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“Oligozoospermia,” “azoospermia,” and other semen-analysis terminology: the need for better science
EDITOR’S CORNER ‘‘Oligozoospermia,’’ ‘‘azoospermia,’’ and other semen-analysis terminology: the need for better science David A. Grimes, M.D., and Laureen M. Lopez, Ph.D. Family Health International, Research Triangle Park, North Carolina
The Greek-based terms used to describe semen-analysis abnormalities (e.g., ‘‘oligozoospermia’’ and ‘‘azoospermia’’) are unscientific, have overlapping definitions, and are often misinterpreted. The best course is to abandon these vague and difficult labels and simply report semen analyses quantitatively. (Fertil Steril 2007;88:1491–4. 2007 by American Society for Reproductive Medicine.)
The terminology used to describe semen variables needs rethinking. The initial definitions proposed in 1970 were not evidence based (1). Authors since then have used overlapping definitions (2), and the words are among the most daunting in the English language (3). The abandonment of quantitative definitions by the World Health Organization (WHO) in 1999 left these terms with little scientific utility (Table 1) (4). Behera et al. recently argued in these pages for the retirement of the term ‘‘polycystic ovary syndrome’’ (5). Similarly, ‘‘oligozoospermia,’’ ‘‘azoospermia,’’ and other descriptors of semen analysis based on Greek should be abandoned for both scientific and linguistic reasons. UNSCIENTIFIC DEVELOPMENT The initial definitions proposed were the antithesis of evidence-based medicine. An ‘‘andrology club’’ met three times, and after a meeting in Hamburg, Germany, in 1970, the ‘‘club’’ proposed new definitions (1). Of note, no scientific evidence relating semen analysis characteristics to fertility (6–9) or other references were provided as justification (1). Guidelines based on expert opinions have been repeatedly shown to be inferior to those based on evidence (10). OVERLAPPING DEFINITIONS A case definition must be clear, specific, and measurable (11). Oligozoospermia and azoospermia do not meet this standard, because of overlapping definitions. The initial definition of oligozoospermia was <40 million sperm/mL, and that of azoospermia was ‘‘no spermatozoa’’ (1). According to these Received February 21, 2007; revised and accepted April 19, 2007. Supported in part by Family Health International (FHI) with funds from the National Institutes of Health (NIH); the views expressed in this article do not necessarily reflect those of FHI or NIH. Reprint requests: David A. Grimes, M.D., Family Health International, P.O. Box 13950, Research Triangle Park, NC 27709 (FAX: 919-544-7261; E-mail: [email protected]).
0015-0282/07/$32.00 doi:10.1016/j.fertnstert.2007.04.013
definitions, a man with azoospermia has both azoospermia and oligozoospermia, because zero sperm is less than 40 million/mL. This overlapping terminology has confused the andrology literature for a third of a century. While reviewing randomized controlled trials of male hormonal contraceptives, we found extensive misuse of these terms (12). Many authors defined these terms as described above yet analyzed their results as if azoospermia and oligozoospermia were separate and distinct entities. The internal inconsistencies precluded comparison of rates of oligozoospermia. For example, one trial (13) reported that, ‘‘In the placebo group 4 out of 14 and in the LNG [levonorgestrel] group 7 out of 14 men achieved severe oligozoospermia (<3 billion/L).’’ However, in an erratum, one of the authors reported severe oligozoospermia in ‘‘12/14 and 14/14 volunteers of the placebo and gestagen-treated groups, respectively’’ (14). In the original report, ‘‘azoospermia’’ was not included in the category of ‘‘severe oligozoospermia,’’ whereas in the erratum it was. VARIABLE (OR NO) DEFINITIONS Definitions of normal morphology vary. The American Urological Association and American Society of Reproductive Medicine’s table of ‘‘reference values’’ for semen analysis is illustrative. Three different values for normal morphology are given: >50%, >30%, and >14% (7). Interpretation of oligozoospermia reports is even more difficult because of inconsistent or no definitions. In the initial recommendations (1), the definition of oligozoospermia was <40 million/mL. In 1981, the U.S. Food and Drug Administration proposed %5 million/mL (15). By the third edition of the World Health Organization (WHO) laboratory manual for semen analysis (1992), the definition had changed to <20 million/mL (16), although the WHO manual continued to cite the original recommendations as the source (1).
Fertility and Sterility Vol. 88, No. 6, December 2007 Copyright ª2007 American Society for Reproductive Medicine, Published by Elsevier Inc.
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TABLE 1 Changing Nomenclature for Semen Variables Recommended by the World Health Organization, 1992 and 1999 (4, 16). Definition Term
1992 (16)
Normozoospermiaa Oligozoospermiaa Asthenozoospermiaa
Teratozoospermiaa Oligoasthenoteratozoospermia
Azoospermia Aspermia a
Normal ejaculate as defined in [Appendix] 1A Sperm concentration fewer than 20 106/mL Fewer than 50% spermatozoa with forward progression (categories ‘a’ and ‘b’) or fewer than 25% spermatozoa with category ‘a’ movement (see Section 2.4.2) Fewer than 30% spermatozoa with normal morphology Signifies disturbance of all three variables (combinations of only two prefixes may also be used) No spermatozoa in the ejaculate No ejaculate
1999 (4) Normal ejaculate as defined by the reference values Sperm concentration less than the reference value Less than the reference value for motility
Less than the reference value for morphology Signifies disturbance of all three variables (combinations of only two prefixes may also be used) No spermatozoa in the ejaculate No ejaculate
Definition changed.
Grimes. Improving semen analysis terminology. Fertil Steril 2007.
By the Fourth Edition of the WHO manual (1999), numerical definitions for these terms had been abandoned altogether, except as they relate to unspecified ‘‘reference values’’ (Table 1) (4). Without a quantitative definition, the term ‘‘oligozoospermia’’ loses any scientific utility (6, 9, 17). The same criticism holds for ‘‘normozoospermia,’’ ‘‘asthenozoospermia,’’ teratozoospermia,’’ and ‘‘oligoasthenoteratozoospermia,’’ all of which now lack quantitative definitions (4). Failing to have quantitative definitions for these terms is analogous to defining obesity as ‘‘more than the reference value,’’ instead of a body mass index (BMI) R30 kg/m2. The mean BMI is higher in Alabama than in Colorado (18). Without a uniform, quantitative definition, some overweight persons in Colorado would immediately lose the diagnosis of ‘‘obesity’’ (but not the weight) upon moving to Alabama. They would be above the BMI ‘‘reference value’’ in Colorado but within the higher ‘‘reference value’’ in Alabama. Medicine and science require uniform definitions, not shifting targets. Similar confusion surrounds ‘‘severe oligozoospermia.’’ Some authors use this phrase without definition (19, 20). Others define ‘‘severe’’ as <100,000/mL (21), <3 million/mL (14), <5 million/mL (22, 23), or <10 million/mL (24). Still others define ‘‘severe’’ as 200,000/mL to 4 million/mL (25). Inconsistent terminology makes comparison of reported ‘‘severe oligozoospermia’’ across studies impossible. 1492
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‘‘POMPOUS DICTION’’ Replacing unnecessarily formal words with simple ones makes diction sharper and more direct (26). Medical writing is justly criticized for its abuse of English; a stubborn problem is ‘‘medicalese’’—jargon that obscures rather than clarifies intent (27–29). Terms such as ‘‘oligozoospermia’’ (and its longer permutations) readily fall into this category of medical ‘‘puffery.’’ Some of these terms are not recognized words; they do not appear in standard medical dictionaries, despite decades of use. An example used by the WHO is ‘‘normozoospermia’’ (4), which is not listed in Stedman’s Medical Dictionary (30). Other unapproved neologisms include ‘‘hyperspermia’’ (31), ‘‘leucocytospermia’’ (23), ‘‘polyzoospermia’’ (32), and ‘‘globozoospermia’’ (33). For those interested in Greek, variations on this theme might include ‘‘planktozoospermia’’ (wandering sperm), ‘‘tachozoospermia’’ (fast swimmers), and ‘‘nosozoospermia’’ (sick but not yet ‘‘necrozoospermia’’) (23). Sperm-count descriptors rival the most cumbersome words in English. As might be anticipated, the longest English word is medical; it contains 30 letters: ‘‘pseudopseudohypoparathyroidism’’ (3). However, the longest nontechnical word is ‘‘floccinaucinihilipilification’’ at 29 letters. ‘‘Oligoasthenoteratozoospermia’’ (4) (28 letters) is not far behind, but because it is not a legitimate word (30) it may not count.
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These terms are tough to spell. For example, a recent report in the journal of the American Society of Andrology misspelled ‘‘oligozoospermia’’ and inadvertently created another neologism: ‘‘oligoazoospermia’’ (34). A report published in the American College of Obstetricians and Gynecologists journal misspelled ‘‘azoospermia’’ throughout (35). These errors were missed by authors, reviewers, editors, and proofreaders alike. No wonder: this is the stuff of spelling bees. Apparently, ‘‘oligozoospermia’’ was misspelled in the past, and the error got legitimized, because ‘‘oligospermia’’ is listed in dictionaries as a synonym for the former (30). LACK OF PREDICTIVE VALUE Because these definitions were not based on empiric evidence, they have poor predictive value (36). Recent studies have confirmed the inability to predict fertility based on these sperm descriptions (7). Morphology appears to be the most informative sperm characteristic, but none of the measures alone or together can diagnose infertility (6–9). Spontaneous pregnancies occur with sperm counts less than 100,000/mL (37). PROPOSED REMEDIES The definitions of sperm characteristics first promulgated by a ‘‘club’’ in 1970 impede rather than facilitate scientific communication. These terms were flawed at inception (1). For example, ‘‘asthenozoospermia’’ is a misnomer, because ‘‘astheneia’’ in Greek refers to weakness, not motility (30). These problems are compounded by inconsistent and often poor laboratory methods for semen analysis (17, 38) as
well as sizeable intraindividual variation in semen quality and quantity (39). Because WHO has now abandoned quantitative definitions, these terms should be discarded as well. Instead, physicians and scientists should report semen analysis numerically (Table 2). Moreover, using arbitrary dichotomous labels for continuous variables (e.g., sperm count) loses information: continuous data should be presented as such, and not be dichotomized above or below some cut point (40). Proportions of sperm with normal form or motility (or, alternatively, abnormal form or lack of motility) should be reported as well. For example, the percentage of motile spermatozoa should replace ‘‘asthenozoospermia.’’ The proportion of round-headed spermatozoa should supplant ‘‘globozoospermia.’’ Simple English adjectives (e.g., ‘‘low’’) could be used if desired, provided they are defined numerically. However, if these unscientific terms are to remain in clinical use, then the overlapping definitions of oligozoospermia and azoospermia must be resolved. For example, azoospermia should be defined as no sperm after centrifugation at 3000g for 15 minutes and examination of the pellet (7). To evaluate vasectomy success, the British Andrology Society also recommends centrifugation if no sperm are seen on direct microscopy (41). However, given the different laboratory techniques used today, detection of azoospermia varies. Oligozoospermia could be defined as >0 but <20 million/mL, for example. Thus, azoospermia and oligozoospermia would finally be mutually exclusive terms. Adoption of better, more scientific terminology will improve both research and clinical practice in andrology. The current nomenclature is simply untenable.
TABLE 2 Proposed replacements for semen-analysis terminology based on Greek. Traditional Term (4)
Proposed Replacement
Normozoospermia
Ejaculate volume in mL
Oligozoospermia
Number of spermatozoa per mL
Asthenozoospermia
Proportion of motile spermatozoa
Teratozoospermia
Proportion of normally shaped spermatozoa
Oligoasthenoteratozoospermia
[discard]
Azoospermia Aspermia
No spermatozoa No ejaculate
Rationale Provides continuous rather than dichotomous data (40); simplifies spelling and definition (26) Provides continuous rather than dichotomous data (40); simplifies spelling and definition (26) Provides continuous rather than dichotomous data (40); simplifies spelling and definition (26) Provides continuous rather than dichotomous data (40); simplifies spelling and definition (26) Avoids dichotomizing combinations of characteristics (40) Simplifies spelling and definition (26) Simplifies spelling and definition (26)
Grimes. Improving semen analysis terminology. Fertil Steril 2007.
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REFERENCES 1. Eliasson R, Hellinga F, Lubcke F, Meyhofer W, Niermann H, Steeno O, et al. Empfehlungen zur Nomenklatur in der Andrologie. Andrologie 1970;2:186–7. 2. Grimes DA, Gallo MF, Grigorieva V, Nanda K, Schulz KF. Steroid hormones for contraception in men: systematic review of randomized controlled trials. Contraception 2005;71:89–94. 3. Wikipedia. Longest word in English. Available at: http://en.wikipedia. org/wiki/Longest_word_in_English. Accessed December 29, 2006. 4. World Health Organization. WHO laboratory manual for the examination of human semen and sperm–cervical mucus interaction. 4th ed. Cambridge, UK: Cambridge University Press, 1999. 5. Behera M, Price T, Walmer D. Estrogenic ovulatory dysfunction or functional female hyperandrogenism: an argument to discard the term polycystic ovary syndrome. Fertil Steril 2006;86:1292–5. 6. Menkveld R, Wong WY, Lombard CJ, Wetzels AM, Thomas CM, Merkus HM, et al. Semen parameters, including WHO and strict criteria morphology, in a fertile and subfertile population: an effort toward standardization of in-vivo thresholds. Hum Reprod 2001;16:1165–71. 7. Male Infertility Best Practice Policy Committee of the American Urological Association; Practice Committee of the American Society for Reproductive Medicine. Report on optimal evaluation of the infertile male. Fertil Steril 2006;86(Suppl 5):S202–9. 8. Guzick DS, Overstreet JW, Factor-Litvak P, Brazil CK, Nakajima ST, Coutifaris C, et al. Sperm morphology, motility, and concentration in fertile and infertile men. N Engl J Med 2001;345:1388–93. 9. Ombelet W, Bosmans E, Janssen M, Cox A, Vlasselaer J, Gyselaers W, et al. Semen parameters in a fertile versus subfertile population: a need for change in the interpretation of semen testing. Hum Reprod 1997; 12:987–93. 10. Grimes DA, Hubacher D, Nanda K, Schulz KF, Moher D, Altman DG. The Good Clinical Practice guideline: a bronze standard for clinical research. Lancet 2005;366:172–4. 11. Grimes DA, Schulz KF. Descriptive studies: what they can and cannot do. Lancet 2002;359:145–9. 12. Grimes D, Lopez LM, Gallo MF, Halper V, Nanda K, Schulz KF. Steroid hormones for contraception in men. Cochrane Database Syst Rev 2007;(2):CD004316. 13. Kamischke A, Ploger D, Venherm S, von Eckardstein S, von Eckardstein A, Nieschlag E. Intramuscular testosterone undecanoate with or without oral levonorgestrel: a randomized placebo-controlled feasibility study for male contraception. Clin Endocrinol (Oxf) 2000;53:43–52. 14. Nieschlag E. Erratum: intramuscular testosterone undecanoate with or without oral levonorgestrel: a randomized placebo-controlled feasibility study for male contraception. Clin Endocrinol 2000;53:661. 15. Schaffenburg CA, Gregoire AT, Gueriguian JL. Guidelines for the clinical testing of male contraceptive drugs. J Androl 1981;2:225–8. 16. World Health Organization. WHO laboratory manual for the examination of human semen and sperm–cervical mucus interaction. 3rd ed. Cambridge, UK: Cambridge University Press, 1992. 17. Riddell D, Pacey A, Whittington K. Lack of compliance by UK andrology laboratories with World Health Organization recommendations for sperm morphology assessment. Hum Reprod 2005;20:3441–5. 18. Mokdad AH, Ford ES, Bowman BA, Dietz WH, Vinicor F, Bales VS, et al. Prevalence of obesity, diabetes, and obesity-related health risk factors, 2001. JAMA 2003;289:76–9.
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19. Cavallini G. Male idiopathic oligoasthenoteratozoospermia. Asian J Androl 2006;8:143–57. 20. Sharlip ID. New options for managing severe oligospermia and azoospermia. West J Med 1996;164:345–6. 21. Sokal D, Irsula B, Chen-Mok M, Labrecque M, Barone MA. A comparison of vas occlusion techniques: cautery more effective than ligation and excision with fascial interposition. BMC Urol 2004;4:12. 22. Strassburger D, Friedler S, Raziel A, Schachter M, Kasterstein E, Ronel R. Very low sperm count affects the result of intracytoplasmic sperm injection. J Assist Reprod Genet 2000;17:431–6. 23. Hirsh A. Male subfertility. BMJ 2003;327:669–72. 24. Centola GM. Successful treatment of severe oligozoospermia with sperm washing and intrauterine insemination. J Androl 1997;18:448–53. 25. Levitas E, Lunenfeld E, Weiss N, Friger M, Har-Vardi I, Koifman A, et al. Relationship between the duration of sexual abstinence and semen quality: analysis of 9,489 semen samples. Fertil Steril 2005;83:1680–6. 26. Williams JM. Style: ten lessons in clarity and grace. 3rd edition. Glenview, IL: Scott, Foresman and Company, 1989. 27. Friedman EA, Pennisi JA. Eschew obfuscation. Obstet Gynecol 1996;87: 795–6. 28. Crichton M. Sounding board: medical obfuscation: structure and function. N Engl J Med 1975;293:1257–9. 29. Ingelfinger FJ. ‘‘Obfuscation’’ in medical writing [editorial]. N Engl J Med 1976;294:546–7. 30. Stedman’s medical dictionary. 27th ed. Philadelphia: Lippincott Williams & Wilkins, 2000. 31. Cooke S, Tyler JP, Driscoll GL. Hyperspermia: the forgotten condition? Hum Reprod 1995;10:367–8. 32. Merino G, Carranza-Lira S. Semen characteristics, endocrine profiles, and testicular biopsies of infertile men of different ages. Arch Androl 1995;35:219–24. 33. Dam AH, Feenstra I, Westphal JR, Ramos L, van Golde RJ, Kremer JA. Globozoospermia revisited. Hum Reprod Update 2007;13:63–75. 34. Anawalt BD, Amory JK, Herbst KL, Coviello AD, Page ST, Bremner WJ, et al. Intramuscular testosterone enanthate plus very low dosage oral levonorgestrel suppresses spermatogenesis without causing weight gain in normal young men: a randomized clinical trial. J Androl 2005;26:405–13. 35. Jamieson DJ, Costello C, Trussell J, Hillis SD, Marchbanks PA, Peterson HB. The risk of pregnancy after vasectomy. Obstet Gynecol 2004;103:848–50. 36. Forti G, Krausz C. Clinical review 100: evaluation and treatment of the infertile couple. J Clin Endocrinol Metab 1998;83:4177–88. 37. Matorras R, Diez J, Corcostegui B, Gutierrez de Teran G, Garcia JM, Pijoan JI, et al. Spontaneous pregnancy in couples waiting for artificial insemination donor because of severe male infertility. Eur J Obstet Gynecol Reprod Biol 1996;70:175–8. 38. De Jonge CJ, Barratt CL. WHO manual . who should care? Hum Reprod 1999;14:2431–3. 39. Tielemans E, Heederik D, Burdorf A, Loomis D, Habbema DF. Intraindividual variability and redundancy of semen parameters. Epidemiology 1997;8:99–103. 40. Lang TA, Secic M. How to report statistics in medicine. Philadelphia: American College of Physicians, 1997. 41. Hancock P, McLaughlin E. British Andrology Society guidelines for the assessment of post vasectomy semen samples (2002). J Clin Pathol 2002;55:812–6.
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The Greek-based terms used to describe semen-analysis abnormalities (e.g., ‘‘oligozoospermia’’ and ‘‘azoospermia’’) are unscientific, have overlapping definitions, and are often misinterpreted. The best course is to abandon these vague and difficult labels and simply report semen analyses quantitatively. (Fertil Steril 2007;88:1491–4. 2007 by American Society for Reproductive Medicine.)
The terminology used to describe semen variables needs rethinking. The initial definitions proposed in 1970 were not evidence based (1). Authors since then have used overlapping definitions (2), and the words are among the most daunting in the English language (3). The abandonment of quantitative definitions by the World Health Organization (WHO) in 1999 left these terms with little scientific utility (Table 1) (4). Behera et al. recently argued in these pages for the retirement of the term ‘‘polycystic ovary syndrome’’ (5). Similarly, ‘‘oligozoospermia,’’ ‘‘azoospermia,’’ and other descriptors of semen analysis based on Greek should be abandoned for both scientific and linguistic reasons. UNSCIENTIFIC DEVELOPMENT The initial definitions proposed were the antithesis of evidence-based medicine. An ‘‘andrology club’’ met three times, and after a meeting in Hamburg, Germany, in 1970, the ‘‘club’’ proposed new definitions (1). Of note, no scientific evidence relating semen analysis characteristics to fertility (6–9) or other references were provided as justification (1). Guidelines based on expert opinions have been repeatedly shown to be inferior to those based on evidence (10). OVERLAPPING DEFINITIONS A case definition must be clear, specific, and measurable (11). Oligozoospermia and azoospermia do not meet this standard, because of overlapping definitions. The initial definition of oligozoospermia was <40 million sperm/mL, and that of azoospermia was ‘‘no spermatozoa’’ (1). According to these Received February 21, 2007; revised and accepted April 19, 2007. Supported in part by Family Health International (FHI) with funds from the National Institutes of Health (NIH); the views expressed in this article do not necessarily reflect those of FHI or NIH. Reprint requests: David A. Grimes, M.D., Family Health International, P.O. Box 13950, Research Triangle Park, NC 27709 (FAX: 919-544-7261; E-mail: [email protected]).
0015-0282/07/$32.00 doi:10.1016/j.fertnstert.2007.04.013
definitions, a man with azoospermia has both azoospermia and oligozoospermia, because zero sperm is less than 40 million/mL. This overlapping terminology has confused the andrology literature for a third of a century. While reviewing randomized controlled trials of male hormonal contraceptives, we found extensive misuse of these terms (12). Many authors defined these terms as described above yet analyzed their results as if azoospermia and oligozoospermia were separate and distinct entities. The internal inconsistencies precluded comparison of rates of oligozoospermia. For example, one trial (13) reported that, ‘‘In the placebo group 4 out of 14 and in the LNG [levonorgestrel] group 7 out of 14 men achieved severe oligozoospermia (<3 billion/L).’’ However, in an erratum, one of the authors reported severe oligozoospermia in ‘‘12/14 and 14/14 volunteers of the placebo and gestagen-treated groups, respectively’’ (14). In the original report, ‘‘azoospermia’’ was not included in the category of ‘‘severe oligozoospermia,’’ whereas in the erratum it was. VARIABLE (OR NO) DEFINITIONS Definitions of normal morphology vary. The American Urological Association and American Society of Reproductive Medicine’s table of ‘‘reference values’’ for semen analysis is illustrative. Three different values for normal morphology are given: >50%, >30%, and >14% (7). Interpretation of oligozoospermia reports is even more difficult because of inconsistent or no definitions. In the initial recommendations (1), the definition of oligozoospermia was <40 million/mL. In 1981, the U.S. Food and Drug Administration proposed %5 million/mL (15). By the third edition of the World Health Organization (WHO) laboratory manual for semen analysis (1992), the definition had changed to <20 million/mL (16), although the WHO manual continued to cite the original recommendations as the source (1).
Fertility and Sterility Vol. 88, No. 6, December 2007 Copyright ª2007 American Society for Reproductive Medicine, Published by Elsevier Inc.
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TABLE 1 Changing Nomenclature for Semen Variables Recommended by the World Health Organization, 1992 and 1999 (4, 16). Definition Term
1992 (16)
Normozoospermiaa Oligozoospermiaa Asthenozoospermiaa
Teratozoospermiaa Oligoasthenoteratozoospermia
Azoospermia Aspermia a
Normal ejaculate as defined in [Appendix] 1A Sperm concentration fewer than 20 106/mL Fewer than 50% spermatozoa with forward progression (categories ‘a’ and ‘b’) or fewer than 25% spermatozoa with category ‘a’ movement (see Section 2.4.2) Fewer than 30% spermatozoa with normal morphology Signifies disturbance of all three variables (combinations of only two prefixes may also be used) No spermatozoa in the ejaculate No ejaculate
1999 (4) Normal ejaculate as defined by the reference values Sperm concentration less than the reference value Less than the reference value for motility
Less than the reference value for morphology Signifies disturbance of all three variables (combinations of only two prefixes may also be used) No spermatozoa in the ejaculate No ejaculate
Definition changed.
Grimes. Improving semen analysis terminology. Fertil Steril 2007.
By the Fourth Edition of the WHO manual (1999), numerical definitions for these terms had been abandoned altogether, except as they relate to unspecified ‘‘reference values’’ (Table 1) (4). Without a quantitative definition, the term ‘‘oligozoospermia’’ loses any scientific utility (6, 9, 17). The same criticism holds for ‘‘normozoospermia,’’ ‘‘asthenozoospermia,’’ teratozoospermia,’’ and ‘‘oligoasthenoteratozoospermia,’’ all of which now lack quantitative definitions (4). Failing to have quantitative definitions for these terms is analogous to defining obesity as ‘‘more than the reference value,’’ instead of a body mass index (BMI) R30 kg/m2. The mean BMI is higher in Alabama than in Colorado (18). Without a uniform, quantitative definition, some overweight persons in Colorado would immediately lose the diagnosis of ‘‘obesity’’ (but not the weight) upon moving to Alabama. They would be above the BMI ‘‘reference value’’ in Colorado but within the higher ‘‘reference value’’ in Alabama. Medicine and science require uniform definitions, not shifting targets. Similar confusion surrounds ‘‘severe oligozoospermia.’’ Some authors use this phrase without definition (19, 20). Others define ‘‘severe’’ as <100,000/mL (21), <3 million/mL (14), <5 million/mL (22, 23), or <10 million/mL (24). Still others define ‘‘severe’’ as 200,000/mL to 4 million/mL (25). Inconsistent terminology makes comparison of reported ‘‘severe oligozoospermia’’ across studies impossible. 1492
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‘‘POMPOUS DICTION’’ Replacing unnecessarily formal words with simple ones makes diction sharper and more direct (26). Medical writing is justly criticized for its abuse of English; a stubborn problem is ‘‘medicalese’’—jargon that obscures rather than clarifies intent (27–29). Terms such as ‘‘oligozoospermia’’ (and its longer permutations) readily fall into this category of medical ‘‘puffery.’’ Some of these terms are not recognized words; they do not appear in standard medical dictionaries, despite decades of use. An example used by the WHO is ‘‘normozoospermia’’ (4), which is not listed in Stedman’s Medical Dictionary (30). Other unapproved neologisms include ‘‘hyperspermia’’ (31), ‘‘leucocytospermia’’ (23), ‘‘polyzoospermia’’ (32), and ‘‘globozoospermia’’ (33). For those interested in Greek, variations on this theme might include ‘‘planktozoospermia’’ (wandering sperm), ‘‘tachozoospermia’’ (fast swimmers), and ‘‘nosozoospermia’’ (sick but not yet ‘‘necrozoospermia’’) (23). Sperm-count descriptors rival the most cumbersome words in English. As might be anticipated, the longest English word is medical; it contains 30 letters: ‘‘pseudopseudohypoparathyroidism’’ (3). However, the longest nontechnical word is ‘‘floccinaucinihilipilification’’ at 29 letters. ‘‘Oligoasthenoteratozoospermia’’ (4) (28 letters) is not far behind, but because it is not a legitimate word (30) it may not count.
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These terms are tough to spell. For example, a recent report in the journal of the American Society of Andrology misspelled ‘‘oligozoospermia’’ and inadvertently created another neologism: ‘‘oligoazoospermia’’ (34). A report published in the American College of Obstetricians and Gynecologists journal misspelled ‘‘azoospermia’’ throughout (35). These errors were missed by authors, reviewers, editors, and proofreaders alike. No wonder: this is the stuff of spelling bees. Apparently, ‘‘oligozoospermia’’ was misspelled in the past, and the error got legitimized, because ‘‘oligospermia’’ is listed in dictionaries as a synonym for the former (30). LACK OF PREDICTIVE VALUE Because these definitions were not based on empiric evidence, they have poor predictive value (36). Recent studies have confirmed the inability to predict fertility based on these sperm descriptions (7). Morphology appears to be the most informative sperm characteristic, but none of the measures alone or together can diagnose infertility (6–9). Spontaneous pregnancies occur with sperm counts less than 100,000/mL (37). PROPOSED REMEDIES The definitions of sperm characteristics first promulgated by a ‘‘club’’ in 1970 impede rather than facilitate scientific communication. These terms were flawed at inception (1). For example, ‘‘asthenozoospermia’’ is a misnomer, because ‘‘astheneia’’ in Greek refers to weakness, not motility (30). These problems are compounded by inconsistent and often poor laboratory methods for semen analysis (17, 38) as
well as sizeable intraindividual variation in semen quality and quantity (39). Because WHO has now abandoned quantitative definitions, these terms should be discarded as well. Instead, physicians and scientists should report semen analysis numerically (Table 2). Moreover, using arbitrary dichotomous labels for continuous variables (e.g., sperm count) loses information: continuous data should be presented as such, and not be dichotomized above or below some cut point (40). Proportions of sperm with normal form or motility (or, alternatively, abnormal form or lack of motility) should be reported as well. For example, the percentage of motile spermatozoa should replace ‘‘asthenozoospermia.’’ The proportion of round-headed spermatozoa should supplant ‘‘globozoospermia.’’ Simple English adjectives (e.g., ‘‘low’’) could be used if desired, provided they are defined numerically. However, if these unscientific terms are to remain in clinical use, then the overlapping definitions of oligozoospermia and azoospermia must be resolved. For example, azoospermia should be defined as no sperm after centrifugation at 3000g for 15 minutes and examination of the pellet (7). To evaluate vasectomy success, the British Andrology Society also recommends centrifugation if no sperm are seen on direct microscopy (41). However, given the different laboratory techniques used today, detection of azoospermia varies. Oligozoospermia could be defined as >0 but <20 million/mL, for example. Thus, azoospermia and oligozoospermia would finally be mutually exclusive terms. Adoption of better, more scientific terminology will improve both research and clinical practice in andrology. The current nomenclature is simply untenable.
TABLE 2 Proposed replacements for semen-analysis terminology based on Greek. Traditional Term (4)
Proposed Replacement
Normozoospermia
Ejaculate volume in mL
Oligozoospermia
Number of spermatozoa per mL
Asthenozoospermia
Proportion of motile spermatozoa
Teratozoospermia
Proportion of normally shaped spermatozoa
Oligoasthenoteratozoospermia
[discard]
Azoospermia Aspermia
No spermatozoa No ejaculate
Rationale Provides continuous rather than dichotomous data (40); simplifies spelling and definition (26) Provides continuous rather than dichotomous data (40); simplifies spelling and definition (26) Provides continuous rather than dichotomous data (40); simplifies spelling and definition (26) Provides continuous rather than dichotomous data (40); simplifies spelling and definition (26) Avoids dichotomizing combinations of characteristics (40) Simplifies spelling and definition (26) Simplifies spelling and definition (26)
Grimes. Improving semen analysis terminology. Fertil Steril 2007.
Fertility and Sterility
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Improving semen analysis terminology
Vol. 88, No. 6, December 2007