Skip to main content
SpringerLink
Log in

The influence of a multidisciplinary intervention program on Achilles tendon structure in children with overweight and obesity

  • Original Article
  • Published:
European Journal of Pediatrics Aims and scope Submit manuscript

Abstract

The effects of childhood obesity on tendon structure and its relation to physical activity are barely known. We aimed to investigate the influence of a 6-month multidisciplinary childhood obesity management program (which included dietary intervention and an exercise program) on Achilles tendon structure in overweight/obese children. Twenty-five overweight/obese children (overweight group) who participated in a 6-month multidisciplinary childhood obesity program, and 27 normal-weight controls were examined for anthropometric measurements and for Achilles tendon structure (using ultrasound tissue characterization to capture a three-dimensional structure of four echo type fibers and the cross-sectional area) at baseline, 3, and 6 months. The BMI of the overweight group significantly decreased from the pre- to the post-intervention period, (p = .002, η2 = .229), yet among the control group, the BMI significantly increased (p = .002, η2 = .222). Interactions (pre-post × group) showed a significant decrease in the prevalence of echo type I and in echo type III fibers and a significant increase in the prevalence of echo type II fibers and in the cross-sectional area along the intervention. No significant changes in echo type fibers were found in the control group along the 6 months.

Conclusion: At pre-intervention, the overweight group had significantly “worse” tendon structure, with a lower prevalence of echo type II fiber and a higher prevalence of echo type III fibers compared with the control group. Following the 6-month intervention, the tendon structure of the overweight group was “positively” changed, with reduced echo type III fibers and increased echo type II fibers.

What is Known:

• Physical activity and weight reduction programs are efficient for obese children.

• Obese children tend to suffer orthopedic problems and pain during physical activity.

What is New:

• Pre-intervention, obese children had ‘worse’ tendon structure compared to controls.

• Following 6-month program, tendon structure of obese children ‘positively’ changed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

BMI:

Body mass index

CSA:

Cross-sectional area

LT:

Left

RT:

Right

References

  1. Dietz WH (2011) Reversing the tide of obesity. Lancet 378(9793):744–746. https://doi.org/10.1016/S0140-6736(11)61218-X

    Article  PubMed  Google Scholar 

  2. Horsak B, Artner D, Baca A, Pobatschnig B, Greber-Platzer S, Nehrer S, Wondrasch B (2015) The effects of a strength and neuromuscular exercise programme for the lower extremity on knee load, pain and function in obese children and adolescents: study protocol for a randomised controlled trial. Trials 16:586. https://doi.org/10.1186/s13063-015-1091-5

    Article  PubMed  PubMed Central  Google Scholar 

  3. Tsiros MD, Buckley JD, Howe PR et al (2014) Musculoskeletal pain in obese compared with healthy-weight children. Clin J Pain 30(7):583–588. https://doi.org/10.1097/AJP.0000000000000017

    Article  PubMed  Google Scholar 

  4. Rubinstein M, Eliakim A, Steinberg N, et al (2018) Biomechanical characteristics of overweight and obese children during five different walking and running velocities. Foottwear Science;In Press

  5. Taylor ED, Theim KR, Mirch MC, Ghorbani S, Tanofsky-Kraff M, Adler-Wailes DC, Brady S, Reynolds JC, Calis KA, Yanovski JA (2006) Orthopedic complications of overweight in children and adolescents. Pediatrics 117(6):2167–2174. https://doi.org/10.1542/peds.2005-1832

    Article  PubMed  PubMed Central  Google Scholar 

  6. Sundin BA, Moreno E, Neher JO et al (2015) FPIN’s clinical inquiries. Obesity and joint injuries in children. Am Fam Physician 91(5):320–322

    PubMed  Google Scholar 

  7. Wearing SC, Hennig EM, Byrne NM, Steele JR, Hills AP (2006) The impact of childhood obesity on musculoskeletal form. Obesity reviews : an official journal of the International Association for the Study of Obesity 7(2):209–218. https://doi.org/10.1111/j.1467-789X.2006.00216.x

    Article  CAS  Google Scholar 

  8. Biancalana A, Velloso LA, Taboga SR, Gomes L (2012) Implications of obesity for tendon structure, ultrastructure and biochemistry: a study on Zucker rats. Micron 43(2–3):463–469. https://doi.org/10.1016/j.micron.2011.11.002

    Article  CAS  PubMed  Google Scholar 

  9. Abate M, Di Gregorio P, Schiavone C et al (2012) Platelet rich plasma in tendinopathies: how to explain the failure. Int J Immunopathol Pharmacol 25(2):325–334. https://doi.org/10.1177/039463201202500202

    Article  CAS  PubMed  Google Scholar 

  10. Heinemeier KM, Kjaer M (2011) In vivo investigation of tendon responses to mechanical loading. J Musculoskelet Neuronal Interact 11(2):115–123

    CAS  PubMed  Google Scholar 

  11. Magnusson SP, Langberg H, Kjaer M (2010) The pathogenesis of tendinopathy: balancing the response to loading. Nat Rev Rheumatol 6(5):262–268. https://doi.org/10.1038/nrrheum.2010.43

    Article  PubMed  Google Scholar 

  12. Reb CW, Schick FA, Karanjia HN, Daniel JN (2015) High prevalence of obesity and female gender among patients with concomitant Tibialis posterior tendonitis and plantar fasciitis. Foot Ankle Spec 8(5):364–368. https://doi.org/10.1177/1938640015583511

    Article  PubMed  Google Scholar 

  13. Abate M, Oliva F, Schiavone C, Salini V (2012) Achilles tendinopathy in amateur runners: role of adiposity (tendinopathies and obesity). Muscles Ligaments Tendons J 2(1):44–48

    PubMed  PubMed Central  Google Scholar 

  14. Gaida JE, Ashe MC, Bass SL, Cook JL (2009) Is adiposity an under-recognized risk factor for tendinopathy? A systematic review. Arthritis Rheum 61(6):840–849. https://doi.org/10.1002/art.24518

    Article  PubMed  Google Scholar 

  15. Park HS, Park JY, Yu R (2005) Relationship of obesity and visceral adiposity with serum concentrations of CRP, TNF-alpha and IL-6. Diabetes Res Clin Pract 69(1):29–35. https://doi.org/10.1016/j.diabres.2004.11.007

    Article  CAS  PubMed  Google Scholar 

  16. Abate M, Silbernagel KG, Siljeholm C et al (2009) Pathogenesis of tendinopathies: inflammation or degeneration? Arthritis Res Ther 11(3):235. https://doi.org/10.1186/ar2723

    Article  PubMed  PubMed Central  Google Scholar 

  17. Fakoya AOJ, Otohinoyi DA, Fakoya FA (2018) Correlation of some predisposing intrinsic conditions with the morphological integrity of the Achilles tendon. Ann Afr Med 17(2):58–63. https://doi.org/10.4103/aam.aam_49_17

    Article  PubMed  PubMed Central  Google Scholar 

  18. van Schie HT, de Vos RJ, de Jonge S et al (2010) Ultrasonographic tissue characterisation of human Achilles tendons: quantification of tendon structure through a novel non-invasive approach. Br J Sports Med 44(16):1153–1159. https://doi.org/10.1136/bjsm.2009.061010

    Article  PubMed  Google Scholar 

  19. van Ark M, Docking SI, van den Akker-Scheek I, Rudavsky A, Rio E, Zwerver J, Cook JL (2016) Does the adolescent patellar tendon respond to 5 days of cumulative load during a volleyball tournament? Scand J Med Sci Sports 26(2):189–196. https://doi.org/10.1111/sms.12426

    Article  PubMed  Google Scholar 

  20. Rosengarten SD, Cook JL, Bryant AL, Cordy JT, Daffy J, Docking SI (2015) Australian football players’ Achilles tendons respond to game loads within 2 days: an ultrasound tissue characterisation (UTC) study. Br J Sports Med 49(3):183–187. https://doi.org/10.1136/bjsports-2013-092713

    Article  PubMed  Google Scholar 

  21. de Sa A, Hart DA, Khan K et al (2018) Achilles tendon structure is negatively correlated with body mass index, but not influenced by statin use: a cross-sectional study using ultrasound tissue characterization. PLoS One 13(6):e0199645. https://doi.org/10.1371/journal.pone.0199645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Nemet D, Barkan S, Epstein Y, Friedland O, Kowen G, Eliakim A (2005) Short- and long-term beneficial effects of a combined dietary-behavioral-physical activity intervention for the treatment of childhood obesity. Pediatrics 115(4):e443–e449. https://doi.org/10.1542/peds.2004-2172

    Article  PubMed  Google Scholar 

  23. Cole TJ, Bellizzi MC, Flegal KM, Dietz WH (2000) Establishing a standard definition for child overweight and obesity worldwide: international survey. Bmj 320(7244):1240–1243. https://doi.org/10.1136/bmj.320.7244.1240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Nemet D, Oren S, Pantanowitz M, Eliakim A (2013) Effects of a multidisciplinary childhood obesity treatment intervention on adipocytokines, inflammatory and growth mediators. Horm Res Paediatr 79(6):325–332. https://doi.org/10.1159/000348732

    Article  CAS  PubMed  Google Scholar 

  25. Kuczmarski RJ, Ogden CL, Grummer-Strawn LM et al (2000) CDC growth charts: United States. Adv Data 314:1–27

    Google Scholar 

  26. van Schie HT, Bakker EM, Jonker AM et al (2003) Computerized ultrasonographic tissue characterization of equine superficial digital flexor tendons by means of stability quantification of echo patterns in contiguous transverse ultrasonographic images. Am J Vet Res 64(3):366–375

    Article  Google Scholar 

  27. Masci L, Spang C, van Schie HT et al (2015) Achilles tendinopathy-do plantaris tendon removal and Achilles tendon scraping improve tendon structure? A prospective study using ultrasound tissue characterisation. BMJ Open Sport Exerc Med 1(1):e000005. https://doi.org/10.1136/bmjsem-2015-000005

    Article  PubMed  PubMed Central  Google Scholar 

  28. Docking SI, Cook J (2016) Pathological tendons maintain sufficient aligned fibrillar structure on ultrasound tissue characterization (UTC). Scand J Med Sci Sports 26(6):675–683. https://doi.org/10.1111/sms.12491

    Article  CAS  PubMed  Google Scholar 

  29. Steinberg N, Eliakim A, Elbaz L, Pantanowitz M, Zeev A, Nemet D (2019) Achilles tendon tissue structure in children with overweight and children with obesity. Phys Occup Ther Pediatr 40:1–15. https://doi.org/10.1080/01942638.2019.1672848

    Article  Google Scholar 

  30. Seynnes OR, Erskine RM, Maganaris CN et al (2009) Training-induced changes in structural and mechanical properties of the patellar tendon are related to muscle hypertrophy but not to strength gains. J Appl Physiol (1985) 107(2):523–530. https://doi.org/10.1152/japplphysiol.00213.2009

    Article  CAS  Google Scholar 

  31. Abate M, Verna S, Di Gregorio P et al (2014) Sonographic findings during and after platelet rich plasma injections in tendons. Muscles Ligaments Tendons J 4(1):29–34

    Article  Google Scholar 

  32. Scott A, Zwerver J, Grewal N, de Sa A, Alktebi T, Granville DJ, Hart DA (2015) Lipids, adiposity and tendinopathy: is there a mechanistic link? Critical review. Br J Sports Med 49(15):984–988. https://doi.org/10.1136/bjsports-2014-093989

    Article  PubMed  Google Scholar 

  33. Docking SI, Rosengarten SD, Daffy J, Cook J (2015) Structural integrity is decreased in both Achilles tendons in people with unilateral Achilles tendinopathy. J Sci Med Sport 18(4):383–387. https://doi.org/10.1016/j.jsams.2014.06.004

    Article  PubMed  Google Scholar 

  34. Waugh CM, Blazevich AJ, Fath F, Korff T (2012) Age-related changes in mechanical properties of the Achilles tendon. J Anat 220(2):144–155. https://doi.org/10.1111/j.1469-7580.2011.01461.x

    Article  CAS  PubMed  Google Scholar 

  35. Malina R, Bouchard C, Bar-Or O (2004) Growth, maturation and physical activity, 2nd edn. Human Kinetics, Champaign

    Book  Google Scholar 

  36. Mersmann F, Bohm S, Schroll A, Boeth H, Duda GN, Arampatzis A (2017) Muscle and tendon adaptation in adolescent athletes: a longitudinal study. Scand J Med Sci Sports 27(1):75–82. https://doi.org/10.1111/sms.12631

    Article  CAS  PubMed  Google Scholar 

  37. Maciel Rabello L, Zwerver J, Stewart RE, den Akker-Scheek I, Brink MS (2019) Patellar tendon structure responds to load over a 7-week preseason in elite male volleyball players. Scand J Med Sci Sports 29(7):992–999. https://doi.org/10.1111/sms.13428

    Article  PubMed  PubMed Central  Google Scholar 

  38. Waugh CM, Alktebi T, de Sa A, Scott A (2018) Impact of rest duration on Achilles tendon structure and function following isometric training. Scand J Med Sci Sports 28(2):436–445. https://doi.org/10.1111/sms.12930

    Article  CAS  PubMed  Google Scholar 

  39. Waugh CM, Korff T, Fath F et al (2014) Effects of resistance training on tendon mechanical properties and rapid force production in prepubertal children. J Appl Physiol (1985) 117(3):257–266. https://doi.org/10.1152/japplphysiol.00325.2014

    Article  CAS  PubMed Central  Google Scholar 

  40. Wong AM, Docking SI, Cook JL et al (2015) Does type 1 diabetes mellitus affect Achilles tendon response to a 10 km run? A case control study. BMC Musculoskelet Disord 16:345. https://doi.org/10.1186/s12891-015-0803-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Rabello LM, van den Akker-Scheek I, Kuipers IF, Diercks RL, Brink MS, Zwerver J (2019) Bilateral changes in tendon structure of patients diagnosed with unilateral insertional or midportion Achilles tendinopathy or patellar tendinopathy. Knee Surg Sports Traumatol Arthrosc 28:1631–1638. https://doi.org/10.1007/s00167-019-05495-2

    Article  PubMed  PubMed Central  Google Scholar 

  42. Esmaeili A, Stewart AM, Hopkins WG, Elias GP, Aughey RJ (2017) Effects of training load and leg dominance on Achilles and patellar tendon structure. Int J Sports Physiol Perform 12(Suppl 2):S2122–S2S26. https://doi.org/10.1123/ijspp.2016-0397

    Article  PubMed  Google Scholar 

  43. Stanley LE, Lucero A, Mauntel TC, Kennedy M, Walker N, Marshall SW, Padua DA, Berkoff DJ (2018) Achilles tendon adaptation in cross-country runners across a competitive season. Scand J Med Sci Sports 28(1):303–310. https://doi.org/10.1111/sms.12903

    Article  CAS  PubMed  Google Scholar 

  44. Cook JL, Rio E, Purdam CR, Docking SI (2016) Revisiting the continuum model of tendon pathology: what is its merit in clinical practice and research? Br J Sports Med 50(19):1187–1191. https://doi.org/10.1136/bjsports-2015-095422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Rudavsky A, Cook J, Docking S (2018) Quantifying proximal patellar tendon changes during adolescence in elite ballet dancers, a 2-year study. Scand J Med Sci Sports 28(11):2369–2374. https://doi.org/10.1111/sms.13235

    Article  CAS  PubMed  Google Scholar 

  46. O’Brien TD, Reeves ND, Baltzopoulos V et al (2010) Mechanical properties of the patellar tendon in adults and children. J Biomech 43(6):1190–1195. https://doi.org/10.1016/j.jbiomech.2009.11.028

    Article  PubMed  Google Scholar 

  47. Kongsgaard M, Qvortrup K, Larsen J, Aagaard P, Doessing S, Hansen P, Kjaer M, Magnusson SP (2010) Fibril morphology and tendon mechanical properties in patellar tendinopathy: effects of heavy slow resistance training. Am J Sports Med 38(4):749–756. https://doi.org/10.1177/0363546509350915

    Article  PubMed  Google Scholar 

  48. Cassel M, Baur H, Hirschmuller A et al (2015) Prevalence of Achilles and patellar tendinopathy and their association to intratendinous changes in adolescent athletes. Scand J Med Sci Sports 25(3):e310–e318. https://doi.org/10.1111/sms.12318

    Article  CAS  PubMed  Google Scholar 

  49. Adamo KB, Wilson S, Harvey AL et al (2016) Does intervening in childcare settings impact fundamental movement skill development? Med Sci Sports Exerc 48(5):926–932. https://doi.org/10.1249/MSS.0000000000000838

    Article  PubMed  Google Scholar 

  50. Tsiros MD, Coates AM, Howe PR et al (2011) Obesity: the new childhood disability? Obesity reviews : an official journal of the International Association for the Study of Obesity 12(1):26–36. https://doi.org/10.1111/j.1467-789X.2009.00706.x

    Article  CAS  Google Scholar 

  51. Pauwaert K, Dejonckheere S, Bruneel E, Van Der Jeugt J, Keersmaekers L, Roggeman S, De Guchtenaere A, Vande Walle J, Everaert K (2019) The effect of a multidisciplinary weight loss program on renal circadian rhythm in obese adolescents. Eur J Pediatr 178(12):1849–1858

  52. Riethmuller AM, Jones R, Okely AD (2009) Efficacy of interventions to improve motor development in young children: a systematic review. Pediatrics 124(4):e782–e792. https://doi.org/10.1542/peds.2009-0333

    Article  PubMed  Google Scholar 

  53. Steinberg N, Rubinstein M, Nemet D, Ayalon M, Zeev A, Pantanowitz M, Brosh T, Eliakim A (2017) Effects of a program for improving biomechanical characteristics during walking and running in children who are obese. Pediatric physical therapy : the official publication of the Section on Pediatrics of the American Physical Therapy Association 29(4):330–340. https://doi.org/10.1097/PEP.0000000000000440

    Article  Google Scholar 

  54. Gómez SF, Casas Esteve R, Subirana I, Serra-Majem L, Fletas Torrent M, Homs C, Bawaked RA, Estrada L, Fíto M, Schröder H (2018) Effect of a community-based childhood obesity intervention program on changes in anthropometric variables, incidence of obesity, and lifestyle choices in Spanish children aged 8 to 10 years. Eur J Pediatr 177(10):1531–1539

Download references

Author information

Authors and Affiliations

  1. The Wingate College of Physical Education and Sport Sciences, Wingate Institute, Netanya, Israel

    Nili Steinberg, Liav Elbaz, Michal Pantanowitz & Aviva Zeev

  2. Child Health and Sport Center, Pediatric Department, Meir Medical Center, Sackler School of Medicine, Tel Aviv University, Tel Aviv, Israel

    Alon Eliakim, Michal Pantanowitz & Dan Nemet

Authors
  1. Nili Steinberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alon Eliakim
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Liav Elbaz
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Michal Pantanowitz
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Aviva Zeev
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Dan Nemet
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

N.S. study conception and design; material preparation, data collection and analysis; write, read and approved the final manuscript.

A.E. study conception and design; material preparation and data analysis; write, read and approved the final manuscript.

L.E. study conception and design; material preparation, data collection and analysis; read and approved the final manuscript.

A.Z. study conception and design; material preparation and data analysis; read and approved the final manuscript.

M.P. study conception and design; material preparation; read and approved the final manuscript.

D.N. study conception and design; material preparationdata analysis; write, read and approved the final manuscript.

Corresponding author

Correspondence to Nili Steinberg.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

The study was approved by the institutional review board of the Meir Medical Center, Tel Aviv University, Israel.

Informed consent

Informed consent was obtained from all children and parents of children included in the study.

Additional information

Communicated by Gregorio Paolo Milani

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Steinberg, N., Eliakim, A., Elbaz, L. et al. The influence of a multidisciplinary intervention program on Achilles tendon structure in children with overweight and obesity. Eur J Pediatr 179, 1787–1796 (2020). https://doi.org/10.1007/s00431-020-03685-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00431-020-03685-6

Keywords

Search

Navigation