The authors have no conflict of interest.
Evidence From Data Searches and Life-Table Analyses for Gender-Related Differences in Absolute Risk of Hip Fracture After Colles' or Spine Fracture: Colles' Fracture as an Early and Sensitive Marker of Skeletal Fragility in White Men†
Article first published online: 20 SEP 2004
Copyright © 2004 ASBMR
Journal of Bone and Mineral Research
Volume 19, Issue 12, pages 1933–1944, December 2004
How to Cite
Haentjens, P., Johnell, O., Kanis, J. A., Bouillon, R., Cooper, C., Lamraski, G., Vanderschueren, D., Kaufman, J.-M. and Boonen, S. (2004), Evidence From Data Searches and Life-Table Analyses for Gender-Related Differences in Absolute Risk of Hip Fracture After Colles' or Spine Fracture: Colles' Fracture as an Early and Sensitive Marker of Skeletal Fragility in White Men. J Bone Miner Res, 19: 1933–1944. doi: 10.1359/jbmr.040917
NEMO is a Thematic Network supported by the European Commission under contract QLK6-CT-2002–00491. Participants in NEMO are listed in the Acknowledgments section.
- Issue published online: 2 DEC 2009
- Article first published online: 20 SEP 2004
- Manuscript Accepted: 15 JUL 2004
- Manuscript Revised: 21 MAY 2004
- Manuscript Received: 28 JAN 2004
- absolute risk;
- hip fracture;
- Colles' fracture;
- spine fracture
Based on data searches and life-table analyses, we determined the long-term (remaining lifetime) and short-term (10- and 5-year) absolute risks of hip fracture after sustaining a Colles' or spine fracture and searched for potential gender-related differences. In aging men, Colles' fractures carry a higher absolute risk for hip fracture than spinal fractures in contrast to women. These findings support the concept that forearm fracture is an early and sensitive marker of male skeletal fragility.
Introduction: Colles' fracture occurrence has been largely ignored in public health approaches to identify target populations at risk for hip fracture. The aim of this study was to estimate the long-term and short-term absolute risks of hip fracture after sustaining a Colles' or spine fracture and to search for potential gender-related differences in the relationship between fracture history and future fracture risk.
Materials and Methods: To determine the long-term (remaining lifetime) and short-term (10- and 5-year) absolute risks of hip fracture, we applied life-table methods using U.S. age- and sex-specific hip fracture incidence rates, U.S. age-specific mortality rates for white women and men, pooled hazard ratios for mortality after Colles' and spine fracture, and pooled relative risks for hip fracture after Colles' and spine fracture, estimated from cohort studies by standard meta-analytic methods.
Results: Our results indicate that the estimated remaining lifetime risks are dependent on age in both genders. In women, remaining lifetime risks increase until the age of 80 years, when they start to decline because of the competing probabilities of fracture and death. The same pattern is found in men until the age of 85 years, the increment in lifetime risk being even more pronounced. As expected, the risk of sustaining a hip fracture was found to be higher in postmenopausal women with a previous spine fracture compared with those with a history of Colles' fracture. In men, on the other hand, the prospective association between fracture history and subsequent hip fracture risk seemed to be strongest for Colles' fracture. At the age of 50, for example, the remaining lifetime risk was 13% in women with a previous Colles' fracture compared with 15% in the context of a previous spine fracture and 9% among women of the general population. In men at the age of 50 years, the corresponding risk estimates were 8%, 6%, and 3%, respectively. Similar trends were observed when calculating 5- and 10-year risks.
Conclusions: In aging men, Colles' fractures carry a higher absolute risk for hip fracture than spinal fractures in contrast to women. These findings support the concept that forearm fracture is an early and sensitive marker of male skeletal fragility. The gender-related differences reported in this analysis should be taken into account when designing screening and treatment strategies for prevention of hip fracture in men.
Of all osteoporosis-related fractures, hip fracture is the most dramatic in terms of mortality, morbidity, and economic expenditure.(1) Various studies have identified a history of a fragility fracture as one of the main risk factors for subsequent hip fracture,(2–13) even after adjusting for BMD.(14,15) Prospective associations have been documented between hip fracture occurrence and spine or Colles' fracture, both in women and in men.(16,17) However, if and to what extent this relationship is different between men and women remains to be clarified.
The aim of this study was to estimate the long-term and short-term absolute risks of hip fracture after sustaining a Colles' or spine fracture and to search for potential gender-related differences in the relationship between fracture history and future fracture risk. In a recent meta-analysis, we provided evidence that a Colles' fracture is a stronger risk factor for future hip fracture in men than in women.(17) While our results provided powerful estimates of relative risk, they gave no information about absolute fracture risk (i.e., how many individuals will actually suffer a hip fracture).(18) Absolute risk figures are increasingly being considered as the optimal basis for individual clinical treatment decisions and public health policy strategies.(18–20) In this regard, this study extends our former findings and provides estimates of absolute (5-year, 10-year, and remaining lifetime) hip fracture risks in aging men and women after the occurrence of a Colles' or spine fracture at ≥50 years of age.
MATERIALS AND METHODS
Overall study design
This study was designed to provide an estimate of long-term and short-term absolute risk of hip fracture in white men and women after Colles' or spine fractures, based on a hypothetical approach (data searches and life-table analyses).
We used pooled relative risks for hip fracture after Colles' and spine fracture,(17) U.S. age-specific mortality rates for white women and men, pooled hazard ratios for mortality after Colles' and spine fracture, U.S. age- and sex-specific hip fracture incidence rates, and life-table methods(19,20) to determine the 5-year, 10-year, and remaining lifetime hip fracture risk for three (hypothetical) cohorts of individuals with or without a history of a Colles' or spine fracture, at a given age.
Briefly, in our model, estimates of hip fracture risk were calculated for three hypothetical 50-year-old women. A woman sustaining a Colles' fracture, one sustaining a spine fracture, and finally, one without Colles' or spine fracture were all modeled from the initial age of 50 until suffering a hip fracture or dying. We calculated the probability of suffering a hip fracture for each year, from the initial age of 50 through age 95. We used this method to estimate the 5-year, 10-year, and remaining lifetime risk of hip fracture for imaginary cohorts of white women for initial ages ranging from 50 to 90 years, year-by-year.(19,20) Calculations started at the age of 50—the mean age of menopause—and stopped at the age of 95, because there are no reliable data about the incidence of fractures beyond that age.
Similar models were applied to hypothetical cohorts of white men 50–90 years of age, again performing analyses year-by-year.
Details of the mathematical calculations, their derivations, and a description of the underlying assumptions of the model are described below.
Relative risk of hip fracture after previous Colles' or spine fracture
In a previous study,(17) we estimated the relative risk of hip fracture after previous Colles' or spine fracture in men and women, based on a systematic review and meta-analysis of published cohort studies. In that recently published meta-analysis, we conducted an Internet-based PubMed search, using the keywords “osteoporosis” and “fracture,” to identify relevant studies published in English, French, and German since 1982. To be included, studies had to fulfill all the following criteria: reporting data on elderly men and/or postmenopausal women ≥50 years of age, defining the exposure unequivocally as a radiographically confirmed wrist or spine fracture, defining the outcome unequivocally as a radiographically or surgically confirmed hip fracture, reporting the relative likelihood of hip fracture (either relative risk with p values or 95% CI, or the observed and expected number of outcome events), and having used a longitudinal (cohort) design. In the absence of statistical heterogeneity, we used a fixed-effects model to combine the evidence. An overall common relative risk (pooled relative risk) was estimated from the average of the logarithms of the individual relative risk, each weighted by the inverse of its variance. When heterogeneity occurred, we planned a DerSimonian and Laird random-effects model analysis.
The nine studies considered eligible(2,3,5–7,8–11) were all written in English. Most studies were conducted in the United States,(2,3,6,10,11) but European countries were also represented.(5,7,8,9) Taken together, the studies included 499 men and 3683 women with a wrist fracture and 894 men and 3399 women with a spine fracture. The occurrence of a subsequent hip fracture was documented during a median follow-up time ranging from 2.9 to 8.3 years (accounting for 126,767 person-years, overall).
We identified four cohort studies(3,8,9,11) that examined the likelihood of hip fracture among postmenopausal women after sustaining a Colles' fracture, and five cohort studies(2,5–7,10) that examined the likelihood of hip fracture in postmenopausal women after sustaining spine fracture(s). Among postmenopausal women, the relative risks for a future fracture of the hip after a Colles' or spine fracture were 1.53 (95% CI, 1.34–1.74; p < 0.001) and 2.20 (95% CI, 1.92–2.51; p < 0.001), respectively.(17)
We identified three cohort studies(3,9,11) that examined the likelihood of hip fracture among aging men after sustaining a Colles' fracture and two cohort studies(5,10) that examined the likelihood of hip fracture among aging men after sustaining spine fracture(s). In older men, these relative risks were 3.26 (95% CI, 2.08–5.11; p < 0.001) and 3.54 (95% CI, 2.01–6.23; p < 0.001), respectively.(17)
Population-based age-specific mortality rates/life expectancy
Population-based, age-specific mortality rates for white women and men were taken from U.S. vital statistics for 2000.(21) These vital statistics provide the average mortality for women and men at each age. At the ages of 50, 60, 70, and 80 years, for example, average life expectancy for white females in the United States of America is about 32, 23, 16, and 9 years, respectively. Likewise, at the ages of 50, 60, 70, and 80 years, life expectancy for white U.S. men is about 28, 20, 13, and 7 years, respectively.(21)
Estimating mortality after previous Colles' or spine fracture
We determined mortality among aging women and men who sustained a Colles' or a clinically diagnosed vertebral fracture compared with members of the general population. To do so with sufficient power, we conducted a systematic review and meta-analysis of studies published in full in the existing literature between 1992 and 2000, selecting only population-based prospective cohort studies and using similar meta-analytic techniques as described previously.(17)
An Internet-based search on PubMed using the keywords “fracture” and “mortality” identified seven relevant papers, all of which were written in English.(22–28) These cohort studies were conducted in the United States,(22,24,25,27) the European Union,(26,28) and Australia.(23)
We identified four cohort studies(22–24,28) that examined mortality among women with a history of a clinically diagnosed Colles' fracture and five cohort studies(23–27) that examined mortality in women who had sustained a clinically diagnosed spine fracture. The pooled relative risks of dying after a Colles' or spine fracture were 0.94 (95% CI, 0.90–0.99; p = 0.01) and 1.43 (95% CI, 1.35–1.52; p < 0.001), respectively.
We identified two studies(23,24) that examined mortality among ageing men who had sustained a Colles' fracture and three studies(23,24,26) that examined mortality in men with a previous clinical spine fracture. The pooled relative risks of dying after a Colles' or spine fracture were 1.04 (95% CI, 1.00–1.09; p = 0.075) and 2.22 (95% CI, 2.05–2.42; p < 0.001), respectively.
Population-based age- and gender-specific fracture incidence
The age- and sex-specific annual hip fracture incidence among white women and men was estimated from U.S. population-based surveys published between 1993 and 1996.(29–31) These incidence rates were reported for discrete (5-year) age intervals. We extracted these rates for first hip fractures as given in each of the cited publications and computed mean age-specific hip fracture rates for each 5-year age group, both in women and men.
We adapted life-table methods previously described by Schlesselman(19) and Pettiti and Sidney.(20) Our method is shown in Table 1, which is the life table for an imaginary cohort of 1,000,000 postmenopausal women sustaining a Colles' fracture at 50 years of age. A similar life table was constructed for postmenopausal women suffering a spine fracture at 50 years of age and for postmenopausal women without previous Colles' or spine fracture at 50 years of age (data not shown). Lifetime estimates were also calculated for initial ages ranging from 50 to 90 years by single year.
We used similar methods to calculate the lifetime risk of hip fracture for imaginary cohorts of aging men for initial ages ranging from 50 to 90 years by single year. Our method in aging men is shown in Table 2, which is the life table for an imaginary cohort of 1,000,000 aging men sustaining a Colles' fracture at 50 years of age.
The 5-year, 10-year, and remaining lifetime risks of hip fracture in the various age and sex groups after Colles' or spine fracture and in the reference population are shown in Table 3. The same estimates are presented graphically in Fig. 1.
The estimated remaining lifetime risks of hip fracture (by 5-year intervals) among three cohorts of white women with initial ages ranging from 50 to 90 years are shown in the fifth column of Table 3. We estimated that a 50-year-old white woman, for example, has a 13% lifetime risk of hip fracture if she suffers a Colles' fracture at the age of 50, a 15% lifetime risk of hip fracture if she suffers a spine fracture at the age of 50, and a 9% lifetime risk of hip fracture if she has no Colles' or spine fracture at the age of 50 (background risk). As shown in Fig. 1, the remaining lifetime risks increase until the age of 80 years. Beyond the age of 80, these risks start to decline because of the competing probabilities of fracture and death. At any given age, the remaining lifetime risk of hip fracture for a postmenopausal woman is higher after spine fracture than after Colles' fracture.
The difference between the lifetime risk after a previous fracture and the lifetime risk in the reference population provides information on the public health impact of exposure (i.e., previous fracture occurrence). For an individual 50-year-old postmenopausal woman, for example, a history of a Colles' fracture results in a 4% (13% − 9%) increase in her lifetime risk of hip fracture. This 4% difference (4 in 100 women over a remaining lifetime) is the increased risk attributable to the Colles' fracture. This absolute risk difference (or attributable risk) varies little between 50 and 90 years of age, both after Colles' and spine fracture. At any given age, the attributable risk of hip fracture is, on average, 6% after Colles' fracture and 8% after spine fracture.
In postmenopausal women, the 5-year and 10-year risks of developing a hip fracture depend largely on age and to a much lesser extent on the type of fracture. At any given age, the 5-year and 10-year risks are higher among women with a history of a spine fracture than among those with a previous Colles' fracture (Table 3; Fig. 1).
In contrast to women, the remaining lifetime risk of hip fracture in white men is always markedly higher after a previous Colles' fracture than after a spine fracture (Table 3; Fig. 1). As in women, lifetime risk increases with age. However, the increment in lifetime risk in men is even more pronounced than in women and only starts to decline after the age of 85.
Also in contrast to women, the absolute risk differences (attributable risks) increase steadily with increasing age, both after Colles' and spine fracture. For example, at the age of 50, the attributable risks are 5% and 3% after Colles' and spine fracture, respectively. At the age of 80, these absolute risk differences are 11% and 6% after Colles' and spine fracture, respectively.
The problem of fractures of the proximal femur in men has recently been recognized as an important public health issue. In addition to an exponential age-associated increase, an age-specific increase in fracture incidence has been consistently documented in all populations of men examined,(32) whereas in women, the rate of hip fracture seems to have stabilized. The clinical consequences of proximal femoral fracture are early mortality and long-term morbidity. Mortality in the first 6 months after fracture is 18–34%, which is about three times higher than in age- and sex-matched controls, and men seem to have a significantlyhigher mortality than age-matched women.(33) This difference is only partially explained by differences in co-morbidity,(34) suggesting that male gender is a major risk factor for hip fracture-associated mortality.(35) However, in personal and economic terms, the morbidity of hip fracture is perhaps even more daunting than the mortality. Almost 50% of men with hip fractures will have to be institutionalized because of the fracture, and up to 80% of those who survive fail to regain their prefracture level of functional independence.(36) The economic impact of hip fracture in men can be calculated from available data as approximately one-fifth of the total cost of osteoporosis, or about $2.75 billion annually in the United States alone.(37)
Fracture models have been developed that can estimate remaining lifetime fracture risk based on initial age, initial BMD, and other factors, including the anticipated rate of bone loss.(38–53) To the best of our knowledge, this study is the first to estimate the effects of Colles' and spine fracture on absolute risks of hip fracture in postmenopausal women and aging men. As expected, our estimates indicate that, in postmenopausal women, the risk of sustaining a hip fracture is higher after a spine fracture than after a Colles' fracture. In aging men, on the other hand, the prospective association between fracture history and subsequent hip fracture risk seems to be strongest for Colles' fracture. Similar trends are observed when calculating remaining lifetime, 10-year, and 5-year risks. These data provide strong evidence for gender-related differences in the relationship between fracture history and future hip fracture occurrence.
The findings presented in this analysis may have important clinical implications. They highlight the predictive risk of Colles' fracture for future hip fracture in men and also the presence of substantial gender-related differences in the association between subsequent osteoporotic fractures.(54–57) From a public health perspective, our results support the need for targeting interventions at men with Colles' fracture to potentially reduce the burden of morbidity and mortality caused by hip fracture in old age.(58–61) The data are consistent with gender-related differences in the pathogenesis of hip fractures. They support the concept that Colles' fracture is an early and sensitive marker of skeletal fragility in men.(1) The incidence of distal forearm fractures is markedly lower in men than in women, with a male-to-female ratio of only about 1:6 at the age of 55, and decreasing even further to 1:10 at >75 years of age.(62–65) This low incidence of Colles' fracture in men is partly explained by differences in bone size and cortical thickness, which is a result of differences in the degree of periosteal bone formation and endocortical bone resorption between sexes,(66) providing a mechanical advantage to the male appendicular skeleton. In those who do suffer a Colles' fracture, impaired skeletal strength (low BMD and/or a deterioration of bone architecture) is likely to be present. Vertebral fractures, on the other hand, are less important risk factors for hip fracture in men than a history of Colles' fracture. These findings suggest that, at least in a subset of men, vertebral fracture occurrence may be a marker of trauma rather than a marker of bone fragility. This assumption is supported by prevalence data, which show little difference in the rates of radiographically detected vertebral deformities among men and women (∼5–10%) at younger ages.(62,63)
In both sexes, we observed an age-associated increase in absolute hip-fracture risk. Our estimates of remaining lifetime risks of hip fracture showed that the absolute risk increases until the age of 80 for women and 85 for men. Beyond the ages of 80–85, age-specific mortality from other causes rises much faster than hip-fracture incidence, and the effect of this competing mortality reduces the absolute risk of hip fracture in these oldest old. As expected, absolute hip fracture risk in women was found to be higher than in men at any given age. Using traditional methods for synthetic life-table analysis based on current mortality rates and fracture-incidence rates, we estimated that about 9% of women of the general population alive at the age of 50 will have at least one hospitalization for hip fracture before dying. Compared with estimates for white women previously reported in the literature, this 9% figure is relatively low.(38–53) In women ≥50 years of age, the reported lifetime risk of hip fracture varies from 11% to 23%, depending on differences in fracture incidence, life expectancy, and methods of calculation. Higher estimates are obtained using models based on the assumptions that life expectancy will continue to improve and that the age- and sex-specific incidences of hip fractures will continue to increase. Using the cumulative risk method rather than the life-table method to calculate lifetime risks will also result in higher risk estimates.(67)
There are several limitations that may affect the inferences derived from our calculations. These include the fact that the life-table method-based analyses used do not take into account the potentially confounding effects of risk factors exposed to and any treatment received for osteoporosis, as well as the potential for bias related to the extent to which fracture rates, mortality rates, and relative risks may vary over time. Also, available information on age-specific mortality and morbidity rates is based on current, cross-sectional data on patients of different ages. There is no guarantee that these rates will remain constant over the time span for which absolute risks are calculated. Secular trends in age-specific fracture rates can cause appreciable errors in projected absolute risk estimates. For example, the incidence of hip fractures in the United States increased dramatically between 1977 and 1995.(68) If a further age-specific increase would occur in the future, absolute risk estimates based on current hip fracture incidence rates would underestimate the true risks experienced by patients in years to come. In addition, relative risks may vary over time. Published relative risks are composite estimates that reflect the typical experience of patients during the years of observation. In most studies, the interval between exposure and subsequent morbidity or mortality ranged from a few years to a few decades. Life-table method-based analyses, as used in our study, assume a constant lifelong relative risk, which may be unrealistic. Although mortality trends are stable in many countries and relative risk functions can be used that vary with the time since exposure, it is not possible to determine how future relative risks would change over time with the data to hand. Moreover, lifetime risk estimates are sensitive to changes in life expectancy, and our calculations may need to be periodically reevaluated as the life expectancy of our reference (United States) population continues to rise and the risk of mortality caused by alternative causes, such as cardiovascular illness and cancer, varies. Also, the mortality hazard after hip fracture is particularly high immediately after the event, but decreases thereafter, albeit not to that of the general population. This might bias short-term probability. One further limitation of our approach is that the analyses to predict future fracture risk had to be based on clinically diagnosed vertebral fractures—which only account for about one-third of all vertebral fractures—as opposed to radiologically defined fractures. In postmenopausal women, all vertebral fractures increase the risk for subsequent osteoporotic fracture, regardless of their clinical presentation.(69) In men, however, information is lacking as to whether the relationship between prior vertebral fracture and future hip fracture is similar for clinical and morphometric fractures. We cannot rule out the possibility that our estimates may have underestimated the impact of prior vertebral fractures on hip fracture risk in men. Finally, the generalizability (external validity) of our absolute risk estimates to other populations and its use in clinical risk prediction are limited by the fact that the data were restricted to a white U.S. population and that we had no information available on the treatment of osteoporosis.(70) Overall, it should be emphasized that our conclusions are based on a hypothetical approach as opposed to an actual prospective study and that direct validation of our data are lacking.
The strengths of our study, on the other hand, include the use of standard meta-analytic procedures for retrieval, assessment of relevance, and statistical processing of the data. All estimates were based on peer-reviewed papers and official U.S. government reports, providing access to well-defined population-based cohort studies, and robust information on age- and sex-specific fracture incidences and all-cause mortality data.(21–31) The life-table methods used took into account the effect of risk factors (i.e., Colles' or spine fracture) on competing mortality, which in turn can affect absolute risk estimates of the event of interest (i.e., hip fracture). Finally, lifetime risk is a well-accepted method to quantify the likelihood of a variety of adverse health outcomes. In this regard, our results allow comparisons with risk estimates for other diseases.(67,71) In the context of a previous Colles' fracture, our calculations indicate that men 50 years of age have a remaining lifetime risk of 10% of sustaining a hip fracture. At the same age, their lifetime risk to develop prostate cancer or Alzheimer's disease is only about 5%.(67,71) From a public health perspective, lifetime risk calculations such as those presented here not only allow to estimate the consequences of various diseases and complications, but also a more appropriate allocation of resources for competing causes of morbidity.
Although we acknowledge the limitations of our approach, our findings suggest that the risk for hip fracture is higher in women after a spine fracture, but for men, the hip fracture risk was strongest after a Colles' fracture. We conclude that, in aging men, Colles' fractures carry a higher absolute risk for hip fracture than spinal fractures in contrast to women. These findings support the concept that forearm fracture is an early and sensitive marker of male skeletal fragility. This information should be taken into account when designing screening and treatment strategies for prevention of hip fracture in aging men.
This work was a collaborative effort within the Network on Male Osteoporosis in Europe (NEMO), supported by the European Commission under contract number QLK6-CT-2002–00491, and was additionally supported by grant G.0171.03 from the Fund for Scientific Research-Flanders, Belgium (F.W.O.-Vlaanderen) to SB. SB and DV are both Senior Clinical Investigators of the Fund for Scientific Research-Flanders, Belgium (F.W.O.-Vlaanderen). SB is holder of the Leuven University Chair for Metabolic Bone Diseases. Participants in NEMO are S Boonen (Leuven University, Belgium), J Blanch (University of Barcelona, Spain), D Chappard (Université d'Angers, France), J Compston (University of Cambridge, UK), C Cooper (MRC, Southampton, UK), JP Devogelaer (St Luc University, Belgium), MC de Vernejoul (INSERM Paris, France), C Glüer (University of Kiel, Germany), O Johnell (Lunds University, Sweden), J Kanis (University of Sheffield, UK), JM Kaufman (NEMO Coordinator, Ghent University, Belgium), P Lips (Free University of Amsterdam, The Netherlands), D Navid (International Osteoporosis Foundation, Lyon, France), R Nuti (University of Siena, Italy), S Ortolani (Instituto Auxologico Italiano, Italy), P Delmas (INSERM Lyon, France), J Reeve (Addenbrooke's Hospital Cambridge, UK), R Rizzoli (CHU Cantonal Geneva, Switzerland), J Stepan (Charles University Prague, Czech Republic), and A Uitterlinden (Erasmus University Rotterdam, The Netherlands).
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