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 firstname.lastname@example.org 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:.(1234567890) 1 3 Knee Surgery, Sports Traumatology, Arthroscopy (2019) 27:44–59 45 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 46 Knee Surgery, Sports Traumatology, Arthroscopy (2019) 27:44–59 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 (2019) 27:44–59 47 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 48 Knee Surgery, Sports Traumatology, Arthroscopy (2019) 27:44–59 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 (2019) 27:44–59 49 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 50 Knee Surgery, Sports Traumatology, Arthroscopy (2019) 27:44–59 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 (2019) 27:44–59 51 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 52 Knee Surgery, Sports Traumatology, Arthroscopy (2019) 27:44–59 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 (2019) 27:44–59 53 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 54 Knee Surgery, Sports Traumatology, Arthroscopy (2019) 27:44–59 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 (2019) 27:44–59 55 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 56 Knee Surgery, Sports Traumatology, Arthroscopy (2019) 27:44–59 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. The understanding Creative Commons license, and indicate if changes were made. of whether and how to protect cartilage (by rest from weight bearing) during initial treatment, when cartilage lacks sup- port from bruised bone [21, 54, 55], or the development of treatments to address both stiffer long-term tissue repair and References altered homeostasis [3, 22, 31], would likely contribute to overall better results. 1. Ahn JH, Jeong SH, Kang HW (2016) Risk factors of false- During ACL injury, the entire joint undergoes a high- negative magnetic resonance imaging diagnosis for meniscal energy trauma, which may alter joint homeostasis and long- tear associated with anterior cruciate ligament tear. Arthros- copy 32:1147–1154 term prognosis. In this light, even if no statistical analysis 2. Ali AM, Pillai JK, Gulati V, Gibbons CER, Roberton BJ (2017) was feasible due to the heterogeneity of the included studies, Hyperextension injuries of the knee: do patterns of bone this systematic review provides evidence-based insights to bruising predict soft tissue injury? Skelet Radiol. https ://doi. understand the significance of this articular derangement, org/10.1007/s0025 6-017-2754-y 3. Andriolo L, Di Matteo B, Kon E, Filardo G, Venieri G, Mar- which can be of clinical relevance for the orthopaedic sur- cacci M (2015) PRP augmentation for ACL reconstruction. geon when dealing with patients affected by bone bruise Biomed Res Int 2015:371746 following ACL injury, by underlining that this MRI find - 4. Ariyoshi M, Nagata K, Sato K, Kubo M, Hiraoka K, Hamada ing may play an important role in the joint derangement T et al (1997) Hemarthrosis of the knee and bone contusion. Kurume Med J 44:135–139 affecting the outcome ACL reconstruction surgery. Future 5. Atkinson PJ, Cooper TG, Anseth S, Walter NE, Kargus R, Haut research should aim at better understanding clinical sig- RC (2008) Association of knee bone bruise frequency with time nificance, factors predicting resolution or long-term con- postinjury and type of soft tissue injury. Orthopedics 31:440 sequences to the affected joint and patient prognosis and, 6. Berger N, Andreisek G, Karer AT, Bouaicha S, Naraghi A, Manoliu A et al (2017) Association between traumatic bone finally, at identifying strategies to restore the overall joint marrow abnormalities of the knee, the trauma mechanism and homeostasis rather than just the ligament lesion. This would associated soft-tissue knee injuries. Eur Radiol 27:393–403 optimize the management of ACL-injured patients with bet- 7. Bisson LJ, Kluczynski MA, Hagstrom LS, Marzo JM (2013) ter long-term results. A prospective study of the association between bone contusion 1 3 Knee Surgery, Sports Traumatology, Arthroscopy (2019) 27:44–59 57 and intra-articular injuries associated with acute anterior cruci- 25. Driban JB, Lohmander S, Frobell RB (2017) Posttraumatic bone ate ligament tear. Am J Sports Med 41:1801–1807 marrow lesion volume and knee pain within 4 weeks after ante- 8. Bolbos RI, Ma CB, Link TM, Majumdar S, Li X (2008) In vivo rior cruciate ligament injury. J Athl Train 52:575–580 T1rho quantitative assessment of knee cartilage after anterior 26. Dunn WR, Spindler KP, Amendola A, Andrish JT, Kaeding CC, cruciate ligament injury using 3 T magnetic resonance imag- Marx RG et al (2010) Which preoperative factors, including bone ing. Invest Radiol 43:782–788 bruise, are associated with knee pain/symptoms at index anterior 9. Brandser EA, Riley MA, Berbaum KS, el-Khoury GY, Bennett cruciate ligament reconstruction (ACLR)? A multicenter ortho- DL (1996) MR imaging of anterior cruciate ligament injury: paedic outcomes network (MOON) ACLR cohort study. Am J independent value of primary and secondary signs. AJR Am J Sports Med 38:1778–1787 Roentgenol 167:121–126 27. Faber KJ, Dill JR, Amendola A, Thain L, Spouge A, Fowler PJ 10. Bretlau T, Tuxoe J, Larsen L, Jorgensen U, Thomsen HS, (1999) Occult osteochondral lesions after anterior cruciate liga- Lausten GS (2002) Bone bruise in the acutely injured knee. ment rupture. Six-year magnetic resonance imaging follow-up Knee Surg Sports Traumatol Arthrosc 10:96–101 study. Am J Sports Med 27:489–494 11. Chang MJ, Chang CB, Choi JY, Je MS, Kim TK (2014) Can 28. Fang C, Johnson D, Leslie MP, Carlson CS, Robbins M, Di magnetic resonance imaging findings predict the degree of Cesare PE (2001) Tissue distribution and measurement of car- knee joint laxity in patients undergoing anterior cruciate liga- tilage oligomeric matrix protein in patients with magnetic reso- ment reconstruction? BMC Musculoskelet Disord 15:214 nance imaging-detected bone bruises after acute anterior cruciate 12. Chen WT, Shih TT, Tu HY, Chen RC, Shau WY (2002) Par- ligament tears. J Orthop Res 19:634–641 tial and complete tear of the anterior cruciate ligament. Acta 29. Fayad LM, Parellada JA, Parker L, Schweitzer ME (2003) MR Radiol 43:511–516 imaging of anterior cruciate ligament tears: is there a gender gap? 13. Chin YC, Wijaya R, Chong le R, Chang HC, Lee YH (2014) Skelet Radiol 32:639–646 Bone bruise patterns in knee injuries: where are they found? 30. Filardo G, de Caro F, Andriolo L, Kon E, Zaffagnini S, Marcacci Eur J Orthop Surg Traumatol 24:1481–1487 M (2016) Do cartilage lesions affect the clinical outcome of ante- 14. Cobby MJ, Schweitzer ME, Resnick D (1992) The deep lateral rior cruciate ligament reconstruction? A systematic review. Knee femoral notch: an indirect sign of a torn anterior cruciate liga- Surg Sports Traumatol Arthrosc. https ://doi.org/10.1007/s0016 ment. Radiology 184:855–858 7-016-4097-y 15. Collins MS, Unruh KP, Bond JR, Mandrekar JN (2008) Magnetic 31. Filardo G, Kon E, Longo UG, Madry H, Marchettini P, Mar- resonance imaging of surgically confirmed anterior cruciate liga- motti A et al (2016) Non-surgical treatments for the management ment graft disruption. Skelet Radiol 37:233–243 of early osteoarthritis. Knee Surg Sports Traumatol Arthrosc 16. Costa-Paz M, Muscolo DL, Ayerza M, Makino A, Aponte-Tinao 24:1775–1785 L (2001) Magnetic resonance imaging follow-up study of bone 32. Filardo G, Kon E, Tentoni F, Andriolo L, Di Martino A, Busacca bruises associated with anterior cruciate ligament ruptures. M et al (2016) Anterior cruciate ligament injury: post-traumatic Arthroscopy 17:445–449 bone marrow oedema correlates with long-term prognosis. Int 17. Culvenor AG, Collins NJ, Guermazi A, Cook JL, Vicenzino Orthop 40:183–190 B, Khan KM et al (2015) Early knee osteoarthritis is evident 33. Fithian DC, Paxton EW, Stone ML, Luetzow WF, Csintalan RP, one year following anterior cruciate ligament reconstruction: a Phelan D et al (2005) Prospective trial of a treatment algorithm magnetic resonance imaging evaluation. Arthritis Rheumatol for the management of the anterior cruciate ligament-injured 67:946–955 knee. Am J Sports Med 33:335–346 18. Culvenor AG, Collins NJ, Guermazi A, Cook JL, Vicenzino B, 34. Frobell RB (2011) Change in cartilage thickness, posttraumatic Whitehead TS et al (2016) Early patellofemoral osteoarthritis bone marrow lesions, and joint fluid volumes after acute ACL features one year after anterior cruciate ligament reconstruction: disruption: a two-year prospective MRI study of sixty-one sub- symptoms and quality of life at three years. Arthritis Care Res jects. J Bone Jt Surg Am 93:1096–1103 (Hoboken) 68:784–792 35. Frobell RB, Le Graverand MP, Buck R, Roos EM, Roos HP, 19. Davies NH, Niall D, King LJ, Lavelle J, Healy JC (2004) Mag- Tamez-Pena J et al (2009) The acutely ACL injured knee assessed netic resonance imaging of bone bruising in the acutely injured by MRI: changes in joint fluid, bone marrow lesions, and carti- knee—short-term outcome. Clin Radiol 59:439–445 lage during the first year. Osteoarthr Cartilage 17:161–167 20. DePhillipo NN, Cinque ME, Chahla J, Geeslin AG, Engebret- 36. Frobell RB, Roos HP, Roos EM, Hellio Le Graverand MP, Buck sen L, LaPrade RF (2017) Incidence and detection of meniscal R, Tamez-Pena J et al (2008) The acutely ACL injured knee ramp lesions on magnetic resonance imaging in patients with assessed by MRI: are large volume traumatic bone marrow anterior cruciate ligament reconstruction. Am J Sports Med lesions a sign of severe compression injury? Osteoarthr Cartilage 45:2233–2237 16:829–836 21. Di Martino A, Kon E, Perdisa F, Sessa A, Filardo G, Neri MP 37. Gentili A, Seeger LL, Yao L, Do HM (1994) Anterior cruci- et al (2015) Surgical treatment of early knee osteoarthritis with a ate ligament tear: indirect signs at MR imaging. Radiology cell-free osteochondral scaffold: results at 24 months of follow- 193:835–840 up. Injury 46(Suppl 8):S33–S38 38. Gong J, Pedoia V, Facchetti L, Link TM, Ma CB, Li X (2016) 22. Di Martino A, Tentoni F, Di Matteo B, Cavicchioli A, Lo Presti Bone marrow edema-like lesions (BMELs) are associated with M, Filardo G et al (2016) Early viscosupplementation after ante- higher T1rho and T2 values of cartilage in anterior cruciate liga- rior cruciate ligament reconstruction: a randomized controlled ment (ACL)-reconstructed knees: a longitudinal study. Quant trial. Am J Sports Med 44:2572–2578 Imaging Med Surg 6:661–670 23. Dimond PM, Fadale PD, Hulstyn MJ, Tung GA, Greisberg J 39. Graf BK, Cook DA, De Smet AA, Keene JS (1993) “Bone (1998) A comparison of MRI findings in patients with acute and bruises” on magnetic resonance imaging evaluation of anterior chronic ACL tears. Am J Knee Surg 11:153–159 cruciate ligament injuries. Am J Sports Med 21:220–223 24. Donohue JM, Buss D, Oegema TR Jr, Thompson RC Jr (1983) 40. Halinen J, Koivikko M, Lindahl J, Hirvensalo E (2009) The The effects of indirect blunt trauma on adult canine articular efficacy of magnetic resonance imaging in acute multi-ligament cartilage. J Bone Jt Surg Am 65:948–957 injuries. Int Orthop 33:1733–1738 1 3 58 Knee Surgery, Sports Traumatology, Arthroscopy (2019) 27:44–59 41. Hanypsiak BT, Spindler KP, Rothrock CR, Calabrese GJ, Rich- articular cartilage pathology associated with inferior outcomes mond B, Herrenbruck TM et al (2008) Twelve-year follow-up on 2 and 6 years after anterior cruciate. Ligament Reconstruction? anterior cruciate ligament reconstruction: long-term outcomes of Cartilage 8:139–145 prospectively studied osseous and articular injuries. Am J Sports 58. Lee K, Siegel MJ, Lau DM, Hildebolt CF, Matava MJ (1999) Med 36:671–677 Anterior cruciate ligament tears: MR imaging-based diagnosis 42. Helito CP, Helito PV, Costa HP, Demange MK, Bordalo-Rodri- in a pediatric population. Radiology 213:697–704 gues M (2017) Assessment of the anterolateral ligament of the 59. Li X, Ma BC, Bolbos RI, Stahl R, Lozano J, Zuo J et al (2008) knee by magnetic resonance imaging in acute injuries of the ante- Quantitative assessment of bone marrow edema-like lesion and rior cruciate ligament. Arthroscopy 33:140–146 overlying cartilage in knees with osteoarthritis and anterior cruci- 43. Herbst E, Hoser C, Tecklenburg K, Filipovic M, Dallapozza C, ate ligament tear using MR imaging and spectroscopic imaging Herbort M et al (2015) The lateral femoral notch sign following at 3 T. J Magn Reson Imaging 28:453–461 ACL injury: frequency, morphology and relation to meniscal 60. Lynch TC, Crues JV, Morgan FW, Sheehan WE, Harter LP, Ryu injury and sports activity. Knee Surg Sports Traumatol Arthrosc R (1989) Bone abnormalities of the knee: prevalence and signifi- 23:2250–2258 cance at MR imaging. Radiology 171:761–766 44. Hernandez-Molina G, Guermazi A, Niu J, Gale D, Goggins J, 61. Mall NA, Chalmers PN, Moric M, Tanaka MJ, Cole BJ, Bach Amin S et al (2008) Central bone marrow lesions in symptomatic BR Jr et al (2014) Incidence and trends of anterior cruciate lig- knee osteoarthritis and their relationship to anterior cruciate liga- ament reconstruction in the United States. Am J Sports Med ment tears and cartilage loss. Arthritis Rheum 58:130–136 42:2363–2370 45. Illingworth KD, Hensler D, Casagranda B, Borrero C, van Eck 62. Mandalia V, Fogg AJ, Chari R, Murray J, Beale A, Henson JH CF, Fu FH (2014) Relationship between bone bruise volume and (2005) Bone bruising of the knee. Clin Radiol 60:627–636 the presence of meniscal tears in acute anterior cruciate ligament 63. Mathis DT, Hirschmann A, Falkowski AL, Kiekara T, Amsler rupture. Knee Surg Sports Traumatol Arthrosc 22:2181–2186 F, Rasch H et al (2018) Increased bone tracer uptake in sympto- 46. Jelic D, Masulovic D (2011) Bone bruise of the knee associated matic patients with ACL graft insufficiency: a correlation of MRI with the lesions of anterior cruciate ligament and menisci on and SPECT/CT findings. Knee Surg Sports Traumatol Arthrosc magnetic resonance imaging. Vojnosanit Pregl 68:762–766 26:563–573 47. Johnson DL, Bealle DP, Brand JC Jr, Nyland J, Caborn DN 64. Mink JH, Deutsch AL (1989) Occult cartilage and bone injuries (2000) The effect of a geographic lateral bone bruise on knee of the knee: detection, classification, and assessment with MR inflammation after acute anterior cruciate ligament rupture. Am imaging. Radiology 170:823–829 J Sports Med 28:152–155 65. Moher D, Liberati A, Tetzlaff J, Altman DG (2009) Preferred 48. Johnson DL, Urban WP Jr, Caborn DN, Vanarthos WJ, Carl- reporting items for systematic reviews and meta-analyses: the son CS (1998) Articular cartilage changes seen with magnetic PRISMA statement. BMJ 339:b2535 resonance imaging-detected bone bruises associated with acute 66. Nawata K, Teshima R, Suzuki T (1993) Osseous lesions asso- anterior cruciate ligament rupture. Am J Sports Med 26:409–414 ciated with anterior cruciate ligament injuries. Assessment by 49. Kaplan PA, Gehl RH, Dussault RG, Anderson MW, Diduch DR magnetic resonance imaging at various periods after injuries. (1999) Bone contusions of the posterior lip of the medial tibial Arch Orthop Trauma Surg 113:1–4 plateau (contrecoup injury) and associated internal derangements 67. Nishimori M, Deie M, Adachi N, Kanaya A, Nakamae A, Motoy- of the knee at MR imaging. Radiology 211:747–753 ama M et al (2008) Articular cartilage injury of the posterior 50. Kijowski R, Sanogo ML, Lee KS, Munoz Del Rio A, McGuine lateral tibial plateau associated with acute anterior cruciate liga- TA, Baer GS et al (2012) Short-term clinical importance of osse- ment injury. Knee Surg Sports Traumatol Arthrosc 16:270–274 ous injuries diagnosed at MR imaging in patients with anterior 68. Palmieri-Smith RM, Wojtys EM, Potter HG (2016) Early carti- cruciate ligament tear. Radiology 264:531–541 lage changes after anterior cruciate ligament injury: evaluation 51. Kim SY, Spritzer CE, Utturkar GM, Toth AP, Garrett WE, with imaging and serum biomarkers-a pilot study. Arthroscopy DeFrate LE (2015) Knee kinematics during noncontact anterior 32:1309–1318 cruciate ligament injury as determined from bone bruise location. 69. Papalia R, Torre G, Vasta S, Zampogna B, Pedersen DR, Denaro Am J Sports Med 43:2515–2521 V et al (2015) Bone bruises in anterior cruciate ligament injured 52. Kluczynski MA, Kang JV, Marzo JM, Bisson LJ (2016) Magnetic knee and long-term outcomes. A review of the evidence. Open resonance imaging and intra-articular findings after anterior cru- Access J Sports Med 6:37–48 ciate ligament injuries in ice hockey versus other sports. Orthop 70. Patel SA, Hageman J, Quatman CE, Wordeman SC, Hewett TE J Sports Med 4:2325967116646534 (2014) Prevalence and location of bone bruises associated with 53. Kluczynski MA, Marzo JM, Rauh MA, Bernas GA, Bisson LJ anterior cruciate ligament injury and implications for mechanism (2016) A case–control study comparing bone bruising and intra- of injury: a systematic review. Sports Med 44:281–293 articular injuries in patients undergoing anterior cruciate liga- 71. Pezeshki S, Vogl TJ, Pezeshki MZ, Daghighi MH, Pourisa M ment reconstruction with and without medial collateral ligament (2016) Association of the type of trauma, occurrence of bone tears. Orthop J Sports Med 4:2325967116660053 bruise, fracture and joint effusion with the injury to the menisci 54. Kon E, Filardo G, Perdisa F, Venieri G, Marcacci M (2014) and ligaments in MRI of knee trauma. Muscles Ligaments Ten- Clinical results of multilayered biomaterials for osteochondral dons J 6:161–166 regeneration. J Exp Orthop 1:10 72. Potter HG, Jain SK, Ma Y, Black BR, Fung S, Lyman S (2012) 55. Kon E, Ronga M, Filardo G, Farr J, Madry H, Milano G et al Cartilage injury after acute, isolated anterior cruciate ligament (2016) Bone marrow lesions and subchondral bone pathology of tear: immediate and longitudinal ee ff ct with clinical/MRI follow- the knee. Knee Surg Sports Traumatol Arthrosc 24:1797–1814 up. Am J Sports Med 40:276–285 56. Lahm A, Erggelet C, Steinwachs M, Reichelt A (1998) Articu- 73. Quelard B, Sonnery-Cottet B, Zayni R, Ogassawara R, Prost T, lar and osseous lesions in recent ligament tears: arthroscopic Chambat P (2010) Preoperative factors correlating with pro- changes compared with magnetic resonance imaging findings. longed range of motion deficit after anterior cruciate ligament Arthroscopy 14:597–604 reconstruction. Am J Sports Med 38:2034–2039 74. Roemer FW, Frobell R, Lohmander LS, Niu J, Guermazi 57. Lattermann C, Jacobs CA, Reinke EK, Scaramuzza EA, Huston A (2014) Anterior cruciate ligament osteoarthritis score LJ, Dunn WR et al (2017) Are bone bruise characteristics and 1 3 Knee Surgery, Sports Traumatology, Arthroscopy (2019) 27:44–59 59 (ACLOAS): longitudinal MRI-based whole joint assessment 89. Van Dyck P, Gielen JL, Vanhoenacker FM, Wouters K, Doss- of anterior cruciate ligament injury. Osteoarthr Cartilage che L, Parizel PM (2012) Stable or unstable tear of the anterior 22:668–682 cruciate ligament of the knee: an MR diagnosis? Skelet Radiol 75. Song GY, Zhang H, Wang QQ, Zhang J, Li Y, Feng H (2016) 41:273–280 Bone contusions after acute noncontact anterior cruciate liga- 90. Vellet AD, Marks PH, Fowler PJ, Munro TG (1991) Occult post- ment injury are associated with knee joint laxity, concomi- traumatic osteochondral lesions of the knee: prevalence, clas- tant meniscal lesions, and anterolateral ligament abnormality. sification, and short-term sequelae evaluated with MR imaging. Arthroscopy 32:2331–2341 Radiology 178:271–276 76. Speer KP, Spritzer CE, Bassett FH, Feagin JA Jr, Garrett WE Jr 91. Vincken PW, Ter Braak BP, van Erkel AR, Coerkamp EG, Mal- (1992) Osseous injury associated with acute tears of the anterior lens WM, Bloem JL (2006) Clinical consequences of bone bruise cruciate ligament. Am J Sports Med 20:382–389 around the knee. Eur Radiol 16:97–107 77. Speer KP, Warren RF, Wickiewicz TL, Horowitz L, Henderson L 92. Viskontas DG, Giuffre BM, Duggal N, Graham D, Parker D, (1995) Observations on the injury mechanism of anterior cruci- Coolican M (2008) Bone bruises associated with ACL rup- ate ligament tears in skiers. Am J Sports Med 23:77–81 ture: correlation with injury mechanism. Am J Sports Med 78. Spindler KP, Schils JP, Bergfeld JA, Andrish JT, Weiker GG, 36:927–933 Anderson TE et al (1993) Prospective study of osseous, articular, 93. Wang X, Wang Y, Bennell KL, Wrigley TV, Cicuttini FM, Fortin and meniscal lesions in recent anterior cruciate ligament tears by K et al (2017) Cartilage morphology at 2–3 years following ante- magnetic resonance imaging and arthroscopy. Am J Sports Med rior cruciate ligament reconstruction with or without concomi- 21:551–557 tant meniscal pathology. Knee Surg Sports Traumatol Arthrosc 79. Stein LN, Fischer DA, Fritts HM, Quick DC (1995) Occult osse- 25:426–436 ous lesions associated with anterior cruciate ligament tears. Clin 94. Wissman RD, England E, Mehta K, Boateng S, Javadi A, Smith Orthop Relat Res 187–193 P et al (2014) Patellotibial contusions: a rare cruciate ligament 80. Sutton KM, Bullock JM (2013) Anterior cruciate ligament rup- injury pattern. J Comput Assist Tomogr 38:495–498 ture: differences between males and females. J Am Acad Orthop 95. Wissman RD, England E, Mehta K, Burch M, Javadi A, New- Surg 21:41–50 ton K (2015) The anteromedial tibial rim sign: an indicator of 81. Szkopek K, Warming T, Neergaard K, Jorgensen HL, Christensen patellotibial impaction in acute anterior cruciate ligament tears. HE, Krogsgaard M (2012) Pain and knee function in relation J Comput Assist Tomogr 39:57–63 to degree of bone bruise after acute anterior cruciate ligament 96. Wittstein J, Vinson E, Garrett W (2014) Comparison between rupture. Scand J Med Sci Sports 22:635–642 sexes of bone contusions and meniscal tear patterns in non- 82. Temponi EF, de Carvalho Junior LH, Saithna A, Thaunat M, contact anterior cruciate ligament injuries. Am J Sports Med Sonnery-Cottet B (2017) Incidence and MRI characterization 42:1401–1407 of the spectrum of posterolateral corner injuries occurring in 97. Wu H, Webber C, Fuentes CO, Bensen R, Beattie K, Adachi JD association with ACL rupture. Skelet Radiol 46:1063–1070 et al (2007) Prevalence of knee abnormalities in patients with 83. Terzidis IP, Christodoulou AG, Ploumis AL, Metsovitis SR, osteoarthritis and anterior cruciate ligament injury identified Koimtzis M, Givissis P (2004) The appearance of kissing con- with peripheral magnetic resonance imaging: a pilot study. Can tusion in the acutely injured knee in the athletes. Br J Sports Med Assoc Radiol J 58:167–175 38:592–596 98. Yeung KW, Liu GC, Wu DK (1998) Tear of the anterior cruciate 84. Theologis AA, Kuo D, Cheng J, Bolbos RI, Carballido-Gamio ligament: evaluation with MR imaging. Kaohsiung J Med Sci J, Ma CB et al (2011) Evaluation of bone bruises and associated 14:88–93 cartilage in anterior cruciate ligament-injured and -reconstructed 99. Yoon JP, Chang CB, Yoo JH, Kim SJ, Choi JY, Choi JA et al knees using quantitative t(1rho) magnetic resonance imaging: (2010) Correlation of magnetic resonance imaging findings with 1-year cohort study. Arthroscopy 27:65–76 the chronicity of an anterior cruciate ligament tear. J Bone Jt Surg 85. Thomas AC, Palmieri-Smith RM (2017) Knee frontal-plane Am 92:353–360 biomechanics in adults with or without bone marrow edema- 100. Yoon JP, Yoo JH, Chang CB, Kim SJ, Choi JY, Yi JH et al (2013) like lesions after anterior cruciate ligament injury. J Athl Train Prediction of chronicity of anterior cruciate ligament tear using 52:581–586 MRI findings. Clin Orthop Surg 5:19–25 86. Thompson RC Jr, Oegema TR Jr, Lewis JL, Wallace L (1991) 101. Yoon KH, Yoo JH, Kim KI (2011) Bone contusion and associ- Osteoarthrotic changes after acute transarticular load. An animal ated meniscal and medial collateral ligament injury in patients model. J Bone Jt Surg Am 73:990–1001 with anterior cruciate ligament rupture. J Bone Jt Surg Am 87. Tiderius CJ, Olsson LE, Nyquist F, Dahlberg L (2005) Cartilage 93:1510–1518 glycosaminoglycan loss in the acute phase after an anterior cruci- 102. Zeiss J, Paley K, Murray K, Saddemi SR (1995) Comparison of ate ligament injury: delayed gadolinium-enhanced magnetic reso- bone contusion seen by MRI in partial and complete tears of the nance imaging of cartilage and synovial fluid analysis. Arthritis anterior cruciate ligament. J Comput Assist Tomogr 19:773–776 Rheum 52:120–127 88. Tung GA, Davis LM, Wiggins ME, Fadale PD (1993) Tears of the anterior cruciate ligament: primary and secondary signs at MR imaging. Radiology 188:661–667 1 3
Knee Surgery, Sports Traumatology, Arthroscopy – Springer Journals
Published: Jun 5, 2018
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