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Risk factors for incident radiographic knee osteoarthritis in the elderly. The framingham study

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Vol. 40, No. 4, April 1997, pp 728-733
0 1997, American College of Rheumatology
The Framingham Study
Objective. Knee osteoarthritis (OA) is highly
prevalent, especially in the elderly. Preventive strategies
require a knowledge of risk factors that precede disease
onset. The present study was conducted to determine the
longitudinal risk factors for knee OA in an elderly
Methods. A longitudinal study of knee OA involving members of the Framingham Study cohort was
performed. Weight-bearing knee radiographs were obtained in 1983-1985 (baseline) and again in 1992-1993.
Incident disease was defined as the occurrence of new
radiographic OA (Kellgren and Lawrence grade 2 2 on
a 0-4 scale) in those without radiographic OA at
baseline. Risk factors assessed at baseline and in the
interim were tested in univariate and multivariate
equations to evaluate their association with incident
knee OA.
Results. Of 598 patients without knee OA at
baseline (mean age 70.5 years, 63.7% women), 93
(15.6%) developed OA. After adjustment for multiple
risk factors, women had a higher risk of OA than did
men (adjusted odds ratio [OR] = 1.8, 95% confidence
interval [95% CI] 1.1-3.1). Higher baseline body mass
Supported by NIH grants AG-09300 and AR-20613 and by an
Arthritis Foundation New Investigator Award to Dr. Zhang.
David T. Felson, MD, MPH, Yuqing Zhang, DSc: Boston
University Arthritis Center, Boston University Medical Center, and
Boston City Hospitals, Boston, Massachusetts; Marian T. Hannan,
DSc: Boston University Arthritis Center, Boston, Massachusetts;
Barbara Weissman, MD, Piran Aliabadi, MD: Brigham and Women’s
Hospital, Boston, Massachusetts; Daniel Levy, MD: The Framingham
Heart Study, Framingham, Massachusetts, and the National Heart,
Lung, and Blood Institute, Bethesda, Maryland.
Dr. Naimark is deceased.
Address reprint requests to David T. Felson, MD, MPH,
Boston University School of Medicine, 80 East Concord Street, Room
A203, Boston, MA 02118.
Submitted for publication June 5, 1996; accepted in revised
form October 14, 1996.
index increased the risk of OA (OR = 1.6 per 5-unit
increase, 95% CI 1.2-2.2), and weight change was directly correlated with the risk of OA (OR = 1.4 per 10-lb
change in weight, 95% CI 1.1-1.8). Physical activity
increased the risk of OA (for those in the highest
quartile, OR = 3.3, 95% CI 1.4-7.5). Smokers had a
lower risk than did nonsmokers (for those who smoked
an average of 1 1 0 cigarettedday, OR = 0.4, 95% CI
0.2-0.8). Factors not associated with the risk of OA
included chondrocalcinosis and a history of hand OA.
Weight-related factors affected the risk of OA only in
Conclusion. Elderly persons at high risk of developing radiographic knee OA included obese persons,
nonsmokers, and those who were physically active. The
direction of weight change correlated directly with the
risk of developing OA.
Osteoarthritis (OA) is the most common joint
disease, especially in the elderly. However, partly because of the slow time course of disease development, no
substantial longitudinal studies of risk factors for the
disease have been performed. Knowledge of the risk
factors for knee OA has been derived from crosssectional studies.
Similar to many chronic diseases, the pathogenesis of OA is likely to be multifactorial. Risk factors
consistently associated with the disease in cross-sectional
studies include older age, female sex, and being overweight (1). In cross-sectional studies, the OA could
develop first, leading a person to become sedentary and
to gain weight. We have reported that higher weight in
early life predisposes patients to knee OA (2), and that
weight loss lowers the risk of developing symptomatic
knee OA (3). Both results were based on a one-time
assessment of OA occurrence (3). We (4) and others ( 5 )
have also reported an association between nonsmoking
and a high risk of OA, although this remains controversial and has not been evaluated in a longitudinal study.
The relationship of physical activity and knee injury to
OA risk has not been studied longitudinally. Physical
activity could affect the risk of OA, but, because of
OA-related reductions in activity, this association cannot
be validly assessed cross-sectionally.
The reported association of chondrocalcinosis, or
radiographic cartilage calcification, with OA in crosssectional studies (6,7) may be due to the deposition of
calcium pyrophosphate dihydrate crystals in already
degenerated cartilage. The relationship of chondrocalcinosis to the development of OA is unknown.
OA is difficult to evaluate because it is a disease
that combines both symptoms and pathologic changes,
the latter of which are usually visualized by radiography.
The standard for epidemiologic studies has been radiographic evaluation, which is a proxy for disease pathology. Recent studies using expensive imaging techniques
such as arthrography, arthroscopy, and magnetic resonance imaging have documented that, when radiographic changes are present, these changes can also be
detected using other techniques (8-11).
To evaluate the risk factors associated with the
development of radiographic knee OA, we studied a
population-based group of elderly patients in Framingham, Massachusetts. We assessed risk factors at the time
of a baseline knee radiograph, and then reevaluated the
patients for the development of radiographic OA -8
years later.
Subjects. The Framingham Heart Study was established in 1948 as a population-based study to evaluate risk
factors for cardiovascular disease. Cohort members have since
been examined every 2 years. A substudy, the Framingham OA
Study, was begun at biennial examination 18 (1983-1985) to
evaluate the prevalence of knee OA and associated risk factors
in a population-based sample of elderly persons. The substudy
population was similar in age, knee symptoms, and sex distribution to the underlying Framingham cohort (12). The OA
examination included an anteroposterior (AP)
knee radiograph and questions about knee symptoms and
previous knee injury.
In 1992-1993, as part of Framingham biennial examination 22, the OA assessment was repeated using the same
methodology, including AP weight-bearing radiographs (13).
The followup study included radiographs obtained at home, or
in a nursing home for those too frail to come to the clinic site.
The longitudinal films were read by 2 different sets of readers.
The reading protocol, including observer agreement and the
team strategy, which was adopted to improve the accuracy and
precision of the readings, is described elsewhere (13). When
the readers disagreed on whether patients had experienced
incident disease, an adjudication session was carried out to
reach a consensus. Radiographs were read according to a
modified Kellgren and Lawrence scale (14), which characterizes knees as having OA (grade 2 2 on a 0-4 scale) if definite
osteophytes are present.
A subject was defined as having incident radiographic
knee OA if, at the baseline examination, both knees had grade
<2 disease, and at least 1 knee developed OA (grade 2 2 ) at
followup. Patients who underwent total knee replacement in at
least 1 knee were characterized as having grade 4 disease at
followup. For all patients who had received total knee replacements (n = 6) in the interim, Framingham charts and hospital
discharge summaries confirmed that the operations were carried out because of the development of knee OA.
Risk factors. The following risk factors were evaluated:
age (in years) at examination 18, sex, and body mass index
(BMI) (calculated as the weight [kg2] at examination 18
divided by the height [m’]at examination 1, before height loss
in later life). Weight change (in Ib) was assessed between
examinations 18 and 20 (the midpoint of the interval between
baseline and followup) rather than between examinations 18
and 22, so as to lessen the likelihood that incident disease
would have developed before weight change occurred. In
addition, we assessed the presence of knee chondrocalcinosis
by knee radiography at examination 18. Knee injury questions
were addressed to patients both at examination 18 and, again,
at examination 22.
We defined 2 different knee injury variables: past knee
injury was recorded if the patients stated at examination 18
that they had a history of knee injury, and, interim knee injury
was considered present if, at examination 22, patients stated
that they had a history of knee injury, yet reported no such
injury at examination 18. Cigarette consumption was assessed
at each examination and defined as the mean number of
cigarettes smoked per day over examinations 1-18. We also
evaluated current cigarette smoking at examination 18.
Physical activity was assessed using the Framingham
Physical Activity Index (15) at biennial examination 20, midway between examinations 18 and 22 (it was not assessed at
examination 18). We also evaluated the mean physical activity
level for each patient at examinations 4 (1954-1957) and 12
(1971-1973). Taking the usual activity during each hour of a
typical day, the Framingham Physical Activity Index assigns to
it a level of activity (i.e., sleep, sedentary, slight, moderate, or
heavy). Based on kilocalories of energy used at each level of
activity, an overall physical activity index is derived as a
weighted sum of activity over 24 hours. This Physical Activity
Index has been shown to correlate with cardiovascular disease
risk (15) and with physical capacity measures such as the
forced expiratory volume in 1 second and the pulse rate (16).
Finally, posteroanterior radiographs of the right hand
were obtained for most subjects at examination 10 (19661969). These were also read using a modified Kellgren and
Lawrence grading scale. We characterized patients either as
having some evidence of hand OA (at least 1joint showing a
grade 22 OA) or as showing no hand OA. Additional analyses
in which we tested the number of joints affected by hand OA
showed no difference from the results presented herein. Moreover, adjusting for femoral neck bone density in the subset of
patients for whom we obtained this measurement at examination 20 did not affect the results presented herein.
Statistical analysis. To examine the relationship between each risk factor and the occurrence of incident OA, we
first calculated the cumulative incidence rate over the study
period according to categories of each risk factor. A crude
odds ratio (OR) was then obtained using, as a reference group,
the risk of disease among subjects who did not have each
factor. To obtain a multivariate-adjusted OR for each risk
factor, a logistic regression model was used, with incident
disease in each knee (not in each person) as the dependent
variable. The standard error for each OR was adjusted for the
correlation between knees (17), according to the approach
described by Liang and Zeger (18). This method provides
more efficient and valid point estimates than either kneespecific analyses or person-specific analyses (17).
The dependent variable in these analyses was the
presence or absence of incident disease. An adjusted OR was
computed, with approximate 95% confidence intervals (95%
CI), based on maximum likelihood-derived standard errors.
In the original Framingham Knee O A Study,
there were 979 subjects, among 1,437 studied, whose
radiographs at baseline showed no evidence of knee OA.
Of these subjects, 256 died prior to the followup study
and 125 who remained alive did not participate. Among
the 598 subjects for whom we obtained radiographs at
followup (82% of survivors), 217 were men and 381 were
women. Compared with participants in the followup
examination, the nonparticipants tended to be older,
were more often male, were more likely to smoke at
least 10 cigarettes a day, and were somewhat more
sedentary (Table 1).
The relationship of each risk factor to the development of incident knee OA is presented in Table 2.
Age had no effect on the risk of incident disease among
this elderly population (mean age 70.5 years, range
63-92). Women were at higher risk than were men, an
association which persisted after adjustment for other
risk factors.
High BMI at the baseline examination was
strongly associated with an increased risk of incident
OA. Analyses using weight at the baseline examination
showed similar results. Weight change correlated directly with risk, with a 40% increase in risk per 10-lb
weight gain and a commensurate decrease in risk for
weight loss (P = 0.02 for weight change as a continuous
measure). In the separate adjusted analyses, subjects
were divided into 3 groups: those gaining 5 lb or more,
those losing at least 5 Ib, and all others. We found that
those with weight gain had an increased risk of O A
(OR = 3.8, 95% CI 0.7-20.7) and those with weight loss
Table 1. Characteristics of participants and nonparticipants in the
current study who had no knee osteoarthritis (OA) at the baseline
examination in the Framingham Knee OA Study*
(n = 598)
= 256)
= 125)
72.0 ? 4.9
75.0 2 6.6
Mean t SD age, years
70.5 -C 4.9
108 (42.2)
73 (58.4)
Sex, no. (%) female
381 (63.7)
25.4 2 4.2
25.2 f 3.7
Mean 2 SD BMI,
25.9 ? 3.9
Mean i SD weight
-1.0 t- 10.1 -5.2 2 10.1 -1.2 t- 10.7
change, lb
(n = 93)
(n = 76)
Cigarette smoking at
1-18, no. (%)
266 (44.5)
100 (39.1)
44 (35.2)
1-9 cigarettes1day
181 (30.3)
70 (27.3)
39 (31.2)
151 (25.3)
86 (33.6)
42 (33.6)
210 cigarettesiday
191582 (3.3) 151251 (6.0) 131122 (2.5)
Knee injury before
examination 18,
no. (%)
Interim knee injury,
16 (2.7)
no. (%)
441581 (7.8) 33/256 (12.9) 71123 (5.7)
no. (%)
Hand OA at
examination 10,
no. (%)
Mean 2 SD Physical
33.5 ? 5.3
32.1 ? 5.8
32.5 ? 4.8
Activity Index?
body mass index; NA
not available.
t This index is a weighted summary of activity based on kilocalories of
energy expended during a typical day.
had a lower risk of O A (OR = 0.5, 95% CI 0.2-1.1).
While BMI at the baseline examination (1983-1985)
affected O A risk, BMI earlier in life (at biennial examination 1 [1948-19511) had a more modest and nonsignificant effect on OA risk (per 5 units of BMI, OR = 1.5,
95% CI 0.95-2.4).
The mean number of cigarettes smoked per day
between examinations 1 and 18 was inversely associated
with the risk of disease (P < 0.001 for trend) (Table 2).
Furthermore, only 16 subjects experienced major knee
injury in the 8 years between the baseline and followup
examinations. There was a slight increase in their risk of
developing incident knee OA, although the point estimates were imprecise. Knee injury prior to the baseline
examination did not affect the risk of incident OA
(OR = 0.7, 95% CI 0.1-3.2).
Presence of chondrocalcinosis at the baseline
examination had little effect on the development of knee
OA. The presence of hand OA -15 years prior to the
baseline examination also did not affect the risk of OA
(OR = 0.9, 95% CI 0.5-1.8).
Habitual physical activity increased the risk of
Table 2. Relationship of risk factors to incident knee osteoarthritis
(OA) among the elderly cohort*
Risk factors
Age per 5-year
BMI per 5-unit
Weight change per
10-lb difference
Cigarette smoking
at examinations
1-9 cigarettesiday
210 cigarettes/
Interim knee injury
Past knee injury
Hand OA
Physical activity
1st quartile
2nd quartile
3rd quartile
4th quartile
incidence of
OA, no. (%)
1.2 (0.9-1.5)
241217 (11.1)
691381 (18.1)
1.8 (1.1-3.1)
1.6 (1.2-2.2)
1.4 (1.1-1.8)
541266 (20.3)
251181 (13.8)
141151 (9.3)
0.7 (0.4-1.2)
0.4 (0.2-0.8)$
891582 (15.3)
4/16 (25.0)
1.6 (0.4-5.7)
911579 (15.7)
2/19 (10.5)
0.7 (0.1-3.2)
831537 (15.5)
8/44 (18.2)
1.2 (0.5-2.7)
381267 (14.2)
0.9 (0.5-1.8)
OR (95% CI)t
141134 (10.4)
2.4 (1.0-5.3)
201134 (14.9)
261132 (19.7)
3.1 (1.4-6.9)
231131 (17.6)
3.3 (1.4-7.5)$
* O R = odds ratio; 95% CI = 95% confidence interval; BMI = body
mass index.
t Adjusted simultaneously for all other risk factors listed.
$ P < 0.001, test for trend.
0 Quartiles are sex-specific and range from sedentary (1st) to high
activity levels (4th).
comparing these subjects with subjects who provided
information on physical activity at examination 20, neither their earlier physical activity levels (33.1 versus 33.6;
P not significant [NS]) nor their rates of OA incidence
(14.9% versus 15.6%; P NS) differed significantly.
To assess whether the effect of each risk factor on
incident knee OA varied according to sex, we stratified
study subjects according to sex (Table 3). For women,
higher levels of adiposity were strongly and significantly
associated with an increased risk of knee OA incidence
(for each 5-unit increase in BMI, OR = 1.8, 95% CI
1.2-2.6). Furthermore, the effect of weight change was
seen only in women (for each 10-lb weight change,
OR = 1.6, 95% CI 1.2-2.3; P = 0.008 for weight change
as a continuous variable). For men, we were limited by
the small number of incident cases (n = 24). Increases in
the BMI in men did not translate into an increased OA
risk (OR = l.O), nor did weight change have a significant
effect in men. Other risk factors differed, but wide
confidence intervals limited the interpretability of the
Physical activity was assessed at examination 20,
midway between the baseline and followup examinations. Because symptoms could conceivably affect physical activity level, we divided subjects into those with
knee symptoms at either baseline or followup versus
those with no knee symptoms (Table 4). Although high
levels of physical activity translated into extremely high
risks of incident disease in the 53 patients with knee
symptoms (OR = 57.4), these estimates were very
imprecise. Importantly, among those with no knee pain,
Table 3. Relationship of risk factors to incident knee OA by sex*
Adjusted O R (95% CI)t
Risk factor
knee OA. Patients in the highest quartile of physical
activity at the baseline examination had 3.3 times the
odds of developing OA (95% CI 1.4-7.5) compared with
those in the lowest quartile of physical activity, the most
sedentary group. For each increase in level of physical
activity, there was a higher risk of knee OA (P < 0.001
for trend). We found no association between OA risk
and physical activity at examinations 4 and 12 (e.g.,
compared with those in the lowest quartile, those in the
highest quartile of physical activity had a risk of developing OA in later life of 1.2 [P = 0.551). Sixty-seven
subjects did not receive an assessment of physical activity at examination 20 (most did not attend examination
20), but were assessed at earlier examinations. When
Age per 5-year difference
BMI per 5-unit difference
Weight change per 10-lb difference
Cigarette smoking at examinations
1-9 cigarettesiday
210 cigarettedday
Interim knee injury
Past knee injury
Hand OA
Physical activity level, 1st quartile vs.
4th auartilei
(n = 24)
0.9 (0.5-1.6)
1.0 (0.5-2.1)
0.9 (0.5-1.5)
(n = 69)
1.3 (0.9-1.7)
1.8 (1.2-2.6)
1.6 (1.2-2.3)
1.2 (0.5-3.3)
0.3 (0.1-1.2)
0.6 (0.3-1.1)
0.5 (0.2-1.2)
2.0 (0.5-7.4)
3.8 (0.3-48.1) 0.3 (0.03-2.4)
1.3 (0.3-6.9)
1.1 (0.4-3.0)
1.7 (0.5-6.0) 0.7 (0.3-1.7)
3.8 (0.9-17.3) 3.1 (1.1-8.6)
* See Table 2 for definitions.
t Adjusted
simultaneously for all risk factors, as listed in Table 2.
$ Quartiles range from sedentary (1st) to high activity levels (4th).
Table 4. Relationship of physical activity to incident knee osteoarthritis (OA) according to symptoms*
Adjusted OR for OA (95% CI)$
Physical activity level
(n = 468)t
Knee symptoms
(n = 53)
Knee symptoms
1st quartile
2nd quartile
3rd quartile
4th quartile
13.7 (0.5-362.5)
6.4 (0.1-320.1)
57.4 (1.6-2,107.3)
1.9 (0.8-5.0)
2.6 (1.0-6.4)
2.1 (0.8-5.5)
* Presence of knee symptoms was based on a positive response to the
knee symptom question (13) at either baseline or the followup
examination. Information on symptoms was missing for 63 patients (48
non-OA, 15 OA). OR = odds ratio. 95% CI = 95% confidence
t Quartiles range from sedentary (1st) to high activity levels (4th).
$ Adjusted simultaneously for all risk factors, as listed in Table 2. P <
0.01, test for trend, in those with knee symptoms; P = 0.04, test for
trend, in those without knee symptoms.
increased physical activity was similarly associated with
elevated risks of OA development.
To further explore the association of smoking
with incident disease, we looked at smoking status at the
baseline examination. Current smokers (n = 70) also
had a somewhat lower risk of incident knee OA than did
nonsmokers (adjusted OR = 0.7, 95% CI 0.3-1.6).
Former smokers at examination 18 had a lower-thanexpected risk of incident OA (adjusted OR = 0.5, 95%
CI 0.3-0.9).
This study of radiographic OA suggests that the
following risk factors increase the risk of incident OA:
female sex, obesity, nonsmoking, and high levels of
physical activity. For adiposity, smoking, and physical
activity, there was a gradient of risk, whereby higher
levels of exposure affected disease risk more than lower
levels. Our study was performed among subjects who
were elderly at baseline.
This is the first large-scale incidence study that
evaluates persons without baseline knee OA. A prior
population-based study was performed (19), but was,
unfortunately, based on a small number of OA cases (13
cases in 123 men followed up and 36 cases in 135
women). Except for an effect of BMI on OA risk in
women, tested risk factors showed no consistent or
significant effect on disease incidence.
Many cross-sectional studies, including a previous one from the Framingham OA Study, have consistently documented the strong association of adiposity
with OA. Our study proves that adiposity precedes OA
development, extending previous results, and also suggests a sex difference in the relationship between adiposity and OA. A sex difference has also been seen in
some (2,19-21), but not all (22), prior studies. Although
our earlier cross-sectional study using a one-time OA
assessment suggested that weight loss protected against
the development of symptomatic OA (3), this is the first
study to document an effect of weight change on the
development of OA. Why obesity causes knee OA is not
entirely clear, although increased joint loading probably
plays a role. The link between obesity and hand OA (23)
and the high risk of OA only among women with a high
BMI suggest that increased joint stress in obese patients
may not be the sole explanation.
We did not find an association between increased
age and the development of OA, but our sample was
elderly at study inception. Other studies of incident
disease (24) have reported that both women and men
face increased risks of disease as they get older, but that
disease incidence may plateau when persons reach their
70s, the mean age of our population.
The effect of physical activity on disease occurrence is of interest. Recent studies of runners (25-28)
reported that those who were highly physically active
may face an increased risk of radiographic OA. Several
small longitudinal studies (29,30) have shown no increased OA risk in runners. Our study, in combination
with most others, suggests that physical activity predisposes to structural changes related to OA. The population we studied was elderly, and many of those in the
referent group were extraordinarily sedentary. High
levels of physical activity in these age groups may fall
into the normal range in younger persons.
While joint injury likely causes knee OA, too few
of our subjects experienced knee injuries for us to
evaluate this definitively as a risk factor for OA. Those
with past knee injury probably had developed knee OA
by baseline and were, therefore, not eligible for this
study. Our null finding regarding chondrocalcinosis is
also limited by imprecision. Our results suggest that the
presence of chondrocalcinosis, a frequent finding in the
elderly that reflects crystal deposition, is not associated
with a high risk of OA development.
Smoking appears to decrease the risk of developing OA. In cross-sectional studies, others (4,5,20,31)
have also reported that subjects with OA are less likely
to be smokers than are their matched controls. However,
this finding is not universal (32). While smokers tend to
be thinner than nonsmokers, adjustments for weight and
change in weight did not affect this negative association.
Smoking is known to favorably affect rates of other
diseases such as inflammatory bowel disease, and it is
conceivable that one of the many constituents of smoke
could act to prevent cartilage destruction. We suspect
that former smokers had a lower risk of OA than
nonsmokers because smoking may delay the gradual
development of cartilage loss and joint degeneration.
In this first large-scale incidence study of knee
OA, we found that female sex, adiposity, and nonsmoking increased the risk of developing disease. Furthermore, elderly persons with high physical activity levels
had a high rate of incident radiographic OA, and weight
change also correlated directly with OA risk.
We are indebted to Nilsa Carrasquillo for her technical
assistance, to Diane Weiland and Bryan Besso for obtaining
the knee radiographs, to Dr. Tim McAlindon for his helpful
suggestions, and to the Framingham Study patients for their
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factors, radiographic, stud, incident, knee, framingham, osteoarthritis, risk, elderly
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