Femoropatellar Joint Reaction Detected During a 4486 KM Ultramarathon with Mobile MRI

Abstract

Almost nothing is known about the condition of the knee joints of multistage ultra-marathon (MSUM) runner. This is first image-based investigation of the femoropatellar joint (FPJ) using a mobile 1.5T MRI accompanying the MSUM TransEurope Foot-Race (TEFR) 64 stages over 4486 km. Twenty-two (20 male) subjects got a knee MRI-protocol at defined measurement intervals during TEFR: T2*-mapping (FLASH T2*-GRE), TIRM, and fat saturated PD -sequence. In the FPJ 12 different regions were evaluated regarding cartilage T2* and thickness changes and cartilage lesions in course of TEFR and a test on possible compounding factors (running burden, BMI, age) was done if being appropriate. No significant changes in cartilage thickness- and T2*-values were found during TEFR. In 8 runners, at least one single cartilage lesion (Grade 2–3) was found at baseline, but no significant race-related adjacent T2*-changes or progress of the defects could be detected. Analyses on compounding factors were negative. In knees with MPP (5) significantly lower adjacent T2*-values were found. The extreme running burden of a MSUM seems not to have a relevant negative influence on the FPJ tissues, even if cartilage lesions are present.

Key word

cartilage - MRI - knee - marathon - running - patella

• References

• 1 Chakravarty EF, Hubert HB, Lingala VB. et al. Long distance running and knee osteoarthritis. A prospective study. Am J Prev Med 2008; 35: 133-138
• 2 Lane NE, Oehlert JW, Bloch DA. et al. The relationship of running to osteoarthritis of the knee and hip and bone mineral density of the lumbar spine: a 9-year longitudinal study. J Rheumatol 1998; 25: 334-341
• 3 Levine BD, Thompson PD. Marathon maladies. N Engl J Med 2005; 352: 1516-1518
• 4 Schäfer M, Dreinhöfer K. Sports and osteoarthrosis. Z Rheumatol 2009; 68: 804-810
• 5 Felson DT. An update on the pathogenesis and epidemiology of osteoarthritis. Radiol Clin North Am 2004; 42: 1-9
• 6 Hohmann E, Wörtler K, Imhoff AB. MR imaging of the hip and knee before and after marathon running. Am J Sports Med 2004; 32: 55-59
• 7 Konradsen L, Hansen EM, Sondergaard L. Long distance running and osteoarthrosis. Am J Sports Med 1990; 18: 379-381
• 8 Miller RH, Edwards WB, Brandon SC. et al. Why don't most runners get knee osteoarthritis? A case for per-unit-distance loads. Med Sci Sports Exerc 2014; 46: 572-579
• 9 Shellock FG, Mink JH. Knees of trained long-distance runners: MR imaging before and after competition. Radiology 1991; 179: 63
• 10 Urquhart DM, Tobing JF, Hanna FS. et al. What is the effect of physical activity on the knee joint? A systematic review. Med Sci Sports Exerc 2011; 43: 432-442
• 11 Cymet TC, Sinkov V. Does long-distance running cause osteoarthritis?. J Am Osteopath Assoc 2006; 106: 342-345
• 12 Krampla WW, Newrkla SP, Kroener AH. et al. Changes on magnetic resonance tomography in the knee joints of marathon runners: A 10-year longitudinal study. Skeletal Radiol 2008; 37: 619-626
• 13 Krampla W, Mayrhofer R, Malcher J. et al. MR imaging of the knee in marathon runners before and after competition. Skeletal Radiol 2001; 30: 72-76
• 14 Driban JB, Hootman JM, Sitler MR. et al. Is Participation in certain sports associated with knee osteoarthritis? A systematic review. J Athl Train 2017; 52: 497-506
• 15 Schueller-Weidekamm C, Schueller G, Uffmann M. et al. Incidence of chronic knee lesions in long-distance runners based on training level: Findings at MRI. Eur J Radiol 2006; 58: 286-293
• 16 Chung CB, Frank LR, Resnick D. Cartilage imaging techniques: Current clinical applications and state of the art imaging. Clin Orthop Relat Res 2001; (391 Suppl) S370-S378
• 17 Domayer SE, Welsch GH, Dorotka R. et al. MRI monitoring of cartilage repair in the knee: A review. Semin Musculoskelet Radiol 2008; 12: 302-317
• 18 Eckstein F, Glaser C. Measuring cartilage morphology with quantitative magnetic resonance imaging. Semin Musculoskelet Radiol 2004; 8: 329-353
• 19 Trattnig S, Mlynárik V, Breitenseher M. et al. MRI visualization of proteoglycan depletion in articular cartilage via intravenous administration of Gd-DTPA. Magn Reson Imaging 1999; 17: 577-583
• 20 Welsch GH, Trattnig S, Hughes T. et al. T2 and T2* mapping in patients after matrix-associated autologous chondrocyte transplantation: Initial results on clinical use with 3.0-Tesla MRI. Eur Radiol 2010; 20: 151515-151523
• 21 Burgkart R, Glaser C, Hyhlik-Dürr A. et al. Magnetic resonance imaging-based assessment of cartilage loss in severe osteoarthritis: Accuracy, precision, and diagnostic value. Arthritis Rheum 2001; 44: 2072-2077
• 22 Eckstein F, Lemberger B, Gratzke C. et al. In vivo cartilage deformation after different types of activity and its dependence on physical training status. Ann Rheum Dis 2005; 64: 291-295
• 23 Graichen H, von Eisenhart-Rothe R, Vogl T. et al. Quantitative assessment of cartilage status in osteoarthritis by quantitative magnetic resonance imaging: technical validation for use in analysis of cartilage volume and further morphologic parameters. Arthritis Rheum 2004; 50: 811-816
• 24 Kessler MA, Glaser C, Tittel S. et al. Recovery of the menisci and articular cartilage of runners after cessation of exercise: Additional aspects of in vivo investigation based on 3-dimensional magnetic resonance imaging. Am J Sports Med 2008; 36: 966-970
• 25 Eckstein F, Cicuttini F, Raynauld JP. et al. Magnetic resonance imaging (MRI) of articular cartilage in knee osteoarthritis (OA): Morphological assessment. Osteoarthritis Cartilage 2006; 14 Suppl A A46-A75
• 26 Behzadi C, Welsch GH, Laqmani A. et al. The immediate effect of long-distance running on T2 and T2* relaxation times of articular cartilage of the knee in young healthy adults at 3.0 T MR imaging. Br J Radiol 2016; 89: 20151075
• 27 Cha JG, Lee JC, Kim HJ. et al. Comparison of MRI T2 relaxation changes of knee articular cartilage before and after running between young and old amateur athletes. Korean J Radiol 2012; 13: 594-601
• 28 Chen M, Qiu L, Shen S. et al. The influences of walking, running and stair activity on knee articular cartilage: Quantitative MRI using T1 rho and T2 mapping. PLoS One 2017; 12: e0187008
• 29 Hesper T, Miese FR, Hosalkar HS. et al. Quantitative T2(*) assessment of knee joint cartilage after running a marathon. Eur J Radiol 2015; 84: 284-289
• 30 Karanfil Y, Babayeva N, Dönmez G. et al. Thirty Minutes of Running Exercise Decreases T2 Signal Intensity but Not Thickness of the Knee Joint Cartilage: A 3.0-T Magnetic Resonance Imaging Study. Cartilage 2018; 1947603518770246
• 31 Mosher TJ, Liu Y, Torok CM. Functional cartilage MRI T2 mapping: Evaluating the effect of age and training on knee cartilage response to running. Osteoarthritis Cartilage 2010; 18: 358-364
• 32 Mosher TJ, Smith HE, Collins C. et al. Change in knee cartilage T2 at MR imaging after running: a feasibility study. Radiology 2005; 234: 245-249
• 33 Souza RB, Stehling C, Wyman BT. et al. The effects of acute loading on T1rho and T2 relaxation times of tibiofemoral articular cartilage. Osteoarthritis Cartilage 2010; 18: 1557-1563
• 34 Stahl R, Luke A, Ma CB. et al. Prevalence of pathologic findings in asymptomatic knees of marathon runners before and after a competition in comparison with physically active subjects-a 3.0 T magnetic resonance imaging study. Skeletal Radiol 2008; 37: 627-638
• 35 Stehling C, Luke A, Stahl R. et al. Meniscal T1rho and T2 measured with 3.0T MRI increases directly after running a marathon. Skeletal Radiol 2011; 40: 725-735
• 36 Regatte RR, Akella SV, Lonner JH. et al. T1rho relaxation mapping in human osteoarthritis (OA) cartilage: comparison of T1rho with T2. J Magn Reson Imaging 2006; 23: 547-553
• 37 Regatte RR, Akella SV, Wheaton AJ. et al. 3D-T1rho-relaxation mapping of articular cartilage: in vivo assessment of early degenerative changes in symptomatic osteoarthritic subjects. Acad Radiol 2004; 11: 741-749
• 38 Subburaj K, Kumar D, Souza RB. et al. The acute effect of running on knee articular cartilage and meniscus magnetic resonance relaxation times in young healthy adults. Am J Sports Med 2012; 40: 2134-2141
• 39 Dardzinski BJ, Mosher TJ, Li S. et al. Spatial variation of T2 in human articular cartilage. Radiology 1997; 205: 546-550
• 40 Kiviranta I, Tammi M, Jurvelin J. et al. Articular cartilage thickness and glycosaminoglycan distribution in the canine knee joint after strenuous running exercise. Clin Orthop Relat Res 1992; 283: 302-308
• 41 Luke AC, Stehling C, Stahl R. et al. High-field magnetic resonance imaging assessment of articular cartilage before and after marathon running: Does long-distance running lead to cartilage damage?. Am J Sports Med 2010; 38: 2273-2280
• 42 Mosher TJ, Dardzinski BJ. Cartilage MRI T2 relaxation time mapping: Overview and applications. Semin Musculoskelet Radiol 2004; 8: 355-368
• 43 Smith HE, Mosher TJ, Dardzinski BJ. et al. Spatial variation in cartilage T2 of the knee. J Magn Reson Imaging 2001; 14: 50-55
• 44 Mamisch TC, Hughes T, Mosher TJ. et al. T2 star relaxation times for assessment of articular cartilage at 3 T: A feasibility study. Skeletal Radiol 2012; 41: 287-292
• 45 Roemer FW, Crema MD, Trattnig S. et al. Advances in imaging of osteoarthritis and cartilage. Radiology 2011; 260: 332-354
• 46 Murphy BJ. Evaluation of grades 3 and 4 chondromalacia of the knee using T2*-weighted 3D gradient-echo articular cartilage imaging. Skeletal Radiol 2001; 30: 305-311
• 47 Welsch GH, Mamisch TC, Hughes T. et al. In vivo biochemical 7.0 Tesla magnetic resonance: Preliminary results of dGEMRIC, zonal T2, and T2* mapping of articular cartilage. Invest Radiol 2008; 43: 619-626
• 48 Welsch GH, Apprich S, Zbyn S. et al. Biochemical (T2, T2* and magnetisation transfer ratio) MRI of knee cartilage: Feasibility at ultra-high field (7T) compared with high field (3T) strength. Eur Radiol 2011; 21: 1136-1143
• 49 Fallon KE. Musculoskeletal injuries in the ultramarathon: The 1990 Westfield Sydney to Melbourne run. Br J Sports Med 1996; 30: 319-323
• 50 Lopes AD, Hespanhol Júnior LC, Yeung SS. et al. What are the main running-related musculoskeletal injuries? A Systematic Review. Sports Med 2012; 42: 891-905
• 51 Knechtle B, Nikolaidis PT. Physiology and Pathophysiology in Ultra-Marathon Running. Front Physiol 2018; 9: 634
• 52 Schütz UH, Schmidt-Trucksäss A, Knechtle B. et al. The Transeurope FootRace Project: Longitudinal data acquisition in a cluster randomized mobile MRI observational cohort study on 44 endurance runners at a 64-stage 4,486km transcontinental ultramarathon. BMC Med 2012; 10: 78
• 53 Harriss DJ, Macsween A, Atkinson G. Standards for Ethics in Sport and Exercise Science Research: 2020 Update. Int J Sports Med 2019; 40: 813-817
• 54 Shellock FG, Spinazzi A. MRI safety update 2008: Part 2, screening patients for MRI. AJR Am J Roentgenol 2008; 191: 1140-1149
• 55 Freund W, Weber F, Billich C. et al. Ultra-marathon runners are different: Investigations into pain tolerance and personality traits of participants of the TransEurope FootRace 2009. Pain Pract 2013; 13: 524-532
• 56 Jungius KP, Schmid MR, Zanetti M. et al. Cartilaginous defects of the femorotibial joint: Accuracy of coronal short inversion time inversion-recovery MR sequence. Radiology 2006; 240: 482-488
• 57 Mosher TJ. MRI of osteochondral injuries of the knee and ankle in the athlete. Clin Sports Med 2006; 25: 843-866
• 58 Cameron ML, Briggs KK, Steadman JR. Reproducibility and reliability of the Outerbridge classification for grading chondral lesions of the knee arthroscopically. Am J Sports Med 2003; 31: 83-86
• 59 Outerbridge RE. The etiology of chondromalacia patellae. J Bone Joint Surg Br 1961; 43-B: 752-757
• 60 Peterfy CG, Guermazi A, Zaim S. et al. Whole-Organ Magnetic Resonance Imaging Score (WORMS) of the knee in osteoarthritis. Osteoarthritis Cartilage 2004; 12: 177-190
• 61 Hunter DJ, Lo GH, Gale D. et al. The reliability of a new scoring system for knee osteoarthritis MRI and the validity of bone marrow lesion assessment: BLOKS (Boston Leeds Osteoarthritis Knee Score). Ann Rheum Dis 2008; 67: 206-211
• 62 Freund W, Weber F, Billich C. et al. The foot in multistage ultra marathon runners: Experience in a cohort study of 22 participants of the Trans Europe FootRace project with mobile MRI. BMJ Open 2012; 2 pii e001118
• 63 Eckstein F, Müller S, Faber SC. et al. Side differences of knee joint cartilage volume, thickness, and surface area, and correlation with lower limb dominance--an MRI-based study. Osteoarthritis Cartilage 2002; 10: 914-921
• 64 Boocock M, McNair P, Cicuttini F. et al. The short-term effects of running on the deformation of knee articular cartilage and its relationship to biomechanical loads at the knee. Osteoarthritis Cartilage 2009; 17: 883-890
• 65 Hinterwimmer S, Feucht MJ, Steinbrech C. et al. The effect of a six-month training program followed by a marathon run on knee joint cartilage volume and thickness in marathon beginners. Knee Surg Sports Traumatol Arthrosc 2014; Jun 22: 1353-1359
• 66 Kersting UG, Stubendorff JJ, Schmidt MC. et al. Changes in knee cartilage volume and serum COMP concentration after running exercise. Osteoarthritis Cartilage 2005; 13: 925-934
• 67 Kessler MA, Glaser C, Tittel S. et al. Volume changes in the menisci and articular cartilage of runners: an in vivo investigation based on 3-D magnetic resonance imaging. Am J Sports Med 2006; 34: 832-836
• 68 Kunz M, Williams A, McKenzie C. et al. No prolonged deformation of knee joint cartilage after the Boston Marathon. Osteoarthritis Cartilage 2005; 13 (Suppl 1) S124
• 69 Niehoff A, Müller M, Brüggemann L. et al. Deformational behaviour of knee cartilage and changes in serum cartilage oligomeric matrix protein (COMP) after running and drop landing. Osteoarthritis Cartilage 2011; 19: 1003-1010
• 70 Burstein D, Gray ML. Is MRI fulfilling its promise for molecular imaging of cartilage in arthritis?. Osteoarthritis Cartilage 2006; 14: 1087-1090
• 71 Hudelmaier M, Glaser C, Hohe J. et al. Age-related changes in the morphology and deformational behavior of knee joint cartilage. Arthritis Rheum 2001; 44: 2556-2561
• 72 Neidhart M, Müller-Ladner U, Frey W. et al. Increased serum levels of non-collagenous matrix proteins (cartilage oligomeric matrix protein and melanoma inhibitory activity) in marathon runners. Osteoarthritis Cartilage 2000; 8: 222-229
• 73 Shin KA, Kim AC, Kim YJ. et al. Effect of Ultra-marathon (308 km) Race on Bone Metabolism and Cartilage Damage Biomarkers. Ann Rehabil Med 2012; 36: 80-87
• 74 Schütz UH, Billich C, Schoss D. et al. MRI Cartilage Assessment of the Subtalar and Midtarsal Joints During a Transcontinental Ultramarathon – New Insights into Human Locomotion. Int J Sports Med 2018; 39: 37-49
• 75 Schütz UHW, Ellermann J, Schoss D. et al. Biochemical cartilage alteration and unexpected signal recovery in T2* mapping observed in ankle joints with mobile MRI during a transcontinental multistage footrace over 4486 km. Osteoarthritis Cartilage 2014; 22: 1840-1850
• 76 Mündermann A, Klenk C, Billich C. et al. Changes in cartilage biomarker levels during a transcontinental multistage footrace over 4486 km. Am J Sports Med 2017; 45: 2630-2636
• 77 Arokoski J, Kiviranta I, Jurvelin J. et al. Long-distance running causes site-dependent decrease of cartilage glycosaminoglycan content in the knee joints of beagle dogs. Arthritis Rheum 1993; 36: 1451-1459
• 78 de Visser SK, Crawford RW, Pope JM. Structural adaptations in compressed articular cartilage measured by diffusion tensor imaging. Osteoarthritis Cartilage 2008; 16: 83-89
• 79 Lun V, Meeuwisse WH, Stergiou P. et al. Relation between running injury and static lower limb alignment in recreational runners. Br J Sports Med 2004; 38: 576-580
• 80 Willems TM, De Clercq D, Delbaere K. et al. A prospective study of gait related risk factors for exercise-related lower leg pain. Gait Posture 2006; 23: 91-98
• 81 Hagemann GJ, Rijke AM, Corr PD. Do knees survive the Comrades Marathon?. S Afr Med J 2008; 98: 873-876
• 82 Schueller-Weidekamm C, Schueller G, Uffmann M. et al. Does marathon running cause acute lesions of the knee? Evaluation with magnetic resonance imaging. Eur Radiol 2006; 16: 2179-2185
• 83 Vellet AD, Marks PH, Fowler PJ. et al. Occult posttraumatic osteochondral lesions of the knee: prevalence, classification, and short-term sequelae evaluated with MR imaging. Radiology 1991; 178: 271-376
• 84 Johnson DP, Eastwood DM, Witherow PJ. Symptomatic synovial plicae of the knee. J Bone Joint Surg Am 1993; 75: 1485-1496
• 85 Dupont JY. Synovial plicae of the knee. Controversies and review. Clin Sports Med 1997; 16: 87-122
• 86 Guney A, Bilal O, Oner M. et al. Short- and mid-term results of plica excision in patients with mediopatellar plica and associated cartilage degeneration. Knee Surg Sports Traumatol Arthrosc 2010; 18: 1526-1531
• 87 Hansen H, Boe S. The pathological plica in the knee. Results after arthroscopic resection. Arch Orthop Trauma Surg 1989; 108: 282-284
• 88 Yuan HF, Guo CA, Yan ZQ. Mediopatellar Plica as a Risk Factor for Knee Osteoarthritis?. Chin Med J 2015; 128: 277-278
• 89 Stehling C, Liebl H, Krug R. et al. Patellar cartilage: T2 values and morphologic abnormalities at 3.0-T MR imaging in relation to physical activity in asymptomatic subjects from the osteoarthritis initiative. Radiology 2010; 254: 509-520
• 90 Teng HL, Calixto NE, MacLeod TD. et al. Associations between patellofemoral joint cartilage T1ρ and T2 and knee flexion moment and impulse during gait in individuals with and without patellofemoral joint osteoarthritis. Osteoarthritis Cartilage 2016; 24: 1554-1564
• 91 Watrin A, Ruaud JP, Olivier PT. et al. T2 mapping of rat patellar cartilage. Radiology 2001; 219: 395-402
• 92 Watrin-Pinzano A, Ruaud JP. et al. Effect of proteoglycan depletion on T2 mapping in rat patellar cartilage. Radiology 2005; Jan 234: 162-170
• 93 Proft F, Grunke M, Reindl C. et al. The influence of long distance running on sonographic joint and tendon pathology: Results from a prospective study with marathon runners. BMC Musculoskelet Disord 2016; 17: 272
• 94 van Poppel D, Scholten-Peeters GGM, van Middelkoop M. et al. Risk models for lower extremity injuries among short- and long distance runners: A prospective cohort study. Muskuloskelet Sci Pract 2018; 36: 48-53
• 95 Schütz UH, Ehrhardt M, Beer M et al. Pre-race determinants influencing performance and finishing of a transcontinental 4486 km ultramarathon over 64 stages. J Sports Med Phys Fitness. 2019; Jul 15
• 96 van Gent RN, Siem D, van Middelkoop M. et al. Incidence and determinants of lower extremity running injuries in long distance runners: A systematic review. Br J Sports Med 2007; 41: 469-480