Skip to main content

Advertisement

Log in

Male circumcision and HIV infection risk

  • Topic Paper
  • Published:
World Journal of Urology Aims and scope Submit manuscript

Abstract

Background

Male circumcision is being promoted to reduce human immunodeficiency virus type 1 (HIV) infection rates. This review evaluates the scientific evidence suggesting that male circumcision reduces HIV infection risk in high-risk heterosexual populations.

Methods

We followed the updated International Consultation on Urological Diseases evidence-based medicine recommendations to critically review the scientific evidence on male circumcision and HIV infection risk.

Results

Level 1 evidence supports the concept that male circumcision substantially reduces the risk of HIV infection. Three major lines of evidence support this conclusion: biological data suggesting that this concept is plausible, data from observational studies supported by high-quality meta-analyses, and three randomized clinical trials supported by high-quality meta-analyses.

Conclusions

The evidence from these biological studies, observational studies, randomized controlled clinical trials, meta-analyses, and cost-effectiveness studies is conclusive. The challenges to implementation of male circumcision as a public health measure in high-risk populations must now be faced.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Auvert B, Taljaard D, Lagarde E, Sobngwi-Tambekou J, Sitta R, Puren A (2005) Randomized, controlled intervention trial of male circumcision for reduction of HIV infection risk: the ANRS 1265 trial. PLoS Med 2(11):e298

    Article  PubMed  Google Scholar 

  2. Bailey RC, Moses S, Parker CB, Agot K, Maclean I, Krieger JN, Williams CF, Campbell RT, Ndinya-Achola JO (2007) Male circumcision for HIV prevention in young men in Kisumu, Kenya: a randomised controlled trial. Lancet 369(9562):643–656

    Article  PubMed  Google Scholar 

  3. Gray RH, Kigozi G, Serwadda D, Makumbi F, Watya S, Nalugoda F, Kiwanuka N, Moulton LH, Chaudhary MA, Chen MZ, Sewankambo NK, Wabwire-Mangen F, Bacon MC, Williams CF, Opendi P, Reynolds SJ, Laeyendecker O, Quinn TC, Wawer MJ (2007) Male circumcision for HIV prevention in men in Rakai, Uganda: a randomised trial. Lancet 369(9562):657–666

    Article  PubMed  Google Scholar 

  4. Krieger JN (2010) Male circumcision and HIV infection risk. In: Naber KG, Schaeffer AJ, Heyns CF, Matsumoto T, Shoskes DA, Bjerklund Johansen TE (eds) Urogenital infections. European Association of Urology, Arnheim, pp 847–859

    Google Scholar 

  5. Weiss HA, Quigley MA, Hayes RJ (2000) Male circumcision and risk of HIV infection in sub-Saharan Africa: a systematic review and meta-analysis. Aids 14(15):2361–2370

    Article  PubMed  CAS  Google Scholar 

  6. Siegfried N, Muller M, Volmink J, Deeks J, Egger M, Low N, Weiss H, Walker S, Williamson P (2003) Male circumcision for prevention of heterosexual acquisition of HIV in men. Cochrane Database Syst Rev (3):CD003362

  7. Price LB, Liu CM, Johnson KE, Aziz M, Lau MK, Bowers J, Ravel J, Keim PS, Serwadda D, Wawer MJ, Gray RH (2010) The effects of circumcision on the penis microbiome. PLoS One 5(1):e8422. doi:10.1371/journal.pone.0008422

  8. Patterson BK, Landay A, Siegel JN, Flener Z, Pessis D, Chaviano A, Bailey RC (2002) Susceptibility to human immunodeficiency virus-1 infection of human foreskin and cervical tissue grown in explant culture. Am J Pathol 161(3):867–873

    Article  PubMed  Google Scholar 

  9. Soilleux EJ, Coleman N (2004) Expression of DC-SIGN in human foreskin may facilitate sexual transmission of HIV. J Clin Pathol 57(1):77–78

    Article  PubMed  CAS  Google Scholar 

  10. McCoombe SG, Short RV (2006) Potential HIV-1 target cells in the human penis. Aids 20(11):1491–1495

    Article  PubMed  Google Scholar 

  11. Fink AJ (1986) A possible explanation for heterosexual male infection with AIDS. N Engl J Med 315:1167

    PubMed  CAS  Google Scholar 

  12. Moses S, Nagelkerke NJ, Blanchard J (1999) Analysis of the scientific literature on male circumcision and risk for HIV infection. Int J STD AIDS 10(9):626–628

    Article  PubMed  CAS  Google Scholar 

  13. Drain PK, Halperin DT, Hughes JP, Klausner JD, Bailey RC (2006) Male circumcision, religion, and infectious diseases: an ecologic analysis of 118 developing countries. BMC Infect Dis 6:172

    Article  PubMed  Google Scholar 

  14. Siegfried N (2005) Does male circumcision prevent HIV infection? PLoS Med 2(11):e393

    Article  PubMed  Google Scholar 

  15. Weiss HA, Halpernr D, Bailey RC, Hayes RJ, Schmid G, Hankins C (2008) Male circumcision for HIV prevention: from evidence to action? AIDS 22(5):567–574

    Article  PubMed  Google Scholar 

  16. Krieger JN, Bailey RC, Opeya J, Ayieko B, Opiyo F, Agot K, Parker C, Ndinya-Achola JO, Magoha GA, Moses S (2005) Adult male circumcision: results of a standardized procedure in Kisumu District, Kenya. BJU Int 96(7):1109–1113

    Article  PubMed  Google Scholar 

  17. Krieger JN, Bailey RC, Opeya JC, Ayieko BO, Opiyo FA, Omondi D, Agot K, Parker C, Ndinya-Achola JO, Moses S (2007) Adult male circumcision outcomes: experience in a developing country setting. Urol Int 78(3):235–240

    Article  PubMed  Google Scholar 

  18. Kahn JG, Marseille E, Auvert B (2006) Cost-effectiveness of male circumcision for HIV prevention in a South African setting. PLoS Med 3(12):e517

    Article  PubMed  Google Scholar 

  19. Gray RH, Li X, Kigozi G, Serwadda D, Nalugoda F, Watya S, Reynolds SJ, Wawer M (2007) The impact of male circumcision on HIV incidence and cost per infection prevented: a stochastic simulation model from Rakai, Uganda. Aids 21(7):845–850

    Article  PubMed  Google Scholar 

  20. Mehta SD, Gray RH, Auvert B, Moses S, Kigozi G, Taljaard D, Puren A, Agot K, Serwadda D, Parker CB, Wawer MJ, Bailey RC (2009) Does sex in the early period after circumcision increase HIV-seroconversion risk? Pooled analysis of adult male circumcision clinical trials. AIDS 23(12):1557–1564. doi:10.1097/QAD.0b013e32832afe95

    Article  PubMed  Google Scholar 

  21. Van Howe RS (1999) Circumcision and HIV infection: review of the literature and meta-analysis. Int J STD AIDS 10(1):8–16

    Article  PubMed  Google Scholar 

  22. O’Farrell N, Egger M (2000) Circumcision in men and the prevention of HIV infection: a ‘meta-analysis’ revisited. Int J STD AIDS 11(3):137–142

    Article  PubMed  Google Scholar 

  23. Siegfried N, Muller M, Deeks JJ, Volmink J (2009) Male circumcision for prevention of heterosexual acquisition of HIV in men. Cochrane Database Syst Rev (2):CD003362. doi:10.1002/14651858.CD003362.pub2

  24. Desai K, Boily MC, Garnett GP, Masse BR, Moses S, Bailey RC (2006) The role of sexually transmitted infections in male circumcision effectiveness against HIV–insights from clinical trial simulation. Emerg Themes Epidemiol 3:19

    Article  PubMed  Google Scholar 

  25. Williams BG, Lloyd-Smith JO, Gouws E, Hankins C, Getz WM, Hargrove J, de Zoysa I, Dye C, Auvert B (2006) The potential impact of male circumcision on HIV in Sub-Saharan Africa. PLoS Med 3(7):e262

    Article  PubMed  Google Scholar 

  26. Orroth KK, Freeman EE, Bakker R, Buve A, Glynn JR, Boily MC, White RG, Habbema JD, Hayes RJ (2007) Understanding the differences between contrasting HIV epidemics in east and west Africa: results from a simulation model of the Four Cities Study. Sex Transm Infect 83(Suppl 1):15–16

    Google Scholar 

  27. Hallett TB, Singh K, Smith JA, White RG, Abu-Raddad LJ, Garnett GP (2008) Understanding the impact of male circumcision interventions on the spread of HIV in southern Africa. PLoS ONE 3(5):e2212

    Article  PubMed  Google Scholar 

  28. Londish GJ, Murray JM (2008) Significant reduction in HIV prevalence according to male circumcision intervention in sub-Saharan Africa. Int J Epidemiol 37(6):1246–1253

    Google Scholar 

  29. Bollinger LA, Stover J, Musuka G, Fidzani B, Moeti T, Busang L (2009) The cost and impact of male circumcision on HIV/AIDS in Botswana. J Int AIDS Soc 12(1):7. doi:10.1186/1758-2652-12-7

    Article  PubMed  Google Scholar 

  30. Andersson KM, Owens DK, Paltiel AD (2010) Scaling up circumcision programs in Southern Africa: the potential impact of gender disparities and changes in condom use behaviors on heterosexual HIV transmission. AIDS Behav. doi:10.1007/s10461-010-9784-y

  31. Gebremedhin S (2010) Assessment of the protective effect of male circumcision from HIV infection and sexually transmitted diseases: evidence from 18 demographic and health surveys in sub-Saharan Africa. Afr J Reprod Health 14(2):105–113

    PubMed  Google Scholar 

  32. Kelly R, Kiwanuka N, Wawer MJ, Serwadda D, Sewankambo NK, Wabwire-Mangen F, Li C, Konde-Lule JK, Lutalo T, Makumbi F, Gray RH (1999) Age of male circumcision and risk of prevalent HIV infection in rural Uganda. Aids 13(3):399–405

    Article  PubMed  CAS  Google Scholar 

  33. Quinn TC, Wawer MJ, Sewankambo N, Serwadda D, Li C, Wabwire-Mangen F, Meehan MO, Lutalo T, Gray RH (2000) Viral load and heterosexual transmission of human immunodeficiency virus type 1. Rakai Project Study Group. N Engl J Med 342(13):921–929

    Google Scholar 

  34. Reynolds SJ, Shepherd ME, Risbud AR, Gangakhedkar RR, Brookmeyer RS, Divekar AD, Mehendale SM, Bollinger RC (2004) Male circumcision and risk of HIV-1 and other sexually transmitted infections in India. Lancet 363(9414):1039–1040

    Article  PubMed  Google Scholar 

  35. Meier AS, Bukusi EA, Cohen CR, Holmes KK (2006) Independent association of hygiene, socioeconomic status, and circumcision with reduced risk of HIV infection among Kenyan men. J Acquir Immune Defic Syndr 43(1):117–118

    Article  PubMed  Google Scholar 

  36. Shaffer DN, Bautista CT, Sateren WB, Sawe FK, Kiplangat SC, Miruka AO, Renzullo PO, Scott PT, Robb ML, Michael NL, Birx DL (2007) The protective effect of circumcision on HIV incidence in rural low-risk men circumcised predominantly by traditional circumcisers in Kenya: two-year follow-up of the Kericho HIV Cohort Study. J Acquir Immune Defic Syndr 45(4):371–379

    Article  PubMed  Google Scholar 

  37. Millett GA, Ding H, Lauby J, Flores S, Stueve A, Bingham T, Carballo-Dieguez A, Murrill C, Liu KL, Wheeler D, Liau A, Marks G (2007) Circumcision status and HIV infection among Black and Latino men who have sex with men in 3 US cities. J Acquir Immune Defic Syndr 46(5):643–650

    Article  PubMed  Google Scholar 

  38. Auvert B, Buve A, Ferry B, Carael M, Morison L, Lagarde E, Robinson NJ, Kahindo M, Chege J, Rutenberg N, Musonda R, Laourou M, Akam E (2001) Ecological and individual level analysis of risk factors for HIV infection in four urban populations in sub-Saharan Africa with different levels of HIV infection. Aids 15(Suppl 4):S15–S30

    Google Scholar 

  39. Auvert B, Buve A, Lagarde E, Kahindo M, Chege J, Rutenberg N, Musonda R, Laourou M, Akam E, Weiss HA (2001) Male circumcision and HIV infection in four cities in sub-Saharan Africa. Aids 15(Suppl 4):S31–S40

    Google Scholar 

  40. MacDonald KS, Malonza I, Chen DK, Nagelkerke NJ, Nasio JM, Ndinya-Achola J, Bwayo JJ, Sitar DS, Aoki FY, Plummer FA (2001) Vitamin A and risk of HIV-1 seroconversion among Kenyan men with genital ulcers. Aids 15(5):635–639

    Article  PubMed  CAS  Google Scholar 

  41. Gray R, Azire J, Serwadda D, Kiwanuka N, Kigozi G, Kiddugavu M, Nalugoda F, Li X, Wawer M (2004) Male circumcision and the risk of sexually transmitted infections and HIV in Rakai, Uganda. Aids 18(18):2428–2430

    PubMed  Google Scholar 

  42. Agot KE, Ndinya-Achola JO, Kreiss JK, Weiss NS (2004) Risk of HIV-1 in rural Kenya: a comparison of circumcised and uncircumcised men. Epidemiology 15(2):157–163

    Article  PubMed  Google Scholar 

  43. Jewkes R, Dunkle K, Nduna M, Levin J, Jama N, Khuzwayo N, Koss M, Puren A, Duvvury N (2006) Factors associated with HIV sero-positivity in young, rural South African men. Int J Epidemiol 35(6):1455–1460

    Article  PubMed  CAS  Google Scholar 

  44. Kapiga SH, Sam NE, Mlay J, Aboud S, Ballard RC, Shao JF, Larsen U (2006) The epidemiology of HIV-1 infection in northern Tanzania: results from a community-based study. AIDS Care 18(4):379–387

    Article  PubMed  CAS  Google Scholar 

  45. Johnson K, Way A (2006) Risk factors for HIV infection in a national adult population: evidence from the 2003 Kenya Demographic and Health Survey. J Acquir Immune Defic Syndr 42(5):627–636

    Article  PubMed  Google Scholar 

  46. Talukdar A, Khandokar MR, Bandopadhyay SK, Detels R (2007) Risk of HIV infection but not other sexually transmitted diseases is lower among homeless Muslim men in Kolkata. Aids 21(16):2231–2235

    Article  PubMed  Google Scholar 

  47. Mishra V, Assche SB, Greener R, Vaessen M, Hong R, Ghys PD, Boerma JT, Van Assche A, Khan S, Rutstein S (2007) HIV infection does not disproportionately affect the poorer in sub-Saharan Africa. Aids 21(Suppl 7):S17–S28

    Google Scholar 

  48. Klavs I, Hamers FF (2008) Male circumcision in Slovenia: results from a national probability sample survey. Sex Transm Infect 84(1):49–50

    Article  PubMed  CAS  Google Scholar 

  49. Foglia G, Sateren WB, Renzullo PO, Bautista CT, Langat L, Wasunna MK, Singer DE, Scott PT, Robb ML, Birx DL (2008) High prevalence of HIV infection among rural tea plantation residents in Kericho, Kenya. Epidemiol Infect 136(5):694–702

    Article  PubMed  CAS  Google Scholar 

  50. Mermin J, Musinguzi J, Opio A, Kirungi W, Ekwaru J, Hladik W, Kaharuza F, Downing R, Bunnell R (2008) Risk factors for recent HIV Infection in Uganda. JAMA 300(5):540–549

    Article  PubMed  CAS  Google Scholar 

  51. Halperin DT, Fritz K, McFarland W, Woelk G (2005) Acceptability of adult male circumcision for sexually transmitted disease and HIV prevention in Zimbabwe. Sex Transm Dis 32(4):238–239

    Article  PubMed  Google Scholar 

  52. Buchbinder SP, Vittinghoff E, Heagerty PJ, Celum CL, Seage GR 3rd, Judson FN, McKirnan D, Mayer KH, Koblin BA (2005) Sexual risk, nitrite inhalant use, and lack of circumcision associated with HIV seroconversion in men who have sex with men in the United States. J Acquir Immune Defic Syndr 39(1):82–89

    Article  PubMed  Google Scholar 

  53. Warner L, Ghanem KG, Newman DR, Macaluso M, Sullivan PS, Erbelding EJ (2009) Male circumcision and risk of HIV infection among heterosexual African American men attending Baltimore sexually transmitted disease clinics. J Infect Dis 199(1):59–65. doi:10.1086/595569

    Article  PubMed  Google Scholar 

  54. Halperin DT, Bailey RC (1999) Male circumcision and HIV infection: 10 years and counting. Lancet 354(9192):1813–1815

    Article  PubMed  CAS  Google Scholar 

  55. Green EC (2000) Male circumcision and HIV infection. Lancet 355(9207):927

    Article  PubMed  CAS  Google Scholar 

  56. Szabo R, Short RV (2000) How does male circumcision protect against HIV infection? Bmj 320(7249):1592–1594

    Article  PubMed  CAS  Google Scholar 

  57. Quigley MA, Weiss HA, Hayes RJ (2001) Male circumcision as a measure to control HIV infection and other sexually transmitted diseases. Curr Opin Infect Dis 14(1):71–75

    Article  PubMed  CAS  Google Scholar 

  58. Lerman SE, Liao JC (2001) Neonatal circumcision. Pediatr Clin North Am 48(6):1539–1557

    Article  PubMed  CAS  Google Scholar 

  59. Shapiro RL (2002) Drawing lines in the sand: the boundaries of the HIV pandemic in perspective. Soc Sci Med 55(12):2189–2191

    Article  PubMed  Google Scholar 

  60. Gisselquist D, Potterat JJ, Brody S (2004) Running on empty: sexual co-factors are insufficient to fuel Africa’s turbocharged HIV epidemic. Int J STD AIDS 15(7):442–452

    Article  PubMed  Google Scholar 

  61. Sahasrabuddhe VV, Vermund SH (2007) The future of HIV prevention: control of sexually transmitted infections and circumcision interventions. Infect Dis Clin North Am 21(1):241–257 (xi)

    Google Scholar 

  62. Short RV (2004) The HIV/AIDS pandemic: new ways of preventing infection in men. Reprod Fertil Dev 16(5):555–559

    Article  PubMed  CAS  Google Scholar 

  63. Short RV (2006) New ways of preventing HIV infection: thinking simply, simply thinking. Philos Trans R Soc Lond B Biol Sci 361(1469):811–820

    Article  PubMed  CAS  Google Scholar 

  64. Nyindo M (2005) Complementary factors contributing to the rapid spread of HIV-I in sub-Saharan Africa: a review. East Afr Med J 82(1):40–46

    PubMed  CAS  Google Scholar 

  65. Inungu J, MaloneBeach E, Betts J (2005) Male circumcision and the risk of HIV infection. AIDS Read 15(3):130–131 (135, 138)

    Google Scholar 

  66. Jones R, Gazzard B, Halima Y (2005) Preventing HIV infection. Bmj 331(7528):1285–1286

    Article  PubMed  Google Scholar 

  67. Flynn P, Havens P, Brady M, Emmanuel P, Read J, Hoyt L, Henry-Reid L, Van Dyke R, Mofenson L (2007) Male circumcision for prevention of HIV and other sexually transmitted diseases. Pediatrics 119(4):821–822

    Article  PubMed  Google Scholar 

  68. Van Howe RS, Svoboda JS, Hodges FM (2005) HIV infection and circumcision: cutting through the hyperbole. J R Soc Health 125(6):259–265

    Article  Google Scholar 

  69. Auerbach JD, Hayes RJ, Kandathil SM (2006) Overview of effective and promising interventions to prevent HIV infection. World Health Organ Tech Rep Ser 938:43–78 (discussion 317–341)

    Google Scholar 

  70. Chan DJ (2006) Fatal attraction: sex, sexually transmitted infections and HIV-1. Int J STD AIDS 17(10):643–651

    Article  PubMed  CAS  Google Scholar 

  71. Mboto CI, Davies A, Fielder M, Jewell AP (2006) Human immunodeficiency virus and hepatitis C co-infection in sub-Saharan West Africa. Br J Biomed Sci 63(1):29–37

    PubMed  CAS  Google Scholar 

  72. Isiugo-Abanihe UC (2006) Sociocultural aspects of HIV/AIDS infection in Nigeria. Afr J Med Sci 35(Suppl):45–55

    Google Scholar 

  73. Weiss HA (2007) Male circumcision as a preventive measure against HIV and other sexually transmitted diseases. Curr Opin Infect Dis 20(1):66–72

    Article  PubMed  Google Scholar 

  74. Sawires SR, Dworkin SL, Fiamma A, Peacock D, Szekeres G, Coates TJ (2007) Male circumcision and HIV/AIDS: challenges and opportunities. Lancet 369(9562):708–713

    Article  PubMed  Google Scholar 

  75. Schenker I, Gross E (2007) [Male circumcision and HIV/AIDS: convincing evidence and their implication for the state of Israel]. Harefuah 146(12):957–963 (997)

    Google Scholar 

  76. Sharp M (2007) 14th annual retrovirus conference (CROI). HIV prevention update. Some bad news, some good news. Posit Aware 18(3):26–27

    Google Scholar 

  77. Quinn TC (2007) Circumcision and HIV transmission. Curr Opin Infect Dis 20(1):33–38

    Article  PubMed  Google Scholar 

  78. Schoen EJ (2007) Should newborns be circumcised? Yes. Can Fam Physician 53(12):2096–2098 (2100–2092)

    Google Scholar 

  79. Clark PA, Eisenman J, Szapor S (2007) Mandatory neonatal male circumcision in Sub-Saharan Africa: medical and ethical analysis. Med Sci Monit 13(12):RA205–RA213

    Google Scholar 

  80. Clark S (2000) Male circumcision could help protect against HIV infection. Lancet 356(9225):225

    Article  PubMed  CAS  Google Scholar 

  81. Morris BJ (2007) Why circumcision is a biomedical imperative for the 21(st) century. Bioessays 29(11):1147–1158

    Article  PubMed  Google Scholar 

  82. Mor Z, Kent CK, Kohn RP, Klausner JD (2007) Declining rates in male circumcision amidst increasing evidence of its public health benefit. PLoS ONE 2(9):e861

    Article  PubMed  Google Scholar 

  83. Jayasuriya A, Robertson C, Allan PS (2007) Twenty-five years of HIV management. J R Soc Med 100(8):363–366

    Article  PubMed  CAS  Google Scholar 

  84. Landovitz RJ (2007) Recent efforts in biomedical prevention of HIV. Top HIV Med 15(3):99–103

    PubMed  Google Scholar 

  85. Vardi A, Guy L, Boiteux JP (2008) Circumcision and HIV. Prog Urol 18(6):331–336

    Google Scholar 

  86. Cohen MS, Hellmann N, Levy JA, DeCock K, Lange J (2008) The spread, treatment, and prevention of HIV-1: evolution of a global pandemic. J Clin Invest 118(4):1244–1254

    Article  PubMed  CAS  Google Scholar 

  87. Gray RH, Wawer MJ, Polis CB, Kigozi G, Serwadda D (2008) Male circumcision and prevention of HIV and sexually transmitted infections. Curr Infect Dis Rep 10(2):121–127

    Article  PubMed  Google Scholar 

  88. Potts M, Halperin DT, Kirby D, Swidler A, Marseille E, Klausner JD, Hearst N, Wamai RG, Kahn JG, Walsh J (2008) Public health. Reassessing HIV prevention. Science 320(5877):749–750

    Google Scholar 

  89. Fieno JV (2008) Costing adult male circumcision in high HIV prevalence, low circumcision rate countries. AIDS Care 20(5):515–520

    Article  PubMed  Google Scholar 

  90. Uthman OA, Popoola TA, Yahaya I, Uthman MM, Aremu O (2011) The cost-utility analysis of adult male circumcision for prevention of heterosexual acquisition of HIV in men in sub-Saharan Africa: a probabilistic decision model. Value Health 14(1):70–79. doi:10.1016/j.jval.2010.10.011

    Article  PubMed  Google Scholar 

Download references

Conflict of interest

The author declares that he has no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to John N. Krieger.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Krieger, J.N. Male circumcision and HIV infection risk. World J Urol 30, 3–13 (2012). https://doi.org/10.1007/s00345-011-0696-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00345-011-0696-x

Keywords

Navigation