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Improved survival in psoriatic arthritis with calendar time.

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ARTHRITIS & RHEUMATISM
Vol. 56, No. 8, August 2007, pp 2708–2714
DOI 10.1002/art.22800
© 2007, American College of Rheumatology
Improved Survival in Psoriatic Arthritis With Calendar Time
Yaser Ali,1 Brian D. M. Tom,2 Catherine T. Schentag,1 Vernon T. Farewell,2
and Dafna D. Gladman1
patients who entered the cohort during the years 1987–
1995, the SMRs were 0.55 and 0.82, while the SMR for
those who entered during 1996–2004 was 0.56.
Conclusion. The drop in SMRs in this PsA clinic
population suggests that the mortality risk has improved over time. This improved survival may reflect
disease severity at presentation in the earlier cohort as
well as earlier diagnosis and more aggressive treatment
in the more recent followup period.
Objective. To determine whether there has been a
change in mortality rates over the last 3 decades in
patients with psoriatic arthritis (PsA) whose cases were
followed prospectively.
Methods. Patients receiving followup care according to a standard protocol at the University of Toronto
PsA Clinic between 1978 and 2004 were included. Information on patient deaths was collected prospectively.
Mortality data for the general population of Ontario,
Canada, stratified by 5-year age bands, sex, and calendar year from 1978 to 2004, were used to calculate the
reference rates. Standardized mortality ratios (SMRs)
were calculated through use of Poisson regression models for the number of observed deaths. Time trend
analyses were performed through the use of 10-year
“rolling-average” SMRs and followup period–specific
SMRs stratified by the period of entry into clinic.
Results. Of 680 patients with PsA, 106 (15.6%) (55
women and 51 men) have died. Major causes of death
were disease of the circulatory system, neoplasms, diseases of the respiratory system, diseases of the gastrointestinal system, injuries/poisoning, and unknown. The
overall SMR for the period 1978–2004 was 1.36 (95%
confidence interval 1.12, 1.64). The estimated number of
life-years lost by the PsA patient cohort overall was 2.99
years (95% confidence interval 1.14, 4.77). For patients
who entered the cohort during the years 1978–1986, the
SMRs were 1.89, 1.83, and 1.21 for followup periods
1978–1986, 1987–1995, and 1996–2004, respectively. For
Psoriatic arthritis (PsA) is a chronic inflammatory arthritis associated with psoriasis. The disease affects men and women almost equally, with a mean age at
onset of 36 years (1). PsA is characterized by bony
proliferation and osteolysis, particularly at tendon, ligament, and capsular insertions (entheses). In the past, it
was thought to be a benign arthropathy (2–4). Recent
investigations, however, suggest that PsA is more severe
than previously considered.
In a study of 220 patients followed up prospectively at the University of Toronto PsA Clinic (5), we
found that 67% of patients had at least 1 erosion on
radiographs obtained at presentation to the clinic, and
20% had complete joint destruction. Moreover, 11% of
the study patients had severe functional limitations or
marked restrictions of daily activities that were attributable to the arthritis (American College of Rheumatology
[ACR] functional class 3 or 4, according to the Steinbrocker criteria). A Spanish cohort of 180 patients with
PsA identified 57% with erosions and 19% with ACR
functional class 3 or 4 (6). Kane et al (7) found that of
129 patients with PsA who were entered into a cohort
within 5 months of the onset of arthritis, 47% developed
at least 1 erosion by the second year of followup.
Queiro-Silva et al (8) and McHugh et al (9) have also
demonstrated progression of disease in PsA.
We previously reported that patients enrolled in
our PsA clinic between 1978 and 1993 had an increased
mortality risk (10). Of the 428 patients with PsA enrolled by January 1993, 53 had died by September 1994.
The University of Toronto Psoriatic Arthritis Program is
supported by the Krembil Foundation.
1
Yaser Ali, MD, Catherine T. Schentag, MSc, Dafna D.
Gladman, MD, FRCPC: University of Toronto, and Toronto Western
Hospital, Toronto, Ontario, Canada; 2Brian D. M. Tom, PhD, Vernon
T. Farewell, PhD: Institute of Public Health, Cambridge, UK.
Address correspondence and reprint requests to Dafna D.
Gladman, MD, FRCPC, Director, Psoriatic Arthritis Program, Centre
for Prognosis Studies in The Rheumatic Diseases, Toronto Western
Hospital, 1E-410B, 399 Bathurst Street, Toronto, Ontario M5T 2S8,
Canada. E-mail: dafna.gladman@utoronto.ca.
Submitted for publication August 3, 2006; accepted in revised
form April 30, 2007.
2708
IMPROVED SURVIVAL IN PsA WITH CALENDAR TIME
The 4 leading causes of death were diseases of the
circulatory (36.2%) or respiratory (21.3%) system, malignant neoplasm (17.0%), and injuries/poisoning
(14.9%). The overall standardized mortality ratio
(SMR) was 1.62 (1.59 for women and 1.65 for men).
However, a more recent study from Olmstead County,
Minnesota (11), found that the rate of survival among
patients with PsA was not different from that of the
general population. Since there have been recent advances in managing PsA, we sought to investigate
whether mortality risk has changed over the last decade
in our patient cohort.
PATIENTS AND METHODS
Patients who were enrolled into, and followed up at,
the University of Toronto PsA Clinic between January 1, 1978
and December 31, 2004 were included in the study. Patients
were entered into the cohort if they had an inflammatory
arthritis associated with psoriasis. Patients with other forms of
arthritis, such as seropositive nodular rheumatoid arthritis
(RA), systemic lupus erythematosus, gout, inflammatory
bowel disease, or grade 4 osteoarthritis were excluded from the
cohort (5). Patients have been referred to the PsA Clinic from
general practitioners, dermatologists, other rheumatologists,
and other physicians. Thus, the clinic serves as a primary,
secondary, or tertiary referral center.
Patients were evaluated at the initial clinic visit and at
6–12-month intervals thereafter according to a standard protocol. Information on patient deaths and causes of death was
collected prospectively and through linkage with the provincial
cancer registry, through telephone interviews and correspondence with family physicians and patients’ relatives, and
through daily checks of death notices in the newspaper. Death
certificates were used, where possible, to verify patient deaths
and to identify the primary cause of death.
To determine whether this cohort of PsA patients had
an excessive number of deaths as compared with the general
population of Ontario, Canada, standardized mortality ratios
(SMRs) were computed. Mortality data for the general population of Ontario, stratified by 5-year age bands, sex, and
calendar year (from 1978 to 2004), were used to calculate the
reference rates. Overall SMRs were calculated, and SMRs by
male and female sex were calculated separately, through the
use of Poisson regression models for the number of observed
deaths, with the logarithm of the expected number of deaths as
an offset in the models.
Time trend analyses were performed through the use
of 10-year “rolling-average” SMRs (through 10-year periods
1978–1987, 1979–1988, 1980–1989 to 1994–2003, and 1995–
2004), as well as followup period–specific SMRs (followup
periods 1978–1986, 1987–1995, and 1996–2004) stratified by
the period of entry into clinic (entry periods 1978–1986,
1987–1995, and 1996–2004).
Unadjusted and adjusted 10-year “rolling-average”
SMRs were computed. The variables adjusted for were radiologic damage, the interaction between sex and radiologic
damage, the logarithm of the sex-standardized erythrocyte
2709
Table 1.
Primary causes of death in the study patients
Primary cause of death
No. (%)
of patients
Cancers
Diseases of the circulatory system
Diseases of the respiratory system
Diseases of the digestive system
Accidents/poisonings
Other
Unknown
Total
25 (23.6)
26 (24.5)
11 (10.4)
7 (6.6)
5 (4.7)
5 (4.7)
27 (25.5)
106 (100)
sedimentation rate (ESR), highest level of medication taken,
presence or absence of hypertension, and disease activity (as
measured by the number of joints with active disease), all of
which were recorded at entry into the clinic; in addition, we
adjusted for smoking status at the time of PsA diagnosis. These
variables were chosen based on previous studies, clinical
judgment, and through use of stratified Cox regression models
to investigate the prognostic indicators of death. The adjustment was made assuming that the effects of these covariates
were calendar time–independent. Also, all analyses performed
were based on the assumption that any patient lost to followup
was still alive at the end of 2004. Life expectancies and
numbers of life-years lost for this PsA patient population
overall and separately by male and female sex were calculated
based on the unadjusted SMRs (overall and by sex).
Statistical analyses were performed using the statistical
packages Stata version 9.0 (StataCorp, College Station, TX)
and S-Plus version 6.2 (Insightful, Seattle, WA).
RESULTS
During the period January 1, 1978 through December 31, 2004, 680 patients were enrolled into the
University of Toronto PsA Clinic. Of these 680 patients,
385 (56.6%) were men and 295 (43.4%) were women.
There were 106 deaths during this time period, of which
51 occurred in men and 55 in women. The primary
causes of death are shown in Table 1. The most common
known causes of death were from cancers (n ⫽ 25) and
cardiovascular diseases (n ⫽ 26). Significantly, there
were 27 deaths for which the primary cause of death was
unknown.
The total number of years of followup, assuming those who were lost to followup were still alive at
the end of 2004, was 9,302 (5,044 men and 4,258
women). Patient characteristics are shown in Table 2.
The mean ⫾ SD age of the patients at entry into the
clinic was 43.7 ⫾ 13.4 years (range 15.5–87.5 years).
The mean ⫾ SD duration of arthritis at entry was
7.6 ⫾ 8.4 years (median 4.5 years; range 0–47.7 years).
Before 1994, the mean arthritis duration at entry was
7.4 years, whereas since 1994, the mean arthritis
2710
ALI ET AL
Table 2. Characteristics of the study patients at first presentation*
Age, mean ⫾ SD years
At entry into the clinic
At onset of PsA
At onset of psoriasis
Arthritis duration, median (range) years
At first visit, all patients
At first visit, by entry period
Years 1978–1993
Years 1994–2004
Joint counts, median (range)
No. with radiologic damage
No. with clinical damage
No. with active disease
No. with effusions
ESR, median (range) mm/hour
Smoking history at diagnosis, no. (%) of patients
Nonsmokers
Smokers
Unknown
Hypertension, no. (%) of patients
No
Yes
Total no. of patients with available data
Highest level of medication taken, no. (%) of patients
None
NSAIDs
DMARDs
Steroids
Total no. of patients with available data
Men (n ⫽ 385)
Women (n ⫽ 295)
Overall (n ⫽ 680)
42.5 ⫾ 12.2
35.8 ⫾ 12.2
29.0 ⫾ 13.1
45.1 ⫾ 14.7
36.6 ⫾ 14.4
28.9 ⫾ 16.0
43.7 ⫾ 13.4
36.1 ⫾ 13.2
28.9 ⫾ 14.4
4.4 (0–41.9)
4.9 (0–47.7)
4.5 (0–47.7)
4.7 (0–39.1)
4.3 (0.1–41.9)
4.3 (0–33.2)
5.0 (0.1–47.7)
4.7 (0–39.1)
4.5 (0.1–47.7)
1 (0–42)
0 (0–53)
6 (0–48)
0 (0–33)
18 (0–99)
1 (0–41)
0 (0–48)
9 (0–55)
0 (0–30)
30 (0–105)
1 (0–42)
0 (0–53)
8 (0–55)
0 (0–33)
23 (0–105)
190 (49)
51 (13)
144 (37)
133 (45)
24 (8)
138 (47)
323 (48)
75 (11)
282 (41)
346 (90)
38 (10)
384
253 (86)
41 (14)
294
599 (88)
79 (12)
678
242 (66)
77 (21)
20 (5)
29 (8)
368
171 (60)
67 (23)
32 (11)
17 (6)
287
413 (63)
144 (22)
52 (8)
46 (7)
655
* PsA ⫽ psoriatic arthritis; ESR ⫽ erythrocyte sedimentation rate; NSAIDs ⫽ nonsteroidal antiinflammatory drugs;
DMARDs ⫽ disease-modifying antirheumatic drugs.
duration was 7.7 years. There was no evidence of any
difference in arthritis duration before or since 1994
(P ⫽ 0.64 by t-test and P ⫽ 0.4 by Mann-Whitney U
test).
The overall SMR in the PsA patient cohort as
compared with the general population of Ontario for the
study period 1978–2004 was estimated to be 1.36 (95%
confidence interval [95% CI] 1.12, 1.64). The sexspecific SMRs for this cohort of patients during the same
study period and using the same reference population
were 1.25 (95% CI 0.95, 1.65) in men and 1.47 (95% CI
1.13, 1.91) in women. The SMRs calculated by Wong et
al (10) for the Toronto cohort of PsA patients during the
period 1978 to September 1994 were 1.62 (95% CI 1.21,
2.12) overall, 1.65 (95% CI 1.09, 2.40) in men, and 1.59
(95% CI 1.04, 2.33) in women. The estimated life
expectancies of the PsA cohort were 78.5 years in the
overall group, 77.4 years in men, and 80.3 years in
women. The corresponding life expectancies for the
Ontario general population were 81.5 years, 79.7 years,
and 83.9 years, respectively. Therefore, the estimated
number of life-years lost by the PsA patient cohort was
2.99 years (95% CI 1.14, 4.77) in the overall group, 2.30
years (95% CI –0.51, 4.96) in men, and 3.60 years (95%
CI 1.15, 5.96) in women.
Figure 1 presents the 10-year rolling-average
unadjusted SMRs. A clear decline with calendar period
is present in the overall cohort, as well as for men and
women separately. Although initially, the SMRs for
women remained relatively constant at ⬃1.5, the values
then increased and gradually declined.
Figure 2 presents the comparable SMR curves
adjusted for patient characteristics at entry into the
clinic (see Patients and Methods for details). The overall
adjusted SMR curve corresponds to that for a randomly
selected PsA patient from the Toronto Clinic population
who had no radiologic damage at first presentation to
the clinic, a median sex-specific ESR value, 8 joints with
active disease, no hypertension, and was receiving no
medication at the first clinic visit, and whose smoking
status at the time of diagnosis was unknown. The
male-specific SMR curve corresponds to that for a male
PsA patient with no radiologic damage, an ESR of 18
mm/hour, 8 joints with active disease, no hypertension,
IMPROVED SURVIVAL IN PsA WITH CALENDAR TIME
Figure 1. Unadjusted rolling standardized mortality ratios in patients with psoriatic arthritis. Shown are
overall rates in the 680 study patients, as well as sex-specific rates (385 men and 295 women).
Figure 2. Adjusted standardized mortality ratios. Data were adjusted for patient characteristics at entry
into the University of Toronto Psoriatic Arthritis Clinic (see Patients and Methods for details). Shown are
overall rates in the 680 study patients, as well as sex-specific rates (385 men and 295 women).
2711
2712
ALI ET AL
Table 3.
SMRs in the study patients, by followup period, sex, and clinic entry period*
Patient group,
clinic entry period
Men
1978–1986
1987–1995
1996–2004
Women
1978–1986
1987–1995
1996–2004
Overall
1978–1986
1987–1995
1996–2004
SMR (95% CI), by followup period
Years 1978–1986
Years 1987–1995
Years 1996–2004
2.40 (1.45, 3.98)
1.45 (0.86, 2.44)
0.47 (0.07, 3.32)
0.97 (0.58, 1.64)
0.85 (0.35, 2.04)
0.88 (0.22, 3.50)
1.30 (0.62, 2.73)
2.18 (1.45, 3.28)
0.67 (0.09, 4.76)
1.45 (0.94, 2.25)
0.79 (0.30, 2.11)
†
1.89 (1.25, 2.87)
1.83 (1.33, 2.52)
0.55 (0.14, 2.20)
1.21 (0.86, 1.69)
0.82 (0.43, 1.58)
0.56 (0.14, 2.25)
* See Patients and Methods for a description of the followup and clinic entry periods used. SMR ⫽
standardized mortality ratio; 95% CI ⫽ 95% confidence interval.
† No deaths occurred in women during the period 1996–2004 for the group who also entered the study
during that period.
and receiving no medication at first presentation, and
whose smoking status at diagnosis was unknown. The
female-specific SMR curve corresponds to that for a
female PsA patient who had no radiologic damage, 8
joints with active disease, no hypertension, and was
receiving no medication at first presentation to the
clinic, but whose ESR at the first visit was 30 mm/hour
and whose smoking status at diagnosis was unknown.
While the dramatic decline for men remained evident,
the decline for the overall population was less marked,
and no decline was apparent for women.
Table 3 presents followup period–specific SMRs
stratified by period of entry into the clinic. While the
confidence intervals were wide, there was a strong
indication that the rates had declined from the early
existence of the clinic to the present, when the SMRs are
compared along the diagonals (corresponding to the
same period of time within the clinic for different
periods of clinic entry). From a sensitivity analysis of the
assumption that any patient lost to followup was still
alive at the end of 2004, there was some indication that
most of the SMRs in Table 3 are quite robust, except for
the patient entries corresponding to entry period 1978–
1986 and followup band 1996–2004. Here, there exists
the possibility that these entries may have been underestimated because of the long followup attributed to, but
not observed for, some patients who entered during the
earliest entry period. The overall SMRs for the followup
bands collapsed over entry period were 1.89 (95% CI
1.25, 2.87), 1.63 (95% CI 1.19, 2.24), and 1.05 (95% CI
0.79, 1.41) for the calendar periods 1978–1986, 1987–
1995, and 1996–2004, respectively.
DISCUSSION
Wright and Moll’s description of PsA (12) suggested that the disease was less severe than RA. Coulton
et al (4) also suggested that PsA was less severe than
RA, since PsA patients were less disabled and no deaths
occurred during their study. However, Sokoll et al (13)
showed that patients with PsA had greater disability and
lower quality of life than did patients with RA, despite
their lower Larsen scores. Rahman et al (14) showed
that radiologic changes in patients with PsA and in age-,
sex-, and disease duration–matched RA patients were
similar. Husted et al (15) showed that patients with PsA
had less vitality than did patients with RA.
Our previous studies revealed that disease progression was common among patients with PsA and that
by 10 years after diagnosis, 55% of the patients had 5 or
more deformed joints (16). We further demonstrated
that the presence of ⱖ5 swollen joints at presentation
and actively inflamed joints at each visit predicted the
progression of clinical damage (17,18). Queiro-Silva et al
(8) and McHugh et al (9) also identified polyarticular
presentation as a predictor of disease progression, in
terms of both clinical and radiologic damage, in their
patients. In contrast, the study from Olmstead County,
Minnesota, suggested that the disease was mild among
the 66 patients with PsA identified in the administrative
database (11). We have previously reported that 17.6%
of our patients achieved a period of remission that lasted
more than 2.5 years. Patients with remission tended to
be males and had fewer inflamed joints at presentation
to the clinic (19).
IMPROVED SURVIVAL IN PsA WITH CALENDAR TIME
RA, the prototypical inflammatory arthritis, has
been associated with a greater mortality risk as compared with the general population (20–22). This risk has
been related to disease activity and severity as well as to
other disease characteristics. We have previously reported that the risk of mortality in our PsA cohort was
increased and was related to disease severity (10,23).
Our previous study of 428 patients registered with the
clinic between 1978 and 1993, reported 53 deaths.
Assuming that the 85 patients who were lost to followup
at that time were alive, the SMR was 1.62. This should
be considered an underestimate, given the possibility of
further deaths among those lost to followup. Causes of
death that were seen more frequently than expected
were diseases of the respiratory system (SMR 5.05), and
injuries/poisoning (SMR 3.54). The study from Olmstead County (11) paints a different picture for
community-based psoriatic arthritis. Followup of the 66
cases of PsA for a mean of 7.2 years, using information
from medical records only, showed that only 8% in the
incident cohort developed erosive changes on radiographs of the hand, and mortality was not significantly
different from that in the general population. Similar
observations were noted in this community for RA,
where there was no increased mortality risk overall, but
in patients with extraarticular features analyzed separately, the mortality risk was similar to that observed in
other series (24).
The current study of 680 patients with PsA from
a longitudinal observational cohort followed prospectively since 1978 demonstrates that there has been an
increased mortality risk in these patients. The overall
SMR for the whole period of observation was 1.36 (95%
CI 1.12, 1.64). The estimated loss of life expectancy for
patients with PsA was 3 years. The SMR for this
extended cohort appears to be better than that identified
for the first 428 patients in 1994. However, after performing 10-year rolling SMR calculations, we found that
the SMR was generally higher in this population earlier
on, and the estimated SMR of 1.05 over approximately
the last decade was much smaller than those for the
previous 2 decades, with SMRs of 1.89 and 1.63, respectively. The study thus demonstrates a trend for improvement in survival in these patients. The mortality risk in
patients with PsA was higher in the 1970s and 1980s.
The reasons for this trend are not yet known.
However, one explanation, which is consistent with our
estimated adjusted rolling average SMRs, could be a
higher severity of disease in patients who entered the
clinic during the first 20 years. Another contribution
could be better control of the disease in the most recent
2713
10-year period. This hypothesis is supported by our
recent observation that in the past 10 years, methotrexate has been given to our patients earlier in their disease
course and at a higher dosage than in the previous 20
years (25). Other possible explanations include earlier
referral of patients, more aggressive patient care (in
addition to methotrexate use), and more effective management of other components of the patients’ conditions, such as hyperlipidemia, diabetes, and heart disease. It should be noted, however, that we have shown
that death reporting is not a function of disease severity
or proximity to the clinic (26).
AUTHOR CONTRIBUTIONS
Dr. Gladman had full access to all of the data in the study and
takes responsibility for the integrity of the data and the accuracy of the
data analysis.
Study design. Schentag, Farewell, Gladman.
Acquisition of data. Ali, Schentag, Gladman.
Analysis and interpretation of data. Ali, Tom, Farewell, Gladman.
Manuscript preparation. Ali, Tom, Schentag, Farewell, Gladman.
Statistical analysis. Tom, Farewell.
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