Journal of Geriatric Oncology
Volume 3, Issue 1 , Pages 17-23, January 2012

Age, sex and gender impact multidimensional geriatric assessment in elderly cancer patients☆

  • C. Valentiny

      Affiliations

    • Department of Internal Medicine V (Hematology and Oncology), Innsbruck Medical University, Innsbruck, Austria
    • ,
  • G. Kemmler

      Affiliations

    • Department of Biological Psychiatry, Innsbruck Medical University, Innsbruck, Austria
    • ,
  • R. Stauder

      Affiliations

    • Department of Internal Medicine V (Hematology and Oncology), Innsbruck Medical University, Innsbruck, Austria
    • Corresponding Author InformationCorresponding author at: Department of Internal Medicine V (Haematology and Oncology), Innsbruck Medical University, Anichstrasse 35; 6020 Innsbruck, Austria. Tel.: +43 512 504 23255.

Received 30 May 2011; received in revised form 21 September 2011; accepted 12 October 2011. published online 21 November 2011.

Article Outline

Abstract 

Objectives

Multidimensional geriatric assessment (MGA) is essential in individualized treatment decisions in the elderly. The goal of this pilot study was to analyze the impact of age, sex and possibly gender on assessment status in senior cancer patients.

Materials and methods

An MGA consisting of 12 scores was applied in 111 patients (range 60–99, median 75years; 51% female). The effect of sex on individual MGA test results was evaluated by analysis of covariance adjusting for the confounding effect of age. The effect of age was investigated by partial correlation analysis adjusting for sex.

Results

Women were significantly older than men (men 76.6 vs. 72.2years, p=0.008), and advanced age was weakly associated with a reduced assessment status in most MGA dimensions. Age as a confounding factor was apparent in WHO performance status and in the “Timed Up and Go Test”; women's weaker performance status disappeared when adjusted for age. A significant effect of sex was observed in iADL (better functional activities in women), F-SozU (less perceived social support in women), BMI (lower BMI in women) and comorbidities (fewer comorbidities in women). The sex differences in iADL disappeared completely after omitting the gender-specific items in the iADL-5, thus implying a pronounced gender effect. Likewise, the significant difference in self-perceived emotional support (F-SozU 4.3 women vs. 4.6 men, p=0.005) suggests a gender effect in this dimension.

Conclusion

Age, sex and gender need to be recognized and integrated as interplaying and confounding factors in the assessment of elderly cancer patients.

Keywords: Gender, Age, Assessment, Geriatric, Elderly, Cancer, Confounding factor

 

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1. Introduction 

Demographic changes and an aging population result in a rapidly growing number of senior cancer patients. Presently, nearly half of the cases of newly diagnosed cancer occur in patients older than 70years.1 Advanced age is not only associated with a growing incidence of tumors, but also with an increase in other health problems.[2], [3], [4], [5], [6] Thus, during the last decade geriatricians and oncologists started to cooperate to integrate principles of geriatrics into the specialized care of senior cancer patients.6 Likewise, the multidimensional geriatric assessment (MGA) was introduced into decision algorithms and treatment concepts in elderly cancer patients to address and integrate symptoms and health limitations related to both senescence and cancer. An MGA represents a comprehensive evaluation for defining and describing in a structured way the dimensions of functional capacities, comorbidities, cognition, quality of life, nutritional status and social support in the elderly person. Recent analyses have demonstrated the ability of an MGA to identify vulnerable elderly, to predict clinical outcome as well as therapy tolerance and to describe therapeutic response.[4], [6], [7], [8]

Pronounced differences between the sexes have been described in most Western countries with respect to parameters such as mortality rate, overall health state, levels of morbidity, functional capacities and self-perceived social support.[9], [10], [11] In addition to sex, the construct of gender was recently introduced. Gender represents a multifaceted construct reflecting biological, genetic and social differences.[9], [10] As gender represents a relevant health determinant, it might deserve attention in the evaluation and assessment of elderly. To the best of our knowledge studies on how sex and gender impact assessment status in elderly cancer patients are rare. Thus, this pilot study was performed to evaluate the effect of age, sex and gender in the geriatric assessment of elderly cancer patients.

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2. Materials and Methods 

2.1. Patients 

111 tumor patients aged 60+ (range 60–99years; median 75years; 57 female, 54 male) were evaluated by geriatric assessment. Patient characteristics are shown in Table 1. All patients were of Caucasian ethnicity. Male patients had a mean age of 72.7 (SD 7.5) and females 76.6 (SD 7.4) years (t=2.72, p=0.008, T test). The majority of men (74%), but only a minority of women (36%), were married at the time of assessment (p<0.001, Fisher's exact test). Only 18% of male patients were widowed as compared to 45% of female patients (p=0.003). Of all patients 27% lived alone, whereas the majority (72%) lived with their family, spouse, domestic partner or friends. Tumors involved included 94 hematological malignancies and 18 cases of solid tumors (Table 1). This analysis was performed in consecutive inpatients at the Department of Internal Medicine V (Haematology and Oncology) of Innsbruck Medical University, Austria, after having obtained informed consent. Patients were admitted to the ward to start chemotherapy in 33 cases, immuno-chemotherapy (mainly R-COP or R-CHOP) in seven cases, bendamustine plus rituximab in five cases, or antibody therapy consisting of rituximab and bevacizumab in eleven cases. The other patients were admitted for supportive therapy or for diagnostic workup. This work was approved by the local ethics committee and was carried out in accordance with The Code of Ethics of the World Medical Association (Declaration of Helsinki) for experiments involving humans.

Table 1. Patient characteristics.
VariableWomenaMenaTest statisticbp-value
Age76.6±7.472.2±7.5t=2.720.008
Marital status Χ32=24.4<0.001
Married/partnership18 (31.6)42 (77.8) <0.001
Single8 (14.0)4 (7.4) n.s.
Divorced4 (7.0)1 (1.9) n.s.
Widowed27 (47.4)7 (13.0) <0.001
Social environment Χ32=18.4<0.001
Living alone25 (43.9)5 (9.3) <0.001
Living with partner/family30 (52.6)48 (88.9) <0.001
Living with friends1 (1.8)1 (1.9) n.s.
Institutionalized1 (1.8)0 (0.0) n.s.
Tumor entity Χ52=7.23n.s.
Non-Hodgkin's lymphoma (indolent) c19 (33.3)22 (40.7) –
Non-Hodgkin's lymphoma (aggressive) d10 (17.5)2 (3.7) –
Multiple Myeloma3 (5.3)5 (9.3) –
Morbus Hodgkin1 (1.8)0 (0.0) –
MDS, AML, CML, PV e16 (28.1)15 (27.8) –
Solid tumor f8 (14.0)10 (18.5) –

n.s. not significant (p>0.1).

aTable entries are mean±standard deviation for age and N (percent) for all other variables.

bThe notation Χ3 2 (Χ5 2) indicates the Chi-square statistic on 3 (5) degrees of freedom. Post-hoc comparisons by means of Fisher's exact test were performed only if the overall comparison by Chi-square test had yielded statistical significance.

c22 cases of chronic lymphocytic leukemia (CLL), 16 cases of follicular lymphoma, 2 cases of morbus Waldenström and one case of hairy cell leukemia.

d12 cases of diffuse large B-cell lymphoma (DLBCL).

e13 cases of myelodysplastic syndrome (MDS), 11 cases of acute myeloid leukemia (AML), 6 cases of chronic myeloid leukemia (CML) and 1 case of polycythemia vera (PV).

fSolid tumors included: lung cancer (3), colorectal cancer (3), breast cancer (2), pleural mesothelioma (2), leiomyosarcoma (2), gastric cancer (2) and one case each of bladder cancer, pancreatic cancer, cancer of unknown primary (adenocarcinoma) and hepatocellular carcinoma.

2.2. Assessment Instruments 

All patients were assessed in the following dimensions: performance status, functional and instrumental capacities, comorbidities, quality of life, cognition, perceived social support and nutritional status. Performance status was assessed by means of the WHO Performance Scale Status12 and the Karnofsky Index (KI).13 Functional capacities were evaluated by means of the following assessment instruments: Activities of Daily Life (ADL) (Barthel Index),14 Instrumental Activities of Daily Living (iADL),15 iADL-516 and the Timed Up and Go Test.17 Screening for depression was evaluated with the Geriatric Depression Scale (GDS-30)18 and cognitive function was assessed with the Mini Mental Status Examination (MMSE).19 Comorbidities were evaluated using the Cumulative Illness Rating Scale for Geriatricians (CIRS-G)20 as well as the Charlson Comorbidity Index (CCI).21 Perceived social support was evaluated with the social support questionnaire F-SozU. The F-SozU is a written self-reported questionnaire measuring self-perceived social support and satisfaction with social support. The original version consists of 54 items; the current study used the abbreviated 22-item version.[22], [23] Body mass index (BMI) was calculated and classified as suggested by the World Health Organisation (WHO).24

2.3. Statistical Methods 

Performance of male and female subjects on the individual tests of the MGA battery was compared by means of a T-test or Mann–Whitney U test, depending on the distribution of the MGA measure (normal, non-normal). To adjust for the confounding effect of age, analysis of covariance (ANCOVA) with age as a covariate was performed for normally distributed MGA variables. Non-normally distributed MGA variables were rank-transformed prior to the ANCOVA in order to closely match the Mann–Whitney U test procedure above. For ordinal MGA variables with five or less categories, ordinal regression with age as a covariate was used instead.

The MGA variable Timed Up and Go showed a substantial percentage of missing values due to permanent limitations in mobility. To avoid biased analysis, the value of these subjects was set to the highest occurring value plus one (poorest performance) for all rank-based analyses involving this variable (percentiles, Mann–Whitney U test).

The effect of age on performance in the individual MGA tests was investigated by correlation analysis and by partial correlation analysis, adjusting for sex. Pearson correlation coefficients were used for normally distributed MGA variables and Spearman correlation coefficients were used for non-normally distributed variables. In addition, patients aged up to 75years and those aged 75+ were compared using ANCOVA, adjusting for sex (for non-normally distributed MGA variables the same modifications as above were applied).

In order to take further potential confounders into account, additional ANCOVAs were performed including sex as a factor and age, marital status (married vs. single/divorced/widowed), living situation (living alone vs. with partner/family, with friends, institutionalized) and tumor type (hematological malignancies vs. solid tumor) as covariates.

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3. Results 

Multidimensional geriatric assessment (MGA) was applied in 111 tumor patients having a median age of 75years with slightly more women (51.35%).

3.1. Impact of Age, Sex and Gender in Geriatric Assessment Status 

Women had a slightly poorer WHO performance status than men (median 2 vs. 1; p=0.068) (Table 2). Because women were significantly older than men in the cohort analyzed (Table 1) and due to the correlation between age and most dimensions (Table 3), we adjusted for age using ANCOVA and the observed difference subsequently disappeared (p>0.2) (Table 2). Thus, the relevance of age as a confounding factor was demonstrated. Performance, as assessed by the Karnofsky Index, did not differ between male and female patients.

Table 2. Relevance of sex and gender in geriatric assessment.

Significant p values <0.05 are marked in dark gray, whereas a trend to significance (p<0.1) is marked in light gray.

a In iADL-5 the items “food preparation,” “house-keeping” and “laundry” from iADL are omitted [15].

b Measured in seconds. Due to limitations in mobility the Timed Up and Go Test was performed in 79 patients. For calculation of rank-based measures (median, percentiles, p-values) patients with permanent limitations in mobility received the highest ranks (see Statistical Methods).

Mean and standard deviation are reported for the 79 patients with a valid Timed Up and Go score.

c Measured in kg/m2; data were available in 108 patients.

d T-test for CIRS-G total and BMI (nearly normally distributed), Mann–Whitney U test for all other GA scores.

e Analysis of covariance (CIRS-G total and BMI), ordinal regression (WHO, iADL, iADL-5, Charlson), or analysis of covariance on rank-transformed data (ADL, Timed Up and Go, MMSE, GDS-30, F-SozU).

Table 3. Association of assessment status with age.

Correlation coefficients >0.3 or <−0.3 are displayed in bold, and p values <0.05 are marked in gray.

⁎ p<0.05 (two-tailed).

⁎⁎ p<0.01 (two-tailed).

a Pearson correlation coefficients are given for F-SozU, CIRS-G total and BMI (nearly normally distributed), Spearman correlation coefficients are shown for all other variables (non-normally distributed).

b For CIRS-G total and BMI the usual partial correlations are shown. In all other cases, partial correlations for rank-transformed variables were calculated.

Pronounced sex differences were observed in iADL, as women had better functional capacities than did men (median 8 vs. 6; p=0.012 unadjusted, and p<0.001 in age-adjusted analysis). It can be presumed that a gender-effect is given here, as this significant difference disappeared after omission of the “gender-specific” items “food preparation,” “housekeeping” and “laundry” (reduction from 8 items to 5 items, resulting in iADL-5 (Table 2)). The “Timed Up and Go Test” was performed more quickly by men than by women (median, 10.4 vs. 15.5 seconds, p=0.030). However, this difference decreased in the age-adjusted analysis, resulting in a trend-level significance of p=0.061.

Remarkably, self-perceived social support was lower in women than in men (4.09 vs. 4.5; p=0.03), and this difference persisted in an age-adjusted analysis (p=0.037). A description of the detailed analysis of perceived social support is given below and in Table 5.

BMI was higher in men than in women (25.42 vs. 23.52 kg/m2; p=0.017). Applying age-specific BMI in patients age 65+25: 24.1% were in the group with low BMI<22, 48.1% were in the group with BMI≤22–26.9, and 27.8% were in the overweight group defined as BMI≥27. A significantly larger proportion of women than men were found in the lowest BMI group (BMI<22) (p=0.043, Fisher's exact test), whereas no significant sex difference regarding the percentage of overweight subjects (BMI≥27) was observed (Table 4).

Table 4. Nutritional status as assessed by age-specific BMI.
BMI (kg/m2)WomenMenTotal
<2218 (32.7%)8 (15.1%)26 (24.1%)
22–26.924 (43.6%)28 (52.8%)52 (48.1%)
≥2713 (23.6%)17 (32.1%)30 (27.8%)
Total55 (100.0%)53 (100.0%)108 (100.0%)

As defined by Alexandre et al.,25

Evaluation of comorbidities, as measured by the Charlson Comorbidity Index, revealed fewer comorbidities in women than in men (median 2 vs. 1; p=0.056 and age-adjusted p=0.017). Similarly higher CIRS-G total scores were observed in men (7 vs. 6), which reached trend-level significance (p=0.062) after adjustment for age.

In ADL, MMSE, and GDS-30 no sex differences were observed.

3.2. Impact of Age on Assessment Status 

The following scales revealed a significant effect of age: KI, WHO, ADL, iADL, iADL-5, MMSE, CIRS-G, CCI. In all these tests older patients showed significantly poorer performance when using age as a numerical variable in correlation analyses (adjusted for sex) (Table 3) as well as in a dichotomized analysis comparing patients ≤75 vs. >75years (data not shown). In contrast, the Timed Up and Go Test, GDS-30, F-SozU and BMI were found to be independent of age.

3.3. Perceived Social Support in Elderly Cancer Patients 

The F-SozU score describes the subjective perception of social support. In this analysis female cancer patients described having significantly lower levels of overall perceived social support than men. Evaluation of the subscales demonstrated that the difference was largely due to the impact of emotional support (Table 5). Interestingly, marital status had no significant influence on the results of the F-SozU, whether on the total scale or on the subscales.

Table 5. Self-perceived social support related to sex and gender.
VariableMaleFemaleP value
MedianMeanSDMedianMeanSD
Practical support4.604.450.584.604.280.800.374
Emotional support4.604.470.544.304.080.850.005
Social integration4.144.160.673.863.920.740.099
F-SozU total score4.504.370.504.094.070.690.033

Self-perceived social support was assessed by the social support questionnaire F-SozU.[21], [22], [23]

3.4. Further Analyses 

An additional analysis adding marital status, living situation and tumor type to the list of covariates in the ANCOVA showed the findings from above to remain essentially unchanged. All statistically significant results regarding the effect of age and sex on MGA variables remained significant. We also checked the MGA variables for interaction between age and sex (differential age effect for men and women). However, no significant age-by-sex interactions were observed.

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4. Discussion 

This pilot study in a single institution aimed to evaluate the impact of age, sex and possibly gender on the assessment status of elderly cancer patients. While sex is a biological fact not amenable to change, gender is a multidimensional construct composed of social roles, behaviors and attitudes that change with time and place. Sex and gender often overlap, but as our study shows they should be considered separately.

In accordance with the concept that aging is associated with a decrease in reserves and capacities,[26], [27], [28] this study reveals a weak to moderate but significant correlation between age of cancer patients and distinct assessment scores, namely KI, WHO, ADL, iADL, iADL-5, MMSE, CIRS-G and CCI. In all of these scores older patients showed poorer performance when using age as a numerical variable in correlation analyses (adjusted for sex) as well as in a dichotomized analysis comparing patients ≤75 vs. >75years. In contrast, the Timed Up and Go Test, GDS-30, F-SozU and BMI did not correlate with advanced age. The moderate correlation between most and the lacking correlation between some assessment scores and advanced age point out that age per se should not be used as a surrogate marker for general condition, but that implementation of an MGA in individualized treatment decisions is essential. Thus, the integration of the MGA in daily practice is one of the essential paradigms raised in geriatric oncology.[3], [5], [6], [7], [29]

So far, studies specifically dealing with sex differences in assessing elderly cancer patients are rare. The otherwise very relevant studies by Repetto27 and Extermann26 mentioned above failed to analyze sex differences. Consequently, this pilot study was performed to address this lack. Comparison of men and women revealed pronounced differences in the dimensions of iADL (higher in women) as well as in perceived social support, comorbidities and BMI (all three lower in women). A trend toward significance was observed for WHO performance status and for the Timed Up and Go Test (both higher in women). Because women are older than men in most Western countries, age was considered a possible confounding factor in this analysis. Against the background of a significantly higher age of women than men (77 vs. 74years) in this cohort, the relevance and impact of age was analyzed using age-adjusted analyses. Thus, age as a confounding factor became apparent in WHO performance status and in the Timed Up and Go Test, as differences in comparison of women and men disappeared after age-adjustment. In contrast, age-adjusted analysis revealed a significant increase in sex differences in the dimensions of iADL, perceived social support, Charlson Comorbidity Index and CIRS-G. These analyses show that both sex and age impact performance in distinct assessment scores.

Besides the clear-cut parameters of sex and age, the less well-defined aspect of gender deserves consideration. Whereas elderly men and women reported similar levels of impairment in traditional ADL activities like bathing, dressing or transferring, a considerable gender difference became evident in functional capacities as assessed by iADL.30 Functional capacities are relevant as they are important indicators of health status and predictors of clinical outcome, therapy tolerance as well as postoperative complications in cancer patients.[6], [32], [33] The iADL contains three items that address household activities (“food preparation”, “housekeeping” and “doing laundry”). The influence of gender on household activities seems to be relevant in the Tyrolean population studied, as household activities are associated with traditional gender roles. That might be explained by the fact that men often cannot handle domestic tasks traditionally done by their spouses or other women.[16], [34], [35] This assumption is supported by the observation that sex differences in iADL disappeared after omitting the three gender-specific items, namely dropping from 8 items to 5 items, resulting in iADL-5. Thus, in the evaluation and comparison of assessment results different manifestations of gender aspects depending on the socio-economic background and the population studied have to be considered.

The possible relevance of gender aspects in other dimensions like the Timed Up and Go Test or comorbidities remains a matter of discussion.16 It can be argued that social roles as well as education and attitudes impact behavior in doing sports or remaining at home, resulting in differences in the Timed Up and Go Test. On the other hand, biological differences must naturally be taken into consideration.36 Such biological differences, for example in the form of greater muscle mass, could be advantageous not only in many sports, but also in the Timed Up and Go Test. The same is true for comorbidities: gender aspects certainly play a relevant role in alcohol and nicotine consumption as well as in general prevention behavior.10 These gender aspects could play an important causal role in the lower prevalence of comorbidities observed in women.

As data on perceived social support in elderly cancer patients are rare, the data from this study are relevant. Perceived social support in elderly persons is important for quality of life and for survival and is associated with better outcome by improving compliance with medical treatment and availability of help and support in the application of cancer treatments.[6], [31], [37] Moreover, socially isolated older adults are particularly vulnerable for emotional distress. Most patients analyzed in our cohort report a high level of perceived social support, and similar to studies performed by Hessel et al.,38 the perception of social support in cancer patients is not age-dependent.[38], [39] Data on perceived social support in the general population (n=395; mean 45.4years) and in patients from a Department of Internal Medicine in Tyrol (n=100; mean 58.3yrs) allow comparisons with the cohort of elderly cancer patients in the present study. Whereas no formal statistical comparison was performed and the age distribution is different, the perceived social support in elderly cancer patients seems to not be inferior in our cohort of elderly cancer patients. These data would lead us to assume that in our study cohort the denied or neglected elderly cancer patient is fortunately very rare. This certainly has something to do with the Austrian healthcare system, with its easy access for everyone and with the traditional family structures in Tyrol, which mean that most people have reference persons who live nearby and can provide perceived social support. However, also to be considered is a possible referral bias: patients with poor perceived social support might not make it to the hospital. In this study women rated their perceived social support significantly lower than did men. Evaluation of the subscales demonstrated that the difference was largely due to the impact of emotional support. Marital status had no significant influence on the results of F-SozU, whether on the total scale or on the subscales. This observation corresponds to the pronounced differences between the sexes that have been described in most Western countries for self-perceived social support and health-related quality of life in the general population.[11], [40], [41] Considering the relevant impact of perceived social support on outcome of cancer patients, it is essential that social support be evaluated in order to be able to organize support and meet the needs of elderly cancer patients.

In summary, both age and sex impact the results of tests used in an MGA. When analyzing the effect of one of the two factors, the possibly confounding role of the other should not be overlooked. While age and sex represent clearly defined parameters, aspects of gender are usually more difficult to assess. However, our findings give evidence that gender aspects indeed play an important role in MGA. Further research is needed in this upcoming field.

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Conflict of Interest 

The authors declare that they have no conflicts of interest.

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Authors Contributions 

Concept and design: G. Kemmler, R. Stauder, Data collection: C. Valentiny, R. Stauder, Analysis and interpretation of data: C. Valentiny, G. Kemmler, R. Stauder, Ms writing and approval: C. Valentiny, G. Kemmler, R. Stauder.

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☆ Supported by Österreichische Krebshilfe-Krebsgesellschaft Tirol (RS), Qualitätsförderungsprogramm des Tiroler Gesundheitsfonds (RS) and Verein Senioren-Krebshilfe (RS).

PII: S1879-4068(11)00060-9

doi:10.1016/j.jgo.2011.10.001

Journal of Geriatric Oncology
Volume 3, Issue 1 , Pages 17-23, January 2012

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