Abstract
Background
Bone bruising is commonly observed on magnetic resonance imaging (MRI) after non-contact anterior cruciate ligament (ACL) injury.
Objectives
The primary objective of this study was to determine if the location and prevalence of tibial and femoral bone bruises after ACL injury can be explained by specific injury mechanism(s). The secondary objective was to determine whether the bone bruise literature supports sex-specific injury mechanism(s). We hypothesized that most studies would report bone bruising in the lateral femoral condyle (LFC) and on the posterior lateral tibial plateau (LTP).
Methods
MEDLINE, PubMed, and SCOPUS were searched for studies that reported bone bruise prevalence and location in ACL-injured subjects. Sex differences in bone bruise patterns were assessed. Time from injury to imaging was assessed to account for confounding effects on bone bruise size and location.
Results
Thirty-eight studies met the inclusion/exclusion criteria. Anterior-posterior location of bone bruises within the tibiofemoral compartment was assessed in eleven studies. Only five of these studies reported bone bruise locations on both the tibia and the femur. The most common bone bruise combination in all five studies was on the LFC and the posterior LTP. Sex differences were only assessed in three studies, and only one reported significantly greater prevalence of LTP bruising in females.
Conclusion
Bone bruise patterns in the current literature support a valgus-driven ACL injury mechanism. However, more studies should report the specific locations of tibial and femoral bone bruises. There is insufficient evidence in the literature to determine whether there are sex-specific bone bruise patterns in ACL-injured subjects.
1. INTRODUCTION
Over the past few decades, male participation in U.S. high school sports has increased by about 3% (3.7 million to 3.8 million) while female participation has roughly doubled every 10 years (from 0.3 million to 2.8 million).[1] The large growth in sports participation has led to a drastic increase in anterior cruciate ligament (ACL) injuries suffered by male and female athletes. Female athletes who participate in pivoting and jumping sports suffer ACL injuries at a 4-to 6-fold greater rate than do male athletes participating in the same sports.[2–6] Previous research has identified sex-specific kinematics during ACL injury that closely resembles documented predictive factors for ACL injury risk in females. Specifically, Hewett et al.[2] reported that high knee abduction moments (KAM) that torque the knee in a valgus position and load the lateral compartment of the knee joint predict future risk for ACL injury and Krosshaug et al.[7] observed videos of female and male basketball players during ACL injury, and reported that females are at 5.3 times higher relative risk of valgus collapse during ACL injury compared to males. However, more research needs to be conducted on the subchondral bone effects formed by the external forces that rupture an ACL.
Magnetic resonance imaging (MRI) studies of acute ACL injury have reported bone bruises, contusions, or edema in the subchondral tibia and femur in greater than 80% of subjects with a complete ACL disruption.[8–13] During ACL injury, large external forces in combination with the patient’s ligament vulnerabilities during certain loading conditions cause a violent impact between the tibial and femoral articular cartilage that is transferred to the bone, and results in bone bruises. These bone bruises are seen on magnetic resonance imaging of the ACL-injured knee as hyperintense signals in the subchondral tibia and femur. The distribution of bone bruises in the knee may provide a footprint of the mechanism of ACL injury.
Quatman et al.[14] compared cartilage pressure distributions in finite element knee models of females that went on to suffer an ACL injury to females who did not suffer an ACL injury during their athletic seasons. Specifically, in vivo three-dimensional kinematics from the females who did not suffer an ACL injury, as well as female athletes who subsequently suffered ACL injury, were used as initial inputs to the model. High magnitude loading scenarios that resulted in injurious strain levels were also applied to the models. Each simulated multi-planar injury mechanism demonstrated cartilage pressure distributions in unique locations. Sanders et al.[15] compared the locations of bone bruises formed from five different ACL injury mechanisms and associated the non-contact valgus loading injury mechanism with bone bruises in the posterior lateral tibial plateau (LTP) and lateral femoral condyle (LFC). The precise location and prevalence of the subchondral bone defects can provide valuable insight into knee loading patterns that led to the ACL rupture. A thorough understanding of the tibiofemoral motions associated with ACL rupture may help clinicians and scientists develop ACL injury prevention programs aimed towards reducing these motions in healthy athletes.
The primary objective of this systematic review was to determine the common knee loading patterns that occur during ACL injury based on the prevalence and location of bone bruises in ACL-injured subjects. It was hypothesized that the majority of bone-bruise studies would report data that support the multi-planar, valgus loading mechanism of ACL injury consistent with bone bruising in the LFC and posterior aspect of the LTP. The secondary objective was to determine whether sex-specific differences in bone bruise location and prevalence exist in subjects with a torn ACL. It was hypothesized that females would have a higher prevalence of posterior LTP bone bruises than males.
2. METHODS
This systematic literature search was conducted using MEDLINE, PubMed, and SCOPUS. The following search terms were entered into both search engines: “(bone OR osseous) AND (bruise OR contusion OR lesion OR edema) AND (anterior cruciate ligament OR ACL).” Two reviewers performed the literature search independently. 663 MEDLINE, PubMed, and SCOPUS article abstracts and titles were reviewed based on the pre-determined inclusion/exclusion criteria. Figure 1 outlines the methods and inclusion/exclusion criteria used to determine the articles that would be used to answer the primary and secondary objectives. Articles were included in the analysis if they met the following criteria:
Involved greater than 10 human ACL-injured subjects.
Used MRI technology to analyze subjects’ bone bruises.
Reported bone bruise location in at least the lateral compartment or medial compartment and reported bone bruise prevalence.
English articles published before April 28, 2012.
Figure 1.
Flow diagram of article selection with inclusion/exclusion criteria. ACL = anterior cruciate ligament.
Excluded articles included those that involved:
Case reports and systematic reviews without empiric data.
Only reports of maximum tibial or femoral bone bruise locations and prevalence, without specifying a medial or lateral compartment.
ACL-injured cadaver models.
After reviewing the abstracts and titles, the articles that clearly met inclusion/exclusion criteria, or those that could not be explicitly excluded were evaluated for full content. Full-text articles whose cohorts were not exclusively ACL-injured subjects were included only if they contained a subset of ACL-injured patients and reported the prevalence and location of bone bruises in those subjects. Studies that analyzed subjects with combined ACL and medial collateral ligament (MCL) injuries were included as long as all other inclusion criteria were met. The references of all included articles were searched to ensure a thorough review. All included articles were then screened to determine whether they could be used to answer the secondary objective. Articles that explicitly reported the bone bruise prevalence and location in ACL-injured males and females were used to answer the secondary objective.
Two independent reviewers assessed the methodological quality and determined the levels of evidence for each study. First, articles were categorized as prognostic or diagnostic studies. Second, the methods of each diagnostic or prognostic article were evaluated based on the specific criteria reported in Spindler et al.[16] Articles that did not specify the patient base as “consecutive” or “non-consecutive” were assumed to be non-consecutive and ruled a level III study. A third reviewer was used to settle any discrepancies between the two primary reviewers.
All bone bruise prevalence and location data was obtained from each study. To answer the primary objective, the prevalence of lateral compartment bone bruising was compared to the prevalence of medial compartment bone bruising in ACL-injured subjects. The prevalence of subjects with different patterns of multiple bone bruises was also compared to each other. Common bone bruise patterns were identified to infer potential ACL injury mechanisms. To answer the secondary objective, we analyzed the sex-specific bone bruise data from the included articles to infer potential sex-specific bone bruise patterns and injury mechanisms. The methodologies used to report the bone bruise data in each study were also analyzed before answering each objective.
All included articles were required to analyze bone bruises on the MRIs of ACL-injured subjects. Since bone bruises have the propensity to resolve and intensify after varying periods of time, the average time between initial ACL injury and MRI collection was reported for each study’s subject cohort. The average MRI collection periods for all studies were then compared.
3. RESULTS
Figure 1 summarizes the results of the literature search. The initial literature search yielded a total of 663 articles. A total of 38 articles met all of the inclusion criteria for the primary objective. Three of the 38 articles met all of the inclusion criteria for the secondary objective. Table 1 summarizes the study designs, subject composition, and MRI collection periods for all 38 studies included in this review.
TABLE 1.
Summary of studies reporting bone bruise prevalence and location in subjects with knee injuries
| Author(s), year | Injured subject composition | Level of evidence | Average MRI collection period(s), within: |
|---|---|---|---|
| Van Dyck et al, 2012 | ACL: n=97 (62 M, 35 F) | Diagnostic, retrospective study (Level IV) |
N/S |
| Potter et al, 2012 | ACL: n=42 knees (18 M, 24 F) | Prognostic, cohort study (Level II) |
8 weeks |
| Stein et al, 2012 | ACL and OA: n=23 | Prognostic, retrospective study (Level II) |
N/S |
| Frobell et al, 2011 | ACL: n=61 | Prognostic, case series study (Level IV) |
4 weeks |
| Jelic et al, 2011 | ACL: n=27 | Prognostic, case series study (Level IV) |
4 weeks |
| Yoon et al, 2011 | ACL: n=81 (59 M, 22 F) | Diagnostic, retrospective study (Level IV) |
6 weeks |
| Quelard et al, 2010 | ACL: n=217 (139 M, 78 F) | Prognostic, prospective cohort study (Level III) |
N/S |
| Halinen et al, 2009 | ACL and MCL: n=44 (19 M, 29 F) | Diagnostic, prospective study (Level III) |
3 weeks |
| Bolbos et al, 2008 | ACL: n=16 (11 M, 5 F) CTL: n=15 (11 M, 4 F) |
Prognostic, case control study (Level III) |
8 weeks |
| Collins et al, 2008 | ACLR: n=48 patients (26 M, 22 F) | Diagnostic, retrospective study (Level III) |
N/S |
| Frobell et al, 2008 | ACL: n=121 (89 M, 32F) | Prognostic, RCT study (Level II) |
5 weeks |
| Hanypsiak et al, 2008 | ACL: n=54 (38 M, 16 F) | Prognostic, prospective cohort study (Level I) |
80 days |
| Hernandez-Molina et al, 2008 |
ACL: n=68 | Prognostic, prospective cohort (Level II) |
N/S |
| Li et al, 2008 | ACL: n=15 patients (23 M, 7 F) | Diagnostic study (Level III) | 8 weeks |
| Nishimori et al, 2008 | ACL: n=39 (25 M, 14 F) | Prognostic study (Level III) | 4 weeks |
| Viskontas et al, 2008 | ACL: n=100 (69 M, 31 F) C: n=14 (13 M, 1 F) NC: n=86 (56 M, 30 F) |
Prognostic, cohort study (Level II) |
6 weeks |
| Fayad et al, 2003 | ACL: n=84 (42 M, 42 F) | Prognostic study (Level III) | N/S |
| Chen et al, 2002 | ACL: n=32 | Prognostic study (Level III) | 6 weeks |
| Bretlau et al, 2002 | ACL: n=24 (33 M, 31 F) | Prognostic, prospective cohort (Level II) |
6 days |
| Costa-Paz et al, 2001 | ACL: n=21 (15 M, 6 F) | Prognostic, case series study (Level IV) |
8 weeks |
| Munshi et al, 2000 | ACL: n=20 | Diagnostic, prospective study (Level II) |
6 weeks |
| Kaplan et al, 1999 | ACL: n=25 (20 M, 5 F) | Prognostic, case series study (Level IV) |
4 weeks |
| Lee et al, 1999 | ACL: n=19 (5 M, 14 F) | Diagnostic, retrospective study (Level III) |
3 weeks |
| Dimond et al, 1998 | ACL: n=87 (50 M, 37 F) | Prognostic, retrospective comparative study (Level III) |
6 weeks |
| Snearly et al, 1996 | ACL: n=15 (10 M, 5 F) | Prognostic, retrospective study (Level IV) |
N/S |
| Speer et al, 1995 | ACL: n=42 (20 M, 22 F) | Prognostic, prospective study (Level IV) |
30 days |
| Stein et al, 1995 | ACL: n=20 (10 M, 10 F) | Prognostic, retrospective case series study (Level IV) |
23 days |
| Zeiss et al, 1995 | ACL: n=71(37 M, 34 F) | Prognostic, prospective study (Level III) |
4 weeks |
| McCauley et al, 1994 | ACL: n=39 (27 M, 12 F) CTL: n=29 (17 M, 12 F) |
Diagnostic, retrospective case-control (Level IV) |
N/S |
| Engebretsen et al, 1993 | ACL: n=18 (9 M, 9 F) | Diagnostic, case series study (Level IV) |
N/S |
| Graf et al, 1993 | ACL: n=98 | Prognostic, case series study (Level IV) |
n=51: <6 weeks n=24: > 6 weeks |
| Kaneko et al, 1993 | ACL: n=33 | Prognostic, retrospective study (Level IV) |
N/S |
| Nawata et al, 1993 | ACL: n=56 (26 M, 30 F) | Prognostic, retrospective case series study (Level IV) |
n=20: 1 month n=16: 1–12 months n=20: > 12 months |
| Spindler et al, 1993 | ACL: n=54 ( 38 M, 16 F) | Prognostic, prospective study (Level 1) |
3 months |
| Tung et al, 1993 | ACL: n=50 (31 M, 19 F) | Diagnostic, retrospective case-control study (Level III) |
n=30: < 9 weeks n=20: > 9 weeks |
| Speer et al, 1992 | ACL: n=54 (34 M, 20 F) | Prognostic, retrospective case series (Level IV) |
45 days |
| Rosen et al, 1991 | ACL: n=75 (57 M, 18 F) | Prognostic, retrospective study (Level IV) |
3 weeks |
| Mink et al, 1989 | ACL: n=25 | Retrospective case series (Level IV) |
2 weeks |
ACL, anterior cruciate ligament; MRI, magnetic resonance imaging; M, males; F, females; N/S, not specified; OA, osteoarthritic patients; MCL, medial collateral ligament; CTL, control; ACLR, anterior cruciate ligament reconstruction; RCT, randomized controlled trial; C, contact anterior cruciate ligament injuries; NC, non-contact anterior cruciate ligament injuries
3.1 Primary objective. Prevalence and Location of Tibial and Femoral Bone Bruises Formed during ACL Injury
The primary objective of the literature review was to analyze the prevalence and location of tibial and/or femoral bone bruises formed during ACL injury and associated loading patterns leading to the formation of those bone bruises. Four studies reported a statistically significantly higher percentage of bone bruises in the lateral compartment compared to the medial compartment.[12, 17–19] All but one study reported a higher number of ACL-injured patients with bone bruises on the LFC or the LTP than on the medial femoral condyle (MFC) or medial tibial plateau (MTP).[20] Table 2 summarizes the bone bruise prevalence and location in all but three studies that reported bone bruise prevalence in specifically the lateral and/or medial compartments of the tibia and femur.[21–23] The three studies were not included in Table 2 because they only reported bone bruise prevalence within the anterior, posterior, and/or middle aspects of the lateral and medial compartments of the tibia and femur. The studies were included in Table 3 and their bone bruise data was compared to other studies that also analyzed bone bruise prevalence within the specific anterior, middle, and/or posterior aspects of the lateral and medial compartments.
TABLE 2.
Summary of reported prevalence of lateral and medial compartment bone bruises in the tibia and femur of ACL-injured subjects
| # of subjects with BB noted in each location |
||||
|---|---|---|---|---|
| Author(s), year of publication |
# of subjects with BB |
Tibia | Femur | Other: compartment or multiple BBs |
| Van Dyck et al, 2012 | 42 | 40, LC | ||
| Potter et al, 2012 | 42 knees | 36, L | 30, L | |
| Stein et al, 2012 | 23a | 10, L | 11, Lb | |
| 17, M | 13, M | |||
| Frobell et al, 2011 | 58 | 58, L | 47, L | |
| Jelic et al, 2011 | 27a | 6, L | 5, L | 4, LF+LT |
| 4, M | 2, MF+MT | |||
| Yoon et al, 2011 | 68 | 59, L | 55, L | 32, LC |
| 21, M | 19, M | 35, LF+LT | ||
| Quelard et al, 2010 | 156 | 52, L | 156, LC | |
| 104, LF+LT | ||||
| Bolbos et al, 2008 | 16 | 13, L | 9, L | 7, LF+ LT |
| Collins et al, 2008 | 33a | 11, LC | ||
| Frobell et al, 2008 | 119 | 117, LC | ||
| Hanypsiak et al, 2008 | 43 | 29, L | 37, L | |
| 9, M | 3, M | |||
| Hernandez-Molina et al, 2008 | 59 | 8, LC | ||
| Li et al, 2008 | 15a | 6, L | 2, L | 6, LF+ LT |
| 4, M | ||||
| Nishimori et al, 2008 | 35 | 35, LC | ||
| Viskontas et al, 2008c,d | 100a | NC: 98%; C: 80%, L | NC: 78%; C: 83%, L | |
| NC: 62%; C: 38%, | NC: 38%; C: 30%, | |||
| M | M | |||
| Fayad et al, 2003 | 84a | 50, L | ||
| 4, M | ||||
| Chen et al, 2002 | 20 | 15, LC | ||
| 9, MC | ||||
| Bretlau et al, 2002 | 15 | 12, L | 8, L | |
| 8, M | 5, M | |||
| Costa-Paz et al, 2001 | 21 | 11, L | 16, L | |
| Munshi et al, 2000 | 14 | 14, LC | ||
| Kaplan et al, 1999e | 25 | 25, M | 5, M | 24, LC |
| Dimond et al, 1998 | 41 | 4, MF+MT | ||
| Snearly et al, 1996 | 13 | 13, LC | ||
| Speer et al, 1995 | 42a | 34, L | 17, L | |
| 12, M | 4, M | |||
| Stein et al, 1995 | 20 | 3, M | 13, L | |
| Zeiss et al, 1995 | 26 | 21, L | ||
| 4, M | ||||
| Engebretsen et al, 1993 | 15 | 12, L | 13, L | 10, LT+ LF |
| Graf et al, 1993c | 47 | 30, L | 38, L | |
| Kaneko et al, 1993c | 21 | 4, L | 15, L | |
| 4, M | 2, M | |||
| Nawata et al, 1993 | 20 | 17, L | 19, L | 15, LT+ LF |
| Spindler et al, 1993c | 43 | 29, L | 37, L | |
| 9, M | 3, M | |||
| Tung et al, 1993 | 22 | 2, M | 20, LC | |
| 5, LF+MF | ||||
| Speer et al, 1992 | 45 | 45, L | ||
| Rosen et al, 1991 | 64 | 31, L | 32, L | 5, LC |
| 16, M | 4, M | 18, MC | ||
| Mink et al, 1989 | 18 | 18, LC | ||
ACL, anterior cruciate ligament; MRI, magnetic resonance imaging; M, males; F, females; N/S, not specified; OA, osteoarthritic patients; MCL, medial collateral ligament; CTL, control; ACLR, anterior cruciate ligament reconstruction; RCT, randomized controlled trial; C, contact anterior cruciate ligament injuries; NC, non-contact anterior cruciate ligament injuries; MTP, medial tibial plateau; LTP, lateral tibial plateau
Assumed all ACL-injured subjects incurred at least one bone bruise
p<0.0025; Larger bone marrow lesions in lateral femur
p<0.03; significantly more bone bruise subjects with lateral compartment than medial compartment bone bruises
p=0.045; significantly more non-contact injury subjects with bone bruises in MTP and LTP than contact injury subjects p=0.019; significantly more LTP bone bruises in the non-contact group than in the contact group
Study conducted to identify contusions of the posterior lip of the medial tibial plateau
TABLE 3.
Summary of reported bone bruise prevalence in the anterior, posterior, and middle aspects of the lateral and medial compartments of the tibia and femur in ACL-injured subjects
| # of subjects with BB noted in each location (% of BB participants)a |
|||
|---|---|---|---|
| Author(s), year of publication |
Tibia | Femur | Other: compartment or multiple BBs |
| Yoon et al, 2011 | 59 (87%), PL | 41 (60%), ML | |
| 19, PM | 15, MM | ||
| 13, AL | |||
| 4, AM | |||
| Halinen et al, 2008b | 8, PLc | 3, AL | 25 (64%), posterior LT + anterior LF |
| 3, anterior LF + posterior LT + posterior | |||
| MT | |||
| Viskontas et al, 2008 | NC: 85%, PL | NC: 70%, ML | |
| NC: 60%, PM | NC: 22%, MM | ||
| C: 65%, PL | NC: 30%, AL | ||
| C: 30%, PM | NC: 7%, AM | ||
| C: 65%, ML | |||
| C: 10%, MM | |||
| C: 32%, AL | |||
| Fayad et al, 2003 | 62 (74%), PLd | ||
| 35, PM | |||
| Lee et al, 1999e | 2, PL | 11 (85%), posterior LT + posterior LF | |
| Dimond et al, 1998 | 13, PL | 17 (41%), posterior LT + middle LF | |
| 7, middle LF + middle MF | |||
| Speer et al, 1995 | 27 (64%), PL | 15, ML | |
| 12, PM | 4, PM | ||
| 2, PL | |||
| Stein et al, 1995 | 20 (100%), PL | ||
| Zeiss et al, 1995 | 20 (77%), PL | 15 (58%), posterior LT + LF | |
| McCauley et al, 1994f | 18 (46%), PL | ||
| Graf et al, 1993 | 27 (57%), PL | 32 (68%), ML | |
| 4, ML | 5, AL | ||
| Tung et al, 1993 | 7, PL | 8 (36%), posterior LT + middle LF | |
ACL, anterior cruciate ligament; BB, bone bruise; PL, posterior lateral; PM, posterior medial; MM, middle medial; AL, anterior lateral; ML, middle lateral; AM, anterior medial; LT, lateral tibia; LF, lateral femur; MT, medial tibia; MRI, magnetic resonance imaging
Percentages reflect proportion of the population of ACL-injured subjects with bone bruises, not the total population
Reported 39/44 (88.6%) of subjects with at least one bone bruise on MRI
Subjects with isolated bone bruise
p<0.05; significantly more bone bruise subjects with posterior lateral tibial plateau bone bruises
Reported 13/19 (68.4% of subjects with at least one bone bruise on MRI
Assumed all ACL-injured subjects incurred at least one bone bruise
Table 3 lists 12 studies that reported bone bruise prevalence in the posterior, anterior, and/or middle sections of the lateral and medial aspects of the tibia and femur. Nine of 12 studies reported greater than 50% of their subjects with at least a posterior LTP bone bruise.[11, 17, 19, 21–22, 24–27] Fayad et al.[24] reported a significantly higher percentage of subjects with a posterior LTP bone bruise than subjects without a posterior LTP bone bruise (p<0.05). Six studies in Table 3 reported the number of subjects that expressed at least a middle LFC bone bruise on MRI.[11, 17, 19, 26, 28–29] All six studies reported a greater number of subjects with at least a middle LFC bone bruise than subjects with at least an anterior LFC or posterior LFC bone bruise.
Five studies in Table 3 reported the prevalence of ACL-injured subjects with at least two bone bruises in various locations.[21–22, 27–29] Three of the five studies reported a higher percentage of their subjects with an LFC and posterior LTP bone bruise pattern over any other multiple bone bruise pattern.[21–22, 28] Halinen et al.[21] reported 64% of their bone bruise subjects with both a posterior LTP and an anterior LFC bone bruise. Lee et al.[22] reported 85% of their subjects with both an LFC and a posterior LTP bone bruise. Dimond et al.[28] reported a higher percentage of subjects with both a posterior LTP and a middle LFC bone bruise than subjects with both a middle LFC and an MFC bone bruise.
Fayad et al.[24] categorized subjects into different ACL injury mechanism groups based on the locations of their bone bruises on MRI. Injury mechanism groups included the pivot-shift1 flexion and extension, hyperextension valgus2 and hyperextension-varus3 mechanisms. Approximately 63% of all 88 subjects demonstrated either a pivot-shift flexion or pivot-shift extension mechanism of injury based on their locations of bone bruises on MRI. The pivot-shift flexion mechanism was associated with posterior LTP and posterior LFC bone bruises. The pivot-shift extension mechanism was associated with posterior LTP and anterior LFC bone bruises. While both pivot-shift mechanisms lead to the formation of an LFC and posterior LTP bone bruise, the specific location of the LFC bone bruise was associated with the subject’s degree of flexion during the ACL injury.
Two studies addressed the possible relationship between the presence of medial compartment bone bruises and loading patterns during an ACL injury.[9, 19] Both studies differed in the way they classified an increased prevalence of medial compartment bone bruises in terms of a specific mechanism of injury. Viskontas et al.[19] compared bone bruise prevalence and loading patterns during an ACL injury rupture between subjects that incurred a contact ACL injury and subjects that incurred a non-contact ACL injury. The study reported a significantly greater proportion of non-contact injury subjects (81%) with grade III bone bruise intensity compared to contact injury subjects (36%) (p<0.001). Non-contact injury subjects experienced significantly more MTP bone bruises than the contact injury group (p=0.045). This increased prevalence of medial compartment bone bruises was associated with sagittal plane loading or anterior tibial translation over valgus loading in non-contact subjects. Kaplan et al.[9] also analyzed contusions at the posterior lip of the medial tibial plateau. However, the medial compartment bone bruises were instead associated with a contrecoup4 or compensatory varus alignment mechanism of injury.
3.2 Secondary Objective. Sex-Specific Differences in Bone Bruise Prevalence and Location
The secondary objective of this literature review was to determine whether sex-specific differences exist in bone bruise location and prevalence in ACL-injured subjects. Three articles met the inclusion criteria for the secondary objective.[24, 26, 30] All three studies reported their subjects’ bone bruise prevalence and location data differently. Engebretsen et al.[30] only classified their sex-specific bone bruise prevalence and location according to medial and lateral compartment, regardless of whether they were on the tibia or the femur. Yoon et al.[26] reported their sex-specific bone bruise data in terms of the compartment and bone (tibia or femur). Fayad et al.[24] reported the prevalence of bone bruises in the anterior, posterior, and middle aspects of the lateral and medial compartments of the tibia in males and females. These discrepancies limited the extent to which the data of all three studies could be combined and meta-analyzed.
Data from Yoon et al.[26] and Engebretsen et al.[30] were combined and analyzed to determine sex-specific differences in the prevalence of bone bruise patients with at least one bone bruise in each of the medial or lateral compartments only(Table 4). Fayad et al.[24] was not included because it only reported the number of isolated bone bruises in the lateral tibia, lateral femur, medial tibia, and medial femur. The study did not report the prevalence of bone bruise patients with multiple bone bruises in the lateral or medial compartment. Therefore, Fayad et al.[24] did not report the necessary multiple bone bruise data to determine the prevalence of bone bruise patients with at least one bone bruise in each of the compartments only. In Table 4, 100% of the male and female bone bruise subjects demonstrated at least one bone bruise in the lateral compartment5 on MRI. Forty-nine percent of male patients with bone bruises exhibited at least one medial compartment bone bruise compared to 41% of females.
Table 4.
Prevalence of lateral and medial compartment bone bruises in ACL-injured males vs. ACL-injured females
| # of subjects with at least one BB noted in each location (% of male or female BB participants) |
|||||
|---|---|---|---|---|---|
| Lateral compartment |
Medial compartment |
||||
| Author(s), year of publication |
# of males and females with BB |
M | F | M | F |
| Engebretsen et al, 1993 | M: 7 F: 8 |
7 | 8 | 1 | 2 |
| Yoon et al, 2011 | M: 48 F: 19 |
48 | 19 | 26 | 9 |
| Total | M: 55 F: 27 |
55(100%) | 27(100%) | 27(49%) | 11(41%) |
ACL, anterior cruciate ligament; BB, bone bruise; M, males; F, females
Data from Fayad et al.[24] and Engebretsen et al.[30] were analyzed to determine sex-specific differences in the prevalence of bone bruise patients with bone bruises in the lateral tibia, lateral femur, medial tibia, and medial femur (Table 5). Yoon et al.[26] was not included because it did not specify whether the compartment bone bruises were located on the tibia or femur. The greatest sex-specific differences in the prevalence of bone bruises were reported in the lateral tibia and medial tibia. The combined data reports a higher percentage of females (85%) with lateral tibial bone bruises compared to males (65%). In addition, 44% of females demonstrated medial tibial bone bruises compared to 29% of males that demonstrated medial tibial bone bruises.
Table 5.
Prevalence of bone bruises in the lateral and medial compartments of the tibia and femur in ACL-injured males vs ACL-injured females
| # of subjects with BB noted in each location (% of male or female BB participants) |
|||||
|---|---|---|---|---|---|
| Lateral compartment |
Medial compartment |
||||
| Author(s), year of publication |
# of males and females with BB |
Tibia | Femur | Tibia | Femur |
| Engebretsen et al, 1993 |
M: 7 F: 8 |
M: 6 F: 6 |
M:7 F: 6 |
M: 0 F: 1 |
M: 1 F: 1 |
| Fayad et al, 2003 | M: 42 F: 42 |
M: 26 F: 36 |
M: 24 F: 26 |
M: 14 F: 21 |
M: 0 F: 4 |
| Total | M: 49 F: 50 |
M : 32 (65%) F: 42 (84%) |
M : 31 F: 32 |
M : 14 ( 29%) F: 22 (44%) |
M : 1 F: 5 |
ACL, anterior cruciate ligament; BB, bone bruise; M, males; F, females
Only data from Fayad et al.[24] was analyzed to determine sex-specific differences in the prevalence of anterior, posterior, and/or middle bone bruises within the lateral compartment of the tibia. The study only reported the prevalence of bone bruises in the lateral and/or medial compartment of the femur. A significantly higher percentage of female subjects exhibited posterior LTP bone bruises compared to males at 86% and 62%, respectively (p<0.05).
3.3 MRI Collection Period
The average time between initial injury and MRI collection for each study’s subject cohort is reported in Table 1. Since bone bruises have the potential to resolve and intensify after varying periods of time, the average MRI collection period for each study were compared to determine the variability of MRI collection periods between studies included in this review. Ten out of 38 studies did not specify the average amount of time it took their subjects to receive an MRI after incurring their initial ACL injury.[18, 20, 23–24, 30–35] Initial MRI collection periods ranged from six days to nine weeks in all included studies.[29, 36] From the studies that did report the average MRI collection period of their subjects, Graf et al.[17] found that bone bruises in their ACL-injured patients resolved approximately six weeks after initial ACL injury. Tung et al.[29] reported that their subjects that demonstrated bone bruises on MRI received MRIs at a mean of 4.3 weeks after initial injury.
4. DISCUSSION
Bone bruises are frequently associated with ACL injuries. Their formation results from the high-pressure collision between the patients’ tibia and femur during an ACL rupture. The location of bone bruises within specific compartments of the tibia and femur can provide evidence about the potential injury mechanism(s). The location and prevalence of bone bruises may be able to provide valuable insight into sex-specific differences in injury mechanisms that could explain the increasing rate of ACL injuries incurred by females.
4.1 Bone Bruise Prevalence and Location and ACL Injury Mechanism
The LFC and posterior LTP bone bruise pattern is most commonly associated with the pivot-shift or multi-planar valgus loading injury mechanism.[15, 37] Nine studies in this review reported greater than 50% of their subjects with posterior LTP bone bruises. [11, 17, 19, 21–22, 24–27] All five studies that reported the number of subjects with at least two bone bruises in the posterior, middle, and/or anterior sections of the lateral and medial compartments of the tibia and femur reported a higher percentage of subjects with LFC and posterior LTP bone bruises than any other bone bruise pattern.[21–22, 27–29] Therefore, the subjects in these studies most commonly demonstrated two bone bruises in their LFC and posterior LTP on MRI. Since the multi-planar valgus loading mechanism is most commonly associated with bone bruises in the LFC and posterior LTP, the results of this review support the hypothesis that the multi-planar valgus loading ACL injury mechanism occurs more frequently than hyperextension valgus or varus mechanisms.[15]
Six studies reported a greater number of subjects with at least a middle LFC bone bruise than subjects with at least an anterior LFC or posterior LFC bone bruise.[11, 17, 19, 26, 28–29] However, subjects with multiple bone bruises did not express an anterior, posterior, or middle LFC bone bruise more frequently over another. Halinen et al.[21] reported 64% of their subjects with posterior LTP and anterior LFC bone bruises, while Dimond et al.[28] reported 41% of their subjects with posterior LTP and middle LFC bone bruises. The wide distribution of LFC bone bruises in the anterior, posterior, and middle sections of subjects with multiple bone bruises may be attributable to varied degrees of flexion during injury.[27]
Only five of the 38 studies reported the number of subjects that demonstrated multiple bone bruises in at least the anterior, posterior, and/or middle compartments of the tibia and femur on MRI. [21–22, 27–29] To gain valuable insight into the external forces causing an ACL to rupture, future studies should focus on identifying the relative locations of multiple bone bruises formed within precise locations of the LFC and LTP. Reporting only bone bruises formed in the lateral compartment or not reporting the relative anterior and posterior locations of multiple bone bruises may lead to the misclassification of loading patterns associated with the ACL rupture. The misclassification of loading patterns may be due to slight differences in their bone bruise patterns that can only be identified by analyzing differences in bone bruise prevalence within anterior, posterior, and middle compartments of the tibia and femur.
Quatman et al.[14] analyzed the cartilage pressure distributions of differing injury mechanisms in finite element knee models. The mechanism of injury that produced cartilage pressure distributions similar to those reported in acutely ACL-injured subjects involved both abduction and anterior tibial translation. Other mechanisms, such as the combined internal tibial rotation/anterior tibial translation mechanism, were also reported to cause cartilage pressure distributions in the same locations as those reported in the combined abduction/anterior tibial translation mechanism. However, the combined internal tibial rotation/anterior tibial translation mechanism demonstrated additional cartilage pressure distributions in the medial compartment. Reporting of both medial compartment cartilage pressure distributions and the precise locations of pressure distributions within the lateral compartment allowed for the determination of the combined abduction/anterior tibial translation mechanism from the internal tibial rotation/anterior tibial translation mechanism. This distinction between injury mechanisms can help specify the exact loading patterns and tibiofemoral motions that cause an ACL to rupture that can aid in the development of effective ACL injury prevention programs.
The presence or absence of medial compartment bone bruises associated with ACL injury is often not reported in the literature. This may be due to the low prevalence or lower intensity compared to lateral compartment bone bruises. Kaplan et al.[9] and Viskontas et al.[19] both discussed the importance of analysis of medial compartment bone bruises in ACL-injured subjects but explained the presence of medial compartment bone bruises with different loading patterns. Kaplan et al.[9] attributed the presence of medial compartment bone bruises to a contrecoup injury mechanism, while Viskontas et al.[19] attributed them to sagittal plane loading or anterior tibial translation mechanism. Viskontas et al.[19] associated the medial compartment bone bruises with sagittal plane loading instead of valgus loading that results in concomitant collisions between the medial and lateral compartments of the tibia and femur as the tibia undergoes anterior subluxation relative to the femur. Therefore, the current literature has not established whether medial compartment bone bruise patterns are associated with a particular loading mechanism during ACL injury. Future studies should report the prevalence of medial compartment bone bruises and analyze potential loading patterns that result in the distributive locations of these bone bruises.
Three studies in this review reported the prevalence of at least grade I bone bruises or lesions on the MRIs of ACL-injured subjects.[8, 19, 34] Hernandez-Molina et al.[34] reported that 51% of bone marrow lesions in the lateral and medial tibiofemoral joint compartments were either grade II or grade III. Speer et al.[8] reported three grade I, eight grade II, and three grade III lesions in 14 of their patients who also experienced concomitant MCL sprains. Because of the limited amount of data reporting bone bruise intensity, the grading of bone bruises was not analyzed in this review. However, the grading of bone bruises may help distinguish between various injury mechanisms in future studies. The differences between the two medial compartment mechanisms could be settled by reporting the percentage of grade III or high-intensity bone bruises in future studies. Medial compartment bone bruises with grade III intensity may be associated with sagittal plane loading since the medial compartment is involved with the initial/ highest energy tibiofemoral collision after the ACL rupture. Viskontas et al.[19] associated the increased prevalence of medial compartment bone bruises in non-contact ACL injury subjects with sagittal plane loading or anterior tibial translation over valgus loading. Non-contact injury subjects were also reported to have a significantly greater proportion of grade III bone bruises compared to contact injury subjects (p<0.001). The contrecoup mechanism may be associated with lower-intensity bone bruises, since it involves a lower-energy medial compartment collision after the initial collision between the lateral compartments.
Differences in bone bruise prevalence and location may exist between subjects that suffered from a non-contact ACL injury and subjects that suffered from a contact ACL injury. Only four studies included in the review separated the number of subjects in their cohorts into subjects that incurred non-contact ACL injuries from those that suffered contact ACL injuries.10, 27, 36, 41 Viskontas et al.[19] reported that non-contact ACL injury subjects demonstrated a significantly higher prevalence of MTP and LTP bone bruises than subjects that suffered from contact ACL injuries (p=0.045). This may indicate that non-contact ACL injuries occur from different loading patterns than contact ACL injuries. Future studies should separate and compare the prevalence and location of bone bruises in contact ACL injuries from non-contact ACL injuries to prevent the possibility of producing misleading results. These analyses will provide valuable insight into potential loading patterns that cause non-contact ACL injuries which compose 70% of total ACL injuries.[38]
4.2 Sex-Specific Differences in Bone Bruise Prevalence and Location
In a study conducted by Hewett et al.[2], it was reported that the incidence of serious knee injury was approximately six-fold higher in female soccer players than male soccer players. Observational studies have reported that female basketball players demonstrate 5.3 times higher relative risk of valgus collapse during ACL injury compared to male basketball players.[7] This increased relative risk has been associated with the increased rate of ACL injury occurrence in female athletes compared to male athletes. Comparing the bone bruise prevalence and location in ACL-injured males and females could provide more insight into sex-specific mechanisms that increase the rate of ACL injuries in females.
Only three studies in this review directly compared the prevalence and location of bone bruises between ACL-injured males and females.[24, 26, 30] Fayad et al.[24] and Engebretsen et al.[30] reported the prevalence of bone bruises within the lateral and medial compartments of the tibia and femur. After combining the data from these two studies, it was found that a higher percentage of females demonstrated lateral tibial (65% vs 44%) and medial tibial (44% vs 29%) plateau bone bruises compared to males.
Bone bruise studies classify ACL injury mechanisms by the location of bone bruises within the anterior, posterior, and/or middle aspects within each lateral and medial compartment of the tibia and femur.[15, 24, 37] Only Fayad et al.[24] reported the prevalence of sex-specific bone bruises in these specific locations and was used to determine whether sex-specific differences in ACL injury mechanisms exist. The study reported a significantly higher percentage of ACL-injured female subjects with posterior LTP bone bruises than ACL-injured males with posterior LTP bone bruises (p<0.05). Posterior LTP bone bruises are most commonly associated with the multi-planar valgus loading mechanism of ACL injury.
Despite the sex-specific differences in tibial plateau bone bruises, it was concluded that there is insufficient published data to determine whether sex-specific differences in bone bruise prevalence and location and ACL injury mechanisms exist. Assuming a moderate effect size of 0.5 to represent a clinically significant effect of sex on LTP or posterior LTP bone bruise prevalence, equal samples of 64 males and 64 females would be required to detect statistical significance with 80% power for an alpha level of 0.05. Since the bone bruise literature reports the prevalence of sex-specific LTP bone bruises in only 49 males and 50 females, there is insufficient data to determine whether sex-specific differences in bone bruise prevalence within the medial and lateral compartments of the tibia and femur exists (Table 5).[24, 30] Similarly, since the bone bruise literature reports the prevalence of sex-specific posterior LTP bone bruises in only 42 males and 42 females, there are also insufficient data to determine whether sex-specific differences in ACL injury mechanisms exist.[24]
Future studies should, at minimum, classify the prevalence of lateral tibial, medial tibial, lateral femoral, and medial femoral bone bruises in males and females. In bone bruise studies, injury mechanisms differ by the specific posterior, middle, and/or anterior locations of bone bruises within each lateral and medial compartment. Therefore, the literature would benefit substantially from a focus on reporting sex-based differences in the prevalence of bone bruises on the posterior LTP by gaining more insight into sex-specific differences in ACL injury mechanisms. If future studies report significant sex-based differences in the prevalence of bone bruises on the posterior LTP, then this finding would likely support a valgus collapse mechanism specific to that sex. Although previous observational studies identified the valgus collapse mechanism as a validated risk factor in women, there has not been a specific ACL injury mechanism identified in males. If future studies do not report significant sex-based differences, but report both sexes with a significantly higher prevalence of bone bruises in the posterolateral tibial plateau and lateral femoral condyle, then this finding may provide insight into potential injury mechanisms in the male population. The documentation of grade III bone bruises in future studies may also provide insight into potential sex-specific differences in injury mechanisms.
4.3 MRI Collection Period
Bone bruises evolve over time from the acute injury time and intensify or resolve after varying periods of time. Significant time differences between time of injury and date of MRI collection could potentially lead to inaccurate comparisons of bone bruise prevalence and location among studies. Reported MRI collection periods ranged from six days to nine weeks. Graf et al.[17] reported that their subjects only expressed bone bruises when MRIs were collected within six weeks post-ACL injury. Tung et al.[29] reported an average MRI collection period of 4.3 weeks for all subjects that demonstrated at least one bone bruise on their MRI. Therefore, future studies should include subjects that received MRIs within four to six weeks of the initial ACL injury. The short collection period will decrease the probability that bone bruises formed during ACL injury will resolve by the time an MRI is collected. In addition, this will ensure more accurate comparisons of bone bruise prevalence and location among studies. Such a comparison is important to be able to make conclusions regarding common loading patterns associated with ACL-injured subjects.
4.4 Limitations to Review
While the current study is a thorough and complete review of the literature regarding bone bruise and ACL injury, there are some limitations to the information. One limitation inherent to the primary objective was the problem of population heterogeneity among the included studies. While all studies reported bone bruise data for ACL-injured subjects, several studies also included subjects who suffered concomitant ipsilateral MCL injury. Therefore, we are limited in our ability to determine whether the bone bruises in some studies were formed as a result of isolated ACL injury, or if concomitant MCL injury was also a potential contributor to the injury pattern.
There are also limitations to our ability to answer the secondary objective. The limited sex-specific bone bruise data and differing methods for reporting bone bruise prevalence and location prevented definitive conclusion regarding the sex-specific differences in bone bruise prevalence, location and likely ACL injury mechanism. More data are needed to detect sex-specific differences in the prevalence of posterior LTP bone bruises that may provide insight into sex-specific injury mechanisms. Only data for 42 males and 42 females was available to answer the question about injury mechanism.[24] Therefore, the lack of sex-specific data limited our ability to determine whether sex-specific differences in bone bruise prevalence and location exist.
5. CONCLUSION
The current literature provides strong evidence that ACL-injured subjects express an increased prevalence of lateral compartment bone bruises, more specifically in the posterior aspect of the LTP and lateral compartment of the femur. Therefore, the bone bruise literature supports a pivot-shift injury mechanism or multi-planar loading mechanism involving valgus loading and subsequent anterior tibial translation. The literature does not provide sufficient data to determine whether sex-specific differences in bone bruise prevalence and location exist in ACL-injured subjects. Future studies should focus on comparison of bone bruise prevalence and location between males and females to further examine whether sex-specific loading patterns exist during ACL injury.
Analyses of medial compartment bone bruises may provide valuable insight into loading patterns during ACL injury and their relative locations to lateral compartment bone bruises should be reported in future studies. The prevalence of multiple bone bruise patterns found in the posterior, anterior, and/or middle aspects of the lateral and medial compartments of a subject’s tibia and femur should be reported to obtain specific insight into the exact external forces and loading patterns associated with an ACL rupture. To ensure the accurate comparison of bone bruise prevalence and location across studies, future studies should have a target MRI collection period within four to six weeks of initial ACL injury for all subjects.
ACKNOWLEDGEMENTS
The authors would like to acknowledge M.M. Manring, PhD, for his contributions to the editing process and manuscript preparation. No funding was received in support of this manuscript.
Footnotes
This mechanism, also known as the multi-planar valgus loading injury mechanism, involves a valgus load applied to the knee during various states of flexion combined with internal rotation of the femur and external rotation of the tibia. The rupture of the ACL is then followed by anterior subluxation of the tibia relative to the femur that results in an impact of the LFC against the posterior aspect of the LFC.
This mechanism is associated with antero-lateral tibial and LFC contusions.
This mechanism is associated with antero-medial tibial and LFC contusions.
After the lateral aspects of the tibia and femur collide during the ACL injury, the knee reduces and goes into compensatory varus alignment. This results in the collision between the medial aspects of the tibia and femur.
This refers to the lateral compartment of either the tibia or femur.
The authors report no conflict of interest.
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