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Rheumatology Advance Access published online on July 18, 2008
Rheumatology, doi:10.1093/rheumatology/ken244
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© The Author 2008. Published by Oxford University Press on behalf of the British Society for Rheumatology. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

The determinants of change in patella cartilage volume—a cohort study of healthy middle-aged women

S. P. Wijayaratne1,*, A. J. Teichtahl1,*, A. E. Wluka1,2, F. Hanna1, R. Bell3, S. R. Davis3, J. Adams3 and F. M. Cicuttini1

1Department of Epidemiology and Preventive Medicine, Monash University Medical School, Alfred Hospital, Prahran, 2Baker Heart Research Institute, Melbourne and 3The Women's; Health Program, Department of Medicine, Monash University Medical School, Alfred Hospital, Prahran, Victoria, Australia.

Correspondence to: F. M. Cicuttini, Department of Epidemiology and Preventive Medicine, Monash University Medical School, Alfred Hospital, Prahran, Victoria 3181, Australia. E-mail: flavia.cicuttini{at}med.monash.edu.au


   Abstract
Top
 Abstract
Introduction
 Participants and methods
 Results
 Discussion
 Acknowledgements
 References
 
Objectives. Although cartilage loss occurs with advancing age and is a hallmark of OA, the factors that affect cartilage change are not well established. The aim of this study was to explore the determinants of change in patella cartilage volume over 2 yrs among healthy middle-aged women with no clinical knee OA.

Methods. One hundred and forty-eight women with no clinical knee OA were recruited from a previous population-based cross-sectional study of healthy women aged 40–67 yrs. MRI was performed at baseline and at 2 yrs, to assess patella cartilage and bone volume. Self-reported exercise was assessed by questionnaire.

Results. Annual loss of patella cartilage volume was 1.6% (95% CI 1.2, 1.9). Age was positively associated with patella cartilage volume loss after adjustment for confounders (P = 0.05). For every 1 mm3 increase in patella bone volume at baseline, annual cartilage loss was reduced by 8.05 mm3 (95% CI 12.91, 3.19; P < 0.001). Fortnightly participation in exercise promoting an increased heart and respiratory rate for at least 20 min also tended to be associated with a reduced rate of patella cartilage volume loss (P = 0.09).

Conclusion. Among middle-aged women with no clinical knee OA, advancing age expedites the rate of patella cartilage volume loss, while increased patella bone volume and exercise participation tends to be associated with a reduction in the rate of patella cartilage volume loss. Interventions targeting modifiable factors, such as physical activity, warrant further investigation as they may help to prevent patellofemoral OA.

KEY WORDS: Patella, Cartilage, Bone, Osteoarthritis, Knee


   Introduction
Top
 Abstract
 Introduction
Participants and methods
 Results
 Discussion
 Acknowledgements
 References
 
Knee OA is a common, painful and debilitating disease that increases in prevalence with age and is more common in women than men after mid-life [1]. Although the majority of epidemiological studies examining knee joint structures in either health or disease have predominantly focused on the tibiofemoral rather than the patellofemoral compartment [2], there is increasing evidence implicating the patellofemoral compartment as a major source of pain and disability [3–5].

A reduction in cartilage volume, assessed either radiographically via joint space narrowing, or directly via MRI, remains the predominant outcome measure in studies examining the natural history of knee OA [6]. Recent data from MRI studies have suggested that a reduction in knee cartilage volume occurs prior to the onset of radiographic knee OA [7–11]. It has been shown that even in the absence of OA, patella cartilage volume is reduced at an annual rate of 2.1% among older adults [12]. However, the factors that affect patella cartilage change are unclear.

The aim of this study was to determine whether age, weight, physical activity and features of patellofemoral joint structure, such as patella bone volume, affect the rate of patella cartilage loss in healthy middle-aged women with no clinical knee OA over 2 yrs.


   Participants and methods
Top
 Abstract
 Introduction
 Participants and methods
Results
 Discussion
 Acknowledgements
 References
 
The women in this study were a sub-group recruited from a larger group of 1423 community-based women who participated in a previous study examining the role of androgens in women [13]. The original group of 1423 was recruited between April 2002 and August 2003 from a database established from the electoral roll in the southern Australian state of Victoria [13]. The database was established using household addresses selected at random on a weekly basis from Australian electoral areas. In Australia, because voting is compulsory, every adult must be registered on the electoral roll. Each electoral area was divided into sampling points of approximately equal numbers of 25 000 each. Melbourne had 105 sampling points, and country Victoria had 43 sampling points. Starting addresses were selected at random from the electoral roll for each of the sampling points. Women were recruited from the database by telephone and were excluded from participation if they were pregnant or <6 weeks post-partum or had experienced any of the following in the preceding 3 months: an acute psychiatric illness; acute renal, liver, cardiovascular disease or any other acute major illness; gynaecological surgery; or active malignancy or cancer treatment, excluding non-melanotic skin cancer [13].

Of the 1423 participants aged 18–75 yrs, who participated in the original study, 292 women met the inclusion criteria for the current study, including being in the desired age range (40–67 yrs), not having had a hysterectomy or past history of cancer and having agreed to be recontacted about participation in further research studies. Women were further excluded for the current study if they had a history of previous significant knee injury requiring non-weight-bearing treatment for >24 h or surgery (including arthroscopy), evidence of radiographic OA, osteoporosis and contraindications to MRI including having a pacemaker, metal sutures, presence of shrapnel or iron filings in an eye. One hundred and seventy-six women underwent a baseline MRI scan on their dominant knee (defined as the knee the subject stepped off from when initiating walking from rest) between October 2003 and August 2004. Alfred Human Research Ethics Committee approved the study and all participants gave written informed consent.

Subjects completed a questionnaire that included demographic data, past medical and surgical history and current participation levels of physical activity at their baseline visit [14]. Participation in fortnightly exercise was assessed by asking whether or not a subject had undertaken at least 20 min of exercise that was severe enough to raise their heart or respiratory rate (e.g. bicycling, brisk walking, jogging, aerobics, etc.). From these data, a nominal scale was created to indicate exercise participation (yes/no). Weight was measured to the nearest 0.1 kg using a single pair of electronic scales with shoes, socks and bulky clothing removed. Height was measured to the nearest 0.1 cm using a stadiometer with shoes and socks removed. BMI [weight (kg)/height2 (m2)] was calculated.

At baseline, each woman had an MRI performed on her dominant knee. This was re-imaged ~2 yrs later. Knees were imaged in the sagittal plane on the same 1.5-T whole body magnetic resonance unit (Signa Advantage HiSpeed GE Medical Systems, Milwaukee, WI, USA) using a commercial receive-only extremities coil. The following sequence and parameters were used: a T1-weighted fat-suppressed 3D gradient recall acquisition in the steady state; flip angle 55°; repetition time 58 ms; echo time 12 ms; field of view 16 cm; 60 partitions; 512 x 192 matrix; one acquisition time 11 min 56 s. Sagittal images were obtained at a partition thickness of 1.5 mm and an in-plane resolution of 0.31 mm x 0.83 mm (512 x 192 pixels). Patella cartilage volumes and patellar bone volume were determined by means of image processing on an independent work station using the software program Osiris as previously described [15, 16]. A single reader measured all the MRIs, blinded regarding the time sequence of the MRI. The coefficients of variation (CVs) were 2.1% for patella cartilage volume and 2.4% for patella bone volume [17, 18].

The principal outcome variables assessed were annual rate of patella cartilage volume loss: [(initial volume–second volume)/(time between scans)] and annual percentage loss of patella cartilage volume: [(initial volume–second volume)/(initial volume)(time between scans) x 100%].

Statistical analysis
With a sample size of 148 participants from the cohort we had a power of 80% to show a correlation as low as 0.2 between the various risk factors and a change in patella cartilage volume, taking into account that multiple variables were going to be examined ({alpha}-error 0.05, two-sided significance). Descriptive statistics for characteristics of the subjects were tabulated. Independent t-tests and chi-square tests or Fisher's exact test (where appropriate) were used to compare characteristics between the study sample and the subjects lost to follow-up. A single sample t-test was used to determine whether the rate of change observed was significantly different from zero. Determinants of change in patella cartilage volume including age, body height, weight, initial patella cartilage and patella bone volume and exercise participation were assessed using linear regression analysis, and potential confounders adjusted for in a multivariate analysis. P-values of <0.05 (two-tailed) were regarded as statistically significant (SPSS Version 14.0, Chicago, USA).


   Results
Top
 Abstract
 Introduction
 Participants and methods
 Results
Discussion
 Acknowledgements
 References
 
The characteristics of the study population are presented in Table 1. One hundred and forty-eight of the original 176 subjects completed the longitudinal MRI component. Twenty-eight of the 176 subjects were lost to follow-up because of death (n = 1), migration (n = 1), knee injury (n = 4), surgery (n = 1), withdrawal of consent (n = 3) and being unable to be contacted (n = 18). Although the subjects that were lost to follow-up were significantly younger than those who completed the study (mean ± S.D., 49.5 ± 6.3 vs 52.8 ± 6.6 yrs; P = 0.01), there were no significant differences in terms of weight, body height, BMI, baseline patella cartilage volume, patella bone volume and fortnightly exercise participation between the two groups (data not shown).


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  		TABLE 1. Characteristics of the study population

 
The annual rate of patella cartilage volume loss was 35 mm3 (95% CI 26.7, 43.2), which is equivalent to 1.6% (95% CI 1.2, 1.9) per annum (Table 2). Of the subjects, 79.7% had participated in at least 20 min of exercise that was severe enough to raise their heart or respiratory rate.


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  		TABLE 2. Rate of patella cartilage change in the cohort

 
In univariate analysis, age was not associated with the annual rate of patella cartilage volume loss (P = 0.20) (Table 3). However, after adjustment for body height, weight, initial patella cartilage and bone volume, age was positively associated with the annual rate of patella cartilage volume loss (P = 0.05). Patella bone volume was negatively associated with the annual rate of patella cartilage volume loss in both univariate (P = 0.02) and multivariate (P < 0.001) analyses. Initial patella cartilage volume, body height and weight were not significantly associated with the annual rate of patella cartilage volume loss.


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  		TABLE 3. Factors affecting annual rate of patella cartilage volume loss

 
Participation in exercise (yes/no) that promoted an increased heart and respiratory rate for at least 20 min in the previous fortnight was not significantly associated with annual rate of patella cartilage volume loss in univariate analysis, but tended towards association after adjustment for age, height, weight, initial patella cartilage volume and patella bone volume (P = 0.09).


   Discussion
Top
 Abstract
 Introduction
 Participants and methods
 Results
 Discussion
Acknowledgements
 References
 
In this 2-yr study of middle-aged women with no clinical knee OA, patella cartilage volume was lost at an annual rate of 1.6% (95% CI 1.2, 1.9%). Advancing age was shown to expedite the annual rate of patella cartilage loss. Conversely, increased patella bone volume at baseline was associated with a reduced annual rate of patella cartilage volume loss and there was a trend towards an inverse relationship between fortnightly participation in exercise that caused an increased heart and respiratory rate for at least 20 min and the annual rate of patella cartilage volume loss.

In our cohort of healthy middle-aged women, the average annual rate of patella cartilage volume loss was 1.6%, which is similar to a smaller longitudinal study of healthy middle-aged men and women, where the average rate of patella cartilage loss was 2.1% per year (95% CI 1.1, 3.2%) [12]. However, in the presence of OA, patella cartilage volume is lost more rapidly, with between 3.5% and 5.3% of total cartilage volume lost annually [19]. Among healthy women, we have shown that advancing age expedites the rate of patella cartilage volume loss. Although previous cross-sectional studies have demonstrated a reduction in patella cartilage volume [20, 21] and progressive cartilage thinning [22] with advancing age, this longitudinal study is the first to demonstrate that advancing age is associated with an increased rate of patella cartilage volume loss.

No previous study has examined the relationship between patella bone volume and patella cartilage volume loss. At the tibiofemoral joint, recent evidence has suggested that bony enlargement may be an important factor initiating cartilage degeneration, whereby larger tibial plateau bone area at baseline was associated with more severe tibial cartilage defects over a 2-yr period [23], as well as reduced knee cartilage volume [24]. In the current study, we have demonstrated that baseline patella bone volume was associated with a reduced rate of annual patella cartilage volume loss. Due to the difficulties associated with assessing the undersurface of the irregular patella, we have measured patella bone volume, rather than the surface area of the bony patella. The reasons for the differences observed between the tibial and patella cartilage change in relation to bone size may be the biomechanical differences acting across the two knee compartments. As tibial plateau surface area expands, articular cartilage is effectively spread over a greater surface area and is subject to axial loads, which may make cartilage more prone to degeneration. The patella, however, is subject to retropatellar and shearing forces throughout knee range of movement, which may predominantly mediate bone volume enlargement without significantly changing the articular surface area of the patella. In turn, the patella cartilage may not be required to conform to a larger articular surface area and may establish a mechanical environment that reduces cartilage degeneration. Moreover, the increased synthetic activity required for increased bone volume may protect against cartilage loss, and Wang et al. [25] showed that higher baseline serum levels of osteocalcin were associated with a decreased rate of knee cartilage loss.

In this study, there was also a trend towards an inverse association between self-reported fortnightly participation in exercise that caused an increased heart and respiratory rate for at least 20 min and a reduced rate of annual patella cartilage volume loss. Previous work has shown that physical activity data yielded from questionnaires similar to the one used in this study yield data that are comparable with activity levels over the previous 3 yrs [26]. Using this questionnaire, we recently demonstrated a positive association between fortnightly exercise participation and medial tibial cartilage volume among these women [27]. Moreover, we have demonstrated that increased tibial cartilage volume was associated with more frequent and longer durations of vigorous activity (activity leading to diaphoresis or dyspnoea) reported 10 yrs previously, as well as recent vigorous activity in the 7 days prior to MRI [28]. This study's results also support a beneficial effect of physical activity, this time at the patellofemoral joint, by demonstrating a trend towards association between exercise participation and a reduction in the rate at which patella cartilage volume is lost.

Why fortnightly exercise participation tended to be associated with a reduced rate of patella cartilage volume loss is unclear. This effect could not be explained by an increase in patella bone volume or younger age, since our results were independent of these factors. It is well recognized that some degree of mechanical stimulation is required to maintain cartilage health [29], and exercise may mediate an optimal mechanical environment. Other cross-sectional and longitudinal studies in children have shown that tibial cartilage development is stimulated by exercise [30, 31], while in adults, forced immobility is associated with marked reductions in cartilage volume at the knee [32]. Nevertheless, future longitudinal investigations are required to clarify the type, frequency, intensity and duration of exercise required to confer a beneficial effect across the knee joint.

This study was limited by the examination of healthy women, and therefore our results cannot be generalized to men or people with knee OA. Moreover, 16% of women with a baseline MRI did not complete the study. The women who did not have follow-up MRI were younger than those who were retained in the study. As the most common reason for not attending for MRI at follow-up was an inability to be recontacted, it is unlikely that the loss of women from this study would have introduced any systematic bias into the study findings. Although we were able to detect a significant rate of patella cartilage loss, we only examined women over a relatively short period (2 yrs), and longer studies would be needed to examine the effect of factors that may have a weaker effect on the rate of change of patella cartilage volume. Although we showed a protective effect of exercise participation and the rate of patella cartilage volume loss, based on the questionnaire used in this study, we cannot distinguish between weight-bearing and non-weight-bearing exercises, and therefore cannot determine whether weight-bearing exercises are more advantageous than non-weight-bearing exercises for the patella cartilage. Furthermore, we did not examine participation in exercises of varying intensity, duration and frequency, all of which may be important.

We have shown that among middle-aged women with no clinical knee OA, patella cartilage volume is lost at 1.6% per annum. Although older age was associated with an increased annual rate of patella cartilage volume loss, increased patella bone volume at baseline was associated with a reduced annual rate of patella cartilage volume loss. Moreover, fortnightly participation in exercise that promoted an increased heart and respiratory rate for at least 20 min tended to be associated with a reduced rate of cartilage loss. Interventions targeting modifiable factors, such as physical activity, warrant further investigation as they may help to prevent the development of patellofemoral OA.

Formula


   Acknowledgements
Top
 Abstract
 Introduction
 Participants and methods
 Results
 Discussion
 Acknowledgements
References
 
We would like to thank the women who took part in this study.

Funding: This work was supported by grants from the National Health and Medical Research Council of Australia (grants number 219279 and 334267). Dr Wluka is the recipient of an NHMRC Public Health (Australia) Fellowship (NHMRC 317840). Dr Hanna is the recipient of an NHMRC Public Health (Australia) Fellowship (NHMRC 418961).

Disclosure statement: The authors have declared no conflicts of interest.


   Notes
 
*S. P. Wijayaratne and A. J. Teichtahl equally contributed to this work. Back


   References
Top
 Abstract
 Introduction
 Participants and methods
 Results
 Discussion
 Acknowledgements
 References
 

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Submitted 2 January 2008; revised version accepted 5 June 2008.
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