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Keywords:

  • osteoporosis;
  • spinal fractures;
  • kyphosis;
  • respiratory function tests;
  • vital capacity

Abstract

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgements
  8. REFERENCES
  9. APPENDIX 1:

We conducted a systematic review to examine the relationship between osteoporotic vertebral fractures, kyphosis, and pulmonary function. Findings suggest modest but predictable declines in vital capacity related to the degree of kyphosis. However, there were only four studies, and all had significant methodologic limitations. Further high-quality research is needed.

Introduction: Our objective was to systematically review the extent to which osteoporosis-related vertebral fractures and kyphosis affect pulmonary function.

Materials and Methods: We used a literature search from 1966 to 2006 (using Medline, EMBASE, and hand searches of references) for studies examining pulmonary function in patients without known lung disease who had vertebral fractures or kyphosis secondary to osteoporosis. Two reviewers independently abstracted data. Heterogeneity precluded formal meta-analysis.

Results: Initial searches yielded 453 articles. After applying eligibility criteria, only four case-control studies of limited quality (e.g., only one study was blinded) remained. Since 1966, only 109 patients (6 men) have been studied. All four studies reported reductions in vital capacity (VC), with values ranging from 68% to 94% of predicted values. This was quantified as a 9% reduction in predicted VC per vertebral fracture in one study. The degree of kyphosis clinically (one study) or radiographically (three studies) correlated with declines in VC; impairments were most notable at kyphotic angles >55°. Statistically significant differences in percent predicted VC were obtained only when arm span or recalled height, rather than measured height, was used (two studies).

Conclusions: Despite conventional teaching, the evidence relating osteoporotic vertebral fractures or kyphosis to pulmonary function is limited. On the basis of available studies, declines in VC secondary to kyphosis seem modest and directly related to the number of vertebral fractures or degree of kyphosis. Future studies need longitudinal follow-up of larger numbers of men and women, appropriate proxies for height, standardized measures for pulmonary function and kyphosis, and efforts to blind outcomes ascertainment.


INTRODUCTION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgements
  8. REFERENCES
  9. APPENDIX 1:

Osteoporosis is a disorder characterized by compromised bone strength and skeletal fragility that predisposes a person to increased risk of fracture.(1) As the population ages, the incidence of osteoporosis-related complications will continue to rise. Attention to disease sequelae and early intervention remain major public health objectives. Among the screening criteria for osteoporosis, guidelines now suggest clinically apparent kyphosis as one of the indications for BMD testing.(2)

In addition to disfiguring kyphosis, height loss, and chronic back pain, osteoporosis of the spine is thought to result in pulmonary compromise. Whereas kyphosis is a well-recognized consequence of osteoporotic fractures of the spine,(3) there is less emphasis in the literature on the concomitant association with impairments in pulmonary function. Based on data from other neuromuscular diseases affecting the chest wall (e.g., poliomyelitis), we would anticipate that osteoporosis-related kyphosis would lead to a restrictive pattern on standard pulmonary function tests.(4–7) Nonetheless, the prevalence, strength of association, and extent of potential derangements relating osteoporosis and pulmonary function have not been well characterized in the literature. Therefore, our objective was to systematically identify and review all of the currently available literature on osteoporotic vertebral fractures and kyphosis as they relate to impairments in pulmonary function as measured by pulmonary function testing.

MATERIALS AND METHODS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgements
  8. REFERENCES
  9. APPENDIX 1:

Necessary background to inform search strategy

To study osteoporosis-related kyphosis and pulmonary function, standardized measurements are required. Briefly, standard pulmonary function tests (PFTs) include spirometry, lung volume and diffusion capacity, and sometimes maximal inspiratory and expiratory pressures. PFT results are analyzed and reported in comparison with standardized reference values for each parameter. Reference values are generally based on age, sex, and height, but variations in the formulas used to generate these values may alter or influence test results. Germane to this review is the ascertainment of “height” in patients with osteoporosis-related kyphosis—it may be recorded as current (as directly measured), historical (as recalled by the patient(6)), or predicted (using arm span(4,8–10)). Test results may vary widely if alternatives for measured height are used or not reported. Several authors have proposed that arm span should be used as a surrogate for height in all patients with clinically apparent kyphosis,(4,8) but this recommendation is rarely followed. Similarly, the degree of kyphosis itself can be measured clinically using a variety of techniques.(11–14) Kyphosis may be measured by rib–pelvis measurements,(12,14) wall-occiput measurements,(12,14) height measurements,(8,15) or radiographically using quantitative vertebral body analysis or calculation of “Cobb's angle.”(16) Again, severity of kyphosis is rarely reported in a standardized fashion.

Search strategy

We systematically searched the published literature using Medline (1966 to February 2006) and EMBASE (1988 to February 2006) for studies that examined the association between osteoporosis-related kyphosis and impairments in pulmonary function. References of all studies included in the review were also hand-searched, and we consulted with content experts. The search strategy itself was constructed with input from expert clinicians, epidemiologists, and professional librarians.

All English-language studies were included if they examined vital capacity (as measured by PFTs) in a series of patients with osteoporosis-related kyphosis or vertebral compression fractures that had been published through February 2006. Studies that considered patients with chronic lung disease that developed osteoporosis as a result of the lung disorder or its treatment were excluded. We also excluded studies that did not use PFT to assess vital capacity; studies of patients with kyphosis or kyphoscoliosis if the reason for these abnormalities was not related to osteoporosis; studies that described respiratory changes secondary to neuromuscular disease rather than osteoporosis-related kyphosis; and case reports or narrative reviews.

The following search terms were used: osteoporosis, kyphosis, spinal fractures, vertebral fractures, respiratory mechanics, lung compliance, forced expiratory volume, respiratory function tests, lung volume measurements, ventilatory capacity, FEFR, FEV1, FVC, vital capacity, VC, and spirometry (see Appendix 1 for the complete search history). Two reviewers (RAH, SRM) independently abstracted all of the data, and any discrepancy related to inclusion/exclusion or data interpretation was resolved by a consensus of investigators. In addition, each of the included studies was assessed by two reviewers for methodologic quality using a previously validated checklist(17) designed for observational (nonrandomized) studies. This checklist, published by Downs and Black,(17) attempts to assess and quantify the quality of reporting, internal and external validity (including bias, confounders, and generalizability), and power. The maximum score is 32; in their initial validation work, the mean (and median) quality scores for nonrandomized studies was ∼12 (38%).(17) In the absence of a reference standard, we considered a score of 12 or greater to define acceptable quality, and for ease of interpretability, present percentage scores out of a total of 32. With the previously mentioned differences in the measurements and reporting of kyphosis and PFT reference values related to height, combined with a paucity of available studies on this subject, we anticipated a priori that it would be difficult to quantitatively summarize the evidence and that the quality and heterogeneity of the data would preclude formal meta-analysis.

RESULTS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgements
  8. REFERENCES
  9. APPENDIX 1:

Figure 1 is a QUOROM(18) diagram that shows the overall yield of our search. The search generated a total of 453 articles in Medline or EMBASE. Of these, 55 articles were duplicated between the databases. A further 250 citations were excluded on our first screen on the basis of their titles and abstracts being deemed not relevant to the question of interest. This left 148 articles. One hundred twenty articles were excluded on the basis of their title and abstract, because they did not relate to osteoporosis (n = 64) or kyphosis (n = 1), they did not use formal PFTs to assess vital capacity (n = 12), they involved an underlying chronic lung disease such as asthma as the primary problem being studied (n = 13), or the title and abstract were not relevant (n = 30). This left 28 articles for review and possible abstraction. After detailed review, this left four articles that both addressed the question of interest and that met our inclusion and exclusion criteria. Agreement between reviewers on inclusion and exclusion of studies was 100%; similarly, there was 100% inter-reviewer agreement for the abstraction of important data elements. A list of excluded references is available on request.

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Figure Figure 1. QUOROM diagram: summary of systematic search. See the Materials and Methods section and reference 18.

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In summary, there were no moderate or large prospective, blinded, longitudinal studies addressing our question of interest. We identified four case-control studies of varying methodologic quality (Tables 1 and 2). The mean (and median) score for the four case-control studies included in our review (and summarized in detail below) was 12 of a possible 32 points (38%). Two of the four studies scored >12 but still only obtained scores of 40% and 47%, respectively. The four studies that were identified are summarized below, in chronological order, and outlined in full detail in Table 1 (study characteristics) and Table 2 (results).

Table Table 1.. Characteristics of Four Case-Control Studies That Evaluated Pulmonary Function in Patients With Osteoporosis-Related Kyphosis
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Table Table 2.. Findings of Four Case-Control Studies That Evaluated Pulmonary Function in Patients With Osteoporosis-Related Kyphosis
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Leech et al. (1990)

These investigators examined 74 consecutively identified Canadian patients referred with clinically “suspected osteoporosis,” identified as eligible by chart review.(4) Although there was not an explicitly stated control group, they compared parameters between 29 patients who did not have vertebral fractures and 45 patients who did (vertebral fractures were defined as ≥4-mm differences in vertebral height between the anterior and posterior vertebral body surfaces); furthermore, they pointed out that some of the participants in the group without fractures may not have actually had osteoporosis as it is currently defined by BMD measurement. They report measured height, arm span, and recalled height at age 25 years, but ultimately, arm span was used to calculate reference values for PFT. This was the only study reviewed that included measures of respiratory muscle strength—specifically, the minimal inspiratory and expiratory pressures.

This study showed that women with vertebral compression fractures had significantly decreased percent predicted vital capacity compared with those participants without fractures. The degree of kyphosis, based on Cobb's angle, also predicted decreased vital capacity. Using a split-sample technique, “approximately half” of their patients were used to derive a regression equation to predict decline in vital capacity attributable to each vertebral fracture. This prediction rule was validated in the rest of their population. The authors concluded that each additional thoracic vertebral compression fracture was statistically significantly associated with an ∼9% incremental decrease in predicted vital capacity.

Limitations of the study include its small size, restriction to women from one specialty clinic, and outcomes ascertainment that was unblinded. Patients who smoked were included in the analysis, although the authors point out that there was no effect of smoking on forced vital capacity (FVC) in the study population when smoking status was entered into the regression model. Nevertheless, this study achieved the highest methodologic quality score(17) of the four articles in our review (15 of 32; 47%).

Culham et al. (1994)

Culham et al.(5) assessed the relationship between thoracic kyphosis and rib mobility and observed the effects of kyphosis-related rib mobility on changes in pulmonary function. They studied a series of 15 women with osteoporosis and kyphosis and 15 healthy women with (presumably) neither osteoporosis nor kyphosis. They measured weight, height, and arm span; kyphosis was evaluated using an inclinometer, and an electromagnetic device was used to measure rib mobility.

They reported that women with osteoporosis-related kyphosis had significantly lower vital capacity, total lung capacity, lateral rib expansion, and vertical rib excursion compared with age- and sex-matched controls (all comparisons, p < 0.05). There was also a statistically significant inverse correlation between the degree of kyphosis and vital capacity.

This study was limited by the small number of participants restricted to women from an unspecified referral source and the fact it was unblinded. Participants were age-matched, and this allowed comparison of absolute rather than percent predicted lung volumes, although typically height is also factored into percent predicted values. No statistically significant differences in measured height were observed between groups, but as previously suggested, measured height may be altered in patients with kyphosis.(4,8) Patients who smoke or had smoked were included in the analysis, but smoking status was not adjusted for in the presented analyses.

Schlaich et al. (1998)

These investigators compared 34 patients (6 men) with osteoporotic fractures and a similar number of patients with chronic low back pain for reasons other than osteoporosis.(8) Osteoporosis was defined as the presence of at least one compression fracture or deformity on spinal radiographs or by formal bone biopsy. They used recalled height at age 25 years for their PFT reference values; to evaluate kyphosis, they used rib–pelvis measurements, wall-occiput measurements, and thoracic circumference; vertebral fractures were defined by experienced radiologist interpretation.

When using height at age 25 years to generate reference values (but not when actual measured heights were used), they found a small but statistically significant decline in vital capacity and forced expiratory volume in 1 s (FEV1) in patients with osteoporosis-related vertebral fractures compared with those with chronic low back pain. They noted that the declines in pulmonary function were minimal, because patients with osteoporosis had vital capacity and FEV1 >80% predicted. In addition, they noted that reductions in the rib–pelvis distance were significantly (p < 0.05) associated with declines in vital capacity.

Whereas this is the only study presented to include men, there was no adjustment of matching for age or sex, and the referral source for patients was not specified. This was an unblinded study. There was a higher proportion of patients who smoked in the control group, but a stratified analysis of the distribution of %FEV1 and %FVC did not show statistically significant differences when accounting for smoking status (although actual data are not presented); a formal multivariable adjustment was not undertaken.

Lombardi et al. (2005)

The most recent study to address this issue(7) enrolled a total of 55 women and divided them into three groups: 15 with osteoporosis-related vertebral fractures, 20 with osteoporosis but without vertebral compression fractures, and 20 controls that had neither osteoporosis nor vertebral fractures. Osteoporosis was defined by World Health Organization criteria using bone mineral densitometry. Vertebral fractures (defined as a 20% or greater loss of vertebral body height) were documented using lateral spine radiographs, and kyphosis was radiographically determined by Cobb's angle. Measured height was used to generate reference values for PFT.

Lombardi et al. reported that women with osteoporosis-related vertebral fractures had lower absolute FVC and lower FEV1 values compared with women with osteoporosis alone or their controls (all reported comparisons, p < 0.05). There were, however, no statistically significant differences between the women with osteoporosis alone and control patients. They also found a negative correlation between kyphosis and percent predicted FEV1 when using measured height for reference values. When they examined kyphosis in more detail, their data suggested that a Cobb's angle of 55° or more caused significant impairments in pulmonary function, with declines in both absolute and percent predicted FEV1 and FVC. This degree of kyphosis is consistent with the data of Culham et al.(5) described above: their patients had a mean Cobb's angle of ∼58°.

Limitations of this study include that it was restricted to female patients from one hospital's specialty clinics, groups were not age-matched, and the sample size was small. However, this was the only study that had blinded ascertainment of outcomes and the only study to exclude patients who smoke.

DISCUSSION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgements
  8. REFERENCES
  9. APPENDIX 1:

In a systematic review of the literature, we found limited, but suggestive, evidence that osteoporosis-related kyphosis is associated with some impairment in pulmonary function. Reviewed studies suggest that a restrictive pattern in pulmonary function predominates and that this is directly related to the number of vertebral fractures present(4) and clinical measures of kyphosis.(5–7) This is not necessarily unexpected, because there is a strong relationship between the number of vertebral fractures and kyphosis(3) and height loss.(15) The relationship, in at least one study, between the number of vertebral fractures and decrements in vital capacity seems direct, graded, and linear.(4) It is also noteworthy that in the only study that was blinded and that excluded smokers,(7) kyphosis angle was negatively correlated with percent predicted FEV1. Declines in maximal forced expiratory flows were also observed in the women with osteoporotic fractures. Whereas both of these findings might suggest the possibility of obstructive deficits, as the authors themselves point out, none of the study groups actually met accepted criteria for the diagnosis of airflow obstruction, and they question whether the changes in forced expiratory flows were simply related to decreases in lung volumes—that is, the known interdependence between degrees of pulmonary restriction and some measures of airflow obstruction.(7) Last, only one study assessed and reported respiratory muscle strength,(4) and none of the studies included assessments of respiratory muscle endurance. Both these factors are thought by some to be associated with impairments in pulmonary function.(19)

Unfortunately, the available studies are all limited by the small numbers of patients included in general (only 109 studied since 1966), and the fact that only six men have apparently ever been studied. Small and limited sample sizes may reflect the fact that osteoporosis is still an under-recognized disease that remains undertreated even when it is recognized.(20,21) We caution readers in interpreting data presented herein because, although results seem consistent between all four included studies, the evidence is not necessarily robust nor high quality in terms of internal or external validity. Clearly there is a need for further study. Why? In addition to the potential for pulmonary and nonpulmonary morbidity,(1,5,7,20) there is mortality associated with osteoporosis-related kyphosis.(20,22–24) Women with radiographic evidence of vertebral fractures have an increased mortality rate and have been noted to have two to three times the likelihood of dying from pulmonary causes than women without vertebral fractures.(22) Furthermore, severe kyphosis is strongly predictive of pulmonary death.(22) It has been proposed that those with underlying lung disease and decreased respiratory reserves may not tolerate the further superimposed restrictive changes resulting from vertebral fractures.(4,22) Delay in recognizing ventilatory compromise, even of a modest degree, may lengthen the time before introducing interventions such as supplemental oxygen, noninvasive ventilation, and perioperative pulmonary care and may lead to a systematic underappreciation of the severity of respiratory tract infections. Severe cases of osteoporosis-related kyphosis are often recognized, but only late in the disease course, and earlier or more subtle cases may be missed altogether. Better understanding of the relationships between osteoporosis, kyphosis, and pulmonary function is thus of clinical importance.

Our review also serves to show some of the endemic problems facing investigators trying to study this difficult question. The lack of standardized techniques used for clinical assessment of kyphosis and PFT measurements between individual studies is problematic. This latter issue is best shown in the context of which “height” measure was used to generate reference values. Whereas a variety of alternatives were used in the studies we reviewed (measured height, recalled height, arm span), the use of arm span as a surrogate for height in special circumstances, such as clinically apparent kyphosis, has been strongly recommended in the past.(4,8) Teramato et al.,(8) for example, have gone so far as to suggest that arm span should be used in all older individuals with osteoporosis, irrespective of the presence of clinically apparent kyphosis.

For future researchers to advance the field, it might be useful to describe what we would consider to be the methodologically ideal approach. We believe that the ideal study would be a prospective, longitudinal, blinded outcomes ascertainment, inception cohort study that includes large numbers of nonsmoking men and women recruited from multiple referral sources and that collects detailed and standardized information at multiple points in time for at least 4–5 years. It should exclude patients with known lung disease and ideally those with any smoking history. The diagnosis of osteoporosis would need to include measures of BMD and information about osteoporosis-related risk factors and prior fracture history. Laboratory measures, at least at baseline, would include PTH and vitamin D levels and inflammatory markers. It would include assessment of multiple variables including clinical measurements for kyphosis and height, standard PFTs, and measures of respiratory muscle strength and endurance, and it would take into account sex, age, and ethnicity to allow for exploratory and multivariate analysis. Obviously, this ideal study is a major (although we think necessary and justifiable) undertaking. A feasible and pragmatic alternative, at the least, would be to collect the same data described above from a population-based cross-section of male and female patients (perhaps even nested within an established cohort study) with large enough numbers to permit adequate power to draw valid conclusions and either refute or confirm the studies included in our review.

Whereas the quality of, and the differences between, the studies included in our review may limit the strength of inference, our aim was to systematically increase awareness of the potential importance of the clinical association between impairments in pulmonary function and osteoporosis-related kyphosis. There is clearly a need for more research. Our review shows the pitfalls that future investigators need to avoid if they are to advance the field. In the meantime, our results suggest that busy physicians should consider paying more attention to the pulmonary status of patients with, or at risk for, osteoporosis-related fractures of the spine.

Acknowledgements

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgements
  8. REFERENCES
  9. APPENDIX 1:

We thank Janice Varney, MLIS, who helped us create and refine our search strategy. Without her generous efforts on our behalf, the study could not have been done with as much rigor or efficiency. We also thank Jeanette Buckingham, MLIS, for her supportive instruction and guidance at earlier stages of this work. Dr Majumdar receives salary support awards from the Alberta Heritage Foundation for Medical Research (Population Health Investigator) and the Canadian Institutes of Health Research (New Investigator).

REFERENCES

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgements
  8. REFERENCES
  9. APPENDIX 1:
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