The Sixth Edition of the WHO Manual for Human Semen Analysis: A Critical Review and SWOT Analysis
Abstract
:1. Introduction
2. Critical Review of the 6th Edition
2.1. Methodological Considerations in the New 6th Edition
2.2. Basic Examination of Semen
2.3. Extended Examination of Semen
2.3.1. Sperm DNA Fragmentation
2.3.2. Genetic and Genomic Tests
2.4. Advanced Examination of Semen
2.4.1. Advanced Tests
2.4.2. Seminal Oxidative Stress and Reactive Oxygen Species
2.5. Sperm Preparation and Sperm Cryopreservation
2.6. SWOT Analysis
3. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Abbreviations
ART | assisted reproductive technology |
DNA | deoxyribonucleic acid |
FISH | fluorescence in situ hybridization |
ICSI | intracytoplasmic sperm injection |
MACS | magnetic-activated cell sorting |
MiOXSYS | male infertility oxidative system |
ORP | oxidation-reduction potential |
OS | oxidative stress |
RNA | ribonucleic acid |
ROS | reactive oxygen species |
SA | semen analysis |
SDF | sperm DNA fragmentation |
SWOT | strengths, weaknesses, opportunities, and threats |
TTP | time to pregnancy |
TUNEL | terminal deoxynucleotidyl transferase dUTP nick-end labeling |
WHO | World Health Organization |
References
- World Health Organization. Towards more objectivity in diagnosis and management of male fertility. Int. J. Androl. 1987, 7, 1–53. [Google Scholar]
- Boivin, J.; Bunting, L.; Collins, J.A.; Nygren, K.G. International estimates of infertility prevalence and treatment-seeking: Potential need and demand for infertility medical care. Hum. Reprod. 2007, 22, 1506–1512. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Available online: https://www.who.int/news-room/fact-sheets/detail/infertility (accessed on 3 December 2021).
- Patel, A.S.; Leong, J.Y.; Ramasamy, R. Prediction of male infertility by the World Health Organization laboratory manual for assessment of semen analysis: A systematic review. Arab. J. Urol. 2018, 16, 96–102. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Agarwal, A.; Baskaran, S.; Parekh, N.; Cho, C.L.; Henkel, R.; Vij, S.; Arafa, M.; Kumar, M.; Selvar, P.; Shah, R. Male infertility. Lancet 2021, 397, 319–333. [Google Scholar] [CrossRef]
- Agarwal, A.; Mulgund, A.; Hamada, A.; Chyatte, M.R. A unique view on male infertility around the globe. Reprod. Biol. Endocrinol. 2015, 13, 37. [Google Scholar] [CrossRef] [Green Version]
- Levine, H.; Jørgensen, N.; Martino-Andrade, A.; Mendiola, J.; Weksler-Derri, D.; Mindlis, I.; Pinotti, R.; Swan, S.H. Temporal trends in sperm count: A systematic review and meta-regression analysis. Hum. Reprod. Update 2017, 23, 646–659. [Google Scholar] [CrossRef]
- Barratt, C.L.R.; Björndahl, L.; De Jonge, C.J.; Lamb, D.J.; Martini, F.O.; McLachlan, R.; Oates, R.D.; Van Der Poel, S.; John, B.S.; Sigman, M.; et al. The diagnosis of male infertility: An analysis of the evidence to support the development of global WHO guidance—Challenges and future research opportunities. Hum. Reprod. Update 2017, 23, 660–680. [Google Scholar] [CrossRef]
- Guzick, D.S.; Overstreet, J.W.; Factor-Litvak, P.; Brazil, C.K.; Nakajima, S.T.; Coutifaris, C.; Carson, S.A.; Cisneros, P.; Steinkampf, M.P.; Hill, J.A.; et al. Sperm Morphology, Motility, and Concentration in Fertile and Infertile Men. N. Engl. J. Med. 2001, 345, 1388–1393. [Google Scholar] [CrossRef]
- Schlegel, P.N.; Sigman, M.; Collura, B.; De Jonge, C.J.; Eisenberg, M.L.; Lamb, D.J.; Mulhall, J.P.; Niederberger, C.; Sandlow, J.I.; Sokol, R.Z.; et al. Diagnosis and treatment of infertility in men: AUA/ASRM guideline part I. Fertil. Steril. 2021, 115, 54–61. [Google Scholar] [CrossRef]
- World Health Organization. WHO Laboratory Manual for the Examination and Processing of Human Semen, 6th ed.; WHO Press: Geneva, Switzerland, 2021; Available online: https://www.who.int/publications/i/item/9789240030787 (accessed on 3 December 2021).
- Kandil, H.; Agarwal, A.; Saleh, R.; Boitrelle, F.; Arafa, M.; Vogiatzi, P.; Henkel, R.; Zini, A.; Shah, R. Editorial Commentary on Draft of World Health Organization Sixth Edition Laboratory Manual for the Examination and Processing of Human Semen. World J. Men’s Health 2021, 39, 577. [Google Scholar] [CrossRef]
- Agarwal, A.; Finelli, R.; Selvam, M.K.P.; Leisegang, K.; Majzoub, A.; Tadros, N.; Ko, E.; Parekh, N.; Henkel, R.; Durairajanayagam, D.; et al. A Global Survey of Reproductive Specialists to Determine the Clinical Utility of Oxidative Stress Testing and Antioxidant Use in Male Infertility. World J. Men’s Health 2021, 39, 470–488. [Google Scholar] [CrossRef] [PubMed]
- World Health Organization. WHO Laboratory Manual for the Examination and Processing of Human Semen, 5th ed.; WHO Press: Geneva, Switzerland, 2010. [Google Scholar]
- Cooper, T.G.; Noonan, E.; Von Eckardstein, S.; Auger, J.; Gordon Baker, H.W.; Behre, H.M.; Haugen, T.B.; Kruger, T.; Wang, C.; Mbizvo, M.T.; et al. World Health Organization reference values for human semen characteristics. Hum. Reprod. Updat. 2009, 16, 231–245. [Google Scholar] [CrossRef]
- Esteves, S.C.; Zini, A.; Aziz, N.; Alvarez, J.G.; Sabanegh, E.S., Jr.; Agarwal, A. Critical appraisal of World Health Organization’s new reference values for human semen characteristics and effect on diagnosis and treatment of subfertile men. Urology 2012, 79, 16–22. [Google Scholar] [CrossRef] [PubMed]
- Björndahl, L. What is normal semen quality? On the use and abuse of reference limits for the interpretation of semen analysis results. Hum. Fertil. 2011, 14, 179–186. [Google Scholar] [CrossRef] [PubMed]
- Campbell, M.J.; Lotti, F.; Baldi, E.; Schlatt, S.; Festin, M.P.R.; Björndahl, L.; Toskin, I.; Barratt, C.L.R. Distribution of semen examination results 2020—A follow up of data collated for the WHO semen analysis manual. Andrology 2021, 9, 817–822. [Google Scholar] [CrossRef]
- Mortimer, D. Practical Laboratory Andrology; Oxford University Press: New York, NY, USA, 1994; 393p. [Google Scholar]
- World Health Organization. WHO Laboratory Manual for the Examination of Human Semen and Sperm-Cervical Mucus Interaction, 4th ed.; Cambridge University Press: Cambridge, UK, 1999; pp. 96–99. [Google Scholar]
- Aitken, R.J.; Sutton, M.; Warner, P.; Richardson, D.W. Relationship between the movement characteristics of human spermatozoa and their ability to penetrate cervical mucus and zona-free hamster oocytes. Reproduction 1985, 73, 441–449. [Google Scholar] [CrossRef]
- Mortimer, D.; Pandya, I.J.; Sawers, R.S. Relationship between human sperm motility characteristics and sperm penetration into human cervical mucus in vitro. Reproduction 1986, 78, 93–102. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Barratt, C.; McLeod, I.; Dunphy, B.; Cooke, I. Prognostic value of two putative sperm function tests: Hypo-osmotic swelling and bovine sperm mucus penetration test (Penetrak). Hum. Reprod. 1992, 7, 1240–1244. [Google Scholar] [CrossRef]
- Björndahl, L. The usefulness and significance of assessing rapidly progressive spermatozoa. Asian, J. Androl. 2010, 12, 33–35. [Google Scholar] [CrossRef] [Green Version]
- Bollendorf, A.; Check, J.H.; Lurie, D. Evaluation of the effect of the absence of sperm with rapid and linear progressive motility on subsequent pregnancy rates following intrauterine insemination or in vitro fertilization. J. Androl. 1996, 17, 550–557. [Google Scholar]
- Comhaire, F.H.; Vermeulen, L.; Hinting, A.; Schoonjans, F. Accuracy of sperm characteristics in predicting the in vitro fertilizing capacity of semen. J. Assist. Reprod. Genet. 1988, 5, 326–331. [Google Scholar] [CrossRef] [PubMed]
- Eliasson, R. Semen analysis with regard to sperm number, sperm morphology and functional aspects. Asian J. Androl. 2010, 12, 26–32. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Irvine, D.; Aitken, R.J. Predictive value of in-vitro sperm function tests in the context of an AID service. Hum. Reprod. 1986, 1, 539–545. [Google Scholar] [CrossRef]
- Sifer, C.; Sasportes, T.; Barraud, V.; Poncelet, C.; Rudant, J.; Porcher, R.; Cedrin-Durnerin, I.; Martin-Pont, B.; Hugues, J.; Wolf, J. World Health Organization grade ‘a’ motility and zona-binding test accurately predict IVF outcome for mild male factor and unexplained infertilities. Hum. Reprod. 2005, 20, 2769–2775. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Van den Bergh, M.; Emiliani, S.; Biramane, J.; Vannin, A.S.; Englert, Y. A first prospective study of the individual straight line velocity of the spermatozoon and its influences on the fertilization rate after intracytoplasmic sperm injection. Hum Reprod. 1998, 13, 3103–3107. [Google Scholar] [CrossRef] [Green Version]
- Ward, W.S. Function of sperm chromatin structural elements in fertilization and development. Mol. Hum. Reprod. 2009, 16, 30–36. [Google Scholar] [CrossRef] [Green Version]
- Miyamoto, T.; Minase, G.; Shin, T.; Ueda, H.; Okada, H.; Sengoku, K. Human male infertility and its genetic causes. Reprod. Med. Biol. 2017, 16, 81–88. [Google Scholar] [CrossRef]
- Godo, A.; Blanco, J.; Vidal, F.; Sandalinas, M.; Garcia-Guixé, E.; Anton, E. Altered segregation pattern and numerical chromosome abnormalities interrelate in spermatozoa from Robertsonian translocation carriers. Reprod. Biomed. Online 2015, 31, 79–88. [Google Scholar] [CrossRef] [Green Version]
- Wang, B.; Nie, B.; Tang, D.; Li, R.; Liu, X.; Song, J.; Wang, W.; Liu, Z. Analysis of meiotic segregation patterns and interchromosomal effects in sperm from 13 robertsonian translocations. Balk. J. Med. Genet. 2017, 20, 43–50. [Google Scholar] [CrossRef]
- Magli, M.C.; Crippa, A.; Benincasa, M.; Terzuoli, G.; Azzena, S.; Maresca, L.; Albanese, C.; Colombo, F.; Ferraretti, A.P.; Gianaroli, L. Sperm chromosome abnormalities in patients with normal karyotype and in translocation carriers: Clinical relevance for assisted reproductive technology. Reprod. Biomed. Online 2020, 41, 1055–1069. [Google Scholar] [CrossRef]
- Hwang, K.; Weedin, J.W.; Lamb, D.J. The use of fluorescent in situ hybridization in male infertility. Ther. Adv. Urol. 2010, 2, 157–169. [Google Scholar] [CrossRef] [Green Version]
- Kohn, T.P.; Kohn, J.R.; Darilek, S.; Ramasamy, R.; Lipshultz, L. Genetic counseling for men with recurrent pregnancy loss or recurrent implantation failure due to abnormal sperm chromosomal aneuploidy. J. Assist. Reprod Genet. 2016, 33, 571–576. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Donkin, I.; Barrès, R. Sperm epigenetics and influence of environmental factors. Mol. Metab. 2018, 14, 1–11. [Google Scholar] [CrossRef]
- Sies, H. Biochemistry of oxidative stress. Chem. Int. Ed. Engl. 1986, 25, 1058–1071. [Google Scholar] [CrossRef]
- Aitken, R.J.; West, K.M. Analysis of the relationship between reactive oxygen species production and leucocyte infiltration in fractions of human semen separated on Percoll gradients. Int. J. Androl. 1990, 13, 433–451. [Google Scholar] [CrossRef] [PubMed]
- Aitken, R. A free radical theory of male infertility. Reprod. Fertil. Dev. 1994, 6, 19–23. [Google Scholar] [CrossRef] [PubMed]
- Agarwal, A.; Said, T. Oxidative stress, DNA damage and apoptosis in male infertility: A clinical approach. BJU Int. 2005, 95, 503–507. [Google Scholar] [CrossRef] [PubMed]
- Agarwal, A.; Prabakaran, S.; Allamaneni, S.S. Relationship between oxidative stress, varicocele and infertility: A meta-analysis. Reprod. Biomed. Online 2006, 12, 630–633. [Google Scholar] [CrossRef]
- Saleh, R.; Agarwal, A.; Kandirali, E.; Sharma, R.; Thomas, A.J.; Nada, E.; Evenson, D.P.; Alvarez, J.G. Leukocytospermia is associated with increased reactive oxygen species production by human spermatozoa. Fertil. Steril. 2002, 78, 1215–1224. [Google Scholar] [CrossRef]
- Ramalho-Santos, S.A.A.P.J.O.J.; Amaral, S.; Oliveira, P. Diabetes and the Impairment of Reproductive Function: Possible Role of Mitochondria and Reactive Oxygen Species. Curr. Diabetes Rev. 2008, 4, 46–54. [Google Scholar] [CrossRef] [PubMed]
- Leisegang, K.; Sengupta, P.; Agarwal, A.; Henkel, R. Obesity and male infertility: Mechanisms and management. Andrology 2021, 53, e13617. [Google Scholar] [CrossRef] [PubMed]
- Cicek, O.S.Y.; Kaya, G.; Alyuruk, B.; Doger, E.; Girisen, T.; Filiz, S. The association of seminal oxidation reduction potential with sperm parameters in patients with unexplained and male factor infertility. Int. Braz. J. Urol. 2021, 47, 112–119. [Google Scholar] [CrossRef] [PubMed]
- Garcia-Segura, S.; Ribas-Maynou, J.; Lara-Cerrillo, S.; Garcia-Peiró, A.; Castel, A.; Benet, J.; Oliver-Bonet, M. Relationship of Seminal Oxidation-Reduction Potential with Sperm DNA Integrity and pH in Idiopathic Infertile Patients. Biology 2020, 9, 262. [Google Scholar] [CrossRef] [PubMed]
- Aitken, R.; De Iuliis, G. On the possible origins of DNA damage in human spermatozoa. Mol. Hum. Reprod. 2010, 16, 3–13. [Google Scholar] [CrossRef] [Green Version]
- ElBardisi, H.; Finelli, R.; Agarwal, A.; Majzoub, A.; Henkel, R.; Arafa, M. Predictive value of oxidative stress testing in semen for sperm DNA fragmentation assessed by sperm chromatin dispersion test. Andrology 2019, 8, 610–617. [Google Scholar] [CrossRef]
- Ferramosca, A.; Provenzano, S.P.; Montagna, D.D.; Coppola, L.; Zara, V. Oxidative Stress Negatively Affects Human Sperm Mitochondrial Respiration. Urology 2013, 82, 78–83. [Google Scholar] [CrossRef]
- Gualtieri, R.; Kalthur, G.; Barbato, V.; Longobardi, S.; Di Rella, F.; Adiga, S.; Talevi, R. Sperm Oxidative Stress during In Vitro Manipulation and Its Effects on Sperm Function and Embryo Development. Antioxidants 2021, 10, 1025. [Google Scholar] [CrossRef]
- Koppers, A.J.; De Iuliis, G.N.; Finnie, J.M.; McLaughlin, E.A.; Aitken, R.J. Significance of Mitochondrial Reactive Oxygen Species in the Generation of Oxidative Stress in Spermatozoa. J. Clin. Endocrinol. Metab. 2008, 93, 3199–3207. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lewis, S.E.; Aitken, R.J.; Conner, S.J.; De Iuliis, G.; Evenson, D.P.; Henkel, R.; Giwercman, A.; Gharagozloo, P. The impact of sperm DNA damage in assisted conception and beyond: Recent advances in diagnosis and treatment. Reprod. Biomed. Online 2013, 27, 325–337. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Morris, A.; Siebert, I.; Agarwal, A.; Henkel, R. Prediction of successful ICSI cycles by Oxidation-reduction potential (ORP) and sperm DNA fragmentation (SDF) analysis. A Prospective study. Hum. Reprod. 2019, 34 (Suppl. 1), i8. [Google Scholar]
- Softness, K.A.; Trussler, J.T.; Carrasquillo, R.J. Advanced sperm testing. Curr. Opin. Urol. 2020, 30, 290–295. [Google Scholar] [CrossRef] [PubMed]
- Agarwal, A.; Arafa, M.; Chandrakumar, R.; Majzoub, A.; Alsaid, S.; ElBardisi, H. A multicenter study to evaluate oxidative stress by oxidation-reduction potential, a reliable and reproducible method. Andrology 2017, 5, 939–945. [Google Scholar] [CrossRef] [PubMed]
- Agarwal, A.; Roychoudhury, S.; Sharma, R.; Gupta, S.; Majzoub, A.; Sabanegh, E. Diagnostic application of oxidation-reduction potential assay for measurement of oxidative stress: Clinical utility in male factor infertility. Reprod. Biomed. Online 2017, 34, 48–57. [Google Scholar] [CrossRef] [Green Version]
- Karabulut, S.; Korkmaz, O.; Yılmaz, E.; Keskin, I. Seminal oxidation–reduction potential as a possible indicator of impaired sperm parameters in Turkish population. Andrology 2021, 53, e13956. [Google Scholar] [CrossRef]
- Nakamura, H.; Hosono, T.; Taniguchi, T.; Kumasawa, K.; Goa, S.; Ono, M.; Kimura, T. Prediction of pregnancy after frozen-thawed embryo transfer via in vivo intrauterine oxidation-reduction potential measurements: A pilot study. Reprod. Med. Biol. 2018, 17, 255–261. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kuroda, S.; Takeshima, T.; Takeshima, K.; Usui, K.; Yasuda, K.; Sanjo, H.; Kawahara, T.; Uemura, H.; Murase, M.; Yumura, Y. Early and late paternal effects of reactive oxygen species in semen on embryo development after intracytoplasmic sperm injection. Syst. Biol. Reprod. Med. 2020, 66, 122–128. [Google Scholar] [CrossRef] [PubMed]
- Rhemrev, J.P.; Menkveld, R.; Roseboom, T.J.; Van Overveld, F.W.; Teerlink, T.; Lombard, C.; Vermeiden, J.P. The acrosome index, radical buffer capacity and number of isolated progressively motile spermatozoa predict IVF results. Hum. Reprod. 2001, 16, 1885–1892. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Halliwell, B.; Gutteridge, J.M.C. Free Radicals in Biology and Medicine, 5th ed.; Oxford University Press: New York, NY, USA, 2015. [Google Scholar] [CrossRef]
- Agarwal, A.; Selvam, M.K.; Arafa, M.; Okada, H.; Homa, S.; Killeen, A.; Balaban, B.; Saleh, R.; Armagan, A.; Roychoudhury, S.; et al. Multi-center evaluation of oxidation-reduction potential by the MiOXSYS in males with abnormal semen. Asian J. Androl. 2019, 21, 565–569. [Google Scholar] [CrossRef]
- Aitken, R.; Wingate, J.K.; De Iuliis, G.; McLaughlin, E. Analysis of lipid peroxidation in human spermatozoa using BODIPY C11. Mol. Hum. Reprod. 2007, 13, 203–211. [Google Scholar] [CrossRef] [Green Version]
- Agarwal, A.; Henkel, R.; Sharma, R.; Tadros, N.N.; Sabanegh, E. Determination of seminal oxidation-reduction potential (ORP) as an easy and cost-effective clinical marker of male infertility. Andrology 2017, 50, e12914. [Google Scholar] [CrossRef] [PubMed]
- Tanaka, T.; Kobori, Y.; Terai, K.; Inoue, Y.; Osaka, A.; Yoshikawa, N.; Shimomura, Y.; Suzuki, K.; Minami, T.; Iwahata, T.; et al. Seminal oxidation–reduction potential and sperm DNA fragmentation index increase among infertile men with varicocele. Hum. Fertil. 2020, 2020, 1–5. [Google Scholar] [CrossRef] [PubMed]
- McDowell, S.; Kroon, B.; Ford, E.; Hook, Y.; Glujovsky, D.; Yazdani, A. Advanced sperm selection techniques for assisted reproduction. Cochrane Database Syst. Rev. 2014, 7, CD010461. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Teoli, D.; Sanvictores, T.; An, J. SWOT Analysis. In StatPearls; StatPearls Publishing: Treasure Island, FL, USA, 2021. [Google Scholar]
WHO 5th Edition (2010) | Page Number WHO 5th | WHO 6th Edition (2021) | Page Number WHO 6th | |
---|---|---|---|---|
Objectives | ● Improve the manual by adding detailed description of semen tests and reference ranges | 1–3 | ● Assist fertility/infertility diagnosis | 1–2 |
● Update SA procedures | 1–3 | ● Assess male reproductive health | 1–2 | |
● Emphasize quality assurance in semen laboratories | 179–202 | ● Guide the choice of ART procedure | 1–2 | |
● Monitor response to treatment | 1–2 | |||
● Measure the efficacy of male contraception | 1–2 | |||
● Update SA procedures | 2–3 | |||
● Eliminate outdated tests | 3 | |||
Methods | ● Reference ranges are provided using 5th centiles based on: | 3 | ● Reference ranges and 5th centiles are insufficient to diagnose infertility; 5th centiles are based on: | 4, 211–213 |
● Multicenter studies with retrospective data analysis | 223–225 | ● Integration of the 2010 data and reanalysis with data published in the last decade | 4, 211–213 | |
● 1953 men with TTP ≤ 12 months | Cooper et al. [15] | ● 3589 men with TTP ≤ 12 months | 211–213 | |
● 8 countries, 4 continents (Oceania, Americas, Europe) | Cooper et al. [15] | ● 13 countries, 6 continents (Asia, Americas, Europe, Africa, Oceania) | Campbell et al. [18] |
WHO 2010 | WHO 2021 | |
---|---|---|
Semen volume (mL) | 1.5 (1.4–1.7) | 1.4 (1.3–1.5) |
Total sperm number (106 per ejaculate) | 39 (33–46) | 39 (35–40) |
Total motility (%) | 40 (38–42) | 42 (40–43) |
Progressive motility (%) | 32 (31–34) | 30 (29–31) |
Non progressive motility (%) | 1 | 1 (1–1) |
Immotile sperm (%) | 22 | 20 (19–20) |
Vitality (%) | 58 (55–63) | 54 (50–56) |
Normal forms (%) | 4 (3–4) | 4 (3.9–4) |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Boitrelle, F.; Shah, R.; Saleh, R.; Henkel, R.; Kandil, H.; Chung, E.; Vogiatzi, P.; Zini, A.; Arafa, M.; Agarwal, A. The Sixth Edition of the WHO Manual for Human Semen Analysis: A Critical Review and SWOT Analysis. Life 2021, 11, 1368. https://doi.org/10.3390/life11121368
Boitrelle F, Shah R, Saleh R, Henkel R, Kandil H, Chung E, Vogiatzi P, Zini A, Arafa M, Agarwal A. The Sixth Edition of the WHO Manual for Human Semen Analysis: A Critical Review and SWOT Analysis. Life. 2021; 11(12):1368. https://doi.org/10.3390/life11121368
Chicago/Turabian StyleBoitrelle, Florence, Rupin Shah, Ramadan Saleh, Ralf Henkel, Hussein Kandil, Eric Chung, Paraskevi Vogiatzi, Armand Zini, Mohamed Arafa, and Ashok Agarwal. 2021. "The Sixth Edition of the WHO Manual for Human Semen Analysis: A Critical Review and SWOT Analysis" Life 11, no. 12: 1368. https://doi.org/10.3390/life11121368