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Controversy and Consensus on Indications for Sperm DNA Fragmentation Testing in Male Infertility: A Global Survey, Current Guidelines, and Expert Recommendations

Agarwal A 1 , Farkouh A 1 , Saleh R 2 , Abdel-Meguid Hamoda TA 3 , Harraz AM 4 , Kavoussi P 5 Show all authors , Arafa M 6 , Salvio G 7 , Rambhatla A 8 , Toprak T 9 , Gül M 10 , Phuoc NHV 11 , Boitrelle F 12 , Birowo P 13 , Ghayda RA 14 , Cannarella R 15 , Kuroda S 16 , Durairajanayagam D 17 , Zini A 18 , Wyns C 19 , Sarikaya S 20 , Tremellen K 21 , Mostafa T 22 , Sokolakis I 23 , Evenson DP 24 , Henkel R 25 , Zohdy W 22 , Chung E 26 , Ziouziou I 27 , Falcone M 28 , Russo GI 29 , Al-Hashimi M 30 , Calogero AE 15 , Ko E 31 , Colpi G 32 , Lewis S 33 , Serefoglu EC 34 , Bahar F 35 , Martinez M 36 , Nguyen Q 37 , Ambar RF 38 , Bakircioglu ME 39 , Kandil H 40 , Mogharabian N 41 , Sabbaghian M 42 , Taniguchi H 43 , Tsujimura A 44 , Sajadi H 42 , Ibrahim W 45 , Atmoko W 13 , Vogiatzi P 46 , Gunes S 47 , Sadighi Gilani MA 42 , Roychoudhury S 48 , Güngör ND 49 , Hakim L 50 , Adriansjah R 51 , Kothari P 52 , Jindal S 53 , Amar E 54 , Park HJ 55 , Long TQT 56 , Homa S 57 , Karthikeyan VS 58 , Zilaitiene B 59 , Maldonado Rosas I 60 , Marino A 61 , Pescatori E 62 , Ozer C 63 , Akhavizadegan H 64 , Garrido N 65 , Busetto GM 66 , Adamyan A 67 , Al-Marhoon M 68 , Elbardisi H 6 , Dolati P 69 , Darbandi M 70 , Darbandi S 70 , Balercia G 7 , Pinggera GM 71 , Micic S 72 , Ho CCK 73 , Moussa M 74 , Preto M 28 , Zenoaga-Barbăroșie C 75 , Smith RP 76 , Kosgi R 77 , de la Rosette J 78 , El-Sakka AI 79 , Abumelha SM 80 , Mierzwa TC 81 , Ong TA 82 , Banihani SA 83 , Bowa K 84 , Fukuhara S 85 , Boeri L 86 , Danacıoğlu YO 87 , Gokalp F 88 , Selim OM 22 , Cho CL 89 , Tadros NN 90 , Ugur MR 91 , Ozkent MS 92 , Chiu P 89 , Kalkanli A 93 , Khalafalla K 6 , Vishwakarma RB 94 , Finocchi F 7 , Andreadakis S 95 , Giulioni C 96 , Çeker G 97 , Ceyhan E 63 , Malhotra V 98 , Yilmaz M 99 , Timpano M 28 , Barrett TL 100 , Kim SHK 101 , Ahn ST 102 , Giacone F 103 , Palani A 104 , Duarsa GWK 105 , Kadioglu A 106 , Gadda F 86 , Zylbersztejn DS 107 , Aydos K 108 , Kulaksız D 109 , Gupte D 110 , Calik G 111 , Karna KK 112 , Drakopoulos P 113 , Baser A 114 , Kumar V 115 , Molina JMC 116 , Rajmil O 117 , Ferreira RH 118 , Leonardi S 119 , Avoyan A 120 , Sogutdelen E 121 , Franco G 122 , Ramsay J 123 , Ramirez L 60 , Shah R 94 , Global Andrology Forum

Affiliations 

  • 1 Global Andrology Forum, American Center for Reproductive Medicine, Moreland Hills, OH, USA
  • 2 Department of Dermatology, Venereology and Andrology, Faculty of Medicine, Sohag University, Sohag, Egypt
  • 3 Department of Urology, King Abdulaziz University, Jeddah, Saudi Arabia
  • 4 Urology and Nephrology Center, Mansoura University, Mansoura, Egypt
  • 5 Department of Reproductive Urology, Austin Fertility & Reproductive Medicine/Westlake IVF, Austin, TX, USA
  • 6 Department of Urology, Hamad Medical Corporation, Doha, Qatar
  • 7 Department of Endocrinology, Polytechnic University of Marche, Ancona, Italy
  • 8 Department of Urology, Henry Ford Health System, Vattikuti Urology Institute, Detroit, MI, USA
  • 9 Department of Urology, Fatih Sultan Mehmet Training and Research Hospital, University of Health Sciences, Istanbul, Turkey
  • 10 Department of Urology, Selçuk University School of Medicine, Konya, Turkey
  • 11 Department of Andrology, Binh Dan Hospital, Ho Chi Minh City, Vietnam
  • 12 Reproductive Biology, Fertility Preservation, Andrology, CECOS, Poissy Hospital, Poissy, France
  • 13 Department of Urology, Cipto Mangunkusumo General Hospital, Faculty of Medicine, Universitas Indonesia, Jakarta, Indonesia
  • 14 Urology Institute, University Hospitals, Case Western Reserve University, Cleveland, OH, USA
  • 15 Department of Clinical and Experimental Medicine, University of Catania, Catania, Italy
  • 16 Department of Urology, Cleveland Clinic, Cleveland, OH, USA
  • 17 Department of Physiology, Faculty of Medicine, Universiti Teknologi MARA, Sungai Buloh Campus, Selangor, Malaysia
  • 18 Department of Surgery, McGill University, Montreal, QC, Canada
  • 19 Department of Gynaecology-Andrology, Cliniques universitaires Saint-Luc, Université Catholique de Louvain, Brussels, Belgium
  • 20 Department of Urology, Gülhane Research and Training Hospital, University of Health Sciences, Ankara, Turkey
  • 21 Department of Obstetrics Gynaecology and Reproductive Medicine, Flinders University, Bedford Park, Australia
  • 22 Department of Andrology, Sexology and STIs, Faculty of Medicine, Cairo University, Cairo, Egypt
  • 23 Department of Urology, Martha-Maria Hospital Nuremberg, Nuremberg, Germany
  • 24 SCSA Diagnostics, Brookings, SD, USA
  • 25 Department of Metabolism, Digestion and Reproduction, Imperial College London, London, UK
  • 26 Department of Urology, Princess Alexandra Hospital, University of Queensland, Brisbane, QLD, Australia
  • 27 Department of Urology, College of Medicine and Pharmacy, Ibn Zohr University, Agadir, Morocco
  • 28 Department of Urology, Molinette Hospital, A.O.U. Città della Salute e della Scienza, University of Turin, Torino, Italy
  • 29 Urology Section, University of Catania, Catania, Italy
  • 30 Department of Urology, Burjeel Hospital, Abu Dhabi, UAE
  • 31 Department of Urology, Loma Linda University Health, Loma Linda, CA, USA
  • 32 Andrology and IVF Center, Next Fertility Procrea, Lugano, Switzerland
  • 33 Examen Lab Ltd., Northern Ireland, UK
  • 34 Department of Urology, Biruni University School of Medicine, Istanbul, Turkey
  • 35 Andrology Section, Siloam Sriwijaya Hospital, Palembang, Indonesia
  • 36 Section of Urology, Department of Surgery, University of Santo Tomas Hospital, Manila, Philippines
  • 37 Center for Andrology and Sexual Medicine, Viet Duc University Hospital, Hanoi, Vietnam
  • 38 Department of Urology, Centro Universitario em Saude do ABC, Santo André, Brazil
  • 39 SENSART Clinic, Urology, Fulya, Istanbul, Turkiye
  • 40 Fakih IVF Fertility Center, Abu Dhabi, UAE
  • 41 Sexual Health and Fertility Research Center, Shahroud University of Medical Sciences, Shahroud, Iran
  • 42 Department of Andrology, Reproductive Biomedicine Research Center, Royan Institute for Reproductive Biomedicine, ACECR, Tehran, Iran
  • 43 Department of Urology and Andrology, Kansai Medical University, Hirakata, Osaka, Japan
  • 44 Department of Urology, Juntendo University Urayasu Hospital, Chiba, Japan
  • 45 Department of Obstetrics Gynaecology and Reproductive Medicine, Fertility Care Center in Cairo, Cairo, Egypt
  • 46 Andromed Health & Reproduction, Fertility & Reproductive Health Diagnostic Center, Athens, Greece
  • 47 Department of Medical Biology, Medical Faculty, Ondokuz Mayis University, Samsun, Turkey
  • 48 Department of Life Science and Bioinformatics, Assam University, Silchar, India
  • 49 Department of Obstetrics and Gynecology, Reproductive Endocrinology and IVF Unit, School of Medicine, Bahcesehir University, Istanbul, Turkey
  • 50 Department of Urology, Faculty of Medicine Universitas Airlangga, Universitas Airlangga Teaching Hospital, Surabaya, Indonesia
  • 51 Department of Urology, Faculty of Medicine Universitas Padjajaran, Hasan Sadikin General Hospital, Bandung, Indonesia
  • 52 Department of Urology, Topiwala National Medical College, B.Y.L Nair Ch Hospital, Mumbai, India
  • 53 Department of Andrology and Reproductive Medicine, Jindal Hospital, Meerut, India
  • 54 Department of Urology, American Hospital of Paris, Paris, France
  • 55 Department of Urology, Pusan National University School of Medicine, Busan, Korea
  • 56 Department of Obstetrics and Gynecology, Hanoi Obstetric and Gynecology Hospital, Hanoi, Vietnam
  • 57 Department of Biosciences, University of Kent, Canterbury, UK
  • 58 Andrology Unit, Department of Urology, Apollo Hospitals, Greams Road, Chennai, India
  • 59 Institute of Endocrinology, Medical Academy, Lithuanian University of Health Sciences, Kaunas, Lithuania
  • 60 IVF Laboratory, CITMER Reproductive Medicine, Mexico City, Mexico
  • 61 Reproductive Medicine Unit, ANDROS Day Surgery Clinic, Palermo, Italy
  • 62 Andrology and Reproductive Medicine Unit, Gynepro Medical, Bologna, Italy
  • 63 Department of Urology, Faculty of Medicine, Baskent University, Ankara, Turkey
  • 64 Department of Urology, Sina Hospital, Tehran University of Medical Sciences, Tehran, Iran
  • 65 IVI Foundation, Instituto de Investigación Sanitaria La Fe (IIS La Fe), Valencia, Spain
  • 66 Department of Urology and Renal Transplantation, University of Foggia, Policlinico Riuniti, Foggia, Italy
  • 67 IVF Department, Astghik Medical Center, Yerevan, Armenia
  • 68 Division of Urology, Department of Surgery, Sultan Qaboos University, Muscat, Sultanate of Oman
  • 69 Department of Animal Science, Faculty of Agriculture, University of Shiraz, Iran
  • 70 Fetal Health Research Center, Hope Generation Foundation, Tehran, Iran
  • 71 Department of Urology, Innsbruck Medical University, Innsbruck, Austria
  • 72 Department of Andrology, Uromedica Polyclinic, Belgrade, Serbia
  • 73 Department of Surgery, School of Medicine, Taylor's University, Subang Jaya, Selangor, Malaysia
  • 74 Department of Urology, Lebanese University, Beirut, Lebanon
  • 75 Department of Genetics, Faculty of Biology, University of Bucharest, Bucharest, Romania
  • 76 Department of Urology, University of Virginia School of Medicine, Virginia, USA
  • 77 Department of Urology, Andrology and Renal Transplant, AIG Hospitals, Hyderabad, India
  • 78 Department of Urology, Istanbul Medipol Mega University Hospital, Istanbul, Turkey
  • 79 Department of Urology, Suez Canal University, Ismailia, Egypt
  • 80 Division of Urology, Department of Surgery, King Abdulaziz Medical City, Riyadh, Saudi Arabia
  • 81 Androlab, Fertility Clinic, Curitiba, PR, Brazil
  • 82 Department of Surgery, University of Malaya, Kuala Lumpur, Malaysia
  • 83 Department of Medical Laboratory Sciences, Jordan University of Science and Technology, Irbid, Jordan
  • 84 Department of Urology, University of Lusaka, Lusaka, Zambia
  • 85 Department of Urology, Graduate School of Medicine, Osaka University, Osaka, Japan
  • 86 Department of Urology, IRCCS Fondazione Ca' Granda, Ospedale Maggiore Policlinico, Milan, Italy
  • 87 Department of Urology, University of Health Science Istanbul Bakırköy Dr. Sadi Konuk Training and Research Hospital, Istanbul, Turkey
  • 88 Department of Urology, Hatay Mustafa Kemal University, Antakya, Turkey
  • 89 S. H. Ho Urology Centre, Department of Surgery, The Chinese University of Hong Kong, Hong Kong
  • 90 Division of Urology, Southern Illinois University, Springfield, IL, USA
  • 91 IVF Michigan, Bloomfield Hills, MI, USA
  • 92 Department of Urology, Konya City Hospital, Konya, Turkey
  • 93 Department of Urology, Taksim Education and Research Hospital, Istanbul, Turkey
  • 94 Department of Urology, Lilavati Hospital and Research Centre, Mumbai, India
  • 95 Private Practice, Thessaloniki, Greece
  • 96 Department of Urology, Polytechnic University of Marche Region, Ancona, Italy
  • 97 Department of Urology, Başakşehir Çam and Sakura City Hospital, Istanbul, Turkey
  • 98 Department of Urology, SCM Clinic and Hospital, New Delhi, India
  • 99 Department of Urology, Faculty of Medicine, University of Freiburg-Medical Centre, Freiburg, Germany
  • 100 Perth Urology Clinic, Perth, WA, Australia
  • 101 IVF Australia, Sydney, Australia
  • 102 Department of Urology, Korea University College of Medicine, Seoul, Korea
  • 103 Centro HERA, Unità di Medicina della Riproduzione, Sant'Agata Li Battiati, Catania, Italy
  • 104 Research Centre, University of Garmian, Kalar, Iraq
  • 105 Department of Urology, Udayana University, Denpasar, Indonesia
  • 106 Section of Andrology, Department of Urology, Istanbul University, Istanbul, Turkey
  • 107 Fleury Group and Hospital Israelita Albert Einstein, São Paulo, Brazil
  • 108 Department of Urology, Ankara University, Ankara, Turkey
  • 109 Department of Obstetrics and Gynecology, University of Health Sciences Kanuni Training and Research Hospital, Trabzon, Turkey
  • 110 Department of Urology, Bombay Hospital and Medical Research Center, Mumbai, India
  • 111 Department of Urology, Istanbul Medipol University, Istanbul, Turkey
  • 112 Department of Molecular Cell and Cancer Biology, University of Massachusetts Medical School, Worcester, MA, USA
  • 113 Centre for Reproductive Medicine, Universitair Ziekenhuis Brussel, Vrije Universiteit Brussel, Brussels, Belgium
  • 114 Department of Urology, Bandirma Onyedi Eylül University, Balikesir, Turkey
  • 115 Department of Microbiology, Kurukshetra University, Kurukshetra, India
  • 116 Urology Department, Hospital Clinic of Barcelona, Barcelona, Spain
  • 117 Department of Andrology, Fundacio Puigvert, Barcelona, Spain
  • 118 Department of Urology, Santa Casa de Ribeirão Preto, São Paulo, Brazil
  • 119 Central Laboratory, Hospital Publico Materno Infantil de Salta, Salta, Argentina
  • 120 Urology Department, Astghik Medical Center, Yerevan, Armenia
  • 121 Department of Urology, Bolu Abant Izzet Baysal University, Bolu, Turkey
  • 122 Department of Urology, Policlinico Umberto I, Sapienza University of Rome, Rome, Italy
  • 123 Department of Andrology, Hammersmith Hospital, London, UK
World J Mens Health, 2023 Jul;41(3):575-602.
PMID: 37118960 DOI: 10.5534/wjmh.220282

Abstract

PURPOSE: Sperm DNA fragmentation (SDF) testing was recently added to the sixth edition of the World Health Organization laboratory manual for the examination and processing of human semen. Many conditions and risk factors have been associated with elevated SDF; therefore, it is important to identify the population of infertile men who might benefit from this test. The purpose of this study was to investigate global practices related to indications for SDF testing, compare the relevant professional society guideline recommendations, and provide expert recommendations.

MATERIALS AND METHODS: Clinicians managing male infertility were invited to take part in a global online survey on SDF clinical practices. This was conducted following the CHERRIES checklist criteria. The responses were compared to professional society guideline recommendations related to SDF and the appropriate available evidence. Expert recommendations on indications for SDF testing were then formulated, and the Delphi method was used to reach consensus.

RESULTS: The survey was completed by 436 experts from 55 countries. Almost 75% of respondents test for SDF in all or some men with unexplained or idiopathic infertility, 39% order it routinely in the work-up of recurrent pregnancy loss (RPL), and 62.2% investigate SDF in smokers. While 47% of reproductive urologists test SDF to support the decision for varicocele repair surgery when conventional semen parameters are normal, significantly fewer general urologists (23%; p=0.008) do the same. Nearly 70% would assess SDF before assisted reproductive technologies (ART), either always or for certain conditions. Recurrent ART failure is a common indication for SDF testing. Very few society recommendations were found regarding SDF testing.

CONCLUSIONS: This article presents the largest global survey on the indications for SDF testing in infertile men, and demonstrates diverse practices. Furthermore, it highlights the paucity of professional society guideline recommendations. Expert recommendations are proposed to help guide clinicians.

* Title and MeSH Headings from MEDLINE®/PubMed®, a database of the U.S. National Library of Medicine.

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