Caregivers' male gender is associated with poor nutrient intake in AD families (NuAD-trial)

Abstract

Objective

Alzheimer patients (AD) are known to be at risk for malnutrition and their older spouses may also have nutritional problems. The aim of our study was to clarify the association of caregivers' sex on the nutrient intake of AD couples.

Setting

Our study uses the baseline data of a randomized nutritional trial exploring the effectiveness of nutrition intervention among home-dwelling AD patients.

Participants

The central AD register in Finland was used to recruit AD patients living with a spousal caregiver, 99 couples participated in our study.

Measurements

Nutritional status was assessed using the Mini-Nutritional Assessment (MNA). Nutrient intakes for both AD patients and their spouses were calculated from 3-day food diaries.

Results

The mean age of caregivers and AD spouses was 75.2 (SD 7.0) and 77.4 years (SD 5.6), respectively. According to the MNA, 40% of male and 52% of female AD spouses were at risk for malnutrition. Among male caregivers, the mean energy and protein intakes were 1605 kcal (SD 458) and 0.93g/body kg (SD 0.30), whereas the respective figures for their female AD spouses were 1313 kcal (SD 340) and 0.86 g/body kg (SD 0.32), respectively. Among female caregivers, the mean energy and protein intakes were 1536 kcal (SD 402) and 1.00 g/body kg (SD 0.30), whereas the respective figures for their male AD spouses were 1897 kcal (SD 416) and 1.04 g/body kg (SD 0.30). The interaction between male caregiver sex and lower energy (p<0.001) and lower protein intake (p=0.0048) (adjusted for age and MMSE) was significant. Similar differences between caregiver sexes were observed with the intake of various nutrients.

Conclusions

A gender difference exists in the ability to cope with caregiver responsibilities related to nutrition. A need exists for tailored nutritional guidance among older individuals and especially among male caregivers.

Introduction

Older adults with Alzheimer's disease (AD) often have nutritional problems, such as unintentional weight loss, poor nutritional status and inadequate nutrient intake (1, 2, 3, 4). Poor nutritional status is associated with infections, functional disabilities and sarcopenia (5, 6, 7). Many AD patients live at home with their older spousal caregivers. Persons with AD may exhibit a wide range of nutritional changes, such as poor appetite, changed food preferences or eating difficulties, and therefore caregivers are confronted by many nutritional challenges when caring for their AD spouse (8). Nutrition is an important part of caring and sufficient nutrient intake is essential in maintaining health and functional ability 5, 7. Nutrition interventions suggested positive effects on nutrition in both AD patients and spouses (9, 12).

Spousal caregivers are often aged with multiple comorbidities and functional disabilities (13). Older caregivers have also been shown to be prone to malnutrition 9, 2, 14, 15. Several cross-sectional studies have suggested that healthy home-dwelling older adults retain adequate nutrient intake 16, 17, whereas other studies report the opposite for this group 18, 19. Furthermore, nutritional status and nutrient intake tend to decrease with age and disabilities 20, 21.

The population of older adults is heterogenic and food intake also differs according to sex, firstly because men have higher energy requirements. In some studies males consumed less fruit and vegetables than females (22, 23, 24). Poor cooking skills and lack of nutritional knowledge among older men have been associated with poor dietary quality 23, 25. As caregivers, males have expressed more concern about nutrition than females when adopting a caregiver's role, because they were not as familiar with the household activities (26).

Food-related activities, such as planning meals, shopping and cooking have traditionally been a woman task. However, the number of male caregivers is increasing and, as caregivers, men will be responsible for providing meals and nutrition for their spouses. To our knowledge, the effect of caregiver's sex on nutrient intake has not been studied. Thus, the aim of our study is to clarify the association of caregiver's sex with the energy and nutrient intake of them and their AD spouses.

Subjects and methods

Setting

Our study is part of a randomized nutritional intervention trial exploring the effectiveness of tailored nutritional intervention among AD persons living at home with their aged spousal caregiver during a year-long intervention. The study procedure has been described elsewhere (27). Our study was approved by the Ethics Committee of the Helsinki University Central Hospital.

Participants

We recruited the participants for our study from the centralized Drug Imbursement Register of the Social Insurance Institution of Finland in 2010-2011. To receive reimbursement for AD medication, AD patients have to undergo a detailed diagnostic assessment, including cognitive and neuropsychological testing, neuroimaging and laboratory tests, to ensure they fulfill the requirements of a probable AD diagnosis according to the NINCDS-ADRDA Alzheimer's criteria (28). Inclusion criteria for our study included living in the greater Helsinki area, being able to communicate in Finnish, an AD diagnosis, age ≥ 65years for AD, the ability to stand on a scale and no acute, severe disease. The nutritionist invited the couples fulfilling these criteria to the first meeting, where she gave them oral and written information about the study and asked them to sign an informed consent. In the case of an AD patient's inability to give informed consent, the spousal caregiver gave proxy consent for both spouses.

Measurements

Both caregivers and their AD spouses were assessed and interviewed during a two-hour visit. The diagnoses and medications were confirmed from medical records provided by the couples, and the Charlson comorbidity index (29) was calculated. The AD participants were assessed using the Mini-Mental State Examination (MMSE) (30) and the Mini-Nutritional Assessment (MNA) (31). The spousal caregivers were assessed using the Zarit Burden Scale (32). The weight and height of all participants were measured and body mass index (BMI) was calculated. The Instrumental Activity of Daily Living (IADL) scale (33) was used to test functional ability.

We used three-day food diaries to assess food intake. During the first visit the nutritionist gave written and spoken instructions to the caregiver on how to keep the food diaries. She also gave the participants 100 mL, 15 mL and 5 mL measuring cups for measuring food items such as drinks and bread spreads. Caregivers were instructed to fill food diaries out over a period of for three days for both spouses while maintaining their usual diet. Participants mailed the completed diaries to the nutritionist and she phoned all the caregivers to check their entries. Common things checked by the nutritionist were the types of milk and fat used, and the trademarks of food items or amounts of food. Energy, protein and nutrient intake were calculated using the Nutrica program (34).

Statistical analyses

Data are presented as means with standard deviations, or numbers with percentages. Statistical comparison was performed using the t-test, Mann-Whitney U-test, or the Chi-Square test when appropriate. Energy and nutrient intakes were compared between groups using a bootstrap-type ANCOVA, adjusted by age and MMSE of caregiver and MMSE of AD spouse. STATA Stata 13.0 statistical package (StataCorp LP College 20 Station, TX, USA) was used for the analyses.

Results

We received a total of 198 food diaries from participants. Females represent 68% of the caregivers. The mean ages of caregivers and AD spouses were 75.2 (SD 7.0) and 77.4 (SD 5.6) years, respectively. According to the MNA, 51.6% of male and 39.7% female AD spouses were at risk for malnutrition. Several differences existed between male and female caregivers. The male caregivers were older than female caregivers (77.4, SD 7.1 vs. 74.2, SD 6.7, p=0.030). Their mean Charlson comorbidity index (CCI) was higher 1.7 (SD 1.8) that of female caregivers (0.9, SD 1.2). Male caregivers’ Zarit score (22.7 points, SD 12.4) was lower than that of female caregivers (31.8 points, SD 15.9), indicating that males reported being less burded. No significant differences were observed between male and female caregivers in nutritional status, BMI or education. No significant differences occurred in the baseline characteristics between male and female spouses with AD, except for the mean MMSE score, which was lower in AD males than in AD females (17.8, SD 4.4 vs. 20.1 SD 5.9; p=0.033). (Table 1)

Table 1.

Baseline characteristics of caregivers and their AD spouses

Caregivers	Males N=31	Females N=68	P-value
Mean age, years (SD)	77.4 (7.1)	74.2 (6.7)	0.030
Mean years of education, (SD)	10.8 (4.5)	10.8 (3.8)	0.96
Income (%)
Good	58.1	35.3
Moderate	41.8	63.2
Poor	0	1.5	0.092
Mean MMSE, (SD)	26.6 (2.7)	27.9 (1.8)	0.044
Mean Charlson comorbidity index (SD)	1.7 (1.8)	0.9 (1.2)	0.049
Mean number of drugs, (SD)	4.5 (2.0)	3.6 (2.4)	0.053
Mean Zarit, (SD)	22.7 (12.5)	31.8 (15.9)	0.010

Spouses with AD	Females N=31	Males N=68
Mean age, years (SD)	76.5 (6.1)	77.8 (5.3)	0.19
Mean years of education, (SD)	9.5 (4.0)	10.4 (4.1)	0.33
Mean MMSE, (SD)	17.8 (4.4)	20.1 (5.9)	0.033
MNA, n (%)
< 17 points	0	0
17-23.5 points	16 (51.6)	27 (39.7)
> 23.5 points	15 (48.4)	41 (60.3)	0.27
Mean Charlson comorbidity index (SD)	1.7 (0.8)	2.1 (1.3)	0.11
Mean number of drugs, (SD)	5.6 (2.6)	5.7 (2.5)	0.84
Mean IADL, (SD)	4.0 (2.2)	3.5 (2.1)	0.25

Differences between groups were tested with X2 –test for categorical variables and Mann Whitney U-test for not normally; distributed continuous variables and with student T-test for normally distributed continuous variables; SD standard deviation; BMI = Body mass index (kg/m2); MNA = Mini-Nutritional Assessment [31](< 24 suggests risk for malnutrition or malnourishment);MMSE = Minimental State Examination[30] BMI= Body mass index, IADL=Instrumental activities of daily living [33]; Charlson comorbidity index [29]; Zarit Burden scale [32].

The mean energy and protein intakes of male caregivers were 1605 kcal (SD 458) and 0.93 g/body kg (SD 0.30), whereas the respective figures for their female AD spouses were 1313 kcal (SD 340) and 0.86 g/body kg (0.32). The mean energy and protein intakes of female caregivers were 1536 kcal (SD 402) and 1.00g/body kg (SD 0.30), whereas the respective figures for male AD spouses were 1897 kcal (SD 416) and 1.04 g/body kg (SD 0.30). Caregivers’ male sex was associated with lower nutrient (p<0.001), lower energy (p<0.001) and lower protein (p=0.0048) intakes adjusted for age and MMSE. Similar differences between caregiver sexes were observed with various nutrient intakes (Table 2). Figure 1 illustrates protein and vitamin C intakes in families with male and female caregivers.

Table 2.

Energy and nutrient intakes of caregivers and AD persons divided according to caregiver's sex

	Families with a male caregiver		Families with a female caregiver		P-value1
	Caregiver (M) N=31	AD (F) N=31	Caregiver (F) N=68	AD (M) N=68
Energy, kcal SD	1605 (458)	1313 (340)	1536 (402)	1897 (416)	<0.001
Protein, g SD	70.3 (21.3)	57.8 (19.6)	67.2 (18.6)	80.4 (22.5)	0.0021
Protein g/ bodykg, SD	0.93 (0.30)	0.86 (0.32)	1.00 (0.30)	1.04 (0.30)	0.0048
Fiber, g SD	20.5 (8.6)	16.8 (7.1)	20.2 (7.2)	23.9 (8.4)	0.015
Calcium, mg SD	946 (405)	843 (328)	859 (361)	1020 (404)	0.28
Vitamin C, mg SD	62.8 (39.9)	54.2 (30.8)	83.8 (41.8)	93.3 (45.6)	<0.001
Vitamin E, mg, SD	8.5 (4.2)	6.4 (2.6)	9.5 (4.0)	10.9 (4.3)	<0.001
Vitamin D, µg, SD	8.0 (4.7)	7.1 (4.1)	9.9 (6.3)	12.0 (8.4)	<0.001
Folate, µg, SD	219 (75)	179 (61)	226 (67)	258 (66)	<0.001

1. Interaction between caregiver and gender. Bootstrap-type ANCOVA adjusted by age and MMSE of caregiver and MMSE of AD spouse.

Figure 1.

The mean protein and vitamin C intakes with 95% confidence intervals in families with a male and a female caregiver

Discussion

Caregiver's male sex was associated with a lower nutrient intake by both the person with AD and the caregiver. Families with male caregivers were at higher risk for nutritional problems and poor energy, protein and other nutrient intakes than families with female caregivers.

The strength of our study is that all AD participants had an appropriate diagnosis, as they were recruited from the AD drug reimbursement register. We also received detailed three-day food diaries from older participants, which are assumed to be a challenging group for nutritional interventions. An additional strength is that although a number of studies showing gender differences in caregiving characteristics exist 35, 36 the differences in nutrient intake of this group have not previously received attention.

The limitation is that food consumption was only assessed for three days, which may not give an accurate picture of the participants’ average food intake over a longer period of time. On the other hand, older people tend to have rather similar daily eating habits. There may also be differences between males and females in filling out the food diaries, as females may have been more diligent in recording food intake. To avoid this, we checked each diary by phone before recording the answers. Food diaries have commonly known limitations such as underreporting and changes in food habits but it is assumed to be a good method for gathering food records among older people (37).

Some explanations for poor nutrient intake in families with male caregivers may be presented besides mere sex. Our male caregivers were older and had more comorbidities and medications than female caregivers which may result in a decreased intake of nutrients 20, 21. However, male caregiver families in our study also had several characteristics that should have resulted in better nutrient intake. Male caregivers in our study had lower Zarit scores, indicating less burden. A previous study (38) found that caregiver's burden was a predictor of weight loss in older home-dwelling adults with mild AD. Thus, lower burden should have resulted in better nutrient intake. In addition, female AD spouses had lower MMSEs, thus indicating more severe dementia. Our analyses were therefore adjusted for MMSE of AD spouses, and also with MMSE and age of caregivers. Even after these adjustments, male caregiver families showed lower nutrient intakes than female caregiver families.

The mean energy intake for female AD spouses was very low, only 1300 kcal per day. This is worrisome, because it is difficult to receive enough nutrients with an energy intake of under1500 kcal per day (39). Low protein intake among female AD spouses is also alarming, as a protein intake of less than 1 g/bodyweight kg per day impairs immunity and accelerates sarcopenia and, furthermore, leads to functional disabilities 7, 40. The interaction between a caregiver's male sex, lower energy and other nutrient intake was widely observed, except for calcium intake, which is probably because milk products are part of a typical Finnish diet (24). Adding milk products to the diet is considered to be a good way to improve nutrient of older adults (41).

Families with a male caregiver received less of vitamins C, E and folate, which indicate a low consumption of fruit, vegetables and wholegrain products, and furthermore poor diet quality. In previous studies older healthy males have been shown to use less fruits and vegetables than females 22, 24. Reasons behind low vegetable intake among families with a male caregiver may be due to poor cooking skills, as the use of many vegetables requires some form of preparation. Furthermore, the low protein intake of female AD spouses may be a result from replacing meals with bread and snacks.

Our study indicates that a gender difference exists in the ability to cope with household responsibilities related to nutrition. Meal planning, shopping and cooking has traditionally been the woman's responsibility in this age group. A prior Finnish study investigating men's attitudes towards cooking showed that most men considered cooking to be women's work (42). Poor cooking skills were reported a reason for poor diet among older men in a study investigating food habits of older men living alone (25). Another study reported that men also had less knowledge about nutrition than women (23). However, Keller's (2008) study showed that many caregivers had nutritional concerns. Especially men who had recently taken on a new role as a caregiver were worried about having insufficient knowledge concerning nutrition (26). Calasanti's (43) study showed that AD females continue to perform household work and cooking despite their illness and males begin taking responsibility step by step. Tailored support for families would be needed at this point. However, a Finnish study concluded that official services do not always meet caregiver needs (44).

Nutrition-related gender differences should be taken into account when planning and offering support for older community-dwelling caregivers. Male caregivers might benefit from cooking courses combined with nutritional guidance directed specifically for them. Community-based nutrition and cooking education for older male caregivers with AD spouses has proved promising (45). As the amount of male caregivers is increasing, it is important to provide specific guidance for this group.

Conclusions

Our study indicates that there is a gender difference in the ability to cope with caregiver responsibilities related to nutrition. There is a need for tailored nutritional guidance and interventions among older individuals and especially among male caregivers.