Technical Aspects and Clinical Limitations of Sperm DNA Fragmentation Testing in Male Infertility: A Global Survey, Current Guidelines, and Expert Recommendations
Ashok Agarwal
(1)
,
Ala’a Farkouh
(1)
,
Ramadan Saleh
(1, 2)
,
Taha Abo-Almagd Abdel-Meguid Hamoda
(3, 4)
,
Gianmaria Salvio
(5)
,
Florence Boitrelle
(6, 7)
,
Ahmed Harraz
,
Ramy Abou Ghayda
(8)
,
Parviz Kavoussi
,
Murat Gül
(9)
,
Tuncay Toprak
,
Giorgio Ivan Russo
(10)
,
Damayanthi Durairajanayagam
(11)
,
Amarnath Rambhatla
(12)
,
Ponco Birowo
(13)
,
Rossella Cannarella
(10)
,
Nguyen Ho Vinh Phuoc
(14)
,
Armand Zini
(15)
,
Mohamed Arafa
(16, 17, 18)
,
Christine Wyns
(19)
,
Kelton Tremellen
(20)
,
Selçuk Sarıkaya
(21)
,
Sheena Lewis
,
Donald Evenson
,
Edmund Ko
(22)
,
Aldo Calogero
,
Fahmi Bahar
,
Marlon Martínez
(23)
,
Rafael Ambar
,
Giovanni Colpi
,
Mustafa Emre Bakircioglu
,
Ralf Henkel
(24, 25)
,
Hussein Kandil
,
Ege Can Serefoglu
(26)
,
Abdullah Alfakhri
(27)
,
Akira Tsujimura
(28)
,
Alireza Kheradmand
(29)
,
Angelo Marino
,
Aram Adamyan
,
Birute Zilaitiene
(30)
,
Cevahir Ozer
(31)
,
Edoardo Pescatori
,
Paraskevi Vogiatzi
,
Gian Maria Busetto
(32)
,
Giancarlo Balercia
(5)
,
Haitham Elbardisi
(16, 17, 33)
,
Hamed Akhavizadegan
(34)
,
Hesamoddin Sajadi
(35)
,
Hisanori Taniguchi
(36)
,
Hyun Jun Park
(37)
,
Israel Maldonado Rosas
,
Mohamed Al-Marhoon
(38)
,
Mohammad Ali Sadighi Gilani
(35)
,
Naif Alhathal
(39)
,
Nguyen Quang
(40)
,
Germar-Michael Pinggera
(41)
,
Priyank Kothari
,
Sava Micic
,
Sheryl Homa
(42)
,
Tran Quang Tien Long
,
Wael Zohdy
(18)
,
Widi Atmoko
,
Wael Ibrahim
,
Marjan Sabbaghian
(35)
,
Saad Mohammed Abumelha
(43)
,
Eric Chung
(44)
,
Muhammet Rasit Ugur
,
Mehmet Serkan Ozkent
,
Osama Selim
(18)
,
Mahsa Darbandi
(45)
,
Shinichiro Fukuhara
(46)
,
Mounir Jamali
(47)
,
Jean de la Rosette
(48)
,
Shinnosuke Kuroda
(1)
,
Ryan Smith
(49)
,
Aykut Baser
,
Arif Kalkanli
,
Nicholas Tadros
(50)
,
Kaan Aydos
(51)
,
Tiago Cesar Mierzwa
,
Kareim Khalafalla
(52, 53, 54)
,
Vineet Malhotra
,
Mohamad Moussa
(55, 56)
,
Federica Finocchi
(5)
,
Rinaldo Indra Rachman
,
Carlo Giulioni
(5)
,
Tomer Avidor-Reiss
(57)
,
Oguzhan Kahraman
,
Gökhan Çeker
,
Cătălina Zenoaga-Barbăroşie
(58)
,
Trenton Barrett
,
Mehmet Yilmaz
,
Ates Kadioglu
(59)
,
Sunil Jindal
,
Huda Omran
,
Kadir Bocu
,
Vilvapathy Senguttuvan Karthikeyan
,
Giorgio Franco
(60)
,
Jesús Fernando Solorzano
,
Ranjit Vishwakarma
(61)
,
Eko Arianto
,
Nicolas Garrido
,
Divyanu Jain
,
Nazim Gherabi
(62)
,
Ioannis Sokolakis
(63)
,
Ayad Palani
(64)
,
Gokhan Calik
(48)
,
Deniz Kulaksiz
,
Vaida Simanaviciene
,
Mara Simopoulou
(65)
,
Nur Dokuzeylül Güngör
(66)
,
Gideon Blecher
(67)
,
Marco Falcone
(68)
,
Davor Jezek
(69)
,
Mirko Preto
(68)
,
Edouard Amar
(70)
,
Tan Le
(14)
,
Sun Tae Ahn
,
Andri Rezano
(71)
,
Keerti Singh
(72)
,
Lucia Rocco
(73)
,
Missy Savira
,
Osvaldo Rajmil
(74)
,
Sara Darbandi
(45)
,
Emrullah Sogutdelen
,
Luca Boeri
,
Guadalupe Hernández
,
Lukman Hakim
(75)
,
Yoshiharu Morimoto
,
Andrian Japari
,
Nikolaos Sofikitis
(76)
,
Baris Altay
(77)
,
Asli Metin Mahmutoglu
(78)
,
Manaf Al Hashimi
(79)
,
Imad Ziouziou
,
Christina Anagnostopoulou
,
Haocheng Lin
(80)
,
Rupin Shah
(61)
1
Cleveland Clinic
2 Sohag University
3 King Abdulaziz University
4 Minia University
5 UNIVPM - Polytechnic University of Marche / Università Politecnica delle Marche
6 CHI Poissy-Saint-Germain
7 BREED - Biologie de la Reproduction, Environnement, Epigénétique & Développement
8 Case Western Reserve University [Cleveland]
9 Faculty of Medicine [Selcuk University Konya, Turkey]
10 Unict - Università degli studi di Catania = University of Catania
11 UiTM - Universiti Teknologi MARA [Shah Alam]
12 Vattikuti Urology Institute
13 Cipto Mangunkusumo Hospital [Jakarta]
14 University of Medicine Pham Ngoc Thach
15 McGill University = Université McGill [Montréal, Canada]
16 Hamad medical corporation
17 Weill Cornell Medicine [Qatar]
18 Cairo University
19 Cliniques Universitaires Saint-Luc [Bruxelles]
20 Flinders University of South Australia
21 Ankara University School of Medicine [Turkey]
22 Loma Linda University
23 University of Santo Tomas [Manila, Philippines]
24 Imperial College London
25 UWC - University of the Western Cape
26 BU - Biruni University [Istanbul]
27 KFMC - King Fahad Medical City [Riyadh]
28 Juntendo University Hospital [Tokyo]
29 AJUMS - Ahvaz Jundishapur University of Medical Sciences
30 LUSH - Lithuanian University of Health Science
31 Başkent University Hospital [Adana, Turkey]
32 Unifg - Università degli Studi di Foggia = University of Foggia
33 Qatar University
34 TUMS - Tehran University of Medical Sciences
35 Royan Institute for Reproductive Biomedicine [Tehran, Iran]
36 Kansai Medical University
37 PNU - Pusan National University
38 SQU - Sultan Qaboos University
39 King Faisal Specialist Hospital and Research Center
40 VNU - Vietnam National University [Hanoï]
41 IMU - Innsbruck Medical University = Medizinische Universität Innsbruck
42 University of Kent [Canterbury]
43 King Abdulaziz Medical City
44 UQ [All campuses : Brisbane, Dutton Park Gatton, Herston, St Lucia and other locations] - The University of Queensland
45 Hope Generation Foundation
46 Osaka University [Osaka]
47 Hôpital militaire d'instruction Mohammed V [Rabat, Maroc]
48 Istanbul Medipol University
49 University of Virginia School of Medicine
50 Southern Illinois University School of Medicine
51 Ankara University = Ankara Üniversitesi
52 Hamad Medical Corporation [Doha, Qatar]
53 McGMS - McGovern Medical School [Houston, TX, USA]
54 MD Anderson Cancer Center [Houston]
55 LU / ULB - الجامعة اللبنانية [بيروت] = Lebanese University [Beirut] = Université libanaise [Beyrouth]
56 ZHUMC - Al-Zahraa Hospital University Medical Center
57 Department of Biological Sciences [Toledo]
58 UniBuc - University of Bucharest
59 Istanbul University
60 UNIROMA - Università degli Studi di Roma "La Sapienza" = Sapienza University [Rome]
61 Lilavati Hospital and Research Centre
62 Algiers University I
63 Aristotle University of Thessaloniki
64 University of Garmian
65 NKUA - National and Kapodistrian University of Athens
66 Bahcesehir University [Istanbul]
67 Monash University [Melbourne]
68 Molinette Hospital
69 Zagreb University Hospital
70 American Hospital of Paris
71 UnPad - Universitas Padjadjaran = Padjadjaran University
72 The University of the West Indies
73 Università degli studi della Campania "Luigi Vanvitelli" = University of the Study of Campania Luigi Vanvitelli
74 Fundació Puigvert [Barcelona, Spain]
75 UNAIR - Universitas Airlangga
76 University of Ioannina
77 Ege university
78 Bozok University, Yozgat
79 Burjeel Hospital
80 Peking University [Beijing]
2 Sohag University
3 King Abdulaziz University
4 Minia University
5 UNIVPM - Polytechnic University of Marche / Università Politecnica delle Marche
6 CHI Poissy-Saint-Germain
7 BREED - Biologie de la Reproduction, Environnement, Epigénétique & Développement
8 Case Western Reserve University [Cleveland]
9 Faculty of Medicine [Selcuk University Konya, Turkey]
10 Unict - Università degli studi di Catania = University of Catania
11 UiTM - Universiti Teknologi MARA [Shah Alam]
12 Vattikuti Urology Institute
13 Cipto Mangunkusumo Hospital [Jakarta]
14 University of Medicine Pham Ngoc Thach
15 McGill University = Université McGill [Montréal, Canada]
16 Hamad medical corporation
17 Weill Cornell Medicine [Qatar]
18 Cairo University
19 Cliniques Universitaires Saint-Luc [Bruxelles]
20 Flinders University of South Australia
21 Ankara University School of Medicine [Turkey]
22 Loma Linda University
23 University of Santo Tomas [Manila, Philippines]
24 Imperial College London
25 UWC - University of the Western Cape
26 BU - Biruni University [Istanbul]
27 KFMC - King Fahad Medical City [Riyadh]
28 Juntendo University Hospital [Tokyo]
29 AJUMS - Ahvaz Jundishapur University of Medical Sciences
30 LUSH - Lithuanian University of Health Science
31 Başkent University Hospital [Adana, Turkey]
32 Unifg - Università degli Studi di Foggia = University of Foggia
33 Qatar University
34 TUMS - Tehran University of Medical Sciences
35 Royan Institute for Reproductive Biomedicine [Tehran, Iran]
36 Kansai Medical University
37 PNU - Pusan National University
38 SQU - Sultan Qaboos University
39 King Faisal Specialist Hospital and Research Center
40 VNU - Vietnam National University [Hanoï]
41 IMU - Innsbruck Medical University = Medizinische Universität Innsbruck
42 University of Kent [Canterbury]
43 King Abdulaziz Medical City
44 UQ [All campuses : Brisbane, Dutton Park Gatton, Herston, St Lucia and other locations] - The University of Queensland
45 Hope Generation Foundation
46 Osaka University [Osaka]
47 Hôpital militaire d'instruction Mohammed V [Rabat, Maroc]
48 Istanbul Medipol University
49 University of Virginia School of Medicine
50 Southern Illinois University School of Medicine
51 Ankara University = Ankara Üniversitesi
52 Hamad Medical Corporation [Doha, Qatar]
53 McGMS - McGovern Medical School [Houston, TX, USA]
54 MD Anderson Cancer Center [Houston]
55 LU / ULB - الجامعة اللبنانية [بيروت] = Lebanese University [Beirut] = Université libanaise [Beyrouth]
56 ZHUMC - Al-Zahraa Hospital University Medical Center
57 Department of Biological Sciences [Toledo]
58 UniBuc - University of Bucharest
59 Istanbul University
60 UNIROMA - Università degli Studi di Roma "La Sapienza" = Sapienza University [Rome]
61 Lilavati Hospital and Research Centre
62 Algiers University I
63 Aristotle University of Thessaloniki
64 University of Garmian
65 NKUA - National and Kapodistrian University of Athens
66 Bahcesehir University [Istanbul]
67 Monash University [Melbourne]
68 Molinette Hospital
69 Zagreb University Hospital
70 American Hospital of Paris
71 UnPad - Universitas Padjadjaran = Padjadjaran University
72 The University of the West Indies
73 Università degli studi della Campania "Luigi Vanvitelli" = University of the Study of Campania Luigi Vanvitelli
74 Fundació Puigvert [Barcelona, Spain]
75 UNAIR - Universitas Airlangga
76 University of Ioannina
77 Ege university
78 Bozok University, Yozgat
79 Burjeel Hospital
80 Peking University [Beijing]
Ashok Agarwal
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Ramadan Saleh
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Taha Abo-Almagd Abdel-Meguid Hamoda
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Gianmaria Salvio
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Florence Boitrelle
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Ahmed Harraz
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Murat Gül
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Tuncay Toprak
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Giorgio Ivan Russo
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Damayanthi Durairajanayagam
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Amarnath Rambhatla
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Ponco Birowo
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Rossella Cannarella
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Nguyen Ho Vinh Phuoc
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Armand Zini
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Mohamed Arafa
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Christine Wyns
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Kelton Tremellen
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Selçuk Sarıkaya
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Sheena Lewis
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Donald Evenson
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Aldo Calogero
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Fahmi Bahar
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Marlon Martínez
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Rafael Ambar
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Giovanni Colpi
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Mustafa Emre Bakircioglu
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Ralf Henkel
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Hussein Kandil
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Ege Can Serefoglu
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Abdullah Alfakhri
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Akira Tsujimura
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Alireza Kheradmand
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Angelo Marino
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Aram Adamyan
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Birute Zilaitiene
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Cevahir Ozer
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Edoardo Pescatori
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Paraskevi Vogiatzi
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Gian Maria Busetto
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Giancarlo Balercia
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Haitham Elbardisi
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Hamed Akhavizadegan
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Hesamoddin Sajadi
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Hisanori Taniguchi
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Hyun Jun Park
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Israel Maldonado Rosas
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Mohamed Al-Marhoon
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Mohammad Ali Sadighi Gilani
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Naif Alhathal
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Nguyen Quang
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Germar-Michael Pinggera
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Priyank Kothari
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Sava Micic
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Sheryl Homa
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Tran Quang Tien Long
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Widi Atmoko
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Wael Ibrahim
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Marjan Sabbaghian
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Saad Mohammed Abumelha
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Eric Chung
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Muhammet Rasit Ugur
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Mehmet Serkan Ozkent
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Mahsa Darbandi
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Shinichiro Fukuhara
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Mounir Jamali
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Jean de la Rosette
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Ryan Smith
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Aykut Baser
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Arif Kalkanli
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Nicholas Tadros
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Kaan Aydos
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Tiago Cesar Mierzwa
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Kareim Khalafalla
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Vineet Malhotra
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Mohamad Moussa
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Federica Finocchi
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Rinaldo Indra Rachman
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Carlo Giulioni
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Tomer Avidor-Reiss
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Oguzhan Kahraman
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Gökhan Çeker
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Cătălina Zenoaga-Barbăroşie
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Trenton Barrett
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Mehmet Yilmaz
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Sunil Jindal
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Huda Omran
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Kadir Bocu
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Vilvapathy Senguttuvan Karthikeyan
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Giorgio Franco
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Nicolas Garrido
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Divyanu Jain
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Ioannis Sokolakis
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Gokhan Calik
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Deniz Kulaksiz
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Vaida Simanaviciene
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Mara Simopoulou
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Nur Dokuzeylül Güngör
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Gideon Blecher
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Davor Jezek
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Edouard Amar
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Tan Le
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Sun Tae Ahn
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Andri Rezano
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Keerti Singh
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Lucia Rocco
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Missy Savira
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Osvaldo Rajmil
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Sara Darbandi
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Emrullah Sogutdelen
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Luca Boeri
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Guadalupe Hernández
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Yoshiharu Morimoto
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Andrian Japari
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Nikolaos Sofikitis
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Asli Metin Mahmutoglu
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Imad Ziouziou
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Christina Anagnostopoulou
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Haocheng Lin
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Abstract
Purpose: Sperm DNA fragmentation (SDF) is a functional sperm abnormality that can impact reproductive potential, for which four assays have been described in the recently published sixth edition of the WHO laboratory manual for the examination and processing of human semen. The purpose of this study was to examine the global practices related to the use of SDF assays and investigate the barriers and limitations that clinicians face in incorporating these tests into their practice.
Materials and methods: Clinicians managing male infertility were invited to complete an online survey on practices related to SDF diagnostic and treatment approaches. Their responses related to the technical aspects of SDF testing, current professional society guidelines, and the literature were used to generate expert recommendations via the Delphi method. Finally, challenges related to SDF that the clinicians encounter in their daily practice were captured.
Results: The survey was completed by 436 reproductive clinicians. Overall, terminal deoxynucleotidyl transferase deoxyuridine triphosphate Nick-End Labeling (TUNEL) is the most commonly used assay chosen by 28.6%, followed by the sperm chromatin structure assay (24.1%), and the sperm chromatin dispersion (19.1%). The choice of the assay was largely influenced by availability (70% of respondents). A threshold of 30% was the most selected cut-off value for elevated SDF by 33.7% of clinicians. Of respondents, 53.6% recommend SDF testing after 3 to 5 days of abstinence. Although 75.3% believe SDF testing can provide an explanation for many unknown causes of infertility, the main limiting factors selected by respondents are a lack of professional society guideline recommendations (62.7%) and an absence of globally accepted references for SDF interpretation (50.3%).
Conclusions: This study represents the largest global survey on the technical aspects of SDF testing as well as the barriers encountered by clinicians. Unified global recommendations regarding clinician implementation and standard laboratory interpretation of SDF testing are crucial.