Medical comorbidity in black and white patients with Alzheimer's disease.

Background: Little is known about co-medical illnesses in black and white patients with probable Alzheimer's disease (AD).

Methods: To address this question, we used two methods. In the first (Group I), black and white probable AD patients were matched on age at presentation to the clinic, age of onset of AD, duration of illness, and Mini-Mental State Examination scores; then, a variety of co-medical illnesses were compared between blacks and whites. In Group II, whites were randomly matched to blacks on the variables listed above.

Results: In Group I, blacks were found to have a higher rate of hypertension than whites, whereas whites had a higher incidence of atrial fibrillation and cancer than blacks. In Group II, age at presentation to the clinic was found to be shorter for men than for women; duration of illness was shorter for black men than for white men, white women, and black women; and Mini-Mental State Examination scores were lower in blacks than whites. As in Group I, blacks were found to have a higher rate of hypertension, whereas whites had higher rates of atrial fibrillation, cancer, coronary artery disease, high cholesterol, and gastrointestinal disease.

Conclusion: In both groups, black patients with probable AD had a higher rate of hypertension than white patients with probable AD, and whites had higher rates of atrial fibrillation and cancer. This finding suggests that these comorbid illnesses in black and white patients with probable AD is not due to a statistical Type II error, but rather to differences in these groups.

Key Words: Alzheimer's disease, comorbid disease, gender, race

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Little is known about differential clinical characteristics of Alzheimer's disease (AD) among and between ethnic populations in the United States. Even less is known about the differences between comorbid diseases associated with AD across ethnic groups. Recent studies, however, do suggest some differences in clinical characteristics and comorbid diseases between whites and blacks with AD. For example, Hargrave et al (1) found that black AD patients, compared with white AD patients, have a shorter duration of illness, lower Mini-Mental State Examination (MMSE) scores, higher Blessed Roth Dementia Rating Scale scores, and higher rates of hypertension at the time of initial diagnosis. Likewise, Shadlen et al (2) also found lower MMSE scores and higher rates of hypertension, without differences in ischemic heart disease or stroke, in black AD patients when compared with white AD patients.

In this study, we sought to determine whether there were differences in comorbid medical diseases in black and white probable AD patients. To test this hypothesis, two methods of matching blacks and whites were used. In the first (Group I), black and white probable AD patients were nonrandomly matched on age at initial presentation to the clinic, age at onset of illness, duration of illness, and MMSE scores. In the second method, blacks and whites with probable AD were randomly matched on the variables listed above (Group II). After these procedures, the frequency of comorbid diseases was determined.

Methods

Both studies were begun after approval of the University of Alabama at Birmingham Institutional Review Board was secured. In our Alzheimer's Disease Center, we have maintained a computerized database for approximately the last 10 years. All individuals seen in our Memory Disorders Clinic are entered into this data file after a diagnosis is determined. Probable and possible AD patients must meet National Institute of Neurological and Communicative Disorders and Stroke/Alzheimer's Disease and Related Disorders Association criteria. (3) Other diagnoses (eg, depression, vascular dementia) are determined clinically and with the Diagnostic and Statistical Manual of Mental Disorders, Third Edition Revised or the Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition. In addition, information is collected on race, gender, and age at initial presentation to the clinic, age at onset of AD, duration of illness, MMSE scores, and other medical illnesses. Approximately 1,700 individuals are enrolled in our database, with approximately 80% carrying the diagnosis of possible or probable AD. The remaining 20% have a variety of diagnoses including vascular dementia, diffuse Lewy body disease, frontal lobe dementia, basal ganglia disorders, normal pressure hydrocephalus, depression, mild cognitive impairment, the "worried well," and other diagnoses. These ratios likely reflect the nature of individuals referred to our academic Memory Disorders Clinic.

For this study, only data from black or white patients with probable AD, seen after 1995, were used. A total of 309 blacks and 690 whites were seen during this time period. The total number of patients was to be determined by the number of blacks with probable AD; because whites would be matched in a nonrandom or in a random fashion to the blacks, the black group was established first. Of the initial 309 blacks, 188 with probable AD were identified. This number was reduced to 167 after eliminating those with missing data points (ie, MMSE scores, age at presentation to clinic, age at disease onset, duration of illness, or comorbid diseases).

Comorbid medical illnesses found in black and white patients with probable AD were obtained from medical records, the patient, or the significant other at the first visit to the Memory Disorders Clinic. In Group I, white patients were matched in a nonrandom fashion by gender, age at presentation to the clinic (within 3 years), age at disease onset (within 3 years), duration of illness (within 1 year), and MMSE scores (within 2 points) to the black probable AD group. We chose to match MMSE scores, because previous research has shown that these scores predict the degree of activities of daily living and instrumental activities of daily living impairment, (4) and thus make our groups equivalent in the severity of illness. In Group II, 167 white patients with probable AD were randomly selected from the 690 white patients seen in the clinic. These patients were representative and did not differ from the remaining 523 patients. White probable AD patients were compared with the 167 black patients on age at initial presentation to the clinic, age at disease onset, duration of illness, and MMSE scores. In Groups I and II, a number of different comorbid medical illnesses were assessed. The criteria for a patient having a particular illness were determined by review of previous medical records indicating the illness, such as being on medications used to treat a specific illness. In the case of stroke, a history of the event, focal neurologic findings, and an infarction on brain imaging were required. For a transient ischemic attack, a focal neurologic event lasting less than 24 hours was required. The illnesses assessed included cerebrovascular accidents; transient ischemic attacks; hypertension; diabetes; coronary artery disease; atrial fibrillation; pulmonary disease (eg, asthma, emphysema, chronic obstructive pulmonary disease); gastrointestinal tract disease (eg, history or presence of ulcer disease, gastroesophageal reflux disease, irritable bowel syndrome, pancreatitis); genitourinary disease (eg, incontinence, renal failure, benign prostate disease); presence of hysterectomy; cancer (every type but skin); thyroid disease; arthritis (degenerative and inflammatory); significant head trauma (ie, loss of consciousness at any time during life); peripheral vascular disease; hypercholesterolemia; eye disease (eg, cataracts, glaucoma, macular degeneration, decreased visual acuity); pernicious anemia; psychiatric diseases occurring before the onset of AD (eg, depression, anxiety, psychosis); and other illnesses that occurred in only one or two patients, such as Parkinson's disease, seizures (before AD), anemia, peripheral neuropathy, and phlebitis.

For Groups I and II, analysis of variance (general linear model, statistical analysis system) followed by least-squared means were used to compare blacks to whites on age at presentation to the clinic, age at onset of AD, duration of illness, and MMSE scores. For the noncontinuous variables (ie, comorbid medical illnesses), the [chi square] test was used. Because of the large number of comparisons, the significance level was set at P < 0.025 for those comparisons performed on comorbid medical conditions in Groups I and II.

Results

Table 1 presents the data by race and gender on age at presentation to the clinic, age at onset of AD, duration of illness, and MMSE scores for white and black probable AD patients assigned to Group I. As planned, there were no significant differences in any of these variables between the two races. Table 2 presents the frequency of various comorbid medical conditions in white and black probable AD patients. As can be seen, black patients were found to have a higher frequency of hypertension (P < 0.025) than white patients, whereas white patients had a higher frequency of atrial fibrillation (P < 0.001) and cancer (P < 0.025) than black patients.

Table 1 also presents the data by race and gender on age at presentation to the clinic, age at onset of AD, duration of illness, and MMSE scores, for white and black probable AD patients randomized to Group II. Age at presentation to the clinic was found to be significantly affected by gender ([F.sub.1,333] = 4.26, P < 0.03), with women (75.1 [+ or -] 0.7 years [mean [+ or -] SEM]; P < 0.03) being approximately 2 years older than men (73.1 [+ or -] 1.2 years). No differences were found between the races or genders in age of onset of AD. Duration of illness showed a significant interaction between gender and race ([F.sub.1,333] = 4.36, P < 0.03), with black men demonstrating a shorter duration of illness (2.6 [+ or -] 0.2 years) than white men (3.7 [+ or -] 0.2 years; P < 0.02), white women (3.4 [+ or -] 0.2 years; P < 0.05), and black women (3.4 [+ or -] 0.2 years; P < 0.03). MMSE scores were found to be affected by race ([F.sub.1,333] = 43.47, P < 0.0001), with blacks having significantly lower scores (13.1 [+ or -] 0.8 points) than white AD patients (18.5 [+ or -] 0.7 points; P < 0.0001).

Table 3 presents the frequency of various comorbid medical conditions in white and black probable AD patients in Group II. As in Group I, blacks were found to have a higher frequency of hypertension (P < 0.025), whereas whites continued to have a higher frequency of atrial fibrillation (P < 0.005) and cancer (P < 0.005). In addition, in this randomized group, white patients compared with black AD patients were found to have a higher frequency of coronary artery disease (P < 0.005), gastrointestinal problems (P < 0.001), and hypercholesterolemia (P < 0.001).

Discussion

To determine whether comorbid medical illnesses differed between black and white probable AD patients, we examined this issue in two ways. In the first, black and white patients were deliberately matched on four variables (ie, age at presentation to the clinic, age at AD onset, duration of illness, and MMSE scores) thought to be important in influencing other medical illnesses. In the second, we randomly chose 167 white probable AD patients to compare with our previously chosen 167 black probable AD patients. Whether groups were deliberately matched or randomly matched, we found that blacks with probable AD had a greater frequency of hypertension than white probable AD patients, whereas white AD patients had a greater frequency of atrial fibrillation and cancer than black patients. Because these results were found in both groups ( including Group II where differences were found in age at presentation to the clinic, duration of AD, and MMSE scores), this suggests that at least these three comorbid medical illnesses do differ between the races.

Previous investigators (1), (2) also found that black probable AD patients have a higher incidence of hypertension than white AD patients. In the general population, the prevalence of hypertension in white men is 25.2% and in white women 20.5%, compared with 36.7% and 36.6% in black men and women, respectively. (5) In our population, the prevalence of hypertension for white men and women was 17% and 20%, respectively. In our blacks, hypertension was found in 34% of men and 29% of women. Thus, except for white men, the prevalence of hypertension among our probable AD patients was very close to that found in the general population.

There is an increased prevalence of atrial fibrillation in dementia, (6), (7) and atrial fibrillation has also been described as an independent risk factor for cognitive impairment. (8), (9) However, the finding that white AD patients have a higher incidence of atrial fibrillation and cancer than blacks has not been previously reported. This would suggest that white AD patients should have a higher rate of coronary artery disease, because atrial fibrillation is generally found in this type of patient. In fact, coronary artery disease was statistically associated with atrial fibrillation in our Group II white patients. Furthermore, the rate of heart attacks in the general population aged [greater than or equal to]65 years is greater for whites than for blacks. (5) At least part of the lower observed cancer rates in blacks may be due to lower rates of cancer screening in this group. (10)

Although diabetes and cerebrovascular disease have a higher incidence among normal blacks than among whites, (11), (12) we found no difference between races in these two illnesses in either Group I or Group II. Because the presence of cerebrovascular disease makes the diagnosis of probable AD impossible, this finding is not surprising. Why white patients in Group II were found to have increased rates of gastrointestinal disease and high cholesterol is unknown. However, this finding may reflect that, in general, white individuals have more access to the medical community than blacks; or the finding may represent a statistical Type II error in Group II, because it was not replicated in Group I.

As in previous studies, (2), (4), (13) we also found that black AD patients had lower MMSE scores than our white AD patients. Although we did not assess educational achievement, it is well known that black patients with AD, compared with white AD patients, score lower on the MMSE, even after taking education into account. (14-19) However, black men had a shorter duration of illness than black women, who also demonstrated lower MMSE scores than white women but whose duration of illness was similar to that of white patients. The reason for this gender difference in blacks is unknown. Perhaps a change in cognitive and functional abilities is perceived more quickly in men in the black community than in women. Furthermore, cultural factors (eg, with respect to acceptance of decline with age) might also play a role in the difference in duration of illness in black men and women. It is also possible that the biologic basis of AD in blacks differs between the genders. Another explanation could be the possible relationship between hypertension and cognitive decline. (20-22) However, hypertension alone cannot account for the observed shorter duration of illness in black men, given the similar prevalence of hypertension in black men and women. Further studies comparing both clinical variables and neuropathologic features in blacks will be necessary before this question can be resolved.

Interestingly, both black and white men presented to the clinic at a younger age than either black or white women. This occurred even though the age of onset of AD was similar between both races and genders. The cause of this finding is unknown. However, as postulated above, perhaps by the nature of what men do for work and hobbies, it is easier to recognize a decline in cognitive or functional abilities. In contrast, it is likely that these men were cared for by a female caregiver. (23), (24) Because women are more likely to seek medical attention for themselves and their loved ones, perhaps men were brought in earlier as a result. This would not explain why AD women were older at presentation. However, denial of cognitive decline in oneself is a clearly recognized feature of AD. Moreover, because women with AD are likely to be cared for by men, (4) who are often reluctant to seek medical care, perhaps a combination of denial in the female patient and less enthusiasm for seeking medical care in the male caregiver combined to cause women with AD to present to the clinic at a later age. Another possible explanation could be the greater prevalence of cardiovascular disease in men than in women, resulting in increased medical visits by men for such conditions. Furthermore, the possible role of cardiovascular disease in enhancing cognitive decline in AD may be another contributing factor. (25), (26)

Conclusion

Our study suggests that at least three major comorbid illnesses differ between blacks and whites with probable AD. As found in previous studies, (1), (2) blacks with AD are much more likely to have hypertension, without associated cerebrovascular disease or heart disease, than white AD patients. White AD patients, however, are much more likely to have cancer and atrial fibrillation than black AD patients. The reasons for these differences are unknown, but given that they were found by two different methods, they are unlikely to be statistical Type II errors. However, as these patients were selected from an academic Memory Disorders Clinic, they might not be representative of the patients residing in the community. Further studies are clearly necessary to understand the racial difference in AD itself as well as accompanying comorbid medical illnesses.

Table 1. Age at presentation to the clinic, age at disease onset,
duration of AD, and MMSE scores by gender and race in Groups I and II
(a), (b)

Groups                                          AAM (n = 41)

Group I

  Age at presentation (mean yr [+ or -] SEM)  73.5 [+ or -] 1.2
  Age at onset (mean yr [+ or -] SEM)         70.8 [+ or -] 1.3
  Duration of AD (mean yr [+ or -] SEM)        3.1 [+ or -] 0.3
  MMSE score (mean points [+ or -] SEM)       14.1 [+ or -] 1.2

                                                AAM ( n = 42)

Group II

  Age at presentation (mean yr [+ or -] SEM)  73.9 [+ or -] 1.3
  Age at Onset (mean yr [+ or -] SEM)         71.3 [+ or -] 1.3
  Duration of AD (mean yr [+ or -] SEM)        2.6 [+ or -] 0.2
  MMSE score (mean points [+ or -] SEM)       13.9 [+ or -] 1.1

Groups                                          AAW (n = 125)

Group I

  Age at presentation (mean yr [+ or -] SEM)  74.8 [+ or -] 0.7
  Age at onset (mean yr [+ or -] SEM)         71.3 [+ or -] 0.7
  Duration of AD (mean yr [+ or -] SEM)        3.4 [+ or -] 0.2
  MMSE score (mean points [+ or -] SEM)       12.3 [+ or -] 0.6

                                                AAW (n = 125)

Group II

  Age at presentation (mean yr [+ or -] SEM)  74.8 [+ or -] 0.7
  Age at Onset (mean yr [+ or -] SEM)         71.3 [+ or -] 0.7
  Duration of AD (mean yr [+ or -] SEM)        3.4 [+ or -] 0.2
  MMSE score (mean points [+ or -] SEM)       12.3 [+ or -] 0.6

Groups                                           WM (n = 41)

Group I

  Age at presentation (mean yr [+ or -] SEM)  73.4 [+ or -] 1.2
  Age at onset (mean yr [+ or -] SEM)         69.3 [+ or -] 1.3
  Duration of AD (mean yr [+ or -] SEM)        3.5 [+ or -] 0.4
  MMSE score (mean points [+ or -] SEM)       14.0 [+ or -] 1.2

                                                 WM (n = 57)

Group II

  Age at presentation (mean yr [+ or -] SEM)  72.4 [+ or -] 1.2
  Age at Onset (mean yr [+ or -] SEM)         68.7 [+ or -] 1.2
  Duration of AD (mean yr [+ or -] SEM)        3.7 [+ or -] 0.2
  MMSE score (mean points [+ or -] SEM)       18.7 [+ or -] 0.8

Groups                                           WW (n = 125)

Group I

  Age at presentation (mean yr [+ or -] SEM)  74.8 [+ or -] 0.7
  Age at onset (mean yr [+ or -] SEM)         70.4 [+ or -] 0.7
  Duration of AD (mean yr [+ or -] SEM)        3.4 [+ or -] 0.5
  MMSE score (mean points [+ or -] SEM)       12.3 [+ or -] 0.6

                                                 WW (n = 110)

Group II

  Age at presentation (mean yr [+ or -] SEM)  75.4 [+ or -] 0.7
  Age at Onset (mean yr [+ or -] SEM)         72.0 [+ or -] 0.7
  Duration of AD (mean yr [+ or -] SEM)        3.4 [+ or -] 0.2
  MMSE score (mean points [+ or -] SEM)       18.4 [+ or -] 0.6

(a) No statistical differences were found in any variable in Group I. In
Group II, age at presentation to the clinic was found to be
significantly affected by gender (P < 0.03), with women (P < 0.03) being
approximately 2 years older than men. Duration of AD showed a
significant interaction between gender and race (P < 0.03), with black
men demonstrating a shorter duration of AD than white men (P < 0.02),
white women (P < 0.05) and black women (P < 0.03). MMSE scores were
found to be affected by race (P < 0.0001), with blacks having
significantly lower scores than white patients (P < 0.0001). Age at
onset was similar between both races and genders.
(b) SEM, standard error of the mean; AAM, African-American (black) men;
AAW, black women; WM, white men; WW, white women; AD, Alzheimer's
disease; MMSE, Mini-Mental State Examination.

Table 2. Comorbid medical illnesses in black and white probable AD
patients, matched on specific variables (a), (b)

                                                           P
System                          Black         White      value

Brain (CVA/TIA)               4% (7/167)    5% (10/167)   NS
Hypertension                 30% (51/167)  19% (32/167)  0.025
Diabetes                     11% (20/167)   7% (13/167)   NS
CAD                           8% (14/167)   8% (15/167)   NS
Atrial fibrillation          <1% (1/167)    8% (14/167)  0.001
Pulmonary                     1% (2/167)    2% (5/167)    NS
GI                            4% (8/167)    9% (16/167)   NS
GU                            2% (5/167)    1% (3/167)    NS
Hysterectomy                  2% (5/167)    7% (12/167)   NS
Cancer                        1% (2/167)    6% (11/167)  0.025
Thyroid                       2% (4/167)   <1% (1/167)    NS
Arthritis                     8% (14/167)   5% (9/167)    NS
Head trauma                   1% (2/167)   <1% (1/167)    NS
Peripheral vascular disease   1% (2/167)    0% (0/167)    NS
Hypercholesterolemia         <1% (1/167)    3% (6/167)    NS
Eye disease (c)               5% (10/167)   5% (9/167)    NS
Pernicious anemia             1% (2/167)    1% (3/167)    NS
Psychiatric disease (d)       2% (5/167)    5% (6/167)    NS
Other (e)                     6% (11/167)  11% (19/167)   NS

(a) Group I: black patients compared with white patients were found to
have a higher rate of hypertension, whereas white patients were found to
have higher rates of atrial fibrillation and cancer than black
patients.
(b) CAD, coronary artery disease; GI, gastrointestinal disease; GU,
genitourinary disease; CVA, cerebrovascular accident; TIA, transient
ischemic attack.
(c) Includes cataracts, glaucoma, decreased visual acuity
(d) Includes depression, psychosis, anxiety, etc.
(e) Includes phlebitis, inner ear problems, Parkinson's disease,
seizures, tuberculosis, decreased hearing, anemia, peripheral
neuropathy, breast lump, etc.

Table 3. Comorbid medical illnesses in black and white probable AD
patients, randomly selected (a), (b)

                                                           P
System                          Black         White      value

Brain (CVA/TIA)               4% (7/167)    2% (5/167)    NS
Hypertension                 30% (51/167)  19% (32/167)  0.025
Diabetes                     11% (20/167)  12% (21/167)   NS
CAD                           8% (14/167)  16% (27/167)  0.025
Atrial fibrillation          <1% (1/167)    4% (8/167)   0.005
Pulmonary                     1% (2/167)    4% (8/167)    NS
GI                            4% (8/167)   17% (29/167)  0.001
GU                            2% (5/167)    6% (11/167)   NS
Hysterectomy                  4% (8/167)   11% (19/167)   NS
Cancer                        1% (2/167)    6% (11/167)  0.005
Thyroid                       2% (4/167)    7% (13/167)   NS
Arthritis                     8% (14/167)  11% (20/167)   NS
Head trauma                   1% (2/167)   <1% (1/167)    NS
Peripheral vascular disease   1% (3/167)    2% (3/167)    NS
Hypercholesterolemia         <1% (1/167)   11% (19/167)  0.001
Eye disease (c)               5% (10/167)   4% (7/167)    NS
Pernicious anemia             1% (2/167)    2% (4/167)    NS
Psychiatric disease (d)       2% (5/167)    4% (7/167)    NS
Other (e)                     6% (11/167)  <1% (1/167)    NS

(a) Group II: black patients compared with white patients were found to
have a higher rate of hypertension, whereas white patients were found to
have higher rates of atrial fibrillation, CAD, cancer, GI
disease, and hypercholesterolemia than black patients.
(b) CAD, coronary artery disease; GI, gastrointestinal disease; GU,
genitourinary disease; CVA, cerebrovascular accident; TIA, transient
ischemic attack.
(c) Includes cataracts, glaucoma, decreased visual acuity
(d) Includes depression, psychosis, anxiety, etc.
(e) Includes phlebitis, deafness, tuberculosis, decreased hearing,
breast lump, etc.

Acknowledgments

We thank Joanne Cage and Monra Tatum for excellent secretarial assistance.

From the Veteran's Administration Hospital, the Alzheimer's Disease Center, and the Department of Neurology, University of Alabama at Birmingham, Birmingham, AL.

This work was supported by National Institute on Aging Grants NIA-P0-06569 and NIA-1P50-AG16582 and by the Veterans Administration Merit Reviews and the Gitenstein Foundation.

Reprint requests to Edward Zamrini, MD, University of Alabama at Birmingham, Sparks Center 454, Birmingham, AL 35294. Email: [e-mail]

Accepted April 9, 2003.

Copyright [c] 2004 by The Southern Medical Association 0038-4348/04/9701-0002

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RELATED ARTICLE: Key Points

* Black and white probable Alzheimer's disease (AD) patients have different co-medical morbidities.

* Blacks with probable AD have higher rates of hypertension than white patients with AD.

* Whites with probable AD have higher rates of atrial fibrillation and cancer than black patients with AD.

Edward Zamrini, MD, Jo Ann Parrish, LPN, Dee Parsons, and Lindy E. Harrell, MD, PHD