (2020). https://doi.org/10.1007/s00455-019-10056-3

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Keywords

  • Deglutition
  • Deglutition disorders
  • Systematic review
  • Aged, 80 and over
  • Healthy volunteers