Poor Taste and Smell Are Associated with Poor Appetite, Macronutrient Intake, and Dietary Quality but Not with Undernutrition in Older Adults ...
←
→
Page content transcription
If your browser does not render page correctly, please read the page content below
The Journal of Nutrition
Nutrition and Disease
Poor Taste and Smell Are Associated with
Poor Appetite, Macronutrient Intake, and
Dietary Quality but Not with Undernutrition
in Older Adults
Kristina S Fluitman,1,2 Anne C Hesp,1 Rachel F Kaihatu,1 Max Nieuwdorp,1,3 Bart JF Keijser,4,5
Richard G IJzerman,1 and Marjolein Visser2,6
1
Department of Internal Medicine, Amsterdam University Medical Centers, Amsterdam, Netherlands; 2 Amsterdam Public Health Research
Downloaded from https://academic.oup.com/jn/article/151/3/605/6131860 by guest on 06 April 2021
Institute, Amsterdam, Netherlands; 3 Department of Vascular Medicine, Amsterdam University Medical Centers, Amsterdam, Netherlands;
4
Department of Microbiology and Systems Biology, TNO Earth, Life and Social Sciences, Zeist, Netherlands; 5 Department of Preventive
Dentistry, Academic Center for Dentistry Amsterdam, University of Amsterdam and VU University, Amsterdam, Netherlands; and
6
Department of Health Sciences, Faculty of Science, Vrije Universiteit Amsterdam, Amsterdam, Netherlands
ABSTRACT
Background: Age-related declines in taste and smell function are widely assumed to contribute to the decrease in
appetite and the development of undernutrition in older adults.
Objectives: Here we aim to assess the associations of both taste and smell function with several nutrition-related
outcomes in a single study, with poor appetite and undernutrition as primary outcomes.
Methods: This is a cross-sectional cohort study of 359 community-dwelling Dutch older adults, aged 65–93 y. Taste
function was measured for all 5 basic tastes. Smell function was assessed with 3 tests: for odor identification,
discrimination, and threshold. Self-reported taste and smell, appetite, energy (kcal/d) and macronutrient (% energy)
intake, and covariates were assessed with extensive questionnaires. Dietary quality was calculated using the Dutch
Healthy Diet index 2015, Alternative Healthy Eating Index 2010, and Mediterranean Diet Score. Body measurements
included body weight (current and 2 y prior), height, and body impedance analysis. Data were analyzed via multiple
logistic and linear regression.
Results: Of our sample, 9.2% had poor taste and 17.0% poor smell, 6.1% had poor appetite, and 21.4% were
undernourished. Self-reported poor taste (OR: 8.44; 95% CI: 1.56, 45.56; P = 0.013) was associated with poor appetite,
but no other taste or smell score was associated with either poor appetite or undernutrition. Some associations were
found of individual taste and smell scores with macronutrient intake and dietary quality. Self-reported poor taste and
smell were both consistently associated with poorer dietary quality.
Conclusions: In community-dwelling older adults, specific taste and smell impairments may have diverse
consequences for appetite, food intake, or dietary quality. However, this does not necessarily result in undernutrition.
The consistent associations of self-reported poor taste and smell with poor dietary quality do underline the usefulness
of this information when screening for nutritional risk. J Nutr 2021;151:605–614.
Keywords: gustatory function, olfactory function, appetite, undernutrition, macronutrient intake, dietary quality,
older adults
Introduction spoiled foods or environmental hazards (4, 5). Moreover,
depending on previous experiences, they help to assign positive
The risk of undernutrition increases with age. It affects 9%–
or negative attributions to certain foods or situations (5, 6),
28% of older adults in Europe (1) and is associated with
possibly directing future food-related behavior (4). However, an
increased morbidity, mortality, and health care costs (2). Impor-
age-related decline has been demonstrated for both olfactory
tant roles in nutritional health are fulfilled by taste (gustatory)
and gustatory function (7–10). This sensory decline is thought
and smell (olfactory) functions (3). Taste and smell guide
to cause decreased food enjoyment, poor appetite, decreased or
individuals toward nutritious foods and away from harmful,
C The Author(s) 2021. Published by Oxford University Press on behalf of the American Society for Nutrition. This is an Open Access article distributed under the terms
of the Creative Commons Attribution-NonCommercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution,
and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
Manuscript received June 1, 2020. Initial review completed July 21, 2020. Revision accepted November 19, 2020.
First published online February 9, 2021; doi: https://doi.org/10.1093/jn/nxaa400. 605altered food intake, and ultimately contribute to the increased Methods
risk of undernutrition in older adults (3).
Design
Many studies have investigated the association of poor olfac- This cross-sectional study was embedded within the ongoing Longi-
tory and gustatory function with undernutrition, but literature tudinal Aging Study Amsterdam (LASA), which included 3107, 1002,
on this topic remains inconclusive. Whereas some studies found and 1023 Dutch community-dwelling older adults in 1992/1993,
poor olfactory function to be associated with low BMI (8, 11– 2002/2003, and 2012/2013, respectively. Data on physical, social,
13), poor appetite (11, 14), altered macronutrient intake (15, emotional, and cognitive functioning are collected in waves every 3 y
16), or poor dietary quality (13), others did not (14, 17–19). In by means of medical and general interviews, the former also including
this context, poor olfactory function is often operationalized by body measurements. The most recent wave took place in 2015/2016.
low scores on odor identification tests (e.g., the Sniffin’ Sticks The design of the LASA has been described more elaborately
test, the San Diego Odor Identification test, or the University elsewhere (23–25). For the current substudy, data were used from the
regular LASA cycle 2015/2016 and from an extra home visit, which
of Pennsylvania Smell Identification Test) (8, 11–14, 17, 18),
took place in between regular data-collection waves in 2017/2018.
whereas other studies also included threshold tests (16, 19) LASA participants who took part in the LASA medical interview
or self-reported poor smell (15). Studies on the association of of 2015/2016 were prescreened on in- and exclusion criteria based
gustatory function with nutritional status are limited. In 1 study, on LASA data. Those who were found eligible were contacted by
gustatory impairment, measured by the Burghart Taste Strip phone in 2017/2018 and screened on the remainder of the in- and
test, tended to be associated with diminished eating pleasure exclusion criteria before the extra home visit was planned. Inclusion
Downloaded from https://academic.oup.com/jn/article/151/3/605/6131860 by guest on 06 April 2021
(18), and a second study found thresholds >0.003% wt:wt for criteria for our substudy were age >65 y, valid measurement of
bitter taste to be associated with having a BMI (in kg/m2 ) 30 or by >2% body
weight gain between the 2 latest LASA examination waves (from
intake, or appetite (14). Although overall gustatory impairments
2011/2013 to 2015/2016), diagnosed active malignancy, and poor
may not affect total food or energy intake, impairments of cognitive status defined as a Mini Mental State Examination (MMSE)
specific tastes have been shown to alter food preferences, scorefrom 0 to 10 (33). Because our FFQ does not adequately measure the to smell identification score (normosmia and hyposmia) and according
intake of salt or type of coffee, these components were left out, leaving to total taste score (normogeusia and hypogeusia). Differences in
a potential score from 0 to 130 (32). Second, the Alternative Healthy characteristics were tested using the unpaired Student’s t test, Mann–
Eating Index 2010 (AHEI) was previously used in the LASA (34) and Whitney U test, Fisher’s exact test, ANOVA test, or Kruskal–Wallis test,
scores 11 dietary components from 0 to 10 based on their predictive as appropriate.
power for chronic disease (35). Again, the AHEI sodium component Then, logistic regression models were run to test the associations
was excluded from our study, leaving a total score of 0–100 (34). Third, of poor total taste score and poor smell identification score with our
the Mediterranean Diet Score (MDS), also previously used in the LASA primary outcomes of undernutrition and poor appetite. These models
(34), scores 11 dietary components from 0 to 5 to assess the adherence were tested for effect modification by age, sex, BMI, and smoking status.
to a typical Mediterranean diet (total score: 0–55) (36). A higher score Next, similar linear models were built to test the associations with the
for all indexes indicates better adherence to a healthy diet (33, 35, 36). secondary outcomes of food intake and dietary quality. All models were
also run for all individual taste and smell scores, as well as self-reported
Gustatory function poor taste and smell. Because the taste test was originally designed
Gustatory function was assessed using taste strips (Burghart Messtech- without the umami flavor, the models were also run using the total
nik GmbH). This taste test commonly consists of 18 paper taste strips, taste score excluding umami. Because the individual taste scores are part
of which 2 are tasteless and 16 are impregnated with 4 increasing of the overall taste test, Bonferroni correction for multiple testing was
concentrations of sweet, sour, salty, and bitter tastes (37). Upon request, carried out for models with the taste test scores as determinants (total
4 umami taste strips were specially added by Burghart to their standard taste, total taste excluding umami, sweet, salty, sour, bitter, and umami).
test, reproducing the taste strip test validated by Mueller et al. (38). The The same was done for models with the smell scores as determinants
Downloaded from https://academic.oup.com/jn/article/151/3/605/6131860 by guest on 06 April 2021
same test design, tastant concentrations, and sequence in which taste (TDI, threshold, discrimination, and identification). The Bonferroni-
strips were presented were used. Participants received 1 point for each corrected α-levels used for statistical significance were 0.007 (= 0.05/7)
correctly identified taste, with each individual taste score ranging from and 0.013 (= 0.05/4), respectively. Bonferroni-corrected P values are
0 to 4, and the total score ranging from 0 to 20. A total taste score reported. All regression models were adjusted for age, sex, education,LASA parcipants in 2015/2016:
n = 2024
LASA parcipants who had not taken part in the
medical interview in 2015/2016 (n = 382)
LASA parcipants screened based
on LASA data: Exclusion based on LASA data:
n = 1642 Age 2% recent body weight gain (n = 219)
BMI ≥ 30kg/m2 (n = 140)
MMSE scoreTABLE 1 Characteristics for all participants and stratified by olfactory and gustatory function1
Hyposmia Normosmia Hypogeusia Normogeusia
n All (n = 66) (n = 292) P value (n = 33) (n = 325) P value
Demographics
Age, y 359 73 [69–77] 75 [71–81] 72 [69–77]TABLE 2 Associations of poor taste and smell with poor appetite and undernutrition1
Poor appetite2 P value3 Undernutrition4 P value3
Poor total taste score5 1.04 (0.19, 5.76) 1.00 1.15 (0.43, 3.05) 1.00
Poor total taste score (no umami) 1.78 (0.33, 9.60) 1.00 1.58 (0.58, 4.31) 1.00
Poor sweet score 0.64 (0.14, 2.96) 1.00 0.83 (0.38, 1.83) 1.00
Poor sour score 0.90 (0.29, 2.79) 1.00 0.80 (0.44, 1.46) 1.00
Poor salty score 1.78 (0.62, 5.07) 1.00 1.27 (0.73, 2.23) 1.00
Poor bitter score 0.25 (0.02, 2.78) 1.00 0.71 (0.22, 2.31) 1.00
Poor umami score 0.68 (0.21, 2.19) 1.00 0.84 (0.46, 1.53) 1.00
Self-reported poor taste 8.44 (1.56, 45.56) 0.01 2.11 (0.49, 9.04) 0.32
Poor smell identification score6 1.50 (0.48, 4.71) 1.00 1.35 (0.69, 2.62) 1.00
Poor TDI score 3.67 (0.78, 17.19) 0.40 2.02 (0.73, 5.58) 0.68
Poor smell threshold score 4.71 (1.11, 19.91) 0.16 1.85 (0.77, 4.44) 0.68
Poor smell discrimination score 0.15 (0.02, 1.26) 0.32 0.99 (0.38, 2.57) 1.00
Self-reported poor smell 2.31 (0.50, 10.74) 0.29 0.85 (0.27, 2.68) 0.78
1
Values are ORs (95% CIs) or P values. All models adjusted for age, sex, educational status, smoking status, medication, Center for
Downloaded from https://academic.oup.com/jn/article/151/3/605/6131860 by guest on 06 April 2021
Epidemiologic Studies Depression score, and Mini Mental State Examination score. TDI, threshold-discrimination-identification.
2
Poor appetite: Council of Nutrition Appetite Questionnaire score 5% body weight loss averaged over 2 y or BMI (in kg/m2 )Values are regression coefficients (β), 95% CIs, or P values. All models adjusted for age, sex, educational status, smoking status, medication, Center for Epidemiologic Studies Depression score, and Mini Mental State Examination score. En%,
to the risk of frailty and disability in older adults (45–47). In
P value2
0.77
1.00
1.00
0.49
1.00
0.04
0.02
1.00
1.00
1.00
1.00
1.00
0.43
our multivariate models, however, significance was lost after
correction for multiple testing. Finally, in a previous study,
Fatty acid intake, En% we hypothesized that perceiving an odor (i.e., odor threshold
function) is more important for food-related behavior and
− 3.45 (−5.76, −1.17)
− 1.72 (−3.86, 0.42)
− 1.19 (−3.50, 1.13)
0.78 (−0.91, 2.47)
− 1.21 (−2.51, 0.09)
− 0.57 (−1.83, 0.69)
0.26 (−1.07, 1.58)
0.51 (−1.09, 2.10)
0.55 (−2.32, 3.43)
− 0.58 (−2.99, 1.83)
0.19 (−2.31, 2.69)
1.05 (−1.54, 3.64)
appetite than being able to identify it (12). On first glance,
3.89 (0.17, 7.61)
this hypothesis did not hold true because poor threshold score
β (95% CI)
was not associated with any of our outcomes. However, the
association of poor threshold score with poor appetite (OR: 4.7;
95% CI: 1.11, 19.91) was only rendered nonsignificant after
adjustment for multiple testing (P = 0.16). The relatively large
OR, combined with the relatively wide 95% CI, does suggest the
analysis was underpowered, possibly owing to the low number
of participants with poor appetite (n = 22).
P value2
1.00
1.00
0.49
1.00
1.00
1.00
1.00
0.02
0.12
1.00
0.68
1.00
0.12
Protein intake, En%
Self-reported taste and smell impairments
An important finding of this study was that poor self-
Downloaded from https://academic.oup.com/jn/article/151/3/605/6131860 by guest on 06 April 2021
reported taste and smell were both consistently associated
− 1.71 (−3.16, −0.26)
− 0.70 (−1.32, −0.08)
0.14 (−0.70, 0.98)
0.12 (−0.79, 1.03)
− 0.61 (−1.27, 0.05)
0.32 (−0.19, 0.83)
0.08 (−0.42, 0.57)
0.57 (−0.34, 1.48)
0.38 (−0.14, 0.90)
− 0.34 (−1.44, 0.76)
− 0.65 (−1.58, 0.28)
− 0.47 (−1.43, 0.48)
− 0.81 (−1.82, 0.20)
with lower scores on all 3 dietary quality indexes, which are
β (95% CI)
related to nutrition-related health conditions (33, 35, 36). For
future research, it would be interesting to evaluate whether
specific food components of the dietary quality scores are
responsible for these associations. Poor self-reported taste
Poor taste: total taste scoreTABLE 4 Associations of poor taste and smell with dietary quality indexes1
Dutch Healthy Diet index Alternative Healthy Eating Index Mediterranean Diet Score
β (95% CI) P value 2
β (95% CI) P value 2
β (95% CI) P value2
Poor total taste score3 − 2.51 (−8.17, 3.14) 1.00 − 0.57 (−4.44, 3.30) 1.00 0.17 (−1.50, 1.84) 1.00
Poor total taste score (no umami) − 0.46 (−6.58, 5.66) 1.00 1.46 (−2.73, 5.64) 1.00 0.30 (−1.51, 2.11) 1.00
Poor sweet score 0.09 (−4.38, 4.56) 1.00 1.59 (−1.46, 4.64) 1.00 1.41 (0.10, 2.72) 0.28
Poor sour score 1.03 (−2.43, 4.50) 1.00 0.45 (−1.91, 2.80) 1.00 1.00 (−0.01, 2.01) 0.35
Poor salty score − 1.65 (−4.99, 1.69) 1.00 − 0.78 (−3.05, 1.49) 1.00 − 0.53 (−1.51, 0.45) 1.00
Poor bitter score − 1.18 (−7.32, 4.95) 1.00 − 1.98 (−6.17, 2.21) 1.00 − 0.84 (−2.65, 0.97) 1.00
Poor umami score − 3.39 (−6.88, 0.10) 0.42 − 1.57 (−3.95, 0.81) 1.00 − 1.39 (−2.41, −0.37) 0.07
Self-reported poor taste − 14.75 (−24.55, −4.95)5. Breslin PA. An evolutionary perspective on food and human taste. Curr 26. Whigham LD, Schoeller DA, Johnson LK, Atkinson RL. Effect of
Biol 2013;23(9):R409–18. clothing weight on body weight. Int J Obes 2013;37(1):160–1.
6. Sarafoleanu C, Mella C, Georgescu M, Perederco C. The importance of 27. Cederholm T, Bosaeus I, Barazzoni R, Bauer J, Van Gossum A, Klek S,
the olfactory sense in the human behavior and evolution. J Med Life Muscaritoli M, Nyulasi I, Ockenga J, Schneider SM, et al. Diagnostic
2009;2(2):196–8. criteria for malnutrition – an ESPEN Consensus Statement. Clin Nutr
7. Methven L, Allen VJ, Withers CA, Gosney MA. Ageing and taste. Proc 2015;34(3):335–40.
Nutr Soc 2012;71(4):556–65. 28. Sergi G, De Rui M, Veronese N, Bolzetta F, Berton L, Carraro S,
8. Karpa MJ, Gopinath B, Rochtchina E, Jie Jin W, Cumming RG, Sue Bano G, Coin A, Manzato E, Perissinotto E. Assessing appendicular
CM, Mitchell P. Prevalence and neurodegenerative or other associations skeletal muscle mass with bioelectrical impedance analysis in free-living
with olfactory impairment in an older community. J Aging Health Caucasian older adults. Clin Nutr 2015;34(4):667–73.
2010;22(2):154–68. 29. Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyère O, Cederholm
9. Rawal S, Hoffman HJ, Bainbridge KE, Huedo-Medina TB, Duffy T, Cooper C, Landi F, Rolland Y, Sayer AA, et al. Sarcopenia:
VB. Prevalence and risk factors of self-reported smell and taste revised European consensus on definition and diagnosis. Age Ageing
alterations: results from the 2011–2012 US National Health and 2019;48(1):16–31.
Nutrition Examination Survey (NHANES). Chem Senses 2016;41(1): 30. Hanisah R, Suzana S, Lee FS. Validation of screening tools to assess
69–76. appetite among geriatric patients. J Nutr Health Aging 2012;16(7):
10. Murphy C, Schubert CR, Cruickshanks KJ, Klein BE, Klein R, Nondahl 660–5.
DM. Prevalence of olfactory impairment in older adults. JAMA 31. Beukers MH, Dekker LH, de Boer EJ, Perenboom CW, Meijboom S,
2002;288(18):2307–12. Nicolaou M, de Vries JH, Brants HA. Development of the HELIUS
food frequency questionnaires: ethnic-specific questionnaires to assess
Downloaded from https://academic.oup.com/jn/article/151/3/605/6131860 by guest on 06 April 2021
11. Seubert J, Laukka EJ, Rizzuto D, Hummel T, Fratiglioni L, Bäckman
L, Larsson M. Prevalence and correlates of olfactory dysfunction in the diet of a multiethnic population in The Netherlands. Eur J Clin Nutr
old age: a population-based study. J Gerontol A Biol Sci Med Sci 2015;69(5):579–84.
2017;72(8):1072–9. 32. Mackenbach JD, Dijkstra SC, Beulens JWJ, Seidell JC, Snijder MB,
12. Fluitman KS, Nadar HJ, Roos DS, Berendse HW, Keijser BJF, Stronks K, Monsivais P, Nicolaou M. Socioeconomic and ethnic
Nieuwdorp M, IJzerman RG, Visser M. The association of olfactory differences in the relation between dietary costs and dietary quality: the
function with BMI, appetite, and prospective weight change in HELIUS study. Nutr J 2019;18(1):21.
Dutch community-dwelling older adults. J Nutr Health Aging 33. Looman M, Feskens EJ, de Rijk M, Meijboom S, Biesbroek S,
2019;23(8):746–52. Temme EH, de Vries J, Geelen A. Development and evaluation of
13. Gopinath B, Russell J, Sue CM, Flood VM, Burlutsky G, Mitchell P. the Dutch Healthy Diet index 2015. Public Health Nutr 2017;20(13):
Olfactory impairment in older adults is associated with poorer diet 2289–99.
quality over 5 years. Eur J Nutr 2016;55(3):1081–7. 34. Elstgeest LEM, Winkens LHH, Penninx B, Brouwer IA, Visser M.
14. de Jong N, Mulder I, de Graaf C, van Staveren WA. Impaired sensory Associations of depressive symptoms and history with three a priori
functioning in elders: the relation with its potential determinants diet quality indices in middle-aged and older adults. J Affect Disord
and nutritional intake. J Gerontol A Biol Sci Med Sci 1999;54(8): 2019;249:394–403.
B324–31. 35. Chiuve SE, Fung TT, Rimm EB, Hu FB, McCullough ML, Wang
15. Kong IG, Kim SY, Kim M-S, Park B, Kim J-H, Choi HG. Olfactory M, Stampfer MJ, Willett WC. Alternative dietary indices both
dysfunction is associated with the intake of macronutrients in Korean strongly predict risk of chronic disease. J Nutr 2012;142(6):
adults. PLoS One 2016;11(10):e0164495. 1009–18.
16. Duffy VB, Backstrand JR, Ferris AM. Olfactory dysfunction and 36. Panagiotakos DB, Pitsavos C, Arvaniti F, Stefanadis C. Adherence
related nutritional risk in free-living, elderly women. J Am Diet Assoc to the Mediterranean food pattern predicts the prevalence of
1995;95(8):879–84; quiz 885–6. hypertension, hypercholesterolemia, diabetes and obesity, among
healthy adults; the accuracy of the MedDietScore. Prev Med 2007;44(4):
17. Smoliner C, Fischedick A, Sieber CC, Wirth R. Olfactory function
335–40.
and malnutrition in geriatric patients. J Gerontol A Biol Sci Med Sci
2013;68(12):1582–8. 37. Landis BN, Welge-Luessen A, Bramerson A, Bende M, Mueller CA,
Nordin S, Hummel T. “Taste Strips” – a rapid, lateralized, gustatory
18. Arganini C, Sinesio F. Chemosensory impairment does not diminish
bedside identification test based on impregnated filter papers. J Neurol
eating pleasure and appetite in independently living older adults.
2009;256(2):242–8.
Maturitas 2015;82(2):241–4.
38. Mueller CA, Pintscher K, Renner B. Clinical test of gustatory function
19. Toussaint N, de Roon M, van Campen JP, Kremer S, Boesveldt S. Loss
including umami taste. Ann Otol Rhinol Laryngol 2011;120(6):
of olfactory function and nutritional status in vital older adults and
358–62.
geriatric patients. Chem Senses 2015;40(3):197–203.
39. Hummel T, Kobal G, Gudziol H, Mackay-Sim A. Normative data
20. Fuchida S, Yamamoto T, Takiguchi T, Kandaudahewa G, Yuyama
for the “Sniffin’ Sticks” including tests of odor identification, odor
N, Hirata Y. Association between underweight and taste sensitivity
discrimination, and olfactory thresholds: an upgrade based on a
in middle- to old-aged nursing home residents in Sri Lanka: a cross-
group of more than 3,000 subjects. Eur Arch Otorhinolaryngol
sectional study. J Oral Rehabil 2013;40(11):854–63.
2007;264(3):237–43.
21. Liu G, Zong G, Doty RL, Sun Q. Prevalence and risk factors of
40. Radloff L. The CES-D scale: a self-reported depression scale for research
taste and smell impairment in a nationwide representative sample of
in the general population. Appl Psychol Meas 1977;1:385–401.
the US population: a cross-sectional study. BMJ Open 2016;6(11):
e013246. 41. Folstein MF, Folstein SE, McHugh PR. “Mini-mental state”. A practical
method for grading the cognitive state of patients for the clinician. J
22. Sergi G, Bano G, Pizzato S, Veronese N, Manzato E. Taste loss in the
Psychiatr Res 1975;12(3):189–98.
elderly: possible implications for dietary habits. Crit Rev Food Sci Nutr
2017;57(17):3684–9. 42. Imoscopi A, Inelmen EM, Sergi G, Miotto F, Manzato E. Taste loss in
the elderly: epidemiology, causes and consequences. Aging Clin Exp Res
23. Hoogendijk EO, Deeg DJ, Poppelaars J, van der Horst M, Broese van
2012;24(6):570–9.
Groenou MI, Comijs HC, Pasman HR, van Schoor NM, Suanet B,
Thomese F, et al. The Longitudinal Aging Study Amsterdam: cohort 43. Kurihara K, Kashiwayanagi M. Physiological studies on umami taste. J
update 2016 and major findings. Eur J Epidemiol 2016;31(9):927–45. Nutr 2000;130(4S Suppl):931S–4S.
24. Huisman M, Poppelaars J, van der Horst M, Beekman AT, Brug J, van 44. Sasano T, Satoh-Kuriwada S, Shoji N, Iikubo M, Kawai M, Uneyama
Tilburg TG, Deeg DJ. Cohort profile: the Longitudinal Aging Study H, Sakamoto M. Important role of umami taste sensitivity in oral and
Amsterdam. Int J Epidemiol 2011;40(4):868–76. overall health. Curr Pharm Des 2014;20(16):2750–4.
25. Hoogendijk EO, Deeg DJH, de Breij S, Klokgieters SS, Kok AAL, Stringa 45. Mendonça N, Kingston A, Granic A, Hill TR, Mathers JC, Jagger
N, Timmermans EJ, van Schoor NM, van Zutphen EM, van der Horst C. Contribution of protein intake and its interaction with physical
M, et al. The Longitudinal Aging Study Amsterdam: cohort update activity to transitions between disability states and to death in
2019 and additional data collections. Eur J Epidemiol 2020;35(1): very old adults: the Newcastle 85+ Study. Eur J Nutr 2020;59(5):
61–74. 1909–18.
Taste, smell, and undernutrition in older adults 61346. Mendonça N, Kingston A, Granic A, Jagger C. Protein intake and 49. Bautista EN, Tanchoco CC, Tajan MG, Magtibay EV. Effect of flavor
transitions between frailty states and to death in very old adults: the enhancers on the nutritional status of older persons. J Nutr Health
Newcastle 85+ study. Age Ageing 2020;49(1):32–8. Aging 2013;17(4):390–2.
47. Houston DK, Tooze JA, Garcia K, Visser M, Rubin S, Harris TB, 50. Essed NH, van Staveren WA, Kok FJ, de Graaf C. No effect of 16 weeks
Newman AB, Kritchevsky SB. Protein intake and mobility limitation in flavor enhancement on dietary intake and nutritional status of nursing
community-dwelling older adults: the Health ABC Study. J Am Geriatr home elderly. Appetite 2007;48(1):29–36.
Soc 2017:65(8):1705–11. 51. Visser M, Elstgeest LEM, Winkens LHH, Brouwer IA, Nicolaou
48. Mathey MF, Siebelink E, de Graaf C, Van Staveren WA. Flavor M. Relative validity of the HELIUS food frequency questionnaire
enhancement of food improves dietary intake and nutritional status for measuring dietary intake in older adult participants of the
of elderly nursing home residents. J Gerontol A Biol Sci Med Sci Longitudinal Aging Study Amsterdam. Nutrients 2020;12(7):
2001;56(4):M200–5. 1998.
Downloaded from https://academic.oup.com/jn/article/151/3/605/6131860 by guest on 06 April 2021
614 Fluitman et al.You can also read
