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Original article
Triglycerides and total serum cholesterol in rotator cuff tears: do they matter?
  1. U G Longo1,
  2. F Franceschi1,
  3. F Spiezia1,
  4. F Forriol2,
  5. N Maffulli3,
  6. V Denaro1
  1. 1Department of Orthopaedic and Trauma Surgery, University Campus Bio-Medico of Rome, Rome, Italy
  2. 2Research Unit FREMAP Hospital, Madrid, Spain
  3. 3Centre for Sports and Exercise Medicine, Barts and The London School of Medicine and Dentistry, Mile End Hospital, London, UK
  1. Correspondence to Prof Nicola Maffulli, Centre Lead and Professor of Sports and Exercise Medicine, Consultant Trauma and Orthopaedic Surgeon, Centre for Sports and Exercise Medicine, Barts and The London School of Medicine and Dentistry, Mile End Hospital, 275 Bancroft Rd, London E1 4DG, UK; n.maffulli{at}qmul.ac.uk

Abstract

Objective In this study, the serum triglycerides and total serum cholesterol levels in patients with rotator cuff tear were determined.

Design Frequency-matched case-control study.

Setting University teaching hospital.

Participants 240 individuals who were operated on at our institution were included in the study. 120 patients (45 men and 75 women; mean age 64.86 years, range 40 to 83 years) who underwent arthroscopic repair of a rotator cuff tear were included in group 1. 120 patients (45 men and 75 women; mean age 63.91 years, range 38 to 78 years) who underwent arthroscopic meniscectomy for a meniscal tear and had no evidence of shoulder pathology were included in group 2 (control group). These patients were frequency-matched by age (within 3 years) and sex with patients of group 1.

Main outcome measures Measurement of serum triglyceride and total cholesterol concentrations.

Results When comparing the two groups, there was no difference either in serum triglyceride concentration or total serum cholesterol concentration.

Conclusions There appears to be no association between serum triglyceride concentration and total serum cholesterol concentration in rotator cuff tears.

https://doi.org/10.1136/bjsm.2008.056440

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    Rotator cuff pathology is a very common orthopaedic problem and is a cause of great healthcare costs in industrialised countries.1 2 Despite the relevance of the problem, the aetiology and pathogenesis of rotator cuff pathology remains unclear.3,–,5 Several theories of tendon injury have been proposed, and the incidence of rotator cuff tears increases with advancing age.6,–,10 Trauma to the shoulder is reported by up to 60% of patients, and the incidence is particularly high in overhead athletes (30%) and labourers (23%).11 Obesity12 and increased plasma glucose levels13 have been indicated as potential risk factors for rotator cuff tears. There are data on the possible relationship between high serum lipid concentration and complete rupture of the Achilles tendon.14 15 However, to our knowledge, no studies have focused on the correlation between serum lipid levels and rotator cuff tears.

    We therefore undertook a cross-sectional study of the serum triglyceride concentration and total serum cholesterol concentration in patients undergoing arthroscopic rotator cuff repair and compared them with a control group of patients of a similar age undergoing arthroscopic meniscectomy.

    Material and methods

    All procedures described in this study were approved by the ethics committee of our institution. All patients provided written informed consent according to the Declaration of Helsinki.

    The study included 240 individuals who were operated on at our institution. One hundred and forty participants (70 in the study group and 70 in the control group) from a previous investigation13 were included in this material, along with a further 100 participants.

    Group 1 included 120 patients (45 men and 75 women; mean age 64.86 years, range 40 to 83 years) (table 1) who underwent arthroscopic repair of a rotator cuff tear. The dominant arm was affected in 83 patients. The rotator cuff tears were classified as small (<1 cm) in 15 patients, medium (1 to 3 cm) in 30 patients, large (3 to 5 cm) in 43 patients, and massive (more than 5 cm) in 32 patients. The tear involved the supraspinatus tendon in 44 patients and the supraspinatus and infraspinatus tendons in 76 patients.

    View this table:
    Table 1

    Anthropometric measures

    Group 2 (control group) included 120 patients (45 men and 75 women; mean age 63.91 years, range 38 to 78 years) (table 1) who underwent arthroscopic meniscectomy for a meniscal tear with no history of rotator cuff symptoms.

    These patients were frequency-matched by age (within 3 years) and sex with patients of group 1.

    Patients in group 1 were included in the study if they had a rotator cuff tear diagnosed on clinical and imaging grounds and a rotator cuff tear found at the time of surgery. Conservative management, including non-steroidal anti-inflammatory drugs, physiotherapy and rest, failed in all patients, and they continued to experience unacceptable pain and weakness in the affected shoulder. None of the patients had undergone previous surgery on the affected shoulder. All patients fulfilled the following criteria: (1) positive rotator cuff lag signs on preoperative examination (at least one among Jobe, Napoleon, lift-off and Patte tests)16; (2) no episodes of shoulder instability; (3) no radiographic sign of fracture of the glenoid or the tuberosities; (4) MRI evidence of cuff tear; (5) rotator cuff tear of one or more tendons at arthroscopic examination; (6) no lesion of the glenoid labrum or of the capsule at arthroscopic examination.

    Patients in group 2 were included in the study if they had a meniscal tear diagnosed on clinical and imaging grounds and a meniscal tear found at the time of surgery.

    Exclusion criteria for all participants were: primary osteoarthritis of the operated or contralateral joint, previous operations on the shoulder or knee, inflammatory joint disease, hypertension, diabetes or hypercholesterolemia managed with statins. Patients in group 2 were also excluded from the study if they had history of shoulder pain, or rotator cuff pathology diagnosed by imaging or on clinical grounds.

    Anthropometric measurements

    Height and weight measurements of every patient were taken by the same examiner before blood sampling was performed; the body mass index (BMI) was calculated on the day of sampling (table 1).

    Measurement of total cholesterol and triglycerides

    All blood samples were collected in an identical manner between 07:00 and 07:30 after an overnight fast that started at 12:00 midnight. Biochemical analyses of blood were performed on fresh samples. Blood samples (5 ml) were collected from each patient into tubes (Vacutainer System, Becton Dickinson, New Jersey, USA), and were centrifuged at the relative centrifugal force of 2750 for 10 min. Sera were extracted from the samples, and the concentrations of total cholesterol (TC) and triglycerides (TG) were measured by enzymatic methods with the CIBA Corning 550 Express Autoanalyzer (Boehringer Mannheim, Mannheim, Germany). Patients were considered to have established hypercholesterolaemia at levels >6.2 mmol/l, and light hypercholesterolaemia at levels between 5.2 and 6.2 mmol/l.17 Patients were considered to have established hypertriglyceridaemia at levels >4.5 mmol/l.17

    Statistics

    Data were entered in a commercially available database. Descriptive statistics were calculated, and analytical statistics were performed with non-paired sample t test using SPSS (version 4). Significance was set at p<0.05.

    Results

    The serum concentrations of triglyceride and total cholesterol were measurable in all patients. We were not able to determine any significant differences in serum concentrations of triglyceride and total cholesterol in patients with small, medium, large and massive tears. Equally, there were no significant differences in serum concentrations of triglyceride or total cholesterol in patients with a supraspinatus tendon tear or supraspinatus and infraspinatus tendon tears. Therefore, for the purposes of this study, all tears were grouped together.

    When comparing the two groups, no statistically significant differences were present in neither triglyceride concentration (p = 0.6) nor total cholesterol concentration (p = 0.1) (tables 2 and 3).

    View this table:
    Table 2

    Levels of serum triglycerides

    View this table:
    Table 3

    Levels of total serum cholesterol

    Group 1

    In group 1 (rotator cuff tears), triglyceride concentration was >4.5 mmol/l in one patient. No patient underwent treatment for high serum triglyceride levels. In the same group, total cholesterol concentration was >6.2 mmol/l in 41 patients (34.1%). Light hypercholesterolaemia (5.2–6.2 mmol/l) was present in 42 patients (35%). No patient underwent treatment for high serum cholesterol levels.

    Group 2

    In group 2 (control group), triglyceride concentration was >4.5 mmol/l in one patient. No patient underwent treatment for high serum triglyceride levels. In the same group, total cholesterol concentration was >6.2 mmol/l in 33 patients (27.5%). Light hypercholesterolaemia (5.2–6.2 mmol/l) was present in 47 patients (39.2%). No patient underwent treatment for high serum cholesterol levels.

    Discussion

    Patients with a rotator cuff tear showed no statistically significant difference in serum triglyceride and total cholesterol concentrations when compared with individuals of the same age and sex undergoing arthroscopic meniscectomy and who had no history of rotator cuff injury. This is the first study, to our knowledge, to examine the serum triglyceride and total cholesterol concentrations in patients with rotator cuff tears. We have previously shown in a comparable population that increasing plasma glucose levels are associated with rotator cuff tears in patients in the higher range of “normal” group.13

    Strengths of the present study include the systematic collection of blood samples, the use of preoperative imaging and of arthroscopy to diagnose rotator cuff and meniscal tears, and the relatively large sample size of our study group. Nevertheless, we acknowledge the cross-sectional nature of the present investigation, which cannot completely resolve issues concerning temporality or rule out other factors that may influence rotator cuff tendinopathy. Another limitation of our study was that we have no data about high-density lipoprotein (HDL), low-density lipoprotein (LDL), and very low density lipoprotein (VLDL) concentrations in our patients. More detailed analysis could reveal lipoprotein abnormalities. The association between LDL and HDL cholesterol and the development of coronary heart disease is well established,18 and the management of coronary heart disease has traditionally focused on reduction of LDL cholesterol or of the total lipid profile.19 We do not know whether such strategies might exert a beneficial effect on tendon problems as well. We are fully aware that more anthropometric measures could be performed (eg, waist and hip girth, and skin-fold measurements). Unfortunately, we did not collect these data in our patients: this could be the subject of future endeavours.

    Ideally, the control group should have been constituted by healthy people. However, as this was a frequency-matched casecontrol study, if, on the one hand, it could have been relatively simple to find a healthy young person, the same would have not applied for an elderly person, especially given the stringent exclusion criteria in our study. Among the various diseases of the lower limb, we choose to enrol in the control group patients with pathology of the lower limb with a likely mechanic, not metabolic cause, different from tendon pathology. Classically, the causative mechanisms of rotator cuff pathology have been subdivided into extrinsic and intrinsic factors.20 Intrinsic factors focus on the pathologic changes lying predominantly within the tendon itself.21,–,23 Extrinsic factors are variables that interact to contribute to rotator cuff damage. They can be broadly grouped into anatomical (acromial morphologic characteristics, os acromiale and acromial spurs) and environmental factors (shoulder overuse, smoking, and any medical condition that impairs the inflammatory and healing response such as diabetes mellitus).20

    In a retrospective cohort study of 205 patients, Harvie et al24 showed a higher risk of symptomatic full-thickness rotator cuff tears in siblings of patients with rotator cuff tears versus controls, implying a role for genetic factors.25 There is an association between obesity and shoulder repair surgery in men and women aged 53 to 70 years, suggesting that increasing BMI is a risk factor for rotator cuff pathologies.12 Obesity could contribute to decreased vascularity through its associations with risk factors for vascular disease, such as elevated cholesterol,26 atherosclerosis,27 diabetes, hypertension, metabolic syndrome and decreased physical activity.28 A correlation between adiposity and rotator cuff tendinopathy has been proposed, but while the association with BMI and tendinopathy has been reported,12 there are no studies focused on serum levels of lipids and rotator cuff tendinopathy.

    What is already known on this topic

    • ▶. Tears of the rotator cuff cause high healthcare costs in industrialised countries.

    • ▶. The mechanisms underlying the aetiopathogenesis of rotator cuff disease remains poorly understood.

    • ▶. No studies have focused on the correlation between plasma serum total cholesterol and triglyceride concentrations and rotator cuff tears.

    What this study adds

    • ▶. There appears to be no association between serum triglycerides and total serum cholesterol levels and rotator cuff tears.

    • ▶. Additional research is required to improve our understanding of aetiopathogenesis of rotator cuff tears.

    A major histopathological feature of tendinopathy is a failed healing response.29 Accumulation of lipids and ground substance (glycosaminoglycans) and calcium deposits represent age-related changes of the tendon.30 During ageing, lipid accumulation is extracellular: lipids with a high content of esterified cholesterol spread along the longitudinal axis of collagen fibres. Lipid deposition disrupts the fibre bundles and may, through this mechanism, decrease tendon strength.30

    The association between tendon injury and adiposity has been examined.31 Elevated adiposity can be frequently associated with tendon injury,31 and it seems that elevated adiposity develops before tendon pathology, even though any definitive conclusion should be reached with caution.32 Although some evidences suggest that there is a possible association between tendinopathy of the lower limb and high cholesterol levels,14 15 we could not find similar results in our population of patients with rotator cuff tears. Moreover, while histopathological examination of specimens harvested during surgery for tendinopathy in the lower limb showed fatty degeneration or tendolipomatosis,33 we failed to show evidence of fatty degeneration in tendon samples from the rotator cuff3 and the long head of the biceps tendon.34 In addition, while there seems to be evidence of a possible role of high serum lipid concentration and complete rupture of the Achilles tendon,14 15 our data suggest no role of the serum cholesterol and triglyceride concentration in rotator cuff tears. We can speculate that, probably, the mechanisms underlying tendinopathy may be different in the lower or upper limbs, even though more studies are needed to confirm this preliminary statement.

    Some authors35 proposed the use of dietary supplements, including omega 3 fatty acids and antioxidants, in the management of tendinopathies, on the basis that high levels of cytokines, (ie, pro-inflammatory interleukin 1b and vascular endothelial growth factor) have been reported in the bursa of patients with rotator cuff pathology. The potential benefits of dietary supplementation in the management of tendinopathy35 36 need further research using appropriately designed, adequately powered, randomised controlled trial studies, with both objective and patient-centred outcome measures.

    On the basis of our study, we doubt that triglyceride serum levels and total serum cholesterol have a causative role in the pathogenesis of rotator cuff tears, even though we advocate more research to reach definitive conclusion. The study of the different fractions of serum cholesterol may shed further light, and is the subject of future research.

    In conclusion, there appears to be no association between serum lipid level and rotator cuff tears. Additional research is required to understand the causative role, if any, of serum triglyceride and total cholesterol concentrations in rotator cuff pathology.

    References

    1. ↵
      1. Ekberg K,
      2. Bjorkqvist B,
      3. Malm P,
      4. et al
      . Controlled two year follow up of rehabilitation for disorders in the neck and shoulders. Occup Environ Med 1994;51:833–8.
      OpenUrlAbstract/FREE Full Text
    2. ↵
      1. Meislin RJ,
      2. Sperling JW,
      3. Stitik TP
      . Persistent shoulder pain: epidemiology, pathophysiology, and diagnosis. Am J Orthop 2005;34:5–9.
      OpenUrlCrossRefPubMed
    3. ↵
      1. Longo UG,
      2. Franceschi F,
      3. Ruzzini L,
      4. et al
      . Histopathology of the supraspinatus tendon in rotator cuff tears. Am J Sports Med 2008;36:533–8.
      OpenUrlAbstract/FREE Full Text
    4. ↵
      1. Longo UG,
      2. Franceschi F,
      3. Ruzzini L,
      4. et al
      . Light microscopic histology of supraspinatus tendon ruptures. Knee Surg Sports Traumatol Arthrosc 2007;15:1390–4.
      OpenUrlCrossRefPubMedWeb of Science
    5. ↵
      1. Maffulli N,
      2. Longo UG,
      3. Denaro V
      . The pathogenesis and surgical treatment of tears of the rotator cuff. J Bone Joint Surg Br 2008. http://www.jbjs.org.uk/cgi/eletters/90-B/7/827#top (accessed 15 January 2009).
    6. ↵
      1. Lewis JS
      . Rotator cuff tendinopathy/subacromial impingement syndrome: Is it time for a new method of assessment? Br J Sports Med 2008;43:259–64.
      OpenUrlCrossRefPubMedWeb of Science
    7. ↵
      1. Lewis JS
      . Rotator cuff tendinopathy: a review. Br J Sports Med 2009;43:236–41.
      OpenUrlAbstract/FREE Full Text
    8. ↵
      1. Matthews TJ,
      2. Hand GC,
      3. Rees JL,
      4. et al
      . Pathology of the torn rotator cuff tendon. Reduction in potential for repair as tear size increases. J Bone Joint Surg Br 2006;88:489–95.
      OpenUrlCrossRefPubMed
    9. ↵
      1. Rees JD,
      2. Wilson AM,
      3. Wolman RL
      . Current concepts in the management of tendon disorders. Rheumatology (Oxford) 2006;45:508–21.
      OpenUrlAbstract/FREE Full Text
    10. ↵
      1. Rees JL
      . The pathogenesis and surgical treatment of tears of the rotator cuff. J Bone Joint Surg Br 2008;90:827–32.
      OpenUrlCrossRefPubMed
    11. ↵
      1. Maffulli N,
      2. Renström P,
      3. Leadbetter WB
      1. Blaine AT,
      2. Bigliani LU
      . Rotator cuff disorders: a North American perspective. In: Maffulli N, Renström P, Leadbetter WB eds. Tendon injuries: basic science and clinical medicine. London: Springer-Verlag, 2005:119–27.
    12. ↵
      1. Wendelboe AM,
      2. Hegmann KT,
      3. Gren LH,
      4. et al
      . Associations between body-mass index and surgery for rotator cuff tendinitis. J Bone Joint Surg Am 2004;86-A:743–7.
    13. ↵
      1. Longo UG,
      2. Franceschi F,
      3. Ruzzini L,
      4. et al
      . Higher fasting plasma glucose levels within the normoglycemic range and rotator cuff tears. Br J Sports Med 2008;43:284–7.
      OpenUrlCrossRefPubMedWeb of Science
    14. ↵
      1. Mathiak G,
      2. Wening JV,
      3. Mathiak M,
      4. et al
      . Serum cholesterol is elevated in patients with Achilles tendon ruptures. Arch Orthop Trauma Surg 1999;119:280–4.
      OpenUrlCrossRefPubMedWeb of Science
    15. ↵
      1. Ozgurtas T,
      2. Yildiz C,
      3. Serdar M,
      4. et al
      . Is high concentration of serum lipids a risk factor for Achilles tendon rupture? Clin Chim Acta 2003;331:25–8.
      OpenUrlCrossRefPubMedWeb of Science
    16. ↵
      1. Reider B
      1. Reider B
      . The orthopaedic physical examination. Reider B ed. Philadelphia: Saunders, 2005:17–66.
    17. ↵
      1. Andreoli M
      . Manuale medico di endocrinologia a metabolismo. Il Pensiero Scientifico 2000:691–718.
    18. ↵
      1. Gotto AM
      . Triglyceride as a risk factor for coronary artery disease. Am J Cardiol 1998;5:22Q–25Q.
      OpenUrl
    19. ↵
      1. Schaefer EJ,
      2. Asztalos BF
      . The effects of statins on high-density lipoproteins. Curr Atheroscler Rep 2006;8:41–9.
      OpenUrlPubMed
    20. ↵
      1. Nho SJ,
      2. Yadav H,
      3. Shindle MK,
      4. et al
      . Rotator cuff degeneration: etiology and pathogenesis. Am J Sports Med 2008;36:987–93.
      OpenUrlAbstract/FREE Full Text
    21. ↵
      1. Longo UG,
      2. Olivia F,
      3. Denaro V,
      4. et al
      . Oxygen species and overuse tendinopathy in athletes. Disabil Rehabil 2008;30:1563–71.
      OpenUrlCrossRefPubMedWeb of Science
    22. ↵
      1. Millar NL,
      2. Wei AQ,
      3. Molloy TJ,
      4. et al
      . Heat shock protein and apoptosis in supraspinatus tendinopathy. Clin Orthop Relat Res 2008;466:1569–76.
      OpenUrlCrossRefPubMedWeb of Science
    23. ↵
      1. Xu Y,
      2. Murrell GA
      . The basic science of tendinopathy. Clin Orthop Relat Res 2008;466:1528–38.
      OpenUrlCrossRefPubMedWeb of Science
    24. ↵
      1. Harvie P,
      2. Ostlere SJ,
      3. Teh J,
      4. et al
      . Genetic influences in the aetiology of tears of the rotator cuff. Sibling risk of a full-thickness tear. J Bone Joint Surg Br 2004;86:696–700.
      OpenUrlCrossRefPubMed
    25. ↵
      1. Magra M,
      2. Maffulli N
      . Genetics: does it play a role in tendinopathy? Clin J Sport Med 2007;17:231–3.
      OpenUrlCrossRefPubMedWeb of Science
    26. ↵
      1. Kim KS,
      2. Owen WL,
      3. Williams D,
      4. et al
      . A comparison between BMI and conicity index on predicting coronary heart disease: the Framingham Heart Study. Ann Epidemiol 2000;10:424–31.
      OpenUrlCrossRefPubMedWeb of Science
    27. ↵
      1. Hubert HB,
      2. Feinleib M,
      3. McNamara PM,
      4. et al
      . Obesity as an independent risk factor for cardiovascular disease: a 26-year follow-up of participants in the Framingham Heart Study. Circulation 1983;67:968–77.
      OpenUrlAbstract/FREE Full Text
    28. ↵
      1. Siervogel RM,
      2. Wisemandle W,
      3. Maynard LM,
      4. et al
      . Lifetime overweight status in relation to serial changes in body composition and risk factors for cardiovascular disease: the Fels Longitudinal Study. Obes Res 2000;8:422–30.
      OpenUrlPubMedWeb of Science
    29. ↵
      1. Maffulli N,
      2. Longo UG,
      3. Franceschi F,
      4. et al
      . Movin and Bonar scores assess the same characteristics of tendon histology. Clin Orthop Relat Res 2008;466:1605–11.
      OpenUrlCrossRefPubMedWeb of Science
    30. ↵
      1. Maffulli N,
      2. Renström P,
      3. Leadbetter WB
      1. Kannus P,
      2. Paavola M,
      3. Józsa L
      . Aging and degeneration of tendons. In: Maffulli N, Renström P, Leadbetter WB eds. Tendon injuries: basic science and clinical medicine. London: Springer-Verlag, 2005:25–31.
    31. ↵
      1. Gaida JE,
      2. Cook JL,
      3. Bass SL
      . Adiposity and tendinopathy. Disabil Rehabil 2008;30:1555–62.
      OpenUrlCrossRefPubMedWeb of Science
    32. ↵
      1. Gaida JE,
      2. Ashe MC,
      3. Bass SL,
      4. et al
      . Is adiposity an under-recognised risk factor for tendinopathy? A systematic review. Arthritis Care Res 2009;61:840–9.
      OpenUrlCrossRefWeb of Science
    33. ↵
      1. Kannus P,
      2. Jozsa L
      . Histopathological changes preceding spontaneous rupture of a tendon. A controlled study of 891 patients. J Bone Joint Surg Am 1991;73:1507–25.
      OpenUrlPubMed
    34. ↵
      1. Longo UG,
      2. Franceschi F,
      3. Ruzzini L,
      4. et al
      . Characteristics at haematoxylin and eosin staining of ruptures of the long head of the biceps tendon. Br J Sports Med 2007 2009;43:603–7.
      OpenUrlAbstract/FREE Full Text
    35. ↵
      1. Lewis JS,
      2. Sandford FM
      . Rotator cuff tendinopathy: is there a role for polyunsaturated fatty acids and antioxidants? J Hand Ther 2008;22:49–55.
      OpenUrlCrossRefPubMedWeb of Science
    36. ↵
      1. Mavrogenis S,
      2. Johannessen E,
      3. Jensen P,
      4. et al
      . The effect of essential fatty acids and antioxidants combined with physiotherapy treatment in recreational athletes with chronic tendon disorders. A randomised, double-blind, placebo-controlled study. Phys Ther Sport 2004;5:194–9.
      OpenUrlWeb of Science

    Footnotes

    • Competing interests None.

    • Ethics approval All procedures described in this study were approved by the Ethics Committee of our institution.

    • Provenance and peer review Not commissioned; externally peer reviewed.