Pathogenesis and Diagnosis of Proximal Hamstring Tendinopathies

Abstract

The proximal hamstring complex is a highly vulnerable area that is especially prone to injury. Proximal hamstring tendinopathies (PHTs) remain challenging in diagnosis, treatment, rehabilitation, and prevention due to a large variety of different injuries, slow healing response, persistent symptoms, and functional impairments. PHTs are often misdiagnosed or underdiagnosed, leading to delayed treatment and therapy failure. In addition, many athletes are at a high risk of PHT recurrence, a leading cause of prolonged rehabilitation and impaired individual performance. Until now, there have been no clear criteria for the diagnosis and classification of PHT. Tendinopathies can be graded based on their symptoms and onset. Additionally, radiological characteristics exist that describe the severity of tendinopathies. The diagnosis usually includes a battery of pain provocation tests, functional tests, and imaging to ensure a proper classification. Understanding the specific tasks in the pathogenesis and diagnostic process of PHT requires knowledge of functional anatomy, injury pattern and pathophysiological mechanisms as well as examination and imaging techniques. This work provides a structured overview of the pathogenesis and diagnostic work-up of PHT, emphasizing structured examination and imaging to enable a reliable diagnosis and rapid treatment decisions.

Zusammenfassung

Die proximale Hamstring-Muskulatur ist ein hochgradig vulnerabler Bereich, der besonders verletzungsanfällig ist. Proximale Hamstring-Tendinopathien (PHT) stellen aufgrund der heterogenen Verletzungsmorphologien, des langsamen Heilungsverlaufs, der diffusen, jedoch erheblichen Symptome und der funktionellen Beeinträchtigungen eine Herausforderung für die Diagnostik, Therapie, Rehabilitation und Prävention dar. PHT werden häufig inadäquat, verspätet oder überhaupt nicht diagnostiziert, was zu einer verzögerten Behandlung und hohen Rate an Therapieversagen führt. Darüber hinaus besteht bei vielen Sportlern ein hohes Rezidivrisiko, welches eine der Hauptursachen für einen langwierigen Heilungsverlauf darstellt. Bislang gibt es keine klaren Kriterien für die Diagnose und Klassifizierung von PHT. Tendinopathien können anhand ihrer Symptome und ihres Auftretens eingeteilt werden. Außerdem gibt es radiologische Merkmale, die den Schweregrad von Tendinopathien beschreiben. Die Diagnose umfasst in der Regel eine Reihe von Schmerzprovokationstests, Funktionstests und bildgebenden Verfahren. Um die spezifischen Aspekte in der Pathogenese und im diagnostischen Prozess der PHT zu verstehen, sind Kenntnisse der funktionellen Anatomie, der Verletzung und der pathophysiologischen Mechanismen sowie der Untersuchungs- und Bildgebungstechniken erforderlich. Die vorliegende Arbeit liefert einen strukturierten Überblick über die Pathogenese und den diagnostischen Ablauf, wobei der Schwerpunkt auf einer strukturierten Untersuchung und Bildgebung liegt, um eine zuverlässige Diagnose und schnelle Behandlungsentscheidungen zu ermöglichen.

Keywords

Hamstring anatomy - tendinopathies - muscle injuries - sports injuries - overuse injuries - ultrasound - MRI

Schlüsselwörter

Anatomie der Hamstrings - Tendinopathien - Muskelverletzungen - Sportverletzungen - Überlastungsverletzungen - Sonografie - MRT

Publication History

Received: 07 April 2022

Accepted after revision: 09 January 2023

Article published online:
22 June 2023

• References

• 1 Ekstrand J, Hägglund M, Waldén M. Epidemiology of muscle injuries in professional football (soccer). Am J Sports Med 2011; 39: 1226-1232
• 2 Feeley BT, Kennelly S, Barnes RP. et al. Epidemiology of National Football League training camp injuries from 1998 to 2007. The American journal of sports medicine 2008; 36: 1597-1603
• 3 Iwamoto J, Takeda T. Stress fractures in athletes: review of 196 cases. Journal of Orthopaedic Science 2003; 8: 273-278
• 4 Lutterbach-Penna RA, Kalume-Brigido M, Morag Y. et al. Ultrasound of the Thigh: Focal, Compartmental, or Comprehensive Examination?. American Journal of Roentgenology 2014; 203: 1085-1092
• 5 Degen RM. Proximal Hamstring Injuries: Management of Tendinopathy and Avulsion Injuries. Curr Rev Musculoskelet Med 2019; 12: 138-146
• 6 Kujala UM, Orava S. Ischial apophysis injuries in athletes. Sports Medicine 1993; 16: 290-294
• 7 Abate M, Silbernagel KG, Siljeholm C. et al. Pathogenesis of tendinopathies: inflammation or degeneration?. Arthritis Res Ther 2009; 11: 235
• 8 Malliaras P, Cook J, Purdam C. et al. Patellar tendinopathy: clinical diagnosis, load management, and advice for challenging case presentations. journal of orthopaedic & sports physical therapy 2015; 45: 887-898
• 9 Robinson J, Cook JL, Purdam C. et al. The VISA-A questionnaire: a valid and reliable index of the clinical severity of Achilles tendinopathy. British journal of sports medicine 2001; 35: 335-341
• 10 Van Mieghem IM, Boets A, Sciot R. et al. Ischiogluteal bursitis: an uncommon type of bursitis. Skeletal radiology 2004; 33: 413-416
• 11 Visentini PJ, Khan KM, Cook JL. et al. The VISA score: an index of severity of symptoms in patients with jumper’s knee (patellar tendinosis). Journal of Science and Medicine in Sport 1998; 1: 22-28
• 12 Docking S, Samiric T, Scase E. et al. Relationship between compressive loading and ECM changes in tendons. Muscles, ligaments and tendons journal 2013; 3: 7
• 13 Huygaerts S, Cos F, Cohen DD. et al. Mechanisms of Hamstring Strain Injury: Interactions between Fatigue, Muscle Activation and Function. Sports (Basel) 2020; 8: 65
• 14 Chumanov ES, Heiderscheit BC, Thelen DG. Hamstring musculotendon dynamics during stance and swing phases of high-speed running. Med Sci Sports Exerc 2011; 43: 525-532
• 15 Chumanov ES, Heiderscheit BC, Thelen DG. The effect of speed and influence of individual muscles on hamstring mechanics during the swing phase of sprinting. J Biomech 2007; 40: 3555-3562
• 16 Beltran L, Ghazikhanian V, Padron M. et al. The proximal hamstring muscle–tendon–bone unit: A review of the normal anatomy, biomechanics, and pathophysiology. European Journal of Radiology 2012; 81: 3772-3779
• 17 Slocum DB, James SL. Biomechanics of running. Jama 1968; 205: 721-728
• 18 Miller SL, Gill J, Webb GR. The proximal origin of the hamstrings and surrounding anatomy encountered during repair. A cadaveric study. J Bone Joint Surg Am 2007; 89: 44-48
• 19 Battermann N, Appell HJ, Dargel J. et al. An anatomical study of the proximal hamstring muscle complex to elucidate muscle strains in this region. International journal of sports medicine 2011; 32: 211-215
• 20 Philippon MJ, Ferro FP, Campbell KJ. et al. A qualitative and quantitative analysis of the attachment sites of the proximal hamstrings. Knee Surgery, Sports Traumatology, Arthroscopy 2015; 23: 2554-2561
• 21 Feucht MJ, Plath JE, Seppel G. et al. Gross anatomical and dimensional characteristics of the proximal hamstring origin. Knee Surg Sports Traumatol Arthrosc 2015; 23: 2576-2582
• 22 Stępień K, Śmigielski R, Mouton C. et al. Anatomy of proximal attachment, course, and innervation of hamstring muscles: a pictorial essay. Knee Surg Sports Traumatol Arthrosc 2019; 27: 673-684
• 23 Sato K, Nimura A, Yamaguchi K. et al. Anatomical study of the proximal origin of hamstring muscles. J Orthop Sci 2012; 17: 614-618
• 24 Thornton GM, Hart DA. The interface of mechanical loading and biological variables as they pertain to the development of tendinosis. J Musculoskelet Neuronal Interact 2011; 11: 94-105
• 25 Kalkhoven J, Watsford M, McLean B. et al. The evidence indicates that the hamstrings do not behave isometrically during the swing phase of the sprint cycle: a narrative review. 2020
• 26 Nourissat G, Berenbaum F, Duprez D. Tendon injury: from biology to tendon repair. Nature Reviews Rheumatology 2015; 11: 223
• 27 Mienaltowski MJ, Birk DE. Structure, physiology, and biochemistry of collagens. Adv Exp Med Biol 2014; 802: 5-29
• 28 Zelzer E, Blitz E, Killian ML. et al. Tendon-to-bone attachment: from development to maturity. Birth Defects Res C Embryo Today 2014; 102: 101-112
• 29 Garrett Jr, Califf J, Bassett F. Histochemical correlates of hamstring injuries. The American journal of sports medicine 1984; 12: 98-103
• 30 Curwin S. Rehabilitation After Tendon Injuries. 2005
• 31 Cassel M, Stoll J, Mayer F. Tendinopathien der unteren Extremität im Sport – Diagnostik und Therapie. OP-JOURNAL 2016; 32: 44-54
• 32 De Smet AA, Blankenbaker DG, Alsheik NH. et al. MRI appearance of the proximal hamstring tendons in patients with and without symptomatic proximal hamstring tendinopathy. AJR Am J Roentgenol 2012; 198: 418-422
• 33 de Vos RJ, Weir A, Tol JL. et al. No effects of PRP on ultrasonographic tendon structure and neovascularisation in chronic midportion Achilles tendinopathy. Br J Sports Med 2011; 45: 387-392
• 34 Fredberg U, Stengaard-Pedersen K. Chronic tendinopathy tissue pathology, pain mechanisms, and etiology with a special focus on inflammation. Scandinavian journal of medicine & science in sports 2008; 18: 3-15
• 35 Maffulli N, Wong J, Almekinders LC. Types and epidemiology of tendinopathy. Clinics in sports medicine 2003; 22: 675-692
• 36 Renström P, Hach T. Insertional Tendinopathy in Sports. In: Maffulli N, Renström P, Leadbetter WB. Tendon Injuries: Basic Science and Clinical Medicine. London: Springer London; 2005: 70-85
• 37 Ekstrand J, Waldén M, Hägglund M. Hamstring injuries have increased by 4% annually in men’s professional football, since 2001: a 13-year longitudinal analysis of the UEFA Elite Club injury study. British journal of sports medicine 2016; 50: 731-737
• 38 Fredericson M, Moore W, Guillet M. et al. High hamstring tendinopathy in runners: meeting the challenges of diagnosis, treatment, and rehabilitation. Phys Sportsmed 2005; 33: 32-43
• 39 Jonhagen S, Nemeth G, Eriksson E. Hamstring injuries in sprinters: the role of concentric and eccentric hamstring muscle strength and flexibility. The American journal of sports medicine 1994; 22: 262-266
• 40 Brooks JH, Fuller C, Kemp S. et al. Epidemiology of injuries in English professional rugby union: part 1 match injuries. British journal of sports medicine 2005; 39: 757-766
• 41 Brooks JH, Fuller C, Kemp S. et al. Epidemiology of injuries in English professional rugby union: part 2 training Injuries. British journal of sports medicine 2005; 39: 767-775
• 42 Khan KM, Cook JL, Bonar F. et al. Histopathology of common tendinopathies. Update and implications for clinical management. Sports Med 1999; 27: 393-408
• 43 Cook JL, Purdam C. Is compressive load a factor in the development of tendinopathy?. British journal of sports medicine 2012; 46: 163-168
• 44 Cook JL, Rio E, Purdam CR. et al. Revisiting the continuum model of tendon pathology: what is its merit in clinical practice and research?. Br J Sports Med 2016; 50: 1187-1191
• 45 Goom T, Malliaras P, Reiman M. et al. Proximal Hamstring Tendinopathy: Clinical Aspects of Assessment and Management. Journal of Orthopaedic & Sports Physical Therapy 2016; 46: 1-32
• 46 Hamming MG, Philippon MJ, Rasmussen MT. et al. Structural properties of the intact proximal hamstring origin and evaluation of varying avulsion repair techniques: an in vitro biomechanical analysis. Am J Sports Med 2015; 43: 721-728
• 47 Lempainen L, Johansson K, Banke IJ. et al. Expert opinion: diagnosis and treatment of proximal hamstring tendinopathy. Muscles Ligaments Tendons J 2015; 5: 23-28
• 48 Ardern CL, Taylor NF, Feller JA. et al. A systematic review of the psychological factors associated with returning to sport following injury. Br J Sports Med 2013; 47: 1120-1126
• 49 Gift AG. Visual analogue scales: measurement of subjective phenomena. Nurs Res 1989; 38: 286-288
• 50 Cacchio A, De Paulis F, Maffulli N. Development and validation of a new visa questionnaire (VISA-H) for patients with proximal hamstring tendinopathy. Br J Sports Med 2014; 48: 448-452
• 51 De-la-Cruz-Torres B, Maffulli N, Hernández-Sánchez S. Cross-cultural adaptation of the Victorian institute of sports assessment – Hamstrings (VISA-H) questionnaire for Spanish speaking athletes with proximal hamstring tendinopathy. Physical Therapy in Sport 2021; 51: 50-57
• 52 Zissen MH, Wallace G, Stevens KJ. et al. High Hamstring Tendinopathy: MRI and Ultrasound Imaging and Therapeutic Efficacy of Percutaneous Corticosteroid Injection. American Journal of Roentgenology 2010; 195: 993-998
• 53 Askling CM, Tengvar M, Saartok T. et al. Acute first-time hamstring strains during slow-speed stretching: clinical, magnetic resonance imaging, and recovery characteristics. Am J Sports Med 2007; 35: 1716-1724
• 54 Bennell K, Wajswelner H, Lew P. et al. Isokinetic strength testing does not predict hamstring injury in Australian Rules footballers. Br J Sports Med 1998; 32: 309-314
• 55 Gabbe BJ, Branson R, Bennell KL. A pilot randomised controlled trial of eccentric exercise to prevent hamstring injuries in community-level Australian Football. J Sci Med Sport 2006; 9: 103-109
• 56 Engebretsen AH, Myklebust G, Holme I. et al. Prevention of injuries among male soccer players: a prospective, randomized intervention study targeting players with previous injuries or reduced function. Am J Sports Med 2008; 36: 1052-1060
• 57 Nazarian LN. The top 10 reasons musculoskeletal sonography is an important complementary or alternative technique to MRI. American Journal of Roentgenology 2008; 190: 1621-1626
• 58 Kohn D, Deiler S, Rudert M. Arterial blood supply of the infrapatellar fat pad. Anatomy and clinical consequences. Arch Orthop Trauma Surg 1995; 114: 72-75
• 59 Becciolini M, Bonacchi G, Bianchi S. Ultrasound Features of the Proximal Hamstring Muscle-Tendon-Bone Unit. J Ultrasound Med 2019; 38: 1367-1382
• 60 Kellis E, Galanis N, Natsis K. et al. Validity of architectural properties of the hamstring muscles: correlation of ultrasound findings with cadaveric dissection. J Biomech 2009; 42: 2549-2554
• 61 Pietrzak MJR, Kayani MB, Tahmassebi MJ. et al. Proximal hamstring tendinopathy: pathophysiology, diagnosis and treatment. British Journal of Hospital Medicine 2018; 79: 389-394
• 62 Pollock N, James SL, Lee JC. et al. British athletics muscle injury classification: a new grading system. British journal of sports medicine 2014; 48: 1347-1351
• 63 Askling CM, Malliaropoulos N, Karlsson J. High-speed running type or stretching-type of hamstring injuries makes a difference to treatment and prognosis. British Journal of Sports Medicine 2012; 46: 86-87
• 64 van der Horst R, Tol J, Weir A. et al. The value of MRI STIR signal intensity on return to play prognosis and reinjury risk estimation in athletes with acute hamstring injuries. Journal of Science and Medicine in Sport 2021; 24 (09) 855-861
• 65 van Dijk CN, van Sterkenburg MN, Wiegerinck JI. et al. Terminology for Achilles tendon related disorders. Knee Surg Sports Traumatol Arthrosc 2011; 19: 835-841
• 66 Romaneehsen B, Kreitner K-F. MRT-Bildgebung bei Sehnenerkrankungen. Der Orthopäde 2005; 34: 543-549
• 67 Bowden DJ, Byrne CA, Alkhayat A. et al. Differing MRI appearances of symptomatic proximal hamstring tendinopathy with ageing: a comparison of appearances in patients below and above 45 years. Clin Radiol 2018; 73: 922-927