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International Journal of Gerontology 11 (2017) 215e219

Contents lists available at ScienceDirect

International Journal of Gerontology


journal homepage: www.ijge-online.com

Original Article

Association Between Nutrition Status and Cognitive Impairment


Among Chinese Nonagenarians and Centenarians
Shan Hai, Li Cao, Xue Yang, Hui Wang, Ping Liu, Qiukui Hao, Birong Dong*
Department of Geriatrics, West China Hospital, Sichuan University, Chengdu 610041, China

a r t i c l e i n f o s u m m a r y

Article history: Background: The association of nutrition status with cognitive impairment has been confirmed by
Received 23 August 2016 previous studies. However, there are no relevant data from a Chinese oldest old population.
Received in revised form Method: Five hundred eighty elderly residents aged 90 years or more were investigated. Socio-
9 November 2016
demographic characteristics and lifestyle habits were collected by using a general questionnaire.
Accepted 9 December 2016
Available online 23 October 2017
Nutritional state was assessed with the Mini Nutritional Assessment (MNA) and biochemical pa-
rameters, whereas cognitive performance was evaluated by the Mini-Mental State Examination
(MMSE). Multiple Logistic regression was used to analyze the association between cognitive impair-
Keywords:
Chinese population,
ment and nutrition status.
cognitive impairment, Results: The total prevalence rate of cognitive impairment was 55.5%, 67 (35.1%) men and 255 (65.6%)
nonagenarians and centenarians, women were classified as cognitive impairment. Compared with cognitively impaired subjects, those
nutrition with normal cognition had a higher MNA score (14.28 ± 1.89 vs.13.51 ± 1.75, p < 0.05), a higher level of
hemoglobin (116.53 ± 16.74 vs.112.62 ± 13.82, p < 0.05) and body mass index (BMI) (19.63 ± 3.8 vs.
18.96 ± 3.59, p < 0.05). Pearson correlation analysis showed a significant correlation between MMSE with
MNA (p < 0.05), the level of HGB (p < 0.05) and BMI (p < 0.05). In the multivariate model, malnutrition
(OR ¼ 4.24, 95% CI: 1.89e9.52) was the risk factor for cognitive impairment.
Conclusion: Among Chinese nonagenarians and centenarians, there were significant associations be-
tween nutrition status and cognitive impairment. Further studies should evaluation if maintaining a
good nutritional status or nutritional intervention may be effective in the management and prevention of
cognitive impairment.
Copyright © 2017, Taiwan Society of Geriatric Emergency & Critical Care Medicine. Published by Elsevier
Taiwan LLC. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/
licenses/by-nc-nd/4.0/).

1. Introduction individual nutritional status influences cognitive function4,5.


Changes of nutrition status, specifically the risk of malnutrition
By 2050, 115 million people worldwide are expected to have may play an important role in the progression of cognitive loss in
some form of cognitive impairment, including mild cognitive hospital and the community-dwelling elderly population6,7. In
impairment and dementia, with the increase of the aging popula- parallel, another study reported cognitive impairment might result
tion1. Many studies have suggested that demographic factors, life- in nutritional risk, in this study, there was a significantly higher
style, functionality status, and chronic diseases (e.g. hypertension, frequency of malnutrition or nutritional risk among older adults
cardiovascular disease, and diabetes mellitus) are associated with with cognitive impairment compared with those with normal
cognitive impairment1e3. Proper nutrition is also important for cognition8.
cognitive function. Recently several epidemiological and observa- As the older population increases, the number of cognitively
tional studies demonstrated the relationship of nutrition status impaired older individuals can be expected to rise. However, most
with cognitive impairment, although it remains unclear how of the studies on nutrition and cognitive decline commonly include
only a small proportion of people over 80 years of age. There still
have been no relevant data for a Chinese oldest old population. In
the present study, we observed the association of nutrition status
* Corresponding author. Department of Geriatrics, West China Hospital, Sichuan
University West China Hospital, Sichuan University, Chengdu 610041, China.
with cognitive impairment among very old people using data from
E-mail address: dongbirong33@163.com (B. Dong). the Project of Longevity and Aging in Dujiangyan.

https://doi.org/10.1016/j.ijge.2016.12.002
1873-9598/Copyright © 2017, Taiwan Society of Geriatric Emergency & Critical Care Medicine. Published by Elsevier Taiwan LLC. This is an open access article under the CC
BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
216 S. Hai et al.

2. Materials and methods the oldest-old sample, only 38 subjects (32 men, 6 women) had
scores higher than 24; Therefore, we refered to some previous
2.1. Participants and data collection studies10,13. and merged those with mild cognitive impairment and
normal cognitive function together as the cognitive non-
The present study is part of the Project of Longevity and Aging in impairment group for data analysis.
Dujiangyan (PLAD).Dujiangyan is a city near Chengdu, the capital of
Sichuan province in southwest China. The PLAD study was per- 2.3. Evaluation of nutritional status
formed by researchers from Sichuan University in conjunction with
local officials and hospitals or clinics on 870 Chinese elderly aged 90 MNA was used because it is an instrument especially designed to
years and older in April 2005. The participants were recruited from assess the nutritional status of older persons. Participants are
a government registry and the Bureau of Statistics at the classified by MNA scores as follows: normal nutritional state (score
Dujiangyan City government has registered each person. Twenty- of 24e30); at risk of malnutrition (score of 17e23.5); and malnu-
one men and 26 women were not eligible for the study because trition (score of <17). Other nutritional state indicators evaluated
they died or moved away from the area. Of the 262 men and 561 included BMI and several serum biochemical values: albumin (g/L),
women interviewed, we excluded 102 persons who did not com- cholesterol (mg/dL), and Hgb (g/L). BMI was calculated as weight in
plete the MMSE test and 141 persons without an MNA score. Finally, kilograms divided by height in meters-squared (kg/m2). We cate-
580 participants (191 men and 389 women) were included in our gorized underweight (BMI<18.5) using the BMI cutoffs for Asian
study and their data were analyzed. populations recommended by the WHO15. Abnormal levels of
Data were collected by trained personnel who visited all the serum lipid/lipoprotein were defined according to the 2004 criteria
participants face to face. Socio-demographic characteristics and provided by the Chinese Medical Association. Normal criteria were:
lifestyle habits were recorded using a general questionnaire. We TC<5.18 mmol/l, TG<1.7 mmol/l, LDL<3.37 mmol/l, and
collected data on age, gender, education level, MMSE and MNA HDL>1.04 mmol/l. Normal level of hemoglobin was: Hgb120 g/L
scores, weight (kilograms), height (centimeters), tea and alcohol for men and 110 g/L for women.
consumption, smoking history, exercise, disease history, and other
items. Habits of smoking, alcohol consumption, tea consumption, 2.4. Statistical analysis
and exercise, which included former and current were collected by
using a general questionnaire. In the questionnaire, every item had SPSS18.0 was used in our statistical analysis. Continuous vari-
2 options (yes or no). The subjects, who did almost every day during ables are presented as means ± standard deviation (M±SD). Sig-
the recent 1 year, were classified as those with these habits current, nificance testing of the difference between the two groups was
otherwise as without. The subjects, who had did almost every day conducted using the independent-samples t-test for continuous
for more than 2 years as of a year before, were classified as those variables, and the Chi-square test or Fisher's exact test for cate-
with these habits previously, otherwise as without. Alcohol con- gorical variables. The association between the indicators of nutri-
sumption included spirits, liqueurs, wine, sherry, martini, beer, tional state and MMSE was assessed using Pearson correlation
lager, cider, stout, and so on. Tea consumption included all types of analysis. Multiple logistic regression analysis was used to evaluate
tea. Right arm blood pressure (BP) was measured twice to the the association between risk factors and cognitive impairment. We
nearest 2 mmHg using a standard mercury sphygmomanometer calculated the 95% confidence interval (CI) for each odds ratio
(phases I and V of Korotkoff) by trained nurses or physicians. The (OR).All p values were two-sided and p < 0.05 was considered to be
mean value of two measurements was used to calculate systolic BP statistically significant.
(SBP) and diastolic BP (DBP). Blood samples were collected after an
overnight fast (at least 8 h) for measurement of plasma glucose, 2.5. Ethical considerations
serum albumin, hemoglobin (Hgb), serum total cholesterol (TC),
triglycerides (TG), low-density lipoprotein (LDL), cholesterol, high- The study protocol was approved by the Research Ethics Com-
density lipoprotein (HDL), and other biochemistry indicators by mittee of Sichuan University. All participants provided written
standard laboratory techniques (performed by a technician in the informed consent.
biochemistry laboratory of Sichuan University). Subjects were
considered to be hypertensive if 3 or more repeated blood pressure 3. Results
readings were above 140 mmHg (SBP) and/or 90 mmHg (DBP), or if
they were taking antihypertensive drugs. Subjects were considered 3.1. Baseline characteristics according to cognitive function and
to be diabetic if they were treated for diabetes or had a fasting prevalence of cognitive impairment
blood glucose of >110 mg/dL.
Among the 580 subjects, the mean age was 93.2 ± 3.1 years
2.2. Assessment of cognitive function (ranging from 90 to 105 years) and 389 (67.0%) were women,
including 17 centenarians. Most (90%) of the subjects lived in the
Cognitive function was measured with the 30-item MMSE, a countryside. Only 24 subjects had scores higher than 24, so we
global test with the following components: attention, orientation, defined subjects with an MMSE score lower than 18 as having a
language, calculation, and recall. Cognitive impairment was defined cognitive impairment. In the oldest group, the total prevalence rate
as a score below 24 on the MMSE (sensitivity 80e90%, specificity of cognitive impairment was 55.5%. Subjects were divided into two
80e100%)9. Subjects were categorized as follows: possible de- groups: cognitive impairment group (n ¼ 322) and normal group
mentia (scores between 0 and 18), mild cognitive impairment (n ¼ 258). The M±SD MMSE score was 11.64 ± 3.48 in the cognitive
(scores between 19 and 24) and normal (scores between 25 and impairment group and 20.39 ± 2.80 in the normal group
30)10. Increasing studies suggest that MMSE scores may be affected (p < 0.001).The prevalence rate of cognitive impairment was 35.1%
by many other factors, including visual, education, and auditory among males and 65.6% among females. Women had a significantly
abilities, especially in advanced age.11 At age 95, the range of MMSE higher prevalence of cognitive impairment than men (255/389 vs.
was 10 (10th percentile) to 27 (90th percentile). Previous findings 67/191 p < 0.05).The total prevalence rate of malnutrition was
provided different norms for MMSE scores in very old subjects12. In 83.8%. The prevalence rate was 81.2% (n ¼ 155) among males and
Association Between Nutrition Status and Cognitive Impairment 217

85.1% (n ¼ 331) among females. Compared with cognitively Table 2


impaired subjects, those with normal cognition had a higher MNA Pearson correlation analysis for cognitive function and nutritional indicators.

score (14.28 ± 1.89 vs.13.51 ± 1.75, p < 0.001; Table 1) and a higher Variable MMSE scores correlation p value
level of Hgb (116.53 ± 16.74 vs.112.62 ± 13.82, p < 0.05) and BMI coefficient
(19.63 ± 3.8 vs. 18.96 ± 3.59, p < 0.05).There was no statistical MNA scores 0.24 <0.001a
difference for lifestyle (smoking habits, alcoholic and tea con- BMI 0.09 0.042a
sumption, exercise habits) between subjects of normal and Hgb 0.17 <0.001a
TG 0.02 0.564
impaired cognition. Demographic and clinical characteristics of the
TC 0.07 0.114
580 subjects, grouped by normal and impaired cognition, are Alb 0.03 0.509
shown in Table 1. LDL-C 0.02 0.649
HDL-C 0.06 0.155
a
3.2. Correlations between cognitive function and indicators of p < 0.05.
nutrition

levels, smoking habits, alcohol and tea consumption, exercise, hy-


Correlations between cognitive function and indicators of
pertension, cardiac disease, diabetes and stroke, malnutrition
nutrition status are shown in Table 2. MMSE scores significantly
(OR ¼ 4.24, 95% CI: 1.89e9.52) was the risk factor for cognitive
correlated with MNA scores (p < 0.001), Hgb levels (p < 0.001) and
impairment. The other indicators (such as underweight and ane-
BMI (p < 0.05). We did not find a correlation with the other
mia) did not reach statistical significance in this model (Table 3).
indicators.

3.3. Multivariate logistic regression for subjects with cognitive 4. Discussion


impairment and those without at baseline
As the elderly population increases, so does the prevalence of
We assessed whether the indicators of nutrition status were cognitive impairment14,15. In our cross-sectional observations of
associated with an increased risk of cognitive impairment. In the Chinese nonagenarians and centenarians, the high prevalence of
multivariate model, after adjustment for gender, ages, educational cognitive impairment (above 55.5%) was greater than that seen in

Table 1
Baseline characteristics according to cognitive function (n ¼ 580).

Cognitive impairment n ¼ 322 Normal cognitive function n ¼ 258 p value

Gender, n (%)
men 67 (20.8) 124 (48.1)
women 255 (79.2) 134 (51.9) <0.001*
Age,years 93.62 ± 3.11 93.03 ± 3.07 0.522
MMSE scores 11.64 ± 3.48 20.39 ± 2.80 <0.001*
MNA scores 13.51 ± 1.75 14.28 ± 1.89 <0.001*
SBP (mm Hg) 140.80 ± 23.58 141.68 ± 22.34 0.649
DBP (mm Hg) 72.36 ± 11.36 72.89 ± 11.83 0.581
BMI (Kg/m2) 18.96 ± 3.59 19.63 ± 3.8 0.027*
FPG (mmol/L) 4.47 ± 1.41 4.40 ± 1.47 0.560
TG (mmol/L) 1.27 ± 0.68 1.25 ± 0.73 0.810
TC (mmol/L) 5.11 ± 1.79 4.14 ± 0.77 0.358
LDL-C (mmol/L) 2.26 ± 0.61 2.25 ± 0.63 0.815
HDL-C (mmol/L) 1.58 ± 0.60 1.64 ± 0.97 0.362
Hgb g/L 112.62 ± 13.82 116.53 ± 16.74 0.002*
Alb g/L 42.74 ± 3.08 42.51 ± 3.39 0.404
Diseases, n (%)
Hypertension 60 (18.6) 106 (41.1) 0.803
Cardiac disease 24 (7.5) 42 (16.3) 0.826
Stroke history 56 (17.4) 64 (24.8) 0.237
Diabetes 73 (22.7) 78 (30.2) 0.628
Smoking, n (%)
Former 188 (58.4) 164 (63.6) 0.333
Current 138 (42.9) 122 (47.3) 0.286
Alcoholic, n (%)
Former 121 (37.6) 112 (43.4) 0.173
Current 73 (22.7) 78 (30.2) 0.267
Tea habits
Former 125 (38.8) 136 (52.8) 0.154
Current 158 (49.1) 131 (50.8) 0.181
Exercise, n (%)
Former 110 (34.2) 89 (34.5) 0.617
Current 137 (42.5) 112 (43.3) 0.933
Education, n (%)
Illiteracy 295 (91.6) 227 (88.0)
Primary school 18 (5.6) 20 (7.8)
Secondary school 6 (1.9) 8 (3.1)
College and postgraduate 3 (0.9) 3 (1.1) 0.521

Abbreviations: SBP, systolic blood pressure; DBP, diastolic blood pressure; FPG, fasting plasma glucose; Mean ± s.d. *p < 0.05; vs. cognitive impairment group using the Chi-
square or Fisher's exact test for categorical variables and Independent-Samples t-test for continuous variables. P value < 0.05 was considered to be statistically significant.
218 S. Hai et al.

Table 3 most of the previous studies commonly include only a small pro-
Multivariate logistic regression for subjects with cognitive impairment and those portion of people over 80 years of age. At present, the oldest old are
without at baseline.
among the fastest growing segment of the population in China. The
Risk factor Unadjusted Adjusted population of the nonagenarians/centenarians (>90 years old)
Malnutrition OR (95%CI) 3.95 (1.89e8.27)* 4.24 (1.89e9.52)* reached a high of 1 million in 2011, so we need to give more
Underweight OR (95%CI) 1.15 (0.82e1.59) 0.92 (0.64e1.33) attention to the increasing population cognitive health. Proper
Anemia OR (95%CI) 1.03 (0.74e1.43) 1.21 (0.84e1.75) nutrition is important for cognitive function. In the present study,
Adjusted for gender, ages, educational levels, smoking habits, alcohol and tea con- multiple logistic regression analysis confirmed that malnutrition
sumption, exercise, hypertension, cardiac disease, diabetes and stroke. *: P < 0.05. was the risk factors for cognitive impairment among Chinese no-
nagenarians and centenarians (Table 3). Despite using different
methods to assess nutritional status and cognitive performance, the
other large surveys16,17 with a very low average score of cognitive results of the present study are consistent with those of previous
function (lower than 18 on the MMSE). Several possible reasons research.
may account for these findings. First, although most subjects in Cognitive impairment has several negative consequences on the
other studies were older than 65 years, few were older than 90 health of the elderly; it can influence the prognosis of various
years. Second, our participants differed from those of previous conditions, reduce quality of life, and increase morbidity/mortality
studies because they were mostly from rural areas and had a lower and hospital admissions. Good nutrition status is important in
education level.Several studies have shown that the prevalence of maintaining cognitive performance, and altered nutrition status
cognitive impairment increases with age18,19. In China, therefore, appears to predict the severity and progression of cognitive
very old people may be becoming an important population for the impairment.
prevention of cognitive impairment. Our study had limitations that deserved mention. First, we did
The elderly are particularly vulnerable to nutritional deficits. In not analyze the different subtypes of cognitive impairment. Second,
our study, we assessed the nutrition status of the nonagenarians we did not adjust for other potential confounding factors, such as
and centenarians. We found that the prevalence rate of malnutri- socio-economic status, the APOE genotype or family history of
tion was 83.8% among the 580 subject. Some studies have shown cognitive impairment. Most (90%) of the participants in the present
the prevalence of malnutrition to be 3%e5% among free-living older study were countryside residents, Thus, our results might not be
adults and 21.3% among home care patients20. In Europe21, preva- generalizable to the urban population. In this study, there was high
lence of malnutrition is 10%e80%, while in long-term-care (LTC) dropout rate because there was the high prevalence of visual or
settings and in nursing homes, the average prevalence is 30%. In the hearing impairment in nonagenarians and centenarians who could
present study, the subjects were all over 90 years old, and the not complete the MMSE and MNA, which may cause selection bias.
prevalence was very high than other previous studies22. Previous In addition, the assessment of cognitive impairment and nutritional
studies have reported that dietary intake patterns, daily activity and status was based on cross-sectional measures, so it was not possible
residential status influenced nutritional status. In the study, most to determine causal relationships.
(90%) of the participants were countryside residents with limited
food and nourishment, which may be the primary reason causing 5. Conclusion
the high prevalence of malnutrition.
The present study confirmed that subjects with cognitive We found the prevalence of cognitive impairment and malnu-
impairment have lower MNA scores, Hgb levels and BMI levels than trition to be high among Chinese nonagenarians and centenarians.
those with normal cognition. The Pearson correlation showed a There were significant associations between nutrition status and
significant correlation between MMSE scores and MNA scores cognitive performance. Prevention and early treatment of malnu-
(p < 0.05), HGB levels (p < 0.05) and BMI (p < 0.05). In our study, the trition may be effective in lowering the risk of cognitive impair-
nutritional state of the subjects with cognitive impairment was ment, but this needs to be confirmed by larger studies.
worse than that of those with normal cognition. Several research
studies have reported cognitive impairment as an important risk Conflicts of Interest
factor for malnutrition. Patients with serious cognitive impairment
are characterized by a poor nutritional state, serious functional None.
impairment, and increased mortality23,24. It was reported that
assessment with the MNA scale among patients with mild to Acknowledgements
moderate dementia showed that 9% belonged to the malnutrition
group and 34% were at in the risk of malnutrition group25. Malara This work was supported by the Discipline Construction Foun-
et al. also reported that 42% of patients with severe cognitive dation of Sichuan University (XK05001) and by grants from the
impairment had malnutrition, but only 4% of malnourished pa- Project of Science and Technology Bureau of Sichuan Province
tients showed a moderate cognitive deficit6. Cognitive impairment (2006Z09-006-4).The authors thank the staff of the Department of
is also a risk factor for weight loss in the elderly. Zhou et al. Geriatrics, West China Hospital and Dujiangyan Hospital, and all
analyzed data from a survey that was conducted on all residents participants for their great contribution.
aged 90 years and reported an association between BMI and
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