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Follow-up of Occult Bone Lesions Detected at MR Imaging: Systematic Review¹

¹ From the Department of Radiology, Rijnmond-Zuid Medical Center, Rotterdam, the Netherlands (S.S.B., D.V.); and Departments of General Practice (S.S.B., B.W.K., S.M.A.B.), Radiology (M.G.M.H.), and Epidemiology and Biostatistics (M.G.M.H.), Erasmus Medical Center, Rotterdam, the Netherlands. Received January 14, 2005; revision requested March 16; revision received April 17; accepted June 1; final version accepted June 1. Address correspondence to S.S.B., Duistere Steeg 4, 8051 ZR Hattem, the Netherlands (e-mail: s.boks{at}erasmusmc.nl).

	ABSTRACT

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Purpose: To perform a systematic review of the literature regarding the natural course of posttraumatic occult bone lesions (often referred to as bone bruises) detected at magnetic resonance (MR) imaging.

Materials and Methods: A systematic review of the literature was performed by searching the MEDLINE database (from January 1966 to February 2003) with the keywords bone bruise, trauma, follow-up, and MRI. Keywords were linked by using the Boolean operator AND. Studies were included if all of the following criteria were fulfilled: patients sustained trauma, MR imaging was used as a diagnostic method, results of clinical or MR imaging follow-up were available, and study was written in English, Dutch, German, French, Spanish, Italian, Swedish, Danish, or Norwegian. The quality of each study was assessed by using a standardized criteria set, and statistics were estimated to rate the level of agreement between the two reviewers. Results were compared with regard to study design and quality scores.

Results: The MEDLINE search identified 266 articles, 13 of which met the inclusion criteria. The quality of the included studies was moderate. The two reviewers initially agreed on 179 quality items ( = 0.84). The study population was generally small, and follow-up periods ranged from 1 to 73 months. Four different classification systems were used, and in two studies bone bruise was not specified. Study results suggest a generally good clinical prognosis of bone bruises. Normalization of MR imaging appearance is possible and is most often encountered after the occurrence of reticular lesions. Cartilage loss at follow-up is often found in cases of initial cartilage damage (impaction or osteochondral fracture).

Conclusion: In general, a healing response was often encountered after sustained posttraumatic occult bone lesions. The initial MR imaging appearance appears to have prognostic value.

© RSNA, 2006

	INTRODUCTION

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Occult bone lesions (often referred to as bone bruises) are seen at magnetic resonance (MR) imaging as signal intensity abnormalities in the subchondral bone and bone marrow and represent a heterogeneous group of injuries. They are called occult because, at direct observation (ie, at arthroscopy), such lesions would be hidden from view by the overlying cartilage (which may appear normal) and because no abnormalities are seen at conventional radiography. There is little histologic evidence of such bone lesions; after trauma, they are presumably the result of microfracture of the medullar trabeculae (1,2). In histologic studies, researchers have found hemorrhage and edema in the region of the signal intensity abnormalities (3–5).

In the literature, different classification systems are used. Most authors use either the Mink and Deutsch classification system or the Vellet classification system. Mink and Deutsch (1) defined four categories of occult fractures at the knee: bone bruise, stress fracture, femoral and tibial fracture, and osteochondral fracture. Vellet et al (6) modified this classification system and defined five categories: reticular fracture, geographic fracture, linear fracture, impaction fracture, and osteochondral fracture.

Although bone bruises are often considered to be benign and self-limiting, this opinion seems to be primarily based on results from the earliest studies on this subject (1,2,7). Most of these studies, however, included nonconsecutive patients and had a nonstructural follow-up or concerned only case reports. In more recent studies, researchers have described osteochondral sequelae after a sustained bone bruise (6,8–11). Thus, the true natural history of a bone bruise remains unclear. We believed that it is important to gain insight into the natural course of bone bruises detected at MR imaging and their clinical consequences. Thus, the purpose of our study was to perform a systematic review of the literature regarding the natural course of posttraumatic occult bone lesions (often referred to as bone bruises) detected at MR imaging.

	MATERIALS AND METHODS

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Identification and Selection of the Literature
Relevant publications on the natural history of posttraumatic occult bone lesions were searched by using the MEDLINE database (from January 1966 to February 2003). The MEDLINE search was performed by two authors (S.S.B., S.M.A.B.). Bone bruise, trauma, follow-up, and MRI were used as keywords and were linked by using the Boolean operator AND. For each of the keywords, one or more synonyms were used (Appendix). The search was extended by screening the reference list of all relevant articles (S.S.B., S.M.A.B.).

A study was determined to be eligible for inclusion if it fulfilled all of the following criteria: (a) The study included patients who had sustained trauma, (b) MR imaging was used as a diagnostic method, (c) after the initial diagnosis, patients returned to the clinic for follow-up, and clinical data or MR imaging outcomes were noted, and (d) the article was written in English, Dutch, German, French, Spanish, Italian, Swedish, Danish, or Norwegian.

	QUALITY ASSESSMENT

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Because the variation in the internal validity of the studies may influence the results and conclusions of a systematic review, the quality of each included study was assessed by using the following procedure. Two reviewers (S.S.B., S.M.A.B.) independently scored the quality of the selected studies by using a set of criteria that were previously used in the field of musculoskeletal disorders; these criteria were then modified to cover the topic of our review (Fig 1). Items were given a binary score of 1 if a particular criterion was fulfilled, and items were given a binary score of 0 if a particular criterion was not fulfilled or if it was unclear whether the criterion was fulfilled. The final quality score of each study was based on the sum of the individual scores. In cases of disagreement, both reviewers discussed the scores to achieve consensus. A prospective cohort study was judged as the preferred study design.

View larger version (44K): [in this window] [in a new window] [Download PPT slide]   Figure 1: Set of criteria used by reviewers to assign quality scores for each of the included studies.

Data Extraction
We extracted the main characteristics of each study—that is, study center, inclusion criteria, study population, study design (ie, prospective or retrospective), study size, and follow-up period. Study results were also extracted, including the type of bone bruise classification system used, descriptions of MR imaging results at baseline and follow-up, the number of cases of persistent bone lesions and/or cartilage abnormalities at follow-up, descriptions of sustained knee surgery during follow-up period, patient complaints, and physical examination results at follow-up. Data extraction was performed in duplicate by two authors (S.S.B., S.M.A.B.).

Data Analysis
Study characteristics and quality scores were presented, and studies were ranked according to their quality score. A statistic was used to rate the level of agreement between the two reviewers on each quality item. The percentage of resolution of bone bruise was estimated for each study. The presence of osseous and cartilage abnormalities was compared according to the different bone bruise classification systems that were used in the separate studies.

When data were available, comparisons were made between initial lesions and clinical follow-up results, as well as between lesions seen at MR imaging follow-up and findings observed at clinical follow-up.

Because the observational studies in this review were considered to be heterogeneous with regard to follow-up, study population, and quality and outcome measures, we refrained from pooling the data.

Because of the scarcity of data, analyses of counts and proportions were used as the main statistic tools. The statistic was estimated by using a commercially available software program (SPSS, version 11.0.1; SPSS, Chicago, Ill).

	RESULTS

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Characteristics of Identified Studies
The primary literature search identified 266 references. On the basis of the title and abstract, 15 articles were read completely and, of these, 11 met our inclusion criteria. After screening the reference list of each article, two more studies were included (2,6,8–18). All included articles were published in English.

Regarding the characteristics and quality scores of the included studies (Table 1), six were retrospective and seven were prospective. The follow-up period of these 13 studies ranged from 1 to 73 months. All studies were hospital-based, and study populations were generally small. In nine studies, less than 30 patients were included. Two studies considered ankle sprains (16,18), whereas the other 11 studies considered bone bruise of the knee.

The quality of the included studies was moderate; eight studies scored 8 points or more of the 15 available quality points. The shortcomings generally involved a poor description of inclusion criteria for arthroscopy and/or arthrotomy, a small study size, and a high percentage of patients lost to follow-up (Table 1).

Initial and Follow-up MR Imaging
Four different classification systems were used (Appendix), and in two studies bone bruise was not specified (Table 2). Comparison of the study results was further hindered by differences in outcome measures; at follow-up, researchers considered the persistence of signal intensity abnormalities in the initial osseous lesions (2,9,11,12,15–17), osteochondral sequelae (6,8,9,11), or chondral sequelae only (10).

Researchers who investigated osteochondral sequelae found signal intensity abnormalities in both bone and cartilage in many patients during follow-up periods ranging from 6 to 73 months (Table 2) (6,8,9,11). The authors of these studies described the possibility of fibrosis, sclerosis, or fatty replacement of the bone marrow; cartilage thinning or defect; and cortical depression or osteochondral defect at follow-up imaging. In two studies, investigators used a more or less comparable classification system and found no apparent sequelae in case of initial reticular bone bruise distant from the subchondral bone plate (6,9). All cases of disrupted articular surfaces (osteochondral defects, cortical impactions [6], or type 3 lesions [9]) were associated with cartilage loss at follow-up in both studies (6,9). Vellet et al (6) found osteochondral sequelae in 14 of 18 cases of geographic fractures after 6–12 months. In the study by Costa-Paz et al (9), only one of 11 geographic lesions was still present after 24–64 months. Stein et al (11) found no correlation between the initial signal intensity type at MR imaging and findings at 24–73-month MR imaging follow-up. In the study by Faber et al (8), it was unclear if the osteochondral lesions at follow-up were preexistent or if they occurred as the result of an initial bone bruise, because different MR imaging sequences were used at baseline and at follow-up.

We found conflicting results on the prognostic value of the location of a bone bruise; in one study, sequelae were seen more often in lesions of the tibial plateau (11), whereas in another study no sequelae were found at this site (8).

By looking at chondral sequelae only, Lahm et al (10) found no cartilage abnormalities in the case of an initial bone bruise (defined as a geographic nonlinear area of abnormal subchondral signal intensity). Initial subchondral or osteochondral fractures, however, were associated with cartilage abnormalities at follow-up in more than 50% of patients after 5.5–41.0 months (10).

Clinical Follow-up
For nine studies, information was presented on the clinical follow-up of bone bruises (Table 3) (2,8–11,13,14,16,18). In only one high-quality study did the authors report on the clinical outcome of isolated bone bruises in the knee (13). These authors found a good short-term clinical outcome, all patients showed normal results at physical examination and had returned to their preinjury activity level within an average of 3.2 months after trauma, and 21 of 23 patients had unchanged activity levels and Lysholm scores of more than 90 points at follow-up.

In four other studies, comparisons were made between lesions detected at follow-up MR imaging and the results of clinical follow-up (8,9,11,16). In two studies, researchers found a generally good clinical outcome after anterior cruciate ligament repair and sustained occult osseous lesions (9,11). In one study, 19 of 21 patients had normal or near normal findings in the knee after 24–64 months of follow-up (9). In the other study, 19 of 20 patients were subjectively normal or improved, with 15 of 20 patients participating fully in athletics (11). In three studies, the authors described "no correlation" or "no significant difference" between follow-up MR imaging, follow-up physical examination results, and subjective complaints, without mentioning statistical data (8,9,11).

	DISCUSSION

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To our knowledge, our study is the first systematic review on the follow-up of occult osseous lesions detected at MR imaging. In general, bone bruises have a good outcome at both clinical examination and MR imaging. Various classification systems are used and appear to have prognostic value.

A potential drawback of the present review might be the literature search. Although we used a sensitive set of keywords, we might have missed some relevant studies. Also, because our search was limited to indexed journals, unpublished studies and nonindexed journals might have been missed. Finally, studies published in languages other than the nine we selected would have been missed.

Because the study outcomes described in each of the articles differed, the possible presence of publication bias could not be estimated by using a funnel plot. We believe, however, that in the field of descriptive studies, publication bias might not be strong. In the field of association studies, there might be a publication bias in that nonsignificant relationships may be published less often than are significant relationships. In our review, however, only three studies reported on relationships, and all of these relationships were nonsignificant. Furthermore, there are fewer conflicts of interest (apart from the researchers' own interest) in this field of research than there are in the field of intervention studies.

In addition, there are several issues to keep in mind when drawing conclusions from this review. A comparison of the results of individual studies is difficult because the included studies used different time intervals between trauma and initial MR imaging. Moreover, there were differences in follow-up periods, techniques used to detect bone lesions, classification systems, and treatment protocols. All of these factors might influence the presence and identification of bone or cartilage lesions (19,20). Most studies contained no information on the initial lesion size and provided no information on the relationship between concomitant lesions and bone bruise; both of these factors might have prognostic value. Despite all these potential problems, the results of the 13 included studies were generally consistent with regard to clinical outcome.

MR Imaging Follow-up
Bone bruises are often regarded as benign and self-limiting lesions, but this opinion is primarily based on findings from the earliest studies on this topic. In the current review, which explores all of the available evidence, we also found a natural healing of bone bruises, and a normalization of bone bruise signal intensity was seen in most cases. In the few patients with persistent bone bruise, lesion size had clearly decreased (2,11,12,15–17). Other lesions often occurred as a consequence of the initial bone bruise (6,8–11); in such cases, the typical bone bruise pattern (ie, low signal intensity on T1-weighted MR images and high signal intensity on T2-weighted fat-suppressed MR images) had disappeared, but some rest lesions (eg, fibrosis or fatty replacement of cancellous bone) often remained. The clinical meaning of these findings is, as yet, unclear.

The results of the studies included in our review suggest a good prognosis for reticular lesions but a loss of cartilage in all cases of initially disrupted articular surfaces. The reported prognosis of geographic lesions differed. For instance, Costa-Paz et al (9) found a better prognosis than Vellet et al (6), but this difference could be accounted for by the much longer follow-up period used by Costa-Paz et al during which further healing was possible.

Clinical Follow-up
Because bone bruises are presumably the result of a trabecular microfracture (3–5), one might assume that they cause pain even in the absence of other substantial soft-tissue injuries. For patients, however, it is not possible to discriminate between pain that is caused by bone bruises and pain that is caused by concomitant posttraumatic knee lesions (eg, meniscal or ligament tear). In only one study in this review did investigators report on the clinical follow-up of isolated bone bruises and describe a good short-term prognosis (13). Results of other studies also showed a generally good clinical prognosis.

In three studies, researchers described the influence of persistent signal abnormalities on subjective complaints and on physical examination results and found no significant relationship (8,9,11). The study populations, however, were small (20–23 patients), and only the total knee symptom scores were reported. An association between the presence of signal intensity abnormalities at follow-up and pain can, therefore, not be excluded. Further studies with a larger study population and clear symptom definition are necessary to clarify the relationship.

Authors of histopathologic studies have reported a profound effect of trauma on cartilage metabolism (8,10,14,21–23). The chondral surface could undergo chondrolysis and death that is proportionate to the impaction force and its distribution (6). This may lead to premature degeneration even in the absence of other substantial soft-tissue trauma. To prove this assumption, further studies with longer follow-up periods are needed. These studies should use a prospective study design, a clearly defined study population, and a structured follow-up that includes at least one physical and MR imaging examination.

In conclusion, there seems to be a healing response that occurs in most patients with posttraumatic occult bone lesions. The clinical prognosis is generally good. Normalization of MR imaging appearance is possible and is most often encountered after the occurrence of reticular lesions (ie, a serpiginous region of diminished T1-weighted signal intensity that is distant from the subchondral bone plate). Cartilage loss at follow-up is often found in cases of initial cartilage damage.

	APPENDIX

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For each of the keywords, one or more synonyms were used (Table A1). In the 13 articles that met our inclusion criteria, four different classification systems were used, and two authors used their own definitions of bone bruise (Fig A1).

View larger version (39K): [in this window] [in a new window] [Download PPT slide]   Figure A1: Definitions and descriptions of each of the classification systems used in the included studies. In two studies, authors supplied their own definitions of bone bruise.

	ADVANCES IN KNOWLEDGE

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS QUALITY ASSESSMENT RESULTS DISCUSSION APPENDIX ADVANCES IN KNOWLEDGE References

• Normalization of MR imaging appearance at follow-up was seen in most cases of initial bone bruise.
  
• Various classification systems are used to describe bone bruises and appear to have prognostic value.
  
• The results of the studies included in our review suggest a good prognosis for reticular lesions but a loss of cartilage in all cases of initially disrupted articular surfaces; the reported prognosis of geographic lesions differed.
  
• In only one study did the authors report on the clinical follow-up of isolated bone bruises and describe a good short-term prognosis.
  

	FOOTNOTES

 
Authors stated no financial relationship to disclose.

See also the other article by Boks et al in this issue.

Author contributions: Guarantor of integrity of entire study, S.S.B.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; approval of final version of submitted manuscript, all authors; literature research, all authors; statistical analysis, S.S.B.; and manuscript editing, all authors

	References

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