Controversy and Consensus on the Management of Elevated Sperm DNA Fragmentation in Male Infertility: A Global Survey, Current Guidelines, and Expert Recommendations
Ala'a Farkouh 1, Ashok Agarwal 1 2, Taha Abo-Almagd Abdel-Meguid Hamoda 3 4, Parviz Kavoussi 5, Ramadan Saleh 6 7, Armand Zini 8, Mohamed Arafa 9 10 11, Ahmed M Harraz 12 13 14, Murat Gul 15, Vilvapathy Senguttuvan Karthikeyan 16, Damayanthi Durairajanayagam 17, Amarnath Rambhatla 18, Florence Boitrelle 19 20, Eric Chung 21, Ponco Birowo 22, Tuncay Toprak 23, Ramy Abou Ghayda 24, Rossella Cannarella 25 26, Nguyen Ho Vinh Phuoc 27 28, Fotios Dimitriadis 29, Giorgio I Russo 30, Ioannis Sokolakis 29, Taymour Mostafa 10, Konstantinos Makarounis 31, Imad Ziouziou 32, Shinnosuke Kuroda 26, Marion Bendayan 19, Raneen Sawaid Kaiyal 26, Andrian Japari 33, Mara Simopoulou 34, Lucia Rocco 35, Nicolas Garrido 36, Nazim Gherabi 37, Kadir Bocu 38, Oguzhan Kahraman 39, Tan V Le 27 28, Christine Wyns 40, Kelton Tremellen 41, Selcuk Sarikaya 42, Sheena Lewis 43, Donald P Evenson 44, Edmund Ko 45, Aldo E Calogero 25, Fahmi Bahar 46, Marlon Martinez 47, Andrea Crafa 25, Quang Nguyen 48 49, Rafael F Ambar 50 51, Giovanni Colpi 52, Mustafa Emre Bakircioglu 53, Ralf Henkel 54 55, Hussein Kandil 56, Ege Can Serefoglu 57, Abdullah Alarbid 13, Akira Tsujimura 58, Alireza Kheradmand 59, Christina Anagnostopoulou 60, Angelo Marino 61, Aram Adamyan 62, Birute Zilaitiene 63, Cevahir Ozer 39, Edoardo Pescatori 64, Paraskevi Vogiatzi 65, Gian Maria Busetto 66, Giancarlo Balercia 67, Haitham Elbardisi 9 10, Hamed Akhavizadegan 68, Hesamoddin Sajadi 69, Hisanori Taniguchi 70, Hyun Jun Park 71 72, Israel Maldonado Rosas 73, Mohamed Al-Marhoon 74, Mohammad Ali Sadighi Gilani 69, Naif Alhathal 75, Germar-Michael Pinggera 76, Priyank Kothari 77, Nasser Mogharabian 78, Sava Micic 79, Sheryl Homa 80, Sara Darbandi 81 82, Tran Quang Tien Long 83, Wael Zohdy 10, Widi Atmoko 22, Marjan Sabbaghian 69, Wael Ibrahim 84, Ryan P Smith 85, Christopher Chee Kong Ho 86, Jean de la Rosette 87, Ahmed I El-Sakka 88, Mirko Preto 89, Cătălina Zenoaga-Barbăroșie 90, Saad Mohammed Abumelha 91, Aykut Baser 92, Kaan Aydos 93, Liliana Ramirez-Dominguez 73, Vijay Kumar 94, Teng Aik Ong 95, Tiago Cesar Mierzwa 96, Ricky Adriansjah 97, Saleem A Banihani 98, Kasonde Bowa 99, Shinichiro Fukuhara 100, Marcelo Rodriguez Peña 101, Mohamad Moussa 102 103, Umut Çağın Ari 104, Chak-Lam Cho 105, Nicholas N Tadros 106, Muhammet Rasit Ugur 107, Edouard Amar 108, Marco Falcone 109, Frederic Romain Santer 76, Arif Kalkanli 110, Keshab Kumar Karna 111, Kareim Khalafalla 9 112 113, Ranjit B Vishwakarma 114, Federica Finocchi 67, Carlo Giulioni 115, Erman Ceyhan 39, Gökhan Çeker 116, Chadi Yazbeck 117, Osvaldo Rajmil 118, Mehmet Yilmaz 119, Baris Altay 120, Trenton L Barrett 121, Kay Seong Ngoo 122, Shubhadeep Roychoudhury 123, Gianmaria Salvio 67, Haocheng Lin 124, Ates Kadioglu 125, Massimiliano Timpano 109, Tomer Avidor-Reiss 126 127, Lukman Hakim 128, Puneet Sindhwani 128, Giorgio Franco 129, Rajender Singh 130, Filippo Giacone 131, Mikhail Ruzaev 132, Raghavender Kosgi 133, Nikolaos Sofikitis 134, Ayad Palani 135, Gokhan Calik 87, Deniz Kulaksız 136, Davor Jezek 137, Manaf Al Hashmi 138 139, Panagiotis Drakopoulos 140 141, Huda Omran 142, Sofia Leonardi 143, Ciler Celik-Ozenci 144, Nur Dokuzeylül Güngör 145, Jonathan Ramsay 146, Toshiyasu Amano 147, Emrullah Sogutdelen 148, Gede Wirya Kusuma Duarsa 149, Koji Chiba 150, Sunil Jindal 151, Missy Savira 22, Luca Boeri 152, Edson Borges 153, Deepak Gupte 154, Fatih Gokalp 155, Guadalupe Hernández Hebrard 73, Suks Minhas 156, Rupin Shah 114; Global Andrology Forum
Affiliations
Affiliations
Global Andrology Forum, American Center for Reproductive Medicine, Moreland Hills, OH, USA.- 2Cleveland Clinic Foundation, Cleveland, OH, USA. agarwaa32099@outlook.com.
- 3Department of Urology, King Abdulaziz University, Jeddah, Saudi Arabia.
- 4Department of Urology, Faculty of Medicine, Minia University, Minia, Egypt.
- 5Department of Reproductive Urology, Austin Fertility & Reproductive Medicine/Westlake IVF, Austin, TX, USA.
- 6Department of Dermatology, Venereology and Andrology, Faculty of Medicine, Sohag University, Sohag, Egypt.
- 7Ajyal IVF Center, Ajyal Hospital, Sohag, Egypt.
- 8Department of Surgery, McGill University, Montreal, QC, Canada.
- 9Department of Urology, Hamad Medical Corporation, Doha, Qatar.
- 10Department of Andrology, Sexology & STIs, Cairo University, Cairo, Egypt.
- 11Department of Urology, Weill Cornell Medical-Qatar, Doha, Qatar.
- 12Urology Department, Urology and Nephrology Center, Mansoura University, Mansura, Egypt.
- 13Department of Surgery, Urology Unit, Farwaniya Hospital, Farwaniya, Kuwait.
- 14Department of Urology, Sabah Al Ahmad Urology Center, Kuwait City, Kuwait.
- 15Department of Urology, Selçuk University School of Medicine, Konya, Turkey.
- 16Andrology Unit, Department of Urology, Apollo Hospitals, Chennai, India.
- 17Department of Physiology, Faculty of Medicine, Universiti Teknologi MARA, Sungai Buloh Campus, Selangor, Malaysia.
- 18Department of Urology, Henry Ford Health System, Vattikuti Urology Institute, Detroit, MI, USA.
- 19Reproductive Biology, Fertility Preservation, Andrology, CECOS, Poissy Hospital, Poissy, France.
- 20Department of Biology, Reproduction, Epigenetics, Environment and Development, Paris Saclay University, UVSQ, INRAE, BREED, Jouy-en-Josas, France.
- 21Department of Urology, Princess Alexandra Hospital, University of Queensland, Brisbane, QLD, Australia.
- 22Department of Urology, Dr. Cipto Mangunkusumo Hospital, Faculty of Medicine, Universitas Indonesia, Jakarta, Indonesia.
- 23Department of Urology, Fatih Sultan Mehmet Training and Research Hospital, University of Health Sciences, Istanbul, Turkey.
- 24Urology Institute, University Hospitals, Case Western Reserve University, Cleveland, OH, USA.
- 25Department of Clinical and Experimental Medicine, University of Catania, Catania, Italy.
- 26Department of Urology, Glickman Urological & Kidney Institute, Cleveland Clinic Foundation, Cleveland, OH, USA.
- 27Department of Andrology, Binh Dan Hospital, Ho Chi Minh City, Vietnam.
- 28Department of Urology and Andrology, Pham Ngoc Thach University of Medicine, Ho Chi Minh City, Vietnam.
- 29Department of Urology, Aristotle University, School of Medicine, Thessaloniki, .
- 30Urology Section, University of Catania, Catania, Italy.
- 31Department of Urology and Andrology, Locus Medicus, Athens, Greece.
- 32Department of Urology, College of Medicine and Pharmacy, Ibn Zohr University, Agadir, Morocco.
- 33Fertility Clinic, Telogorejo Hospital, Semarang, Indonesia.
- 34Department of Physiology, School of Medicine, National and Kapodistrian University of Athens, Athens, Greece.
- 35Department of Environmental, Biological and Pharmaceutical Sciences and Technologies, University of Campania Luigi Vanvitelli, Caserta, Italy.
- 36IVI Foundation, Instituto de Investigación Sanitaria La Fe (IIS La Fe), Valencia, Spain.
- 37Department of Urology, University of Algiers, Algiers, Algeria.
- 38Department of Urology, Silopi State Hospital, Sirnak, Turkey.
- 39Department of Urology, Faculty of Medicine, Baskent University, Ankara, Turkey.
- 40Cliniques Universitaires Saint-Luc, Université Catholique de Louvain, Brussels, Belgium.
- 41Department of Obstetrics Gynaecology and Reproductive Medicine, Flinders University, South Australia, Australia.
- 42Department of Urology, Gülhane Research and Training Hospital, University of Health Sciences, Ankara, Turkey.
- 43Examen Lab Ltd., Northern Ireland, UK.
- 44SCSA Diagnostics, Brookings, SDUSA, USA.
- 45Department of Urology, Loma Linda University Health, Loma Linda, CA, USA.
- 46Andrology Section, Siloam Sriwijaya Hospital, Palembang, Indonesia.
- 47Section of Urology, Department of Surgery, University of Santo Tomas Hospital, Manila, Philippines.
- 48Center for Andrology and Sexual Medicine, Viet Duc University Hospital, Hanoi, Vietnam.
- 49Department of Urology, Andrology and Sexual Medicine, University of Medicine and Pharmacy, Vietnam National University, Hanoi, Vietnam.
- 50Department of Urology, Centro Universitario em Saude do ABC, Santo André, Brazil.
- 51Andrology Group at Ideia Fertil Institute of Human Reproduction, Santo André, Brazil.
- 52Andrology and IVF Center, Next Fertility Procrea, Lugano, Switzerland.
- 53SENSART Clinic, Urology, Fulya, Istanbul, Turkey.
- 54Department of Metabolism, Digestion and Reproduction, Imperial College London, London, UK.
- 55Department of Medical Bioscience, University of the Western Cape, Bellville, South Africa.
- 56Fakih IVF Fertility Center, Abu Dhabi, UAE.
- 57Department of Urology, Biruni University School of Medicine, Istanbul, Turkey.
- 58Department of Urology, Juntendo University Urayasu Hospital, Chiba, Japan.
- 59Urology Department, Golestan Hospital, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran.
- 60Unit of Reproductive Medicine-EmbryoART, Leto Maternity Hospital, Athens, Greece.
- 61ANDROS Day Surgery Clinic, Reproductive Medicine Unit, Palermo, Italy.
- 62IVF Department, Astghik Medical Center, Yerevan, Armenia.
- 63Institute of Endocrinology, Medical Academy, Lithuanian University of Health Sciences, Kaunas, Lithuania.
- 64Andrology and Reproductive Medicine Unit, Gynepro Medical, Bologna, Italy.
- 65Andromed Health & Reproduction, Fertility & Reproductive Health Diagnostic Center, Athens, Greece.
- 66Department of Urology and Renal Transplantation, University of Foggia, Policlinico Riuniti, Foggia, Italy.
- 67Department of Endocrinology, Polytechnic University of Marche, Ancona, Italy.
- 68Department of Urology, Sina Hospital, Tehran University of Medical Sciences, Tehran, Iran.
- 69Department of Andrology, Reproductive Biomedicine Research Center, Royan Institute for Reproductive Biomedicine, ACECR, Teheran, Iran.
- 70Department of Urology and Andrology, Kansai Medical University, Hirakata, Osaka, Japan.
- 71Department of Urology, Pusan National University School of Medicine, Busan, Korea.
- 72Medical Research Institute of Pusan National University Hospital, Busan, Korea.
- 73IVF Laboratory, CITMER Reproductive Medicine, Mexico City, Mexico.
- 74Division of Urology, Department of Surgery, Sultan Qaboos University, Muscat, Sultanate of Oman.
- 75King Faisal Specialist Hospital and Research Center, Riyadh, Saudi Arabia.
- 76Department of Urology, Innsbruck Medical University, Innsbruck, Austria.
- 77Department of Urology, Topiwala National Medical College, B.Y.L Nair Ch Hospital, Mumbai, India.
- 78Sexual Health and Fertility Research Center, Shahroud University of Medical Sciences, Shahroud, Iran.
- 79Department of Andrology, Uromedica Polyclinic, Belgrade, Serbia.
- 80Department of Biosciences, University of Kent, Canterbury, UK.
- 81Fetal Health Research Center, Hope Generation Foundation, Tehran, Iran.
- 82Gene Therapy and Regenerative Medicine Research Center, Hope Generation Foundation, Tehran, Iran.
- 83Department of Obstetrics and Gynecology, Hanoi Obstetrics and Gynecology Hospital, Hanoi, Vietnam.
- 84Department of Obstetrics Gynaecology and Reproductive Medicine, Fertility Care Center in Cairo, Cairo, Egypt.
- 85Department of Urology, University of Virginia School of Medicine, Virginia, USA.
- 86Department of Surgery, School of Medicine, Taylor's University, Subang Jaya, Selangor, Malaysia.
- 87Department of Urology, Istanbul Medipol University, Istanbul, Turkey.
- 88Department of Urology, Suez Canal University, Ismailia, Egypt.
- 89Department of Urology, University of Turin, Turin, Italy.
- 90Department of Genetics, Faculty of Biology, University of Bucharest, Bucharest, Romania.
- 91Division of Urology, Department of Surgery, King Abdulaziz Medical City, Riyadh, Saudi Arabia.
- 92Department of Urology, Bandirma Onyedi Eylül University, Balikesir, Turkey.
- 93Department of Urology, Ankara University, Ankara, Turkey.
- 94Department of Microbiology, Kurukshetra University, Kurukshetra, India.
- 95Department of Surgery, University of Malaya, Kuala Lumpur, Malaysia.
- 96Androlab, Fertility Clinic, Curitiba, PR, Brazil.
- 97Department of Urology, Faculty of Medicine of Padjadjaran University, Hasan Sadikin General Hospital, Bandung, Indonesia.
- 98Department of Medical Laboratory Sciences, Jordan University of Science and Technology, Irbid, Jordan.
- 99Department of Urology, University of Lusaka, Lusaka, Zambia.
- 100Department of Urology, Graduate School of Medicine, Osaka University, Osaka, Japan.
- 101Instituto de Ginecologia y Fertilidad (IFER), Buenos Aire, Argentina.
- 102Department of Urology, Lebanese University, Beirut, Lebanon.
- 103Department of Urology, Al Zahraa Hospital, UMC, Lebanon.
- 104Department of Reproduction, Kafkas University, Kars, Turkey.
- 105S. H. Ho Urology Centre, Department of Surgery, The Chinese University of Hong Kong, Hong Kong.
- 106Division of Urology, Southern Illinois University, Springfield, IL, USA.
- 107IVF Michigan, Bloomfield Hills, MI, USA.
- 108American Hospital of Paris, Paris, France.
- 109Department of Urology, Molinette Hospital, A.O.U. Città della Salute e della Scienza, University of Turin, Torino, Italy.
- 110Department of Urology, Taksim Education and Research Hospital, Istanbul, Turkey.
- 111Department of Molecular Cell and Cancer Biology, University of Massachusetts Medical School, Worcester, MA, USA.
- 112Urology Department, University of Texas McGovern Medical School, Houston, TX, USA.
- 113Urology Department, MD Anderson Cancer Center, Houston, TX, USA.
- 114Division of Andrology, Department of Urology, Lilavati Hospital and Research Centre, Mumbai, India.
- 115Department of Urology, Polytechnic University of Marche Region, Ancona, Italy.
- 116Department of Urology, Başakşehir Çam and Sakura City Hospital, Istanbul, Turkey.
- 117Obstetrics Gynecology and Reproductive Medicine, Reprogynes Medical Institute, Paris, France.
- 118Department of Andrology, Fundacio Puigvert, Barcelona, Spain.
- 119Asklepios Clinic Triberg, Urology, Freiburg, Germany.
- 120Department of Urology, Ege University, Izmir, Turkey.
- 121Perth Urology Clinic, Perth, WA, Australia.
- 122Hospital Angkatan Tentera Tuanku Mizan, Kuala Lumpur, Malaysia.
- 123Department of Life Science and Bioinformatics, Assam University, Silchar, India.
- 124Department of Urology, Peking University Third Hospital, Beijing, China.
- 125Section of Andrology, Department of Urology, Istanbul University, Istanbul, Turkey.
- 126Department of Biological Sciences, University of Toledo, Toledo, OH, USA.
- 127Department of Urology and Transplantation, University of Toledo, Toledo, OH, USA.
- 128Department of Urology, Universitas Airlangga, Rumah Sakit Universitas Airlangga Teaching Hospital, Surabaya, Indonesia.
- 129Department of Urology, Policlinico Umberto I, Sapienza University of Rome, Rome, Italy.
- 130Division of Endocrinology, Central Drug Research Institute, Lucknow, India.
- 131Centro HERA, Unità di Medicina della Riproduzione, Sant'Agata Li Battiati, Catania, Italy.
- 132Private Clinic, Moscow, Russia.
- 133Department of Urology, Andrology and Renal Transplant, AIG Hospitals, Hyderabad, India.
- 134Department of Urology, Ioannina University School of Medicine, Ioannina, Greece.
- 135Research Centre, University of Garmian, Kalar, Iraq.
- 136Department of Obstetrics and Gynecology, University of Health Sciences Kanuni Training and Research Hospital, Trabzon, Turkey.
- 137Department for Transfusion Medicine and Transplantation Biology, Reproductive Tissue Bank, University Hospital Zagreb, Zagreb, Croatia.
- 138Department of Urology, Burjeel Hospital, Abu Dhabi, UAE.
- 139Department of Urology, College of Medicine and Health Science, Khalifa University, Abu Dhabi, UAE.
- 140Centre for Reproductive Medicine, Universitair Ziekenhuis Brussel, Vrije Universiteit Brussel, Brussels, Belgium.
- 141IVF Athens, Athens, Greece.
- 142Al Aljenan Medical Center, Pulse Health Training Center, Manama, Kingdom of Bahrain.
- 143Central Laboratory, Hospital Público Materno Infantil de Salta, Salta, Argentina.
- 144Department of Histology and Embryology, Faculty of Medicine, Koç University, Istanbul, Turkey.
- 145Department of Obstetrics and Gynecology, Reproductive Endocrinology and IVF Unit, School of Medicine, Bahcesehir University, Istanbul, Turkey.
- 146Department of Andrology, Hammersmith Hospital, London, UK.
- 147Department of Urology, Nagano Red Cross Hospital, Nagano, Japan.
- 148Department of Urology, Bolu Abant Izzet Baysal University, Bolu, Turkey.
- 149Department of Urology, Udayana University, Denpasar, Indonesia.
- 150Department of Urology, Kobe University Graduate School of Medicine, Kobe, Japan.
- 151Department of Andrology and Reproductive Medicine, Jindal Hospital, Meerut, India.
- 152Department of Urology, IRCCS Fondazione Ca' Granda, Ospedale Maggiore Policlinico, Milan, Italy.
- 153Fertility Assisted Fertilization Center, São Paulo, Brazil.
- 154Department of Urology, Bombay Hospital and Medical Research Center, Mumbai, India.
- 155Department of Urology, Hatay Mustafa Kemal University, Antakya, Turkey.
- 156Division of Surgery, Department of Surgery and Cancer, Imperial College, London, UK.
Abstract
Purpose: Sperm DNA fragmentation (SDF) has been associated with male infertility and poor outcomes of assisted reproductive technology (ART). The purpose of this study was to investigate global practices related to the management of elevated SDF in infertile men, summarize the relevant professional society recommendations, and provide expert recommendations for managing this condition.
Materials and methods: An online global survey on clinical practices related to SDF was disseminated to reproductive clinicians, according to the CHERRIES checklist criteria. Management protocols for various conditions associated with SDF were captured and compared to the relevant recommendations in professional society guidelines and the appropriate available evidence. Expert recommendations and consensus on the management of infertile men with elevated SDF were then formulated and adapted using the Delphi method.
Results: A total of 436 experts from 55 different countries submitted responses. As an initial approach, 79.1% of reproductive experts recommend lifestyle modifications for infertile men with elevated SDF, and 76.9% prescribe empiric antioxidants. Regarding antioxidant duration, 39.3% recommend 4-6 months and 38.1% recommend 3 months. For men with unexplained or idiopathic infertility, and couples experiencing recurrent miscarriages associated with elevated SDF, most respondents refer to ART 6 months after failure of conservative and empiric medical management. Infertile men with clinical varicocele, normal conventional semen parameters, and elevated SDF are offered varicocele repair immediately after diagnosis by 31.4%, and after failure of antioxidants and conservative measures by 40.9%. Sperm selection techniques and testicular sperm extraction are also management options for couples undergoing ART. For most questions, heterogenous practices were demonstrated.
Conclusions: This paper presents the results of a large global survey on the management of infertile men with elevated SDF and reveals a lack of consensus among clinicians. Furthermore, it demonstrates the scarcity of professional society guidelines in this regard and attempts to highlight the relevant evidence. Expert recommendations are proposed to help guide clinicians.
Keywords: DNA fragmentation; Delphi method; Disease management; Male infertility; Practice guideline; Survey.
Conflict of interest statement
The authors have nothing to disclose.
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