Skip to main content

Extensor/flexor ratio of neck muscle strength and electromyographic activity of individuals with migraine: a cross-sectional study

Abstract

Purpose

Neck pain is considered a common characteristic of migraine attacks. The relationship between neck pain and migraine can be explained by central sensitization of the trigeminocervical complex, where superior cervical afferents and the trigeminal nerve converge. However, few studies have evaluated motor control of cervical muscles in individuals with migraine. Thus, the purpose of the present study was to determine the extensor/flexor ratio of neck muscle strength and electromyographic activity during a test of maximal voluntary isometric contraction and craniocervical flexion in individuals with migraine and individuals without history of migraine or other headaches.

Methods

Fifty-two women with the disease and 52 women with neither a history of migraine nor neck pain, between 18 and 55 years old, were included in the study. The electromyographic activities of the sternocleidomastoid, anterior scalene, splenius capitis, and upper trapezius muscles were evaluated during a test of maximal voluntary isometric contraction and craniocervical flexion.

Results

The migraine group presented lower flexor muscle strength and a higher extensor/flexor muscle strength ratio than the control group. In addition, the migraine group showed a reduced electromyographic extensor/flexor muscle ratio during maximal voluntary isometric contraction in flexion. The results demonstrated worse performance in the craniocervical flexion test of the migraine group and a lower electromyographic ratio of extensor/flexor neck muscles in the last stage of the test.

Conclusion

Altogether, the migraine group presented an imbalance in cervical muscles verified not only during force production, but also during muscle activity.

Graphic abstract

These slides can be retrieved under Electronic Supplementary Material.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Goadsby PJ, Holland PR, Martins-Oliveira M, Hoffmann J, Schankin C, Akerman S (2017) Pathophysiology of migraine: a disorder of sensory processing. Physiol Rev 97(2):553–622. https://doi.org/10.1152/physrev.00034.2015

    Article  PubMed  PubMed Central  Google Scholar 

  2. Smith TR, Nicholson RA, Banks JW (2010) Migraine educations improves quality of life in a primary care setting. Headache 50(4):600–612. https://doi.org/10.1111/j.1526-4610.2010.01618.x

    Article  PubMed  PubMed Central  Google Scholar 

  3. Kassebaum NJ, Arora M, Barber RM et al (2016) Global, regional, and national disability-adjusted life-years (DALYs) for 315 diseases and injuries and healthy life expectancy (HALE), 1990–2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet 388(10053):1603–1658. https://doi.org/10.1016/S0140-6736(16)31460-X

    Article  Google Scholar 

  4. Lampl C, Rudolph M, Deligianni CI, Mitsikostas DD (2015) Neck pain in episodic migraine: premonitory symptom or part of the attack? J Headache Pain 16:566. https://doi.org/10.1186/s10194-015-0566-9

    Article  PubMed  Google Scholar 

  5. Lipton RB, Fanning KM, Buse DC, Martin VT, Reed ML, Manack Adams A, Goadsby PJ (2018) Identifying natural subgroups of migraine based on comorbidity and concomitant condition profiles: results of the chronic migraine epidemiology and outcomes (CaMEO) study. Headache 58(7):933–947. https://doi.org/10.1111/head.13342

    Article  PubMed  Google Scholar 

  6. Charles A (2018) The pathophysiology of migraine: implications for clinical management. Lancet Neurol 17(2):174–182. https://doi.org/10.1016/S1474-4422(17)30435-0

    CAS  Article  PubMed  Google Scholar 

  7. Florencio LL, Oliveira AS, Lemos TW, Carvalho GF, Dach F, Bigal ME, Falla D, Fernández-de-las-Peñas C, Bevilaqua-Grossi D (2016) Patients with chronic, but not episodic, migraine display altered activity of their neck extensor muscles. J Electromyogr Kinesiol 30:66–72. https://doi.org/10.1016/j.jelekin.2016.06.003

    Article  PubMed  Google Scholar 

  8. Florencio LL, Oliveira AS, Carvalho GF, de Tolentino GA, Dach F, Bigal ME, Fernández-de-las-Peñas C, Bevilaqua-Grossi D (2015) Cervical muscle strength and muscle coactivation during isometric contractions in patients with migraine: a cross-sectional study. Headache 55(10):1312–1322. https://doi.org/10.1111/head.12644

    Article  PubMed  Google Scholar 

  9. Alpayci M, Şenköy E, Delen V, Şah V, Yazmalar L, Erden M, Toprak M, Kaplan Ş (2016) Decreased neck muscle strength in patients with the loss of cervical lordosis. Clin Biomech (Bristol, Avon) 33:98–102. https://doi.org/10.1016/j.clinbiomech.2016.02.014

    Article  Google Scholar 

  10. Madsen BK, Søgaard K, Andersen LL, Skotte JH, Jensen RH (2016) Neck and shoulder muscle strength in patients with tension-type headache: a case-control study. Cephalalgia 36(1):29–36. https://doi.org/10.1177/0333102415576726

    Article  PubMed  Google Scholar 

  11. Bokaee F, Rezasoltani A, Manshadi FD, Naimi SS, Baghban AA, Azimi H (2016) Comparison of isometric force of the craniocervical flexor and extensor muscles between women with and without forward head posture. Cranio 34(5):286–290. https://doi.org/10.1080/08869634.2016.1169616

    Article  PubMed  Google Scholar 

  12. Strimpakos N, Sakellari V, Gioftsos G, Oldham J (2004) Intratester and intertester reliability of neck isometric dynamometry. Arch Phys Med Rehabil 85(8):1309–1316

    Article  PubMed  Google Scholar 

  13. Headache Classification Committee of the International Headache Society (IHS) (2018) The International Classification of Headache Disorders, 3rd edition. Cephalalgia 38(1):1–211. https://doi.org/10.1177/0333102417738202

    Article  Google Scholar 

  14. Vernon H, Mior S (1991) The Neck Disability Index: a study of reliability and validity. J Manipulative Physiol Ther. 14(7):409–415

    CAS  PubMed  Google Scholar 

  15. Cook C, Richardson JK, Braga L, Menezes A, Soler X, Kume P, Zaninelli M, Socolows F, Pietrobon R (2006) Cross-cultural adaptation and validation of the Brazilian Portuguese version of the Neck Disability Index and Neck Pain and Disability Scale. Spine (Phila Pa 1976) 31(14):1621–1627

    Article  Google Scholar 

  16. Stewart WF, Lipton RB, Dowson AJ, Sawyer J (2001) Development and testing of the Migraine Disability Assessment (MIDAS) Questionnaire to assess headache-related disability. Neurology. 56(Suppl 1):S20–S28

    CAS  Article  PubMed  Google Scholar 

  17. Florencio LL, Chaves TC, Branisso LB, Gonçalves MC, Dach F, Speciali JG, Bigal ME, Bevilaqua-Grossi D (2012) 12 item allodynia symptom checklist/Brasil: cross-cultural adaptation, internal consistency and reproducibility. Arq Neuropsiquiatr. 70(11):852–856

    Article  PubMed  Google Scholar 

  18. Lipton RB, Bigal ME, Ashina S et al (2008) Cutaneous allodynia in the migraine population. Ann Neurol. 63(2):148–158

    Article  PubMed  PubMed Central  Google Scholar 

  19. Falla D, Dall'Alba P, Rainoldi A, Merletti R, Jull G (2002) Location of innervation zones of sternocleidomastoid and scalene muscles–a basis for clinical and research electromyography applications. Clin Neurophysiol. 113(1):57–63

    CAS  Article  PubMed  Google Scholar 

  20. Falla D, Farina D, Dahl MK, Graven-Nielsen T. Muscle pain induces task-dependent changes in cervical agonist/antagonist activity. J Appl Physiol 2007;102(2):601–9.

    CAS  Article  PubMed  Google Scholar 

  21. SENIAM. Recommendations for sensor locations on individual muscles. https://seniam.org/trapeziusdescendens.html. Accessed 03 July 2018

  22. Jull GA, O'Leary SP, Falla DL (2008) Clinical assessment of the deep cervical flexor muscles: the craniocervical flexion test. J Manipulative Physiol Ther. 31(7):525–533

    Article  PubMed  Google Scholar 

  23. Jull G, Amiri M, Bullock-Saxton J, Darnell R, Lander C (2007) Cervical musculoskeletal impairment in frequent intermittent headache. Part 1: Subjects with single headaches. Cephalalgia 27(7):793–802

    CAS  Article  PubMed  Google Scholar 

  24. Fernandez-de-las-Peñas C, Pérez-de-Heredia M, Molero-Sánchez A, Miangolarra-Page JC (2007) Performance of the craniocervical flexion test, forward head posture, and headache clinical parameters in patients with chronic tension-type headache: a pilot study. J Orthop Sports Phys Ther. 37(2):33–39

    Article  PubMed  Google Scholar 

  25. Luedtke K, Starke W, May A (2018) Musculoskeletal dysfunction in migraine patients. Cephalalgia 38(5):865–875

    Article  PubMed  Google Scholar 

  26. Benatto MT, Bevilaqua-Grossi D, Carvalho GF et al (2018) Kinesiophobia is associated with migraine. Pain Med. https://doi.org/10.1093/pm/pny206

    Article  Google Scholar 

  27. O'Leary S, Jull G, Kim M, Vicenzino B (2007) Cranio-cervical flexor muscle impairment at maximal, moderate, and low loads is a feature of neck pain. Man Ther 12(1):34–39

    Article  PubMed  Google Scholar 

  28. Patwardhan AG, Khayatzadeh S, Havey RM, Voronov LI et al (2018) Cervical sagittal balance: a biomechanical perspective can help clinical practice. Eur Spine J 27(Suppl 1):25–38

    Article  PubMed  Google Scholar 

  29. Eguchi Y, Suzuki M, Yamanaka H et al (2017) Associations between sarcopenia and degenerative lumbar scoliosis in older women. Scoliosis Spinal Disord 12:9

    Article  PubMed  PubMed Central  Google Scholar 

  30. Miyakoshi N, Hongo M, Mizutani Y, Shimada Y (2013) Prevalence of sarcopenia in Japanese women with osteopenia and osteoporosis. J Bone Miner Metab 31(5):556–561

    Article  PubMed  Google Scholar 

  31. Szikszay TM, Hoenick S, von Korn K et al (2019) Which examination tests detect differences in cervical musculoskeletal impairments in people with migraine? A systematic review and meta-analysis. Phys Ther. https://doi.org/10.1093/ptj/pzz007

    Article  PubMed  Google Scholar 

Download references

Funding

This project was funded by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (Process Numbers 2016/14621-5 and 2018/17191-7).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mariana Tedeschi Benatto.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

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

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (PPTX 134 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Benatto, M.T., Florencio, L.L., Bragatto, M.M. et al. Extensor/flexor ratio of neck muscle strength and electromyographic activity of individuals with migraine: a cross-sectional study. Eur Spine J 28, 2311–2318 (2019). https://doi.org/10.1007/s00586-019-06097-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00586-019-06097-9

Keywords

  • Migraine disorders
  • Electromyographic
  • Neck pain
  • Extension/flexion ratio