- Email: [email protected]
Abnormal sperm count and motility on semen analysis are not sufficiently predictive of abnormal Kruger morphology
Abnormal sperm count and motility on semen analysis are not sufficiently predictive of abnormal Kruger morphology Abnormal morphology by Kruger’s strict criteria cannot be predicted reliably by the presence of other abnormal parameters on semen analysis. Assessment of Kruger morphology therefore remains a necessary component of a complete semen analysis in the workup of the infertile couple. (Fertil Steril 2010;94:2882–4. 2010 by American Society for Reproductive Medicine.) Key Words: Semen analysis, Kruger strict morphology, sperm count, sperm motility
Semen analysis is performed routinely to evaluate the male partner in infertile couples but does not provide a direct measure of functional capacity of sperm. Although no single semen parameter will predict definitively the potential of an individual couple to achieve success after assisted reproduction (1), the percentage of sperm with normal morphology (as assessed by strict criteria) has been demonstrated previously to be predictive of fertilization and pregnancy rates in IVF (2–7). Moreover, multiple studies have revealed that, in comparison with other parameters on semen analysis (i.e., motility and concentration), sperm morphology is the best predictor of fertilization potential both in vivo (8–10) and in vitro (11, 12). Assessment of morphology can be subjective and highly variable between laboratories and technicians (1). In addition, couples often present with semen analyses in which either [1] only the older, World Health Organization morphology scale was used to
Sara S. Morelli, M.D.a Aimee Seungdamrong, M.D.a,b David H. McCulloh, Ph.D.a,b Peter G. McGovern, M.D.a,b a University of Medicine and Dentistry of New Jersey—New Jersey Medical School, Department of Obstetrics, Gynecology and Women’s Health, Newark, New Jersey b University Reproductive Associates, Hasbrouck Heights, New Jersey Received February 20, 2010; revised May 31, 2010; accepted June 16, 2010; published online August 2, 2010. D.H.M. has received an honorarium from Columbia Laboratories. P.G.M. has received grants or has grants pending from Ferring and EMD Serono. S.S.M. has nothing to disclose. A.S. has nothing to disclose. Presented at the 62nd Annual Meeting of the American Society for Reproductive Medicine, New Orleans, Louisiana, October 21–25, 2006. Reprint requests: Sara S. Morelli, M.D., University of Medicine and Dentistry of New Jersey—New Jersey Medical School, Department of Obstetrics, Gynecology and Women’s Health, 185 South Orange Avenue, MSB E506, Newark, NJ 07103 (FAX: 973-972-4574; E-mail: [email protected]).
2882
assess morphology or [2] there was no morphology measured at all. These men often are reluctant to submit another sample for analysis. We therefore wanted to determine whether the presence of abnormal sperm count or motility on routine semen analysis would be a useful predictor of concurrent abnormal morphology as assessed by Kruger’s strict criteria. Data from semen analyses performed between January 1, 2002, and December 31, 2005, were collected retrospectively from the andrology laboratory database at University Reproductive Associates (Hasbrouck Heights, NJ). Only the first semen analysis was considered for each patient (N ¼ 1,384). This study was approved by the Institutional Review Board of New Jersey Medical School in Newark, New Jersey. Patients provided semen samples produced by masturbation after a period of abstinence ranging from 2 to 7 days. Analyses were performed within 1 hour of production. All analyses included measurements of sperm concentration (million per milliliter), motility (percentage of sperm with progressive motility), and strict Kruger morphology (percent normal). Concentration and motility were measured with use of computer-assisted semen analysis (IVOS Sperm Analyzer, Hamilton-Thorne, Beverly, MA) provided the specimen was sufficient in concentration. Manual counts were performed if fewer than five sperm were seen per high-power field. Normal concentration was considered at least 2 107 sperm per milliliter and normal motility was considered at least 50% motile. For sperm morphology evaluation, 5 mL of raw semen was smeared on a glass slide and air dried. The slide was then fixed and stained with the Stat III Andrology Stain kit (MidAtlantic Diagnostics, Mount Laurel, NJ). Sperm morphology was evaluated with use of the strict criteria described by Kruger et al. (3). At least 100 sperm were evaluated, and the percentages of sperm with complete normal forms according to strict criteria were noted. Semen samples were evaluated by one of four technicians, all of whom undergo semiannual proficiency testing. We considered a sample with %4% normal forms to be abnormal (or ‘‘poor prognosis’’ as defined by Kruger et al. [3]). Sensitivity (incidence of abnormal concentration and/or motility among patients with abnormal Kruger morphology), specificity
Fertility and Sterility Vol. 94, No. 7, December 2010 Copyright ª2010 American Society for Reproductive Medicine, Published by Elsevier Inc.
0015-0282/$36.00 doi:10.1016/j.fertnstert.2010.06.061
TABLE 1 Classification of semen analyses. Count (R2 3 107/mL)
Motility (R50%)
Kruger morphology (>4%)
No.
Percentage of total
Low Low Normal Normal Low Low Normal Normal
Low Normal Low Normal Low Normal Low Normal
158 58 48 41 69 92 187 731 1,384
11 4 3 3 5 7 14 53
Low Low Low Low Normal Normal Normal Normal Total Morelli. Correspondence. Fertil Steril 2010.
(incidence of normal concentration and/or motility among patients with normal Kruger morphology), positive predictive value (incidence of abnormal Kruger morphology among patients with abnormal concentration and/or motility), and negative predictive value (incidence of normal Kruger morphology among patients with normal concentration and/or motility) were obtained from 2 2 contingency tables of sperm count and motility against Kruger morphology. Fisher’s exact test was used to compare the proportion of samples with normal count (or normal motility) and abnormal morphology with the proportion of samples with abnormal count (or abnormal motility) and abnormal morphology. See Table 1 for classification of semen samples (N ¼ 1,384). Of 1,384 specimens, 731 (52.8%) had normal count, motility, and morphology. Four hundred sixty-two (33.4%) had abnormal morphology. Of these 462 specimens with abnormal morphology, 187 (40.5%) had normal motility and concentration. Thus, 40.5% of specimens with abnormal morphology would have been classified falsely as normal had morphology assessment been omitted. Of 462 specimens with abnormal morphology, 69 (14.9%) had low motility and normal count, 48 (10.4%) had normal motility and low count, and 158 (34.2%) had both low count and low motility. When comparing samples with abnormal sperm count with those with normal sperm count, a significantly greater proportion of samples with abnormal sperm count also exhibited abnormal morphology (206 of 305 samples [67.5%] with abnormal count vs. 256 of 1079 [23.7%] with normal count, P<.0001). An abnormal count predicted concurrent abnormal morphology with a positive predictive value of 67.5%, a negative predictive value of 76.3%, a sensitivity of 44.6%, and a specificity of 89.3%. However, 256 of the 462 samples (55.4%) with abnormal morphology were not detected by sperm count. When comparing samples with abnormal motility with those with normal motility, a significantly greater proportion of samples with abnormal motility also exhibited abnormal morphology (227 of 377 samples [60.2%] with abnormal motility vs. 235 of 1,007 samples [23.3%] with normal motility, P<.0001). Abnormal motility predicted concurrent abnormal morphology with a positive predictive value of 60.2%, a negative predictive value of 76.7%, a sensitivity of 49.1%, and a specificity of 83.7%. However, 235 of the 462 samples (50.9%) with abnormal morphology were not detected by motility.
Fertility and Sterility
When comparing samples with abnormal count and/or abnormal motility with those with both normal count and motility, a significantly greater proportion of samples with either or both abnormal count and/or motility also exhibited abnormal morphology (275 of 466 samples [59.0%] with either abnormal count or motility vs. 187 of 918 samples [20.4%] with both normal, P<.0001). The presence of either abnormal count or abnormal motility predicted concurrent abnormal morphology with a positive predictive value of 59.0% and a sensitivity of 59.5%. The presence of both abnormal count and motility predicted an abnormal Kruger morphology with a positive predictive value of 73.1%, a negative predictive value (defined as percentage of specimens with both normal count and motility that had normal Kruger morphology) of 79.6%, a sensitivity of 34.2%, and a specificity of 79.3% (defined as percentage of specimens with normal Kruger morphology that had both normal count and motility). However, 187 of 462 samples (40.5%) with abnormal morphology were not detected by an abnormal sperm count or motility. The objective of this study was to determine whether abnormal sperm count or motility on semen analysis is predictive of abnormal morphology (Kruger’s strict criteria morphology assessment). In summary, we found that abnormal count predicted abnormal Kruger morphology with a positive predictive value of 67.5% and a sensitivity of only 44.6%, and abnormal motility predicted abnormal Kruger morphology with a positive predictive value of 60.2% and sensitivity of only 49.1%. Combining the presence of either abnormal count or abnormal motility conferred the highest sensitivity for the detection of abnormal morphology (59.5%). Of note, as many as 187 of 462 specimens (40.5%) with abnormal Kruger morphology had normal count and motility. Further study of the outcomes of non–intracytoplasmic sperm injection cycles in couples with isolated severe teratozoospermia is necessary to determine the clinical relevance of this finding. To our knowledge, the present study is the first to evaluate the predictive value of sperm count and motility on morphology as assessed by strict criteria. It is possible that using a Kruger score cutoff of 4% to define abnormal morphology may contribute, in this study, to the poor predictive values of abnormal count and/or motility in the detection of abnormal morphology. We chose a cutoff of 4% based on Kruger’s initial observation that specimens with %4% normal forms had an extremely poor fertilization rate
2883
in vitro (7.6%) as compared with specimens with >4% normal forms (63.9%) (3). Changing the definition of abnormal morphology (e.g., raising the cutoff from 4% to 8%) would raise both the specificity and positive predictive value of abnormal count or motility in the detection of abnormal morphology, at the expense of a higher false-negative rate (i.e., poorer sensitivity). Similar to the findings of Kruger, other studies similarly have demonstrated that a strict morphology score of <4% is associated with significantly lower fertilization and pregnancy rates (6, 7) in patients undergoing IVF when compared with morphology scores R4%. Severe teratozoospermia is thus a widely accepted indication for the performance of intracytoplasmic sperm injection in IVF procedures. Our laboratory’s prior success with standard IVF insemination demonstrated that the incidence of
fertilization dropped from approximately 75% (of inseminated oocytes) fertilized when sperm had a Kruger morphology of R13% normal down to 40% fertilized with a Kruger morphology of 10% normal. In conclusion, we have found that abnormal morphology is more likely in the presence of abnormal sperm count and/or motility compared with normal count and/or motility. However, 40.5% of specimens with severely abnormal Kruger morphology displayed otherwise normal parameters. Because sperm morphology is an independently important predictor of sperm fertilization potential and cannot be predicted accurately by the presence of other abnormal parameters, assessment of morphology with use of strict Kruger criteria remains an important component of the complete semen analysis.
REFERENCES 1. Kruger TF, Coetzee K. The role of sperm morphology in assisted reproduction. Hum Reprod Update 1999;5:172–8. 2. Kruger TF, Menkveld R, Stander FSH, Lombard CJ, Van der Merwe JP, van Zyl JA, et al. Sperm morphologic features as a prognostic factor in in vitro fertilization. Fertil Steril 1986;46: 1118–23. 3. Kruger TF, Acosta AA, Simmons KF, Swanson RJ, Matta JF, Oehninger S. Predictive value of abnormal sperm morphology in in vitro fertilization. Fertil Steril 1988;49:112–7. 4. Oehninger S, Acosta AA, Morshedi M, Veeck L, Swanson RJ, Simmons K, et al. Corrective measures and pregnancy outcome in in vitro fertilization in patients with severe sperm morphology abnormalities. Fertil Steril 1988;50: 283–7.
2884
Morelli et al.
Correspondence
5. Enginsu ME, Pieters MH, Dumoulin JC, Evers JL, Geraedts JP. Male factor as determinant of in-vitro fertilization outcome. Hum Reprod 1992;7:1136–40. 6. Grow DR, Oehninger S, Seltman HJ, Toner JP, Swanson RJ, Kruger TF, et al. Sperm morphology as diagnosed by strict criteria: probing the impact of teratozoospermia on fertilization rate and pregnancy outcome in a large in vitro fertilization population. Fertil Steril 1994;62:559–67. 7. Hernandez M, Molina R, Olmedo J, Olmedo SB, Coetzee K, Estofan D. Prognostic value of the strict criteria: an Argentinian experience. Arch Androl 1996;37:87–9. 8. 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.
9. 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. 10. Menkveld R, Wong WY, Lombard CJ, Wetzels AMM, Thomas CMG, Merkus HMWM, et al. Semen parameters, including WHO and strict criteria morphology, in a fertile and subfertile population: an effort towards standardization of in-vivo thresholds. Hum Reprod 2001;16:1165–71. 11. Vawda AI, Gunby J, Younglai EV. Semen parameters as predictors of in-vitro fertilization: the importance of strict criteria sperm morphology. Hum Reprod 1996;11:1445–50. 12. Rogers BJ, Bentwood BJ, van Campen H, Helmbrecht G, Soderdahl D, Hale RW. Sperm morphology assessment as an indicator of human fertilizing capacity. J Androl 1983;4:119–25.
Vol. 94, No. 7, December 2010
Semen analysis is performed routinely to evaluate the male partner in infertile couples but does not provide a direct measure of functional capacity of sperm. Although no single semen parameter will predict definitively the potential of an individual couple to achieve success after assisted reproduction (1), the percentage of sperm with normal morphology (as assessed by strict criteria) has been demonstrated previously to be predictive of fertilization and pregnancy rates in IVF (2–7). Moreover, multiple studies have revealed that, in comparison with other parameters on semen analysis (i.e., motility and concentration), sperm morphology is the best predictor of fertilization potential both in vivo (8–10) and in vitro (11, 12). Assessment of morphology can be subjective and highly variable between laboratories and technicians (1). In addition, couples often present with semen analyses in which either [1] only the older, World Health Organization morphology scale was used to
Sara S. Morelli, M.D.a Aimee Seungdamrong, M.D.a,b David H. McCulloh, Ph.D.a,b Peter G. McGovern, M.D.a,b a University of Medicine and Dentistry of New Jersey—New Jersey Medical School, Department of Obstetrics, Gynecology and Women’s Health, Newark, New Jersey b University Reproductive Associates, Hasbrouck Heights, New Jersey Received February 20, 2010; revised May 31, 2010; accepted June 16, 2010; published online August 2, 2010. D.H.M. has received an honorarium from Columbia Laboratories. P.G.M. has received grants or has grants pending from Ferring and EMD Serono. S.S.M. has nothing to disclose. A.S. has nothing to disclose. Presented at the 62nd Annual Meeting of the American Society for Reproductive Medicine, New Orleans, Louisiana, October 21–25, 2006. Reprint requests: Sara S. Morelli, M.D., University of Medicine and Dentistry of New Jersey—New Jersey Medical School, Department of Obstetrics, Gynecology and Women’s Health, 185 South Orange Avenue, MSB E506, Newark, NJ 07103 (FAX: 973-972-4574; E-mail: [email protected]).
2882
assess morphology or [2] there was no morphology measured at all. These men often are reluctant to submit another sample for analysis. We therefore wanted to determine whether the presence of abnormal sperm count or motility on routine semen analysis would be a useful predictor of concurrent abnormal morphology as assessed by Kruger’s strict criteria. Data from semen analyses performed between January 1, 2002, and December 31, 2005, were collected retrospectively from the andrology laboratory database at University Reproductive Associates (Hasbrouck Heights, NJ). Only the first semen analysis was considered for each patient (N ¼ 1,384). This study was approved by the Institutional Review Board of New Jersey Medical School in Newark, New Jersey. Patients provided semen samples produced by masturbation after a period of abstinence ranging from 2 to 7 days. Analyses were performed within 1 hour of production. All analyses included measurements of sperm concentration (million per milliliter), motility (percentage of sperm with progressive motility), and strict Kruger morphology (percent normal). Concentration and motility were measured with use of computer-assisted semen analysis (IVOS Sperm Analyzer, Hamilton-Thorne, Beverly, MA) provided the specimen was sufficient in concentration. Manual counts were performed if fewer than five sperm were seen per high-power field. Normal concentration was considered at least 2 107 sperm per milliliter and normal motility was considered at least 50% motile. For sperm morphology evaluation, 5 mL of raw semen was smeared on a glass slide and air dried. The slide was then fixed and stained with the Stat III Andrology Stain kit (MidAtlantic Diagnostics, Mount Laurel, NJ). Sperm morphology was evaluated with use of the strict criteria described by Kruger et al. (3). At least 100 sperm were evaluated, and the percentages of sperm with complete normal forms according to strict criteria were noted. Semen samples were evaluated by one of four technicians, all of whom undergo semiannual proficiency testing. We considered a sample with %4% normal forms to be abnormal (or ‘‘poor prognosis’’ as defined by Kruger et al. [3]). Sensitivity (incidence of abnormal concentration and/or motility among patients with abnormal Kruger morphology), specificity
Fertility and Sterility Vol. 94, No. 7, December 2010 Copyright ª2010 American Society for Reproductive Medicine, Published by Elsevier Inc.
0015-0282/$36.00 doi:10.1016/j.fertnstert.2010.06.061
TABLE 1 Classification of semen analyses. Count (R2 3 107/mL)
Motility (R50%)
Kruger morphology (>4%)
No.
Percentage of total
Low Low Normal Normal Low Low Normal Normal
Low Normal Low Normal Low Normal Low Normal
158 58 48 41 69 92 187 731 1,384
11 4 3 3 5 7 14 53
Low Low Low Low Normal Normal Normal Normal Total Morelli. Correspondence. Fertil Steril 2010.
(incidence of normal concentration and/or motility among patients with normal Kruger morphology), positive predictive value (incidence of abnormal Kruger morphology among patients with abnormal concentration and/or motility), and negative predictive value (incidence of normal Kruger morphology among patients with normal concentration and/or motility) were obtained from 2 2 contingency tables of sperm count and motility against Kruger morphology. Fisher’s exact test was used to compare the proportion of samples with normal count (or normal motility) and abnormal morphology with the proportion of samples with abnormal count (or abnormal motility) and abnormal morphology. See Table 1 for classification of semen samples (N ¼ 1,384). Of 1,384 specimens, 731 (52.8%) had normal count, motility, and morphology. Four hundred sixty-two (33.4%) had abnormal morphology. Of these 462 specimens with abnormal morphology, 187 (40.5%) had normal motility and concentration. Thus, 40.5% of specimens with abnormal morphology would have been classified falsely as normal had morphology assessment been omitted. Of 462 specimens with abnormal morphology, 69 (14.9%) had low motility and normal count, 48 (10.4%) had normal motility and low count, and 158 (34.2%) had both low count and low motility. When comparing samples with abnormal sperm count with those with normal sperm count, a significantly greater proportion of samples with abnormal sperm count also exhibited abnormal morphology (206 of 305 samples [67.5%] with abnormal count vs. 256 of 1079 [23.7%] with normal count, P<.0001). An abnormal count predicted concurrent abnormal morphology with a positive predictive value of 67.5%, a negative predictive value of 76.3%, a sensitivity of 44.6%, and a specificity of 89.3%. However, 256 of the 462 samples (55.4%) with abnormal morphology were not detected by sperm count. When comparing samples with abnormal motility with those with normal motility, a significantly greater proportion of samples with abnormal motility also exhibited abnormal morphology (227 of 377 samples [60.2%] with abnormal motility vs. 235 of 1,007 samples [23.3%] with normal motility, P<.0001). Abnormal motility predicted concurrent abnormal morphology with a positive predictive value of 60.2%, a negative predictive value of 76.7%, a sensitivity of 49.1%, and a specificity of 83.7%. However, 235 of the 462 samples (50.9%) with abnormal morphology were not detected by motility.
Fertility and Sterility
When comparing samples with abnormal count and/or abnormal motility with those with both normal count and motility, a significantly greater proportion of samples with either or both abnormal count and/or motility also exhibited abnormal morphology (275 of 466 samples [59.0%] with either abnormal count or motility vs. 187 of 918 samples [20.4%] with both normal, P<.0001). The presence of either abnormal count or abnormal motility predicted concurrent abnormal morphology with a positive predictive value of 59.0% and a sensitivity of 59.5%. The presence of both abnormal count and motility predicted an abnormal Kruger morphology with a positive predictive value of 73.1%, a negative predictive value (defined as percentage of specimens with both normal count and motility that had normal Kruger morphology) of 79.6%, a sensitivity of 34.2%, and a specificity of 79.3% (defined as percentage of specimens with normal Kruger morphology that had both normal count and motility). However, 187 of 462 samples (40.5%) with abnormal morphology were not detected by an abnormal sperm count or motility. The objective of this study was to determine whether abnormal sperm count or motility on semen analysis is predictive of abnormal morphology (Kruger’s strict criteria morphology assessment). In summary, we found that abnormal count predicted abnormal Kruger morphology with a positive predictive value of 67.5% and a sensitivity of only 44.6%, and abnormal motility predicted abnormal Kruger morphology with a positive predictive value of 60.2% and sensitivity of only 49.1%. Combining the presence of either abnormal count or abnormal motility conferred the highest sensitivity for the detection of abnormal morphology (59.5%). Of note, as many as 187 of 462 specimens (40.5%) with abnormal Kruger morphology had normal count and motility. Further study of the outcomes of non–intracytoplasmic sperm injection cycles in couples with isolated severe teratozoospermia is necessary to determine the clinical relevance of this finding. To our knowledge, the present study is the first to evaluate the predictive value of sperm count and motility on morphology as assessed by strict criteria. It is possible that using a Kruger score cutoff of 4% to define abnormal morphology may contribute, in this study, to the poor predictive values of abnormal count and/or motility in the detection of abnormal morphology. We chose a cutoff of 4% based on Kruger’s initial observation that specimens with %4% normal forms had an extremely poor fertilization rate
2883
in vitro (7.6%) as compared with specimens with >4% normal forms (63.9%) (3). Changing the definition of abnormal morphology (e.g., raising the cutoff from 4% to 8%) would raise both the specificity and positive predictive value of abnormal count or motility in the detection of abnormal morphology, at the expense of a higher false-negative rate (i.e., poorer sensitivity). Similar to the findings of Kruger, other studies similarly have demonstrated that a strict morphology score of <4% is associated with significantly lower fertilization and pregnancy rates (6, 7) in patients undergoing IVF when compared with morphology scores R4%. Severe teratozoospermia is thus a widely accepted indication for the performance of intracytoplasmic sperm injection in IVF procedures. Our laboratory’s prior success with standard IVF insemination demonstrated that the incidence of
fertilization dropped from approximately 75% (of inseminated oocytes) fertilized when sperm had a Kruger morphology of R13% normal down to 40% fertilized with a Kruger morphology of 10% normal. In conclusion, we have found that abnormal morphology is more likely in the presence of abnormal sperm count and/or motility compared with normal count and/or motility. However, 40.5% of specimens with severely abnormal Kruger morphology displayed otherwise normal parameters. Because sperm morphology is an independently important predictor of sperm fertilization potential and cannot be predicted accurately by the presence of other abnormal parameters, assessment of morphology with use of strict Kruger criteria remains an important component of the complete semen analysis.
REFERENCES 1. Kruger TF, Coetzee K. The role of sperm morphology in assisted reproduction. Hum Reprod Update 1999;5:172–8. 2. Kruger TF, Menkveld R, Stander FSH, Lombard CJ, Van der Merwe JP, van Zyl JA, et al. Sperm morphologic features as a prognostic factor in in vitro fertilization. Fertil Steril 1986;46: 1118–23. 3. Kruger TF, Acosta AA, Simmons KF, Swanson RJ, Matta JF, Oehninger S. Predictive value of abnormal sperm morphology in in vitro fertilization. Fertil Steril 1988;49:112–7. 4. Oehninger S, Acosta AA, Morshedi M, Veeck L, Swanson RJ, Simmons K, et al. Corrective measures and pregnancy outcome in in vitro fertilization in patients with severe sperm morphology abnormalities. Fertil Steril 1988;50: 283–7.
2884
Morelli et al.
Correspondence
5. Enginsu ME, Pieters MH, Dumoulin JC, Evers JL, Geraedts JP. Male factor as determinant of in-vitro fertilization outcome. Hum Reprod 1992;7:1136–40. 6. Grow DR, Oehninger S, Seltman HJ, Toner JP, Swanson RJ, Kruger TF, et al. Sperm morphology as diagnosed by strict criteria: probing the impact of teratozoospermia on fertilization rate and pregnancy outcome in a large in vitro fertilization population. Fertil Steril 1994;62:559–67. 7. Hernandez M, Molina R, Olmedo J, Olmedo SB, Coetzee K, Estofan D. Prognostic value of the strict criteria: an Argentinian experience. Arch Androl 1996;37:87–9. 8. 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.
9. 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. 10. Menkveld R, Wong WY, Lombard CJ, Wetzels AMM, Thomas CMG, Merkus HMWM, et al. Semen parameters, including WHO and strict criteria morphology, in a fertile and subfertile population: an effort towards standardization of in-vivo thresholds. Hum Reprod 2001;16:1165–71. 11. Vawda AI, Gunby J, Younglai EV. Semen parameters as predictors of in-vitro fertilization: the importance of strict criteria sperm morphology. Hum Reprod 1996;11:1445–50. 12. Rogers BJ, Bentwood BJ, van Campen H, Helmbrecht G, Soderdahl D, Hale RW. Sperm morphology assessment as an indicator of human fertilizing capacity. J Androl 1983;4:119–25.
Vol. 94, No. 7, December 2010