Purpose During anterior cruciate ligament (ACL) injury, the large external forces responsible for ligament rupture cause a violent impact between tibial and femoral articular cartilage, which is transferred to bone resulting in bone bruise detect- able at MRI. Several aspects remain controversial and await evidence on how this MRI finding should be managed while addressing the ligament lesion. Thus, the aim of the present review was to document the evidence of all available literature on the role of bone bruise associated with ACL lesions. Methods A systematic review of the literature was performed on bone bruise associated with ACL injury. The search was conducted in September 2017 on three medical electronic databases: PubMed, Web of Science, and the Cochrane Collabora- tion. Preferred Reporting Items for Systematic Reviews and Meta-analysis (PRISMA) guidelines were used. Relevant articles were studied to investigate three main aspects: prevalence and progression of bone bruise associated with ACL lesions, its impact on the knee in terms of lesion severity and joint degeneration progression over time and, finally, the influence of bone bruise on patient prognosis in terms of clinical outcome. Results The search identified 415 records and, after an initial screening according to the inclusion/exclusion criteria, 83 papers were used for analysis, involving a total of 10,047 patients. Bone bruise has a high prevalence (78% in the most recent papers), with distinct patterns related to the mechanism of injury. This MRI finding is detectable only in a minority of cases the first few months after trauma, but its presence and persistence have been correlated to a more severe joint damage that may affect the degenerative progression of the entire joint, with recent evidence suggesting possible effects on long-term clinical outcome. Conclusion This systematic review of the literature documented a growing interest on bone bruise associated with ACL injury, highlighting aspects which could provide to orthopaedic surgeons evidence-based suggestions in terms of clinical relevance when dealing with patients affected by bone bruise following ACL injury. However, prospective long-term stud- ies are needed to better understand the natural history of bone bruise, identifying prognostic factors and targets of specific treatments that should be developed in light of the overall joint derangements accompanying ACL lesions. Levels of evidence IV, Systematic review of level I–IV studies. Keywords Bone bruise · Bone contusion · ACL · Knee Introduction * Giorgio di Laura Frattura The large external forces responsible for anterior cruciate email@example.com ligament (ACL) rupture also cause a violent impact between II Orthopaedic and Traumatologic Clinic, Rizzoli tibial and femoral articular cartilage, which is transferred Orthopaedic Institute, Via di Barbiano, 1/10, Via G. C. to bone and results in bone bruise [60, 70, 80]. Such MRI Pupilli, 1, 40136 Bologna, Italy finding is best diagnosed on fluid-sensitive sequences such Ospedale Regionale di Lugano, EOC, Via Tesserete, 46, as T2-weighted images showing increased signal intensity, Lugano, Switzerland with or without decreased signal intensity on T1-weighted Nano-Biotechnology Laboratory, Rizzoli Orthopaedic images. In addition, short tau inversion recovery (STIR) Institute, Via di Barbiano, 1/10, Bologna, Italy Vol.:(0123456789) 1 3 Knee Surgery, Sports Traumatology, Arthroscopy sequences can provide more sensitive information by sup- Materials and methods pressing the signal from normal medullary fat [55, 62]. Sensitivity and specificity of MRI detection have already A systematic review of the literature was performed on been documented to be 83/96 and 86/96%, respectively. bone bruise associated with ACL injury. This search was Moreover, histological studies allowed to correlate these conducted on September 4th, 2017, using the following MRI findings to tissue alterations, including microfracture string on three medical electronic databases, PubMed, Web of the subarticular spongiosa, with osteocyte necrosis and of Science, and the Cochrane Collaboration: [(subchondral empty lacunae, bleeding in the fatty marrow and edema edema) OR (bone bruise) OR (bone marrow edema) OR [55, 62]. Bone bruise associated with ACL rupture has been (bone marrow lesion) OR (bone contusion)] AND [(ACL) extensively investigated [62, 63], but several aspects remain OR (anterior cruciate ligament)]. The Preferred Reporting controversial and await evidence on how this MRI finding Items for Systematic Reviews and Meta-analysis (PRISMA) should be managed while addressing the ligament lesion. guidelines were used  (Fig. 1). Two independent authors The aim of this systematic review was to document the separately performed the screening process according to available evidence on bone bruise associated with ACL preset inclusion and exclusion criteria, study analysis and lesions, investigating its prevalence and progression, as data tabulation. A final literature summary was obtained by well as the impact on joint and prognosis, with the hypoth- consensus, with disagreements solved by discussion with a esis that bone bruise can influence knee degeneration and third reviewer (GdLF, FN and GF). patient clinical outcome. This would provide orthopaedic First, articles were screened by title and abstract accord- surgeons with evidence-based suggestions in terms of clini- ing to the following inclusion criteria: clinical reports of cal relevance when dealing with patients affected by bone any level of evidence, written in English language, with no bruise following ACL injury. time limitation, on the association of bone bruise with ACL lesions. Exclusion criteria were articles written in other lan- guages, preclinical or ex vivo studies, reviews, case reports or clinical studies not evaluating prevalence, progression and impact on the joint and on prognosis. Second, the full texts of the selected articles were screened, with further Fig. 1 PRISMA flowchart of the systematic literature review 1 3 Knee Surgery, Sports Traumatology, Arthroscopy exclusions according to the previously described criteria. males (in 11 studies sex was not specified) with different Reference lists from the selected papers were also screened. sport participation (four articles focusing on athletes, the Relevant data (type of study, no of patients and demograph- others on patients with various activity levels). Age ranged ics, injury–MRI time and sequence, follow-up, edema size/ from children (only one study), to young adults and to senior grading, edema distribution, prevalence and progression, patients (5–81 years). correlation with other joint lesions and prognosis) were then extracted and collected in a unique database to be analysed for the purposes of the present manuscript. All relevant arti- Bone bruise prevalence and progression cles included in this systematic review were studied to inves- tigate three main aspects: the prevalence and progression Prevalence of bone bruise ranged from 8 to 98% (reported in of bone bruise associated with ACL lesions, its impact on 40/83 papers), being higher in the most recent papers (78% the knee in terms of lesion severity and progression of joint in the last 10 years vs. 62% in previous papers). Most of the degeneration over time and, finally, the influence of bone studies also investigated its distribution in the joint com- bruise on patient prognosis in terms of clinical outcome. partments, showing a higher prevalence in the lateral side of the knee (52/55), with lateral tibial plateau (31/43) being the most commonly affected site (Fig. 3). The evaluation of Results progression, investigated in 20 studies (seven retrospective, with heterogeneous follow-ups from 2 weeks to 13 years), This systematic review underlined a growing interest on documented a wide time range: from series showing com- this topic, with an increasing number of papers published plete resolution at 2 months, to others documenting persis- over time, more than half in the last 10 years (Fig. 2). The tence of subchondral marrow changes in 65% of the cases database search identified 83 papers used for the analysis at 1 year, or even an increase of bone bruise in one-third of (a detailed study description is reported in Table 1; Fig. 1). the patients over time. This systematic review revealed heterogeneous MRI Some factors were reported to influence frequency, dis- sequences and assessment strategies. Bone bruise was quan- tribution, and progression of bone bruise. Female sex, high tified in 43/83 studies with the following approaches: scor - BMI, complete vs. partial ACL tears and combined lesions ing systems were used in 9/43 articles, including WORMS, were correlated to higher prevalence, while specific distri- Costa-Paz, ICRS, Lynch, Beattie and Colleagues score and bution patterns were influenced by injury mechanism, such MOAK, while different parameters such as area/volume of as pivoting (more lateral), hyperextension (more anterior), the region of interest (either with absolute or percentage motor vehicles accident and patellar dislocation (more ante- values), depth, signal intensity, distribution and diameter rior with patella involvement), as well as by gender and age were used as criteria in 42/43 cases to quantify bone bruise. (female and older patients presented more lateral lesions). These articles analysed heterogeneous populations, for a Finally, progression was also influenced by some factors, total of 10,047 patients, including 2,675 females and 4,665 with slower resolution in the presence of osteochondral Fig. 2 The analysis of publications per year shows growing interest on bone bruise in ACL lesions with an increasing number of published stud- ies over time 1 3 Knee Surgery, Sports Traumatology, Arthroscopy 1 3 Table 1 Detailed description of the 83 studies selected in this systematic review References Type of study No. of pts, sex, MRI–injury time Follow-up Edema size grad- Edema distribution Prevalence and progression Correlation with age, mean (range) sequences (months) ing other joint lesions and prognosis Mink  NR 25, NR, NR ≤ 2 weeks, 1.5 T, 2 NR NR 72% NR NR seq T1 Cobby  NR 103, 75 M, 28 F, NR, 1.5T, seq NS NR NR NR NR NR NR 38 (15–70) Speer  Retrospective 54, 30 M, 24 F, 28 ≤ 45 dd, 1.5 T, seq NR NR NR 83% NR NR (14–44) T1, spin density, and T2 Graf  NR 98, NR, NR ≤ 6 weeks; NR Area 30 LTP, 38 LFC 48% NR NR 7 weeks–6 mm; 12 MTP, 9 MFC >6 mm, 1.5 T, seq T1 and T2 Spindler  Prospective 54, NR, 24.5 ≤ 3 mm, 1.0 or NR NR 29 LTP, 37 LFC 9 80% NR Osteochondral 1.5 T, seq T1, T2 MTP, 3 MFC and GE Tung  Retrospective 99, 62 M, 37 F, 31 ≤ 20.5 and 16.9 NR NR 15 LTP, 13 LFC 7 26% NR NR (14–47) weeks, 1.5 and MFC 1.0 T, seq T1, T2 and PD Nawata  Retrospective 56, 26 M, 30 F, 28 ≤ 1; 1–12;≥ NR NR 17 LTP, 19 LFC 1 36% NR NR (13–59) 12 mm, 1.0 and MFC 1.5 T, seq T2, and PD Gentili  Retrospective 89, 62 M, 27 F, 30 ≤ 1; 1–3; > 3 mm. NR NR NR NR NR NR (16–75) 1.5 T, seq T2 Speer  Retrospective 42, 20 M, 22 F, 32 ≤ 1 mm, 0.35, 0.50 NR Area 34 LTP, 17 LFC NR NR NR (16–58) and 1.5 T, seq 12 MTP, 4 MFC T1, T2 SE and GE Stein  Retrospective 20, 10 M, 10 F, 24 ≤ 4 dd(1 to 23 dd), 40 (24 to 73) NR 20 LTP, 13 LFC 3 100% NR NR (13–48) 1.5 T, seq PD MTP, 1 PAT and T2 Zeiss  Retrospective 71, 37 M, 34 F, ≤ 1 mm, 1.5 T, seq NR NR NR 36.60% NR NR (14–36) GE, T1 and T2 Brandser  Retrospective 74, NR, NR ≤ 6 weeks, 1.5 T, NR NR NR NR NR NR seq PD, T2 and T1 Yeung  NR 16, 10 M, 6 F, 25 6 dd to 3 y, 0.5 and NR NR NR NR NR NR (13–43) 1.5 T, seq T1, SE, GE, T2, PD, T1 TSE and TFE Knee Surgery, Sports Traumatology, Arthroscopy 1 3 Table 1 (continued) References Type of study No. of pts, sex, MRI–injury time Follow-up Edema size grad- Edema distribution Prevalence and progression Correlation with age, mean (range) sequences (months) ing other joint lesions and prognosis Johnson  Prospective 10, 10 M, 21 ≤ 2 weeks, 1.5 T, NR NR NR NR NR NR (15–36) seq T1 Dimond  Retrospective 87, 50 M, 37 F, 29 ≤ 6 weeks, seq T1, NR NR 30 LTP, 24 LFC 4 68% NR NR (16–43) T2 and PD MTP, 11 MFC Lahm  Prospective 38, NR, 31 NR, seq T1, T2 5.5 and 40.8 NR NR 62% NR NR and STIR Faber  Retrospective 23, 18 M, 5 F, 30 ≤ 12 dd 1.5 T, seq 72 NR 23 LTP, 23 LFC NR 65% NR (20–49) T1 and T2 FSE Kaplan Retrospective 25, 20 M, 5 F, 28 ≤ 4 weeks, 1.5 T, NR NR 25 LTP, 24 LFC NR NR NR (16–52) seq T1, GRE, WE DESS and STIR Lee  Retrospective 19, 5 M, 14 F, ≤ 2; 2–8;> 8 NR NR NR 68% NR NR (5–16) weeks, 1.5 T, seq T1 and T2 Johnson  Prospective 40, NR, 18 ≤ 1 week, NR, seq 0.2, 0.5, 0.7 and 1 NR NR NR NR NR (15–23) NS Costa-Paz  Cohort study 21, 15 M, 6 F, 31 NR 34 NR 11 LTP, 16 LFC 1 NR NR NR (20–58) MTP, 1 MFC Fang  Prospective 12, 9 M, 3 F, 18 NR NR NR 12 LTP, 12 LFC NR NR NR (17–23) Bretlau  Prospective 64, 33 M, 31 F, 36 ≤ 5 dd, 0.1 T, seq 4 and 12 NR 13 LTP, 8 LFC 8 63% NR NR (15–68) T2, PD 3D-GE MTP, 5 MFC and STIR Chen  Retrospective 32, 22 M, 10 F, 29 < 6; > 6 weeks, NR NR NR 63% NR NR 1.5 T, seq T1, T, GE and PD Fayad  Retrospective 84, 42 M, 42 F, NS, 1.5 T, seq T1, NR NR 62 LTP, 50 LFC NR NR NR (16–39) T2, T2 FS and 35 MTP, 4 MFC FSE Davies  Prospective 30, 16 M, 14 F, 28 ≤ 3.4 weeks, 1.0 T, 3,2 Volume NR NR NR Osteochondral (17–39) seq T1, GE and STIR Terzidis  NR 255, 197 M, 58 F, ≤ 1; 2–4 mm, 31 NR 4 LTP, 29 LFC 4 NR NR NR 24 1.0 T, seq T1 SE, MTP,5 MFC T2 and STIR Tiderius  NR 24, 14 M, 10 F, 27 ≤ 3 weeks, 1.5 T, NR Area 6 LTP, 15 LFC 96% NR Osteochondral (17–40) seq T1 Gd Knee Surgery, Sports Traumatology, Arthroscopy 1 3 Table 1 (continued) References Type of study No. of pts, sex, MRI–injury time Follow-up Edema size grad- Edema distribution Prevalence and progression Correlation with age, mean (range) sequences (months) ing other joint lesions and prognosis Fithian  Prospective 209, 101 M, 108 F, ≤ 4 weeks, 1.5 T, 79 NR NR 53% NR NR 39 (16–69) seq NR Vincken  Prospective 664, 460 M, 204 F, ≤ 4 weeks, 0.5 T, 6 NR 43 LTP, 44 LFC 18.70% NR LM (16–45) seq DSE and 3D 31 MTP, 7 MFC MCL–LCL T1 GE 6 PAT Wu  Pilot study 52, 22 M, 30 F, NS 1.0 T, seq FSE, NR Beattie and col- NR 7.70% NR NR NR FS T1, GE, T1 leagues FSE and T2 FS FSE Hernandez-Molina NR 258, 148 M, 110 F, NR, 1.5 T, seq SE 15 and 30 NR NR 53.80% NR Osteochondral  67 PD, T2, SE, FS and PD Nishimori  NR 39, 25 M, 14 F, 23 ≤ 8 dd, 0.3 T, seq NR NR NR 89.70% NR Osteochondral (14–55) SE PD and T2 LM Collins  Retrospective 48, 26 M, 22 F, 29 ≤ 6 mm, 1.5 T, seq NR NR NR 33% NR NR FSE PD, FS FSE T2, T2 GRE, CSE PD and CSE T2 Hanypsiak  Cohort study 54, NR, NR ≤ 3 weeks, 1.0 T, 153 (141–165) NR 29 LTP, 37 LFC 9 80% 0% NR seq T1, PD, MTP, 3 MFC T2, T2 FS and FLASH Atkinson  Retrospective 1546, NR, NR 0–4, 4–10, 10–26 NR NR NR NR NR MM and 26–52 LM weeks, 1.5 T, seq MCL multiplanar FS Viskontas  Prospective 100, 69 M, 31 F, ≤ 6 weeks, 1.5 T, NR Area ICRS NR NR NR NR 29 (13–61) seq FS and FSE Frobell  RCT 121, 89 M, 32 F, ≤ 19 ± 6.5 dd, NR Volume NR 98% NR Cortical depression 26 1.5 T, seq fractures 3D-FLASH, T2 3D-GRE, DETSE and STIR Bolbos  Retrospective 31, 22 M, 9 F, 31 ≤ 2 mm, 3 T, seq NR Area 13 LTP, 9 LFC 93% NR Osteochondral 2D T2 FS FSE and 3D-SPGR Knee Surgery, Sports Traumatology, Arthroscopy 1 3 Table 1 (continued) References Type of study No. of pts, sex, MRI–injury time Follow-up Edema size grad- Edema distribution Prevalence and progression Correlation with age, mean (range) sequences (months) ing other joint lesions and prognosis Frobell  NR 58, 42 M, 16 F, 26 ≤ 5 weeks, 1.5 T, 3, 6 and 12 Volume NR 100% NR NR seq 3D-FLASH, T2 3D-GRE, DETSE and STIR Xiaojuan  Prospective 38, 28 M, 10 F, 35 ≤ 2 mm, 3 T, seq NR Volume NR NR NR Osteochondral (20–66) T2 FS FSE, SPGR and 3D MRSI Halinen  Prospective 44, 19 M, 25 F, 39 NS, 0.23 T or NR NR NR 88.60% NR NR (21–64) 1.5 T, seq T1, T2, FSE, DE, SE, FS, PD FSE, PD SE and STIR Yoon  Retrospective 145, 124 M, 21 F, ≤ 6 weeks; NR Area NR 60.70% NR NR 31 (10–56) 1.5–3 mm; 3–12 mm; >12 mm, 1.5 T, seq T1, T2 FS, PD, PD DE and FS Dunn  Prospective 525, 304 M, 221 F, NR NR NR NR NR NR NR Quelard  Prospective 217, 139 M, 78 F, ≤ 6 mm, NR 1.5 and 3 NR 156 LTP, 104 LFC 72% NR NR 29 (14–62) Theologis  Cohort study 9, 5 M, 4 F, 35 ≤ 8 weeks, 3 T, seq 0.5, 6 and 12 Volume NR NR NR Osteochondral (27–45) T2 FS FSE Frobell  NR 61, 45 M, 16 F, 26 NR, 1.5 T, seq 3, 6, 12 and 24 Volume 58 LTP, 47 LFC NR NR NR FLASH, T2, DETSE and STIR Yoon  Retrospective 80, 58 M, 22 F, 30 ≤ 8 dd, 1.5 T, seq NR NR 50 LTP, 46 LFC 84% NR MM T1 and T2 18 MTP, 16 LM MFC Jelić  NR 120, 88 M, 32 F, ≤ 1 mm, 0.3 T, seq NR NR 18 LFC, 4 MFC 33% NR MM 31 SE T1W1, FS LM T2W1 and STIR Potter  Prospective 40, 16 M, 24 F, 37 ≤ 8 weeks, 1.5 T, 132 Area 36 LTP, 30 LFC NR NR Osteochondral (15–53) seq T2 and CPMG Knee Surgery, Sports Traumatology, Arthroscopy 1 3 Table 1 (continued) References Type of study No. of pts, sex, MRI–injury time Follow-up Edema size grad- Edema distribution Prevalence and progression Correlation with age, mean (range) sequences (months) ing other joint lesions and prognosis Van Dyck  Retrospective 97, 62 M, 35 F, 49 ≤ 6 weeks, 1.5 and NR NR NR 41% NR NR (12–81) 3.0 T, seq FS TSE WI, SE T1 WI, TSE PD and T2 WI Kijowski  Retrospective 114, 57 M, 57 F, ≤ 3 weeks, 1.5 and 12 Volume 106 LTP, 88 LFC 96% NR Cortical fractures 26 3.0 T, seq T2 FS 57 MTP, 30 FSE and FSE MFC Szkopek  Prospective 17, 10 M, 7 F, 28 ≤ 2 dd, 1.5 T, seq 0.5, 1 and 2 Volume NR NR NR NR (23–34) T2 FS, T1 and 3D Ge T2 Yoon  Retrospective 151, 130 M, 21 F, ≤ 6 weeks; 6 NR Area NR NR NR NR 31 (10–56) weeks − 3 mm; 3–12 mm;> 12 mm, 1.5 T, seq T1, T2 FS, PD, PD DE and FS Bisson  Case control 171, 89 M, 82 F, ≤ 6 weeks, NR, NR Volume Area 145 LTP, 132 LFC 90% NR LM NR seq NR 44 MTP, 11 MFC Roemer  NR 62, 50 M, 12 F, 26 NS, 1.5 T, seq 12, 24, 36, 48, 60 Volume NR NR NR NR 3D FLASH, T2 and 72 GRE, DETSE and STIR Chang  Retrospective 154, 130 M, 24 F, < 3, > 3 mm, NR NR NR NR NR NR 32 (14–56) 1.5 T, seq FS T2, T1 and PD Wittstein  Case series 73, 28 M, 45 F, 16 ≤ 6 weeks, 1.5 T, NR Volume 67 LTP, 70 LFC NR NR NR seq FS FSE T2 45 MTP, 31 MFC Wissman  Retrospective 7, 5 M, 2 F, NS NR, 1.5–3 T, seq NR NR 4 LTP, 4 LFC 4 NR NR NR T2, FS FSE and MTP, 4 MFC PD Illingworth  Retrospective 50, 26 M, 24 F, 19 ≤ 30 dd, 1.5 T, seq NR Volume Area NR 86% NR Menisci T2 TSE FS, PD TSE, T1 SE and TSE PD Knee Surgery, Sports Traumatology, Arthroscopy 1 3 Table 1 (continued) References Type of study No. of pts, sex, MRI–injury time Follow-up Edema size grad- Edema distribution Prevalence and progression Correlation with age, mean (range) sequences (months) ing other joint lesions and prognosis Chin  Retrospective 88, 72 M, 16 F, 27 ≤ 10 weeks, 1.5 T, NR NR 37 LTP, 43 LFC 65.90% NR NR seq T1 and T2 23 MTP, 16 MFC, 4 PAT Wissman  Retrospective 132, 82 M, 50 F, ≤ 4 weeks, 1.5 or NR NR NR NR NR NR 30 (14–70) 3 T, seq T2, FSE and PD Culvenor  NR 111, 71 M, 40 F, ≤ 12 mm, 3 T, seq 12 Area MOAKS 15 LTP, 10 LFC 9 NR NR Osteochondral 26 (18–50) 3D PD VISTA, MTP, 10 MFC 5 PD TSE and PAT, 22 TRO STIR Herbst  Retrospective 500, NR, 29 ≤ 1 mm, NR, seq NR Area 396 LTP, 257 LFC NR NR NR NR Kim  Retrospective 8, 5 M, 3 F, 23 ≤ 1 mm, 1.5 and NR Volume NR NR NR NR (16–30) 3 T, seq FSE Filardo  Retrospective 134, 98 M, 36 F, ≤ 6 mm, 1.5 T, seq 80 Area WORMS 22 LTP, 12 LFC 55.20% NR NR 32 FSE, PD FS and 4 MTP, 4 MFC dual FSE 2 PAT Pezeshki  Prospective 175, 149 M, 26 F, ≤ 1 mm, 0.3 T, seq 12 Area NR 30,90% NR MM < 45 (18–45) T1 and T2 FS, MCL fluid suppres- sion, GE and T2 SE Kluczynski  Cross sectional 59, 59 M, 23 ≤ 6 weeks, NR, NR NR 48 LTP, 46 LFC NR NR NR seq NR 14 MTP, 3 MFC Ahn  Retrospective 249, 33 M, 216 F, ≤ 15.4 ± 15.6 NR Area NR NR NR Meniscal injuries 38 (18–53) (1–52) and 4.2 ± 5.7 (1–50) weeks, 1.5 T, seq T1, T2 and PD Culvenor  Prospective 93, 56 M, 37 F, 29 NS, 3 T, seq PD 12 and 36 Area NR NR 22% (12 mm) NR VISTA, PD TSE and STIR Palmieri-Smith Prospective 22, 10 M, 12 F, 20 ≤ 2 weeks, 3 T, seq 12 Area 10 LTP, 11 LFC NR NR Osteochondral  FSE and T2 2 PAT Kluczynski  Case control 384, 209 M, 175 F, ≤ 6 weeks, NS, NR NR 290 LTP, 251 LFC NR NR NR NS seq NR 105 MTP, 27 MFC Song  Retrospective 193, 141 M, 52 F, ≤ 6 weeks, 1.5 T, NR Area ICRS 141 LTP, 117 LFC NR NR LM 32.3 (15–55) seq FS and T2 41 MTP, 12 ALL MFC Knee Surgery, Sports Traumatology, Arthroscopy 1 3 Table 1 (continued) References Type of study No. of pts, sex, MRI–injury time Follow-up Edema size grad- Edema distribution Prevalence and progression Correlation with age, mean (range) sequences (months) ing other joint lesions and prognosis Gong  Prospective 54, 31 M, 23 F, 30 ≤ 55.5 ± 45.3 dd, 6, 12 and 24 Volume WORMS 33 LTP, 22 LFC 77,80% 20.7% 13.8% Osteochondral 3 T, seq CUBE 21 MTP, 6 MFC 87.2% and T2 4 PAT, 1 TRO Helito  Retrospective 101, 79 M, 22 F, ≤ 3 weeks, 1.5 and NR NR NR NR NR NR 33 3.0 T, seq T1, T2 and PD Berger  Retrospective 220, 148 M, 72 F, ≤ 8 weeks, 1.5 T, NR Volume WORMS 48 LTP, 44 LFC NR NR NR 34 (16–71) seq FS and T2 43 MTP, 5 MFC FSE 7 PAT Wang  Cross sectional 130, 85 M, 45 F, NR, 1.5 and 3.0 T, 24 and 36 Volume 130 LTP, 130 LFC NR NR NR (18–40) seq T1 and PD 130 MTP, 130 FS SE MFC Lattermann  Prospective 81, NR, 35 NR, NS, seq T1, 24 and 72 Volume Costa-Paz 76 LTP, 66 LFC 100% NR LM T2 and PD 46 MTP, 20 Osteochondral MFC Thomas  Descriptive 35, NR, 20 NR, 3 T, seq PD NR Area 12 LTP, 12 LFC NR NR NR laboratory and FS study Driban  Cross sectional 121, 89 M, 32 F, ≤ 4 weeks NR Volume 116 LTP, 101 LFC 96% NR Depression fracture 26 (18–35) (19 ± 6.5), 1.5 T, 101 MTP, 64 seq DETSE MFC DePhillipo  Case series 50, 33 M, 17 F, 30 NR, 1.5 and 3.0 T, NR NR 36 MTP 76% NR NR (14–61) seq PD, FS and T2 Temponi  Retrospective 162, NR, NR ≤ 1 week, 1.5 T, NR NR 24 LTP, 24 LFC 75% NR Superior pop- seq NS 15 MTP, 9 MFC liteomeniscal fascicle Ali  Retrospective 25, 15 M, 10 F, 30 ≤ 24 dd NR NR 4 LTP, 2 LFC 4 60% NR LCL (13.5–55) (0–10 mm), MTP, 2 MFC MCL 1.5 T, seq PD The studies are analysed for type of study, number of initial patients, mean (range) age, sex, follow-up time in months, edema distribution, prevalence, progression and correlation with other joint lesions. Some data discrepancies between overall population and subgroups are due to lack of patient details in some of the studies NR not reported, MFC medial femoral condyle, LFC lateral femoral condyle, MTP medial tibial plateau, LTP lateral tibial plateau, TRO trochlea, PAT patella, LCL lateral collateral ligament, MCL medial collateral ligament, LM lateral meniscus, MM medial meniscus, ALL anterolateral ligament, ICRS International Cartilage Research Society, MOAK MRI Osteoarthritis Knee Score, WORMS Whole-Organ Magnetic Resonance Imaging Score Knee Surgery, Sports Traumatology, Arthroscopy fluid level. Homeostatic alterations were also supported by changes of synovial fluid, which presented a higher pres - ence of glycosaminoglycans. The impact of bone bruise on joint damage over time was explored, showing (4/8 papers) a correlation of bone bruise with persisting and progres- sive damage of the articular surface, suggesting early OA development . Factors influencing lesion severity of joints presenting bone bruise were found in 20 studies, the most frequent being higher bone bruise size and severity, followed by taller patients and higher BMI. A larger bone bruise was also cor- related with osteochondral lesion progression. Influence of bone bruise on the clinical outcome Papers evaluating the influence of bone bruise on clinical outcome (19/83) studied 2822 patients, with a follow-up ranging from 1 week to 13 years. Several methods were used: subjective scoring systems, such as KOOS, Tegner, IKDC, SF-36; ADL, Lysholm, Noyes, and VAS, and other Fig. 3 Percentage of bone bruise distribution in the affected anatomic evaluation methods including ROM, clinical examination, bone locations. LTP lateral tibial plateau, LFC lateral femoral con- dyle, MTP medial tibial plateau, MFC medial femoral condyle and gait analysis. Among these studies, five focused on baseline clinical findings, two of them showing a correlation of bone bruise lesions and after ACL reconstruction compared to more with higher pain and laxity, especially in case of bone bruise conservative treatments. with higher volume and at the medial side. Four studies focused on short-term recovery and documented a longer Impact of bone bruise on joint lesion severity time to reach normal ROM and non-antalgic gait before liga- and progression ment reconstruction, with a lower clinical outcome for up to 6 months, especially in case of larger size and medial side The severity of joint lesions, investigated in 30/83 studies, bone bruise distribution. Ten studies explored the mid-/long- was correlated to the presence of bone bruise in 26/30 stud- term outcome: only one was able to document the influence ies. The most affected tissue was cartilage: osteochondral of bone bruise on the mid-term clinical outcome, showing lesions were reported to correlate significantly in 11/13 stud- a lower return to sport after ACL reconstruction in joints ies, ranging from 59% to more than 80% of patients (80% in presenting bone bruise at baseline MRI. the lateral tibial plateau or 94% in the lateral femoral con- Finally, factors found to influence clinical findings were dyle) affected by bone bruise; this was followed by menis - associated chondral lesions and osteochondral fractures, as cus lesions and, less frequently, by collateral ligaments and well as bone bruise severity, location (lateral distribution presence of fractures. Some reports also suggested a possible with higher instability and ROM limitation, medial distri- correlation with other lesions, such as those involving the bution with higher pain) and persistence over time; bone anterolateral ligament, superior popliteomeniscal fascicle, as bruise detected at MRI performed more than 3 months after well as more abundant and slower resolving effusion. The trauma was suggestive of a more difficult return to full activ - rim sign, with anteromedial bone bruise distribution, was ity recovery. reported to be associated with greater joint derangement. Moreover, the presence of a > 1.5 mm notch sign, a bone depression due to more frequent impaction at the lateral Discussion femoral condyle after pivoting lesions, was reported to be associated with cartilage lesions and lateral meniscus tears. The most important finding of this systematic review of the Finally, few studies evaluated articular samples showing sof- literature is that bone bruise in ACL lesions is a frequently tening, fissuring, with degeneration of chondrocytes and loss detected MRI finding that entails a more severe joint damage of proteoglycans, together with necrosis of osteocytes and affecting joint degenerative progression. empty lacunae in subchondral bone, as well as elevation of Several articles have been published over the past COMP degradative fragments, both at cartilage and synovial 30 years and the interest on this topic is still growing, with 1 3 Knee Surgery, Sports Traumatology, Arthroscopy an increasing number of studies in the recent past. Nonethe- been reported despite continuous efforts to optimize ACL less, the contribution of the existing literature is limited, as treatment . This has prompted researchers to look at pos- most of the findings are accompanied by still open ques- sible factors affecting the evolution of joint degeneration. tions, which will be addressed in the following paragraphs. A correlation between bone bruise and cartilage lesions The first factor hindering the possibility to effectively sum- has been demonstrated, and it is well acknowledged that the marize the study results is the lack of a common language presence of cartilage lesions increases with the time elapsed in the literature. In fact, besides the overall accepted defi- between ACL rupture and reconstruction: chondral lesions nition of bone bruise, when looking at lesion assessment may increase the chances of osteoarthritis development, and description, the literature showed no common strategy. even after ACL surgical repair . Even though in most The sequences used differed among studies, and half of the cases normal cartilage is initially found during arthroscopy, authors did not even describe the MRI findings observed. the osteochondral unit absorbs compression forces during Moreover, those who aimed at further assessing the pres- impaction, and this could cause a double long-term mecha- ence of bone bruise, applied heterogeneous methods relying nism of damage of the articular surface. Cartilage metabo- on different grading systems or quantifying area or volume lism may be significantly affected, with long-term conse- in the affected compartment in either absolute or relative quences . Moreover, abnormality  of subchondral values. The complexity of this scenario is further increased bone may precede and favour cartilage destruction, since the by the heterogeneity of the populations analysed, as well as rigid callus resulting from bone fracture may cause cartilage outcomes and follow-up times investigated. In this light, the to absorb more of the load force, with abnormal stresses evidence on each specific aspect (prevalence, natural history leading to a progressive degeneration of the articular surface and impact on joint and outcome) is often driven only by few . In ACL reconstructed knees, the cartilage overlying the low-quality studies, which explains the current persisting area of bone bruise presents signs of damage with altered effort of physicians and researchers to further explore the extracellular matrix: cartilage evaluated at 12 months’ fol- role of bone bruise in ACL lesions. low-up with recent MRI sequences showed elevated T1ρ Prevalence of bone bruise in the MRI of patients affected values compared to the surrounding tissue, thus suggesting by ACL lesions has been investigated in most of the selected that despite the resolution of abnormal bone signal, cartilage studies, showing a wide range from 12 to 96%. This hetero- lesions persist . These imaging data have been confirmed geneity can be explained by several factors, such as the dif- by histological data, and the analysis of joint samples docu- ferences of the analysed populations in terms of bone bruise mented an alteration of the entire joint homeostasis . joint distribution, mechanism of trauma, age, sex, activity Bone bruise in ACL injury is correlated with osteochon- and BMI. Among all, the main factor was the resolution time dral lesions that can act as a catalyst for osteoarthritis even of the abnormal MRI signal, which makes the presence of after a successful reconstruction. In this light, it appears log- bone bruise strongly related to the time passed from injury ical to suppose that such an important trauma causing these to MRI examination. To this regard, it is also interesting to deleterious consequences on joint tissues might also affect observe how the reported prevalence increased in the past clinical prognosis. However, results on this matter are con- few years, which could be explained by different patients troversial [32, 67]. The lack of evidence on the correlation included but, possibly, also by the evolution of the MRI between the presence of bone bruise at MRI after trauma technology and sequences. While earlier reports tended to and the long-term effect on the joint with the reconstructed show a swift complete resolution, more recent findings show ACL may be explained by several factors, starting from the persistence or even increase of MRI abnormality over time lack of long-term studies, which could better detect the effect . However, if from one side, modern MRI can allow a on the joint of the cascade started with the initial trauma more in-depth study of tissue alterations compared to ear- . Moreover, current classification systems contribute lit- lier studies; on the other hand, the clinical significance of tle towards the understanding of the underlying pathology this more subtle, but now detectable changes, still remains defined as bone bruise. Relatively less severe trauma causes controversial . marrow edema without injury to cells and subchondral bone This systematic review evidenced several questions architecture. However, when the extent of trauma is big- remaining still open, but at the same time it showed an ger, trabecular fractures and haemorrhage are seen together increasing awareness on the importance of bone bruise. The with edema, but current MRI sequences and bone bruise attention on this matter can be better understood looking definition do not help in distinguishing between these two at the impact of ALC lesions on society: ACL reconstruc- patterns . Similarly, it is not always easy to distinguish tion is one of the most common procedures in orthopaedics between bone bruise involving only the marrow with occult . Associated injuries and earlier onset of degenerative fractures not breaching the adjacent cortex, and those involv- changes influence the affected knee: high rate (from 10 to ing the osteochondral surface. Moreover, factors predictive 90%) of osteoarthritis development after ACL injury has of subsequent trabecular fracture development have not been 1 3 Knee Surgery, Sports Traumatology, Arthroscopy identified yet. In fact, even bone bruise without cortical dis- Conclusion ruption may represent a region of bone at increased risk for the subsequent development of insufficiency fractures, if Bone bruise has a high prevalence, with distinct patterns bone is not adequately protected during trabecular healing. related to the mechanism of injury, and its presence and Some efforts have been made to identify predicting fac- persistence have been correlated to a more severe joint tors, such as the importance of the localization of the imag- damage, which may affect the degenerative progression ing finding and its evolution pattern, with resolution pro- of the entire joint, with recent evidence suggesting pos- ceeding from periphery to joint margin (opposite to lesions sible effects on the long-term clinical outcome. However, proceeding toward the centre of bone bruise lesion) being prospective long-term studies are needed to better under- suggested to be associated with osteochondral injuries. stand the natural history of bone bruise, identifying prog- However, these correlations are mainly related to sporadic nostic factors and targets of specific treatments that could evidence [19, 34, 55, 90]. In fact, most of the studies do not be developed in light of the overall joint derangements address the different evolution patterns according to possible accompanying ACL lesions. influencing variables, but rather report overall outcomes on Funding There is no funding source. heterogeneous populations. The lack of focus on specific patient populations is another aspect that may hinder a better Compliance with ethical standards understanding of the long-term clinical impact, since joint tissue damage can variably affect patients with a different Conflict of Interest The authors declare that they have no conflict of activity level . interest. Prospective studies are needed to look at the natural his- tory of bone bruise and at identifying factors affecting its Ethical approval This article does not contain any studies with human participants or animals performed by any of the authors. radiological and clinical course. At the moment, clinical management remains complicated, both because it is very Informed consent For this type of study formal consent is not required. difficult to identify specific clinical signs and symptoms due to concomitant knee damages (soft tissue lesions and effu- Open Access This article is distributed under the terms of the Crea- sion), and because of the lack of correlation between symp- tive Commons Attribution 4.0 International License (http://creat iveco toms and imaging findings. Imaging resolution is largely mmons.or g/licenses/b y/4.0/), which permits unrestricted use, distribu- delayed compared to clinical symptomatology , which tion, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the currently guides clinical management. 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Knee Surgery, Sports Traumatology, Arthroscopy – Springer Journals
Published: Jun 5, 2018
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