Advanced search
Publication Cover
Expert Review of Obstetrics & Gynecology Volume 8, 2013 - Issue 3
Journal homepage
1,438
Views
5
CrossRef citations to date
0
Altmetric
Review

Safety and efficacy of the levonorgestrel-releasing intrauterine system: recent insights

Kristina Gemzell-Danielsson Department of Women’s and Children’s Health, Division of Obstetrics and Gynecology, Karolinska Institutet/Karolinska University Hospital, Solna, 171 76 Stockholm, Sweden. [email protected]; Department of Women’s and Children’s Health, Division of Obstetrics and Gynecology, Karolinska Institutet/Karolinska University Hospital, Solna, 171 76 Stockholm, Sweden. [email protected]
,
Pirjo Inki Bayer HealthCare Pharmaceuticals AG, Berlin, Germany; Bayer HealthCare Pharmaceuticals AG, Berlin, Germany
&
Oskari Heikinheimo Department of Obstetrics and Gynecology, Helsinki University Central Hospital, Helsinki, Finland; Department of Obstetrics and Gynecology, Helsinki University Central Hospital, Helsinki, Finland
Pages 235-247 | Published online: 10 Jan 2014

References

  • Thonneau PF, Almont T, Almont TE. Contraceptive efficacy of intrauterine devices. Am. J. Obstet. Gynecol. 198(3), 248–253 (2008).
  • Winner B, Peipert JF, Zhao Q et al. Effectiveness of long-acting reversible contraception. N. Engl. J. Med. 366(21), 1998–2007 (2012).
  • Römer T, Linsberger D. User satisfaction with a levonorgestrel-releasing intrauterine system (LNG-IUS): data from an international survey. Eur. J. Contracept. Reprod. Health Care 14(6), 391–398 (2009).
  • Peipert JF, Madden T, Allsworth JE, Secura GM. Preventing unintended pregnancies by providing no-cost contraception. Obstet. Gynecol. 120(6), 1291–1297 (2012).
  • ACOG Practice Bulletin. Clinical management guidelines for obstetricians–gynecologists no. 73 June 2006: use of hormonal contraception in women with coexisting medical conditions. Obstet. Gynecol. 107 (1453–1472) 2006.
  • Gemzell-Danielsson K, Inki P, Heikinheimo O. Recent developments in the clinical use of the levonorgestrel-releasing intrauterine system. Acta Obstet. Gynecol. Scand. 90(11), 1177–1188 (2011).
  • Heikinheimo O, Gemzell-Danielsson K. Emerging indications for the levonorgestrel-releasing intrauterine system (LNG-IUS). Acta Obstet. Gynecol. Scand. 91(1), 3–9 (2012).
  • Mattinson A, Mansour D. Female sterilisation: is it what women really want or are alternative contraceptive methods acceptable? J. Fam. Plann. Reprod. Health Care 32(3), 181–183 (2006).
  • Jensen JT, Nelson AL, Costales AC. Subject and clinician experience with the levonorgestrel-releasing intrauterine system. Contraception 77(1), 22–29 (2008).
  • National Institute for Health and Clinical Excellence. Long-acting reversible contraception. Clinical Guideline 30 developed by the National Collaborating Centre for Women’s and Children’s Health. London, UK (2005).
  • Lete I, Cristóbal I, Febrer L et al. Economic evaluation of the levonorgestrel-releasing intrauterine system for the treatment of dysfunctional uterine bleeding in Spain. Eur. J. Obstet. Gynecol. Reprod. Biol. 154(1), 71–80 (2011).
  • Blumenthal PD, Dawson L, Hurskainen R. Cost–effectiveness and quality of life associated with heavy menstrual bleeding among women using the levonorgestrel-releasing intrauterine system. Int. J. Gynaecol. Obstet. 112(3), 171–178 (2011).
  • Bhattacharya S, Middleton LJ, Tsourapas A et al.; International Heavy Menstrual Bleeding Individual Patient Data Meta-analysis Collaborative Group. Hysterectomy, endometrial ablation and Mirena® for heavy menstrual bleeding: a systematic review of clinical effectiveness and cost–effectiveness analysis. Health Technol. Assess. 15(19), iii–xvi, 1–252 (2011).
  • Roberts TE, Tsourapas A, Middleton LJ et al. Hysterectomy, endometrial ablation, and levonorgestrel releasing intrauterine system (Mirena) for treatment of heavy menstrual bleeding: cost–effectiveness analysis. BMJ 342, d2202 (2011).
  • Heimovitch S. Profile of long-acting reversible contraception users in Europe. Eur. J. Contracept. Reprod. Health Care 14, 187–195 (2009).
  • Gemzell-Danielsson K, Inki P, Boubli L, O’Flynn M, Kunz M, Heikinheimo O. Bleeding pattern and safety of consecutive use of the levonorgestrel-releasing intrauterine system (LNG-IUS) – a multicentre prospective study. Hum. Reprod. 25(2), 354–359 (2010).
  • Heikinheimo O, Inki P, Kunz M et al. Double-blind, randomized, placebo-controlled study on the effect of misoprostol on ease of consecutive insertion of the levonorgestrel-releasing intrauterine system. Contraception 81(6), 481–486 (2010).
  • Heikinheimo O, Inki P, Kunz M, Gemzell-Danielsson K. Predictors of bleeding and user satisfaction during consecutive use of the levonorgestrel-releasing intrauterine system. Hum. Reprod. 25(6), 1423–1427 (2010).
  • Lewis RA, Taylor D, Natavio MF, Melamed A, Felix J, Mishell D Jr. Effects of the levonorgestrel-releasing intrauterine system on cervical mucus quality and sperm penetrability. Contraception 82(6), 491–496 (2010).
  • Haliloglu B, Celik A, Ilter E, Bozkurt S, Ozekici U. Comparison of uterine artery blood flow with levonorgestrel intrauterine system and copper intrauterine device. Contraception 83(6), 578–581 (2011).
  • Hohmann HL, Reeves MF, Chen BA, Perriera LK, Hayes JL, Creinin MD. Immediate versus delayed insertion of the levonorgestrel-releasing intrauterine device following dilation and evacuation: a randomized controlled trial. Contraception 85(3), 240–245 (2012).
  • Grimes DA, Lopez LM, Schulz KF, Stanwood NL. Immediate postabortal insertion of intrauterine devices. Cochrane Database Syst. Rev. 6, CD001777 (2010).
  • Drey EA, Reeves MF, Ogawa DD, Sokoloff A, Darney PD, Steinauer JE. Insertion of intrauterine contraceptives immediately following first- and second-trimester abortions. Contraception 79(5), 397–402 (2009).
  • Betstadt SJ, Turok DK, Kapp N, Feng KT, Borgatta L. Intrauterine device insertion after medical abortion. Contraception 83(6), 517–521 (2011).
  • Shimoni N, Davis A, Ramos ME, Rosario L, Westhoff C. Timing of copper intrauterine device insertion after medical abortion: a randomized controlled trial. Obstet. Gynecol. 118(3), 623–628 (2011).
  • Sääv I, Stephansson O, Gemzell-Danielsson K. Early versus delayed insertion of intrauterine contraception after medical abortion – a randomized controlled trial. PLoS ONE 7(11), e48948 (2012).
  • Goodman S, Hendlish SK, Reeves MF, Foster-Rosales A. Impact of immediate postabortal insertion of intrauterine contraception on repeat abortion. Contraception 78(2), 143–148 (2008).
  • Heikinheimo O, Gissler M, Suhonen S. Can the outcome of the next pregnancy be predicted at the time of induced abortion? Hum. Reprod. 24(4), 820–826 (2009).
  • Niinimäki M, Pouta A, Bloigu A et al. Frequency and risk factors for repeat abortions after surgical compared with medical termination of pregnancy. Obstet. Gynecol. 113(4), 845–852 (2009).
  • Roberts H, Silva M, Xu S. Post abortion contraception and its effect on repeat abortions in Auckland, New Zealand. Contraception 82(3), 260–265 (2010).
  • Ames CM, Norman WV. Preventing repeat abortion in Canada: is the immediate insertion of intrauterine devices postabortion a cost-effective option associated with fewer repeat abortions? Contraception 85(1), 51–55 (2012).
  • Cameron ST, Glasier A, Chen ZE, Johnstone A, Dunlop C, Heller R. Effect of contraception provided at termination of pregnancy and incidence of subsequent termination of pregnancy. BJOG 119(9), 1074–1080 (2012).
  • Kapp N, Curtis KM. Intrauterine device insertion during the postpartum period: a systematic review. Contraception 80(4), 327–336 (2009).
  • Chen BA, Reeves MF, Hayes JL, Hohmann HL, Perriera LK, Creinin MD. Postplacental or delayed insertion of the levonorgestrel intrauterine device after vaginal delivery: a randomized controlled trial. Obstet. Gynecol. 116(5), 1079–1087 (2010).
  • Dahlke JD, Terpstra ER, Ramseyer AM, Busch JM, Rieg T, Magann EF. Postpartum insertion of levonorgestrel–intrauterine system at three time periods: a prospective randomized pilot study. Contraception 84(3), 244–248 (2011).
  • Stuart GS, Bryant AG, O’Neill E, Doherty IA. Feasibility of postpartum placement of the levonorgestrel intrauterine system more than 6 h after vaginal birth. Contraception 85(4), 359–362 (2012).
  • Hayes JL, Cwiak C, Goedken P, Zieman M. A pilot clinical trial of ultrasound-guided postplacental insertion of a levonorgestrel intrauterine device. Contraception 76(4), 292–296 (2007).
  • Chen BA, Reeves MF, Creinin MD, Schwarz EB. Postplacental or delayed levonorgestrel intrauterine device insertion and breast-feeding duration. Contraception 84(5), 499–504 (2011).
  • Shaamash AH, Sayed GH, Hussien MM, Shaaban MM. A comparative study of the levonorgestrel-releasing intrauterine system Mirena versus the Copper T380A intrauterine device during lactation: breast-feeding performance, infant growth and infant development. Contraception 72(5), 346–351 (2005).
  • Rogovskaya S, Rivera R, Grimes DA et al. Effect of a levonorgestrel intrauterine system on women with Type 1 diabetes: a randomized trial. Obstet. Gynecol. 105(4), 811–815 (2005).
  • Heikinheimo O, Lehtovirta P, Aho I, Ristola M, Paavonen J. The levonorgestrel-releasing intrauterine system in human immunodeficiency virus-infected women: a 5-year follow-up study. Am. J. Obstet. Gynecol. 204(2), 126.e1–126.e4 (2011).
  • Chi C, Huq FY, Kadir RA. Levonorgestrel-releasing intrauterine system for the management of heavy menstrual bleeding in women with inherited bleeding disorders: long-term follow-up. Contraception 83(3), 242–247 (2011).
  • Pisoni CN, Cuadrado MJ, Khamashta MA, Hunt BJ. Treatment of menorrhagia associated with oral anticoagulation: efficacy and safety of the levonorgestrel releasing intrauterine device (Mirena coil). Lupus 15(12), 877–880 (2006).
  • Kilic S, Yuksel B, Doganay M et al. The effect of levonorgestrel-releasing intrauterine device on menorrhagia in women taking anticoagulant medication after cardiac valve replacement. Contraception 80(2), 152–157 (2009).
  • Rana M, Saxena P, Firdous N. Comparison of levonorgestrel and copper releasing intrauterine contraceptive device on body iron stores and menstrual bleeding patterns: experience on Indian women. Eur. Rev. Med. Pharmacol. Sci. 16(2), 230–234 (2012).
  • Vilos GA, Marks J, Tureanu V, Abu-Rafea B, Vilos AG. The levonorgestrel intrauterine system is an effective treatment in selected obese women with abnormal uterine bleeding. J. Minim. Invasive Gynecol. 18(1), 75–80 (2011).
  • Hillman JB, Miller RJ, Inge TH. Menstrual concerns and intrauterine contraception among adolescent bariatric surgery patients. J. Womens. Health (Larchmt) 20(4), 533–538 (2011).
  • Brahmi D, Steenland MW, Renner RM, Gaffield ME, Curtis KM. Pregnancy outcomes with an IUD in situ: a systematic review. Contraception 85(2), 131–139 (2012).
  • Bahamondes L, Espejo-Arce X, Hidalgo MM, Hidalgo-Regina C, Teatin-Juliato C, Petta CA. A cross-sectional study of the forearm bone density of long-term users of levonorgestrel-releasing intrauterine system. Hum. Reprod. 21(5), 1316–1319 (2006).
  • Bahamondes MV, Monteiro I, Castro S, Espejo-Arce X, Bahamondes L. Prospective study of the forearm bone mineral density of long-term users of the levonorgestrel-releasing intrauterine system. Hum. Reprod. 25(5), 1158–1164 (2010).
  • Ferreira RA, Vieira CS, Rosa-E-Silva JC, Rosa-e-Silva AC, Nogueira AA, Ferriani RA. Effects of the levonorgestrel-releasing intrauterine system on cardiovascular risk markers in patients with endometriosis: a comparative study with the GnRH analogue. Contraception 81(2), 117–122 (2010).
  • Heliövaara-Peippo S, Oksjoki R, Halmesmäki K et al. The effect of hysterectomy or levonorgestrel-releasing intrauterine system on cardiovascular disease risk factors in menorrhagia patients: a 10-year follow-up of a randomised trial. Maturitas 69(4), 354–358 (2011).
  • Ng YW, Liang S, Singh K. Effects of Mirena (levonorgestrel-releasing intrauterine system) and Ortho Gynae T380 intrauterine copper device on lipid metabolism – a randomized comparative study. Contraception 79(1), 24–28 (2009).
  • Morin-Papunen L, Martikainen H, McCarthy MI et al. Comparison of metabolic and inflammatory outcomes in women who used oral contraceptives and the levonorgestrel-releasing intrauterine device in a general population. Am. J. Obstet. Gynecol. 199(5), 529.e1–529.e10 (2008).
  • Kayikcioglu F, Gunes M, Ozdegirmenci O, Haberal A. Effects of levonorgestrel-releasing intrauterine system on glucose and lipid metabolism: a 1-year follow-up study. Contraception 73(5), 528–531 (2006).
  • Lidegaard O, Nielsen LH, Skovlund CW, Løkkegaard E. Venous thrombosis in users of non-oral hormonal contraception: follow-up study, Denmark 2001-10. BMJ 344, e2990 (2012).
  • Lidegaard Ø, Løkkegaard E, Jensen A, Skovlund CW, Keiding N. Thrombotic stroke and myocardial infarction with hormonal contraception. N. Engl. J. Med. 366(24), 2257–2266 (2012).
  • Lessard T, Simões JA, Discacciati MG, Hidalgo M, Bahamondes L. Cytological evaluation and investigation of the vaginal flora of long-term users of the levonorgestrel-releasing intrauterine system (LNG-IUS). Contraception 77(1), 30–33 (2008).
  • Neale R, Knight I, Keane F. Do users of the intrauterine system (Mirena) have different genital symptoms and vaginal flora than users of the intrauterine contraceptive device? Int. J. STD AIDS 20(6), 423–424 (2009).
  • Donders GG, Berger J, Heuninckx H, Bellen G, Cornelis A. Vaginal flora changes on Pap smears after insertion of levonorgestrel-releasing intrauterine device. Contraception 83(4), 352–356 (2011).
  • Kaliterna V, Kucišec-Tepeš N, Pejkovic L, Zavorovic S, Petrovic S, Barišic Z. An intrauterine device as a possible cause of change in the microbial flora of the female genital system. J. Obstet. Gynaecol. Res. 37(8), 1035–1040 (2011).
  • van Grootheest K, Sachs B, Harrison-Woolrych M, Caduff-Janosa P, van Puijenbroek E. Uterine perforation with the levonorgestrel-releasing intrauterine device: analysis of reports from four national pharmacovigilance centres. Drug Saf. 34(1), 83–88 (2011).
  • Kaislasuo J, Suhonen S, Gissler M, Lähteenmäki P, Heikinheimo O. Intrauterine contraception: incidence and factors associated with uterine perforation – a population-based study. Hum. Reprod. 27(9), 2658–2663 (2012).
  • Merki-Feld GS, Schwarz D, Imthurn B, Keller PJ. Partial and complete expulsion of the Multiload 375 IUD and the levonorgestrel-releasing IUD after correct insertion. Eur. J. Obstet. Gynecol. Reprod. Biol. 137(1), 92–96 (2008).
  • Bahamondes MV, Monteiro I, Canteiro R, Fernandes Ados S, Bahamondes L. Length of the endometrial cavity and intrauterine contraceptive device expulsion. Int. J. Gynaecol. Obstet. 113(1), 50–53 (2011).
  • Skrzypulec V, Drosdzol A. Evaluation of quality of life and sexual functioning of women using levonorgestrel-releasing intrauterine contraceptive system – Mirena. Coll. Antropol. 32(4), 1059–1068 (2008).
  • Witting K, Santtila P, Jern P et al. Evaluation of the female sexual function index in a population based sample from Finland. Arch. Sex. Behav. 37(6), 912–924 (2008).
  • Halmesmäki K, Hurskainen R, Teperi J et al. The effect of hysterectomy or levonorgestrel-releasing intrauterine system on sexual functioning among women with menorrhagia: a 5-year randomised controlled trial. BJOG 114(5), 563–568 (2007).
  • Bastianelli C, Farris M, Benagiano G. Use of the levonorgestrel-releasing intrauterine system, quality of life and sexuality. Experience in an Italian family planning center. Contraception 84(4), 402–408 (2011).
  • Enzlin P, Weyers S, Janssens D et al. Sexual functioning in women using levonorgestrel-releasing intrauterine systems as compared to copper intrauterine devices. J. Sex. Med. 9(4), 1065–1073 (2012).
  • Heliövaara-Peippo S, Halmesmäki K, Hurskainen R et al. The effect of hysterectomy or levonorgestrel-releasing intrauterine system on lower urinary tract symptoms: a 10-year follow-up study of a randomised trial. BJOG 117(5), 602–609 (2010).
  • Heliövaara-Peippo S, Halmesmäki K, Hurskainen R et al. The effect of hysterectomy or levonorgestrel-releasing intrauterine system on lower abdominal pain and back pain among women treated for menorrhagia: a five-year randomized controlled trial. Acta Obstet. Gynecol. Scand. 88(12), 1389–1396 (2009).
  • Trinh XB, Tjalma WA, Makar AP, Buytaert G, Weyler J, van Dam PA. Use of the levonorgestrel-releasing intrauterine system in breast cancer patients. Fertil. Steril. 90(1), 17–22 (2008).
  • Dinger J, Bardenheuer K, Minh TD. Levonorgestrel-releasing and copper intrauterine devices and the risk of breast cancer. Contraception 83(3), 211–217 (2011).
  • Lyytinen HK, Dyba T, Ylikorkala O, Pukkala EI. A case–control study on hormone therapy as a risk factor for breast cancer in Finland: intrauterine system carries a risk as well. Int. J. Cancer 126(2), 483–489 (2010).
  • Jaakkola S, Lyytinen HK, Dyba T, Ylikorkala O, Pukkala E. Endometrial cancer associated with various forms of postmenopausal hormone therapy: a case–control study. Int. J. Cancer 128(7), 1644–1651 (2011).
  • Backman T, Rauramo I, Jaakkola K et al. Use of the levonorgestrel-releasing intrauterine system and breast cancer. Obstet. Gynecol. 106(4), 813–817 (2005).
  • Secura GM, Allsworth JE, Madden T, Mullersman JL, Peipert JF. The Contraceptive CHOICE Project: reducing barriers to long-acting reversible contraception. Am. J. Obstet. Gynecol. 203(2), 115.e1–115.e7 (2010).
  • Bahamondes MV, Hidalgo MM, Bahamondes L, Monteiro I. Ease of insertion and clinical performance of the levonorgestrel-releasing intrauterine system in nulligravidas. Contraception 84(5), e11–e16 (2011).
  • Marions L, Lövkvist L, Taube A, Johansson M, Dalvik H, Øverlie I. Use of the levonorgestrel releasing-intrauterine system in nulliparous women–a non-interventional study in Sweden. Eur. J. Contracept. Reprod. Health Care 16(2), 126–134 (2011).
  • Brockmeyer A, Kishen M, Webb A. Experience of IUD/IUS insertions and clinical performance in nulliparous women – a pilot study. Eur. J. Contracept. Reprod. Health Care 13(3), 248–254 (2008).
  • Aslam N, Blunt S, Latthe P. Effectiveness and tolerability of levonorgestrel intrauterine system in adolescents. J. Obstet. Gynaecol. 30(5), 489–491 (2010).
  • Pillai M, O’Brien K, Hill E. The levonorgestrel intrauterine system (Mirena) for the treatment of menstrual problems in adolescents with medical disorders, or physical or learning disabilities. BJOG 117(2), 216–221 (2010).
  • Paterson H, Ashton J, Harrison-Woolrych M. A nationwide cohort study of the use of the levonorgestrel intrauterine device in New Zealand adolescents. Contraception 79(6), 433–438 (2009).
  • Godfrey EM, Memmel LM, Neustadt A et al. Intrauterine contraception for adolescents aged 14–18 years: a multicenter randomized pilot study of levonorgestrel-releasing intrauterine system compared to the Copper T 380A. Contraception 81(2), 123–127 (2010).
  • Behringer T, Reeves MF, Rossiter B, Chen BA, Schwarz EB. Duration of use of a levonorgestrel IUS amongst nulliparous and adolescent women. Contraception 84(5), e5–e10 (2011).
  • Mansour D, Gemzell-Danielsson K, Inki P. Fertility after discontinuation of contraception: a systematic review of the literature. Eur. J. Contracept. Reprod. Health Care 15, 4–16 (2010).
  • Middleton AJ, Naish J, Singer N. General practitioners’ views on the use of the levonorgestrel-releasing intrauterine system in young, nulligravid women, in London, UK. Eur. J. Contracept. Reprod. Health Care 16(4), 311–318 (2011).
  • Leppälahti S, Gissler M, Mentula M, Heikinheimo O. Trends in teenage termination of pregnancy and its risk factors: a population-based study in Finland, 1987-2009. Hum. Reprod. 27(9), 2829–2836 (2012).
  • Kaunitz AM, Bissonnette F, Monteiro I, Lukkari-Lax E, Muysers C, Jensen JT. Levonorgestrel-releasing intrauterine system or medroxyprogesterone for heavy menstrual bleeding: a randomized controlled trial. Obstet. Gynecol. 116(3), 625–632 (2010).
  • Kaunitz AM, Inki P. The levonorgestrel-releasing intrauterine system in heavy menstrual bleeding: a benefit-risk review. Drugs 72(2), 193–215 (2012).
  • Shabaan MM, Zakherah MS, El-Nashar SA, Sayed GH. Levonorgestrel-releasing intrauterine system compared to low dose combined oral contraceptive pills for idiopathic menorrhagia: a randomized clinical trial. Contraception 83, 48–54 (2011).
  • Chattopdhyay B, Nigam A, Goswami S, Chakravarty PS. Clinical outcome of levonorgestrel intra-uterine system in idiopathic menorrhagia. Eur. Rev. Med. Pharmacol. Sci. 15(7), 764–768 (2011).
  • Endrikat J, Vilos G, Muysers C, Fortier M, Solomayer E, Lukkari-Lax E. The levonorgestrel-releasing intrauterine system provides a reliable, long-term treatment option for women with idiopathic menorrhagia. Arch. Gynecol. Obstet. 285(1), 117–121 (2012).
  • Depypere HT, Hillard T, Erkkola R et al. A 60-month non-comparative study on bleeding profiles with the levonorgestrel intrauterine system from the late transition period to estrogen supplemented menopause. Eur. J. Obstet. Gynecol. Reprod. Biol. 153(2), 176–180 (2010).
  • Somboonporn W, Panna S, Temtanakitpaisan T, Kaewrudee S, Soontrapa S. Effects of the levonorgestrel-releasing intrauterine system plus estrogen therapy in perimenopausal and postmenopausal women: systematic review and meta-analysis. Menopause 18(10), 1060–1066 (2011).
  • Wan YL, Holland C. The efficacy of levonorgestrel intrauterine systems for endometrial protection: a systematic review. Climacteric 14(6), 622–632 (2011).
  • Gemzell-Danielsson K, Schellschmidt I, Apter D. A randomized, Phase II study describing the efficacy, bleeding profile, and safety of two low-dose levonorgestrel-releasing intrauterine contraceptive systems and Mirena. Fertil. Steril. 97(3), 616–622 (2012).

Websites

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Order Reprints Request Corporate Permissions

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

Request Academic Permissions

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.

Related research

People also read lists articles that other readers of this article have read.

Recommended articles lists articles that we recommend and is powered by our AI driven recommendation engine.

Cited by lists all citing articles based on Crossref citations.
Articles with the Crossref icon will open in a new tab.