Abstract
This study reports the favourable semen characteristics of 73 subfertile oligozoospermic men with short abstinence periods up to 40 min. Semen characteristics were compared between initial and consecutive ejaculate showing improved semen parameters: progressive grade A spermatozoa, morphology and sperm concentration. Median concentrations in initial and consecutive ejaculates were 10 million/ml and 17 million/ml, respectively. The second sample had a higher median normal morphology (7% versus 6%, P < 0.001). The median of non-progressive spermatozoa (Grade C) was significantly lower in the consecutive sample than the initial sample (0% versus 5%, P < 0.01). Medians for slow progression spermatozoa (B grade) and immotile spermatozoa (D grade) were lower in the consecutive samples (20% versus 13%, P < 0.01 and 60% versus 50%, P < 0.001, respectively). The median for rapid motility (Grade A) was significantly higher in the consecutive sample than the first (30% versus 5%, P < 0.001). Overall median progressive motility as benchmarked by the WHO 2010 criteria was significantly higher in the consecutive sample (43% versus 25%, P < 0.001). Semen analyses of consecutive semen samples collected 30 min (mean) apart in oligozoospemic men should be checked routinely for diagnostic purposes and for managing potential subfertility treatment.
Keywords
Introduction
Abstinence between 2 and 7 days before diagnostic semen analyses is recommended in the World Health Organization (
WHO, 2010
guidelines (WHO, 2010
). The data derived from fertile males in a number of countries over three continents represents sound reference distributions of semen characteristics of fertile men, providing an appropriate tool to measure semen characteristics to evaluate a patient's prospects for fertility (Cooper et al, 2010
, Esteves et al, 2012
). At least two semen analyses should be performed at least 3 months apart and such timespans may not always be practical when treating patients. However, when it comes to subfertile men it is unclear how the recommendations for abstinence can be applied to gain an optimal sample to benefit the couples clinically. Clinics generally rely on the 3 days abstinence provided in the WHO, 1999
guidance (WHO, 1999
) or the 2–7 days from the WHO manual 2010, without questioning what this period could be for specific subfertile men.Old reports suggest the commonly held belief that sperm count is inversely related to frequency of intercourse. In normozoospermic men, sperm counts were shown to decrease significantly with sequential ejaculation. A nearly 60% decrease in the total motile sperm count of the second ejaculate compared with the first has been reported (
Olderid et al, 1984
). Similarly, a correlation between sperm count and frequency of ejaculation confirmed that sperm concentration, volume and total sperm count decreased with frequent ejaculation, but concluded that to increase the chance of fertilization it might be more efficient to have intercourse every other day rather than daily (Levin et al, 1986
).The semen characteristics can be affected considerably by abstinence times and the semen characteristics will define first-line treatment options. A cost-effective analysis shows that if only cost per live birth is considered for each treatment, above a pre-wash total motile sperm count (TMSC) of three million intrauterine insemination (IUI) is more cost-effective than IVF. Below a pre-wash TMSC of three million, intracytoplasmic sperm injection (ICSI) is more cost-effective than IUI (
Moolenaar et al, 2015
). Therefore, it is important to secure sufficient total progressive sperm count (TPMS) numbers if first-line IUI treatment is to be efficiently managed (Bahadur et al, 2015
, - Bahadur G.
- Homburg R.
- Ilahibuccus A.
- Al-Habib A.
- Okolo S.
IVF and intrauterine inseminationcannot be compared.
Reprod. Biomed. Online. 2015; 31 (Epub 2015 May 8): 246-247https://doi.org/10.1016/j.rbmo.2015.04.009
Hamilton et al, 2015
).Clues to sperm quality and abstinence times for subfertile men can be found embedded in studies where the objective was to gain a sample with optimal motile sperm parameters for treatment purpose. The 3–4 day abstinence period before IUI was originally based on maximizing TMSC in an ejaculate (
Freund, 1963
). Semen parameters vary depending on the abstinence period, with some groups suggesting better sperm characteristics can be obtained for the purposes of fertility treatment with much shorter abstinence periods of less than 1 day (Levitas et al, 2005
). One study has used a 1 h abstinence period, whereby a consecutive ejaculate, within 1 h of the first in cases of unacceptable ejaculate quality (compared with previous occasions) or very poor semen characteristics, has shown the second sample to be superior in quality to the first and was therefore used for the fertilization process (Bar-Hava et al, 2000
). Studies appearing in non-mainstream fertility literature, in an IVF setting support the benefits of short abstinence time (Sugiyam et al, 2008
). Data also exist on how semen quality is affected by environmental factors and the method of sample production (Elzanaty, Malm, 2008
, Jørgensen et al, 2001
) and therefore it is important to recognize and control for these factors.There is no specific report on the diagnostic quality of semen from subfertile men with short abstinence, and we questioned whether the potential worth of a consecutive ejaculate can help men with oligozoospermia. The aim of this study was therefore to report on the diagnostic semen analyses and compare the semen characteristics between the initial ejaculate and a consecutive ejaculate obtained within 40 min in men with oligozoospermia being profiled for IUI treatment.
Materials and methods
In 73 couples undergoing IUI in our reproductive unit within a large NHS teaching hospital between June 2013 and April 2014, oligozoospermic men were profiled before treatment regarding their semen analyses with a view to checking whether five million motile and progressive (Grade A and B) spermatozoa were available for an IUI procedure. Where the initial sample was deemed unsuitable (<five million motile spermatozoa) the patient was asked to provide a second ejaculate within 40 min in order to assess whether the TPMS increased to > five million per ml. An abstinence time of 2–7 days for the initial ejaculate was compliant with the
WHO, 2010
standard (WHO, 2010
). The scope of this report was restricted to reporting the semen characteristics between the initial and consecutive ejaculate only. The WHO, 2010
semen analyses criteria were adhered to for the semen analyses profiling, but the WHO, 1999
criteria were retained for the motility assessment, as this allowed for discrimination of the Grade A (rapid) and B (slow) spermatozoa, which was equally important to understand the outcomes within the IUI programme. Progression was classified as:- (i)Grade A: rapid progressive movement. At least 25 µm/s at 37°C (25 µm is approximately equal to five head lengths or half a tail length).
- (ii)Grade B: progressive motile with moderate to poor progression.
- (iii)Grade C: twitching spermatozoa with minimal forward progression. Non-progressive motility. <5 µm/s at 37°C.
- (iv)Grade D: immotile.
Morphology assessment was performed on Diff Quick stained slides (Medion Diagnostics AG, Bonnestrasse 9, CH-3186 Dudingen, Switzerland). Viscosity was reported as follows: samples leaving the pipette in small discrete drops were graded as normal viscosity and samples forming threads longer than 2 cm were graded as abnormal or viscous samples.
All semen samples were produced by masturbation within the clinic environment, thereby minimizing factors that may contribute to semen variations caused by method of production or by environmental change. Men were counselled beforehand on the possible benefits of producing a consecutive ejaculate, produced in the same environment by masturbation. The short abstinence time was dictated by how long it took men to provide the consecutive ejaculate.
Semen samples were initially analysed using a Makler counting chamber (Sefi-Medical Instruments, Haifa, Israel) immediately after liquefaction to assess whether a “consecutive ejaculate” was required and to facilitate the speed for potential sperm preparation time for IUI. Accurate sperm concentration measurement was performed using a Neubaur counting chamber. The analyses were performed by one experienced andrologist, who performed sperm counts, motility and sperm morphology assessments on 400 spermatozoa. Motility analyses were performed on a 10 µl drop on a glass slide with a 22 × 22 mm cover slip and on a heated stage at 37°C, and the lens had a graticule.
The Reproductive Medicine Unit participates fully with the external quality assessment by UK NEQAS, Sub-Fertility Laboratory, Saint Mary's Hospital, Manchester, UK.
Information regarding round cells and debris was not included as it is not part of our database.
Morphology was investigated among 400 spermatozoa using a magnification of 400 and 1,000. Multiple slides were prepared to obtain 400 spermatozoa for analyses to avoid technical difficulties in cases with severe oligozoospermia.
TPMS per ejaculate was calculated by multiplying the sperm concentration by the volume of semen in each sample and then by multiplying the total sperm count by the percentage progressive motility (Grade A and B spermatozoa only).
Antisperm antibody testing was performed on semen samples for the presence of IgG and IgA antibodies. 5 µl of Sperm Mar latex particles was mixed with 5 µl of semen followed by 5 µl of Sperm Mar antiserum and mixed thoroughly for 5 s as per supplier instructions (Microm UK Ltd, Bicester, UK) on a 22 × 22 mm glass cover slip. After 2–3 min in a humidified chamber at room temperature the slide was read for latex particles attached to motile spermatozoa, on a phase contrast microscope using ×40 magnification, counting 200 spermatozoa to determine the percentage of reactive spermatozoa. If 50% or more of the spermatozoa were attached to latex particles the sample was considered positive for antisperm antibody test. If the test was negative, the slide was kept in a humidified atmosphere for a further 7 min and read after a total of 10 min.
Excluded from this study were men with reversal of vasectomy, chemotherapy patients and couples using donated spermatozoa. Only oligozoospermic men provided a consecutive ejaculate.
Ethical approval
The Institutional Review Board indicated that ethical approval was not required for this study (project ID: 184558, 05/06/2015).
Statistical methods
This is a within subject analysis for influence of very short abstinence on sperm quality. The initial and consecutive ejaculates were treated as paired samples. Both samples were analysed and the following parameters were compared: volume, viscosity, concentration, motility and morphology.
Non-parametric tests were used and data analysed using Stata IC version 13 software (StataCorp, Texas) statistical package. For paired samples the Wilcoxon matched pairs signed-rank test was used when comparing parameters between the two ejaculates. The Kruskal–Wallis test and chi-squared or Fisher's exact test were used to test for any associations where appropriate. Spearman's non-parametric correlation was used to test for associations between duration of abstinence and sperm volume. The level of statistical significance was assumed to be P < 0.05.
All results are presented as the mean (SD), median and range or proportion.
Results
This is a single centre retrospective case series study and 73 men were identified where sperm parameter readings had a low sampling error of ≤5% only (
WHO, 2010
). Sampling errors (%) according to total number of spermatozoa counted are shown in Table 2.2 of the WHO, 2010
Manual.The men included in the study had a mean (SD) age of 37 (8.4) years (median 36, range 22–60 years). Data analysis comparing the initial and consecutive ejaculated samples in this cohort of subfertile men is shown in Table 1. Although the sperm concentration did not show any significant differences between the initial and consecutive ejaculates, there were improvements in the sperm motility and morphology in the consecutive ejaculates. The volume in the consecutive ejaculate was significantly lower (P < 0.001).
Table 1Baseline and consecutive ejaculate data.
| Parameter | Sample 1 | Sample 2 | Pair-wise differences | ||||||
|---|---|---|---|---|---|---|---|---|---|
| Mean (SD) | Median | Min | Max | Mean (SD) | Median | Min | Max | Mean ± SEM, median | |
| Abstinence (days) | 4.04 (1.6) | 3 | 2 | 7 | – | – | |||
| Abstinence (hours) | – | 0.54 (0.09) | 0.5 | 0.25 | 0.67 | – | |||
| Volume (ml) | 2.7 (1.8) | 2.5 | 0.3 | 14 | 1.1 (1) | 1 | 0.2 | 7.5 | −1.6 ± 0.14, −1.3 |
| concentration (mill/ml) | 17.8 (16.3) | 10 | 1 | 72 | 19.7 (15.8) | 17 | 1 | 72 | 1.9 ± 1.7, 1 |
| Normal morphology (%) | 5.7 (1.9) | 6 | 0 | 9 | 6.2 (1.9) | 7 | 0 | 11 | 0.5 ± 0.18, 0 |
| Immotile (D) (%) | 62.5 (14.9) | 60 | 8 | 90 | 51.6 (15.3) | 50 | 0 | 100 | −10.9 ± 1.7, −10 |
| Non-progressive(C) (%) | 6.8 (9) | 5 | 0 | 60 | 4 (6.8) | 0 | 0 | 40 | −2.8 ± 0.8, 0 |
| Slow motility (B) (%) | 22.3 (10.8) | 20 | 0 | 50 | 17.4 (10.5) | 13 | 0 | 50 | −4.9 ± 1.6, −10 |
| Rapid motility (A) (%) | 8.8 (10.5) | 5 | 0 | 40 | 26.5 (15.2) | 30 | 0 | 60 | 17.8 ± 1.6, 20 |
| Viscosity (% High) | 25 | – | – | – | 39 | – | – | – | 14 ± 5.6 |
Sample 1 = initial ejaculate; Sample 2 = consecutive ejaculate.
a Abstinence before the first sample.
b Abstinence before the second sample.
* P < 0.01;
** P < 0.001.
The ejaculate volume was weakly but positively correlated with the duration of first abstinence (Spearman's rho = 0.43, P = 0.002). The median concentrations in the initial and consecutive ejaculates were 10 million/ml and 17 million/ml, respectively. There was a significant difference between the proportion of samples with high viscosities in the initial and consecutive ejaculates: 25% and 39%, respectively (Fisher's exact test, P < 0.001). The consecutive sample had a higher median normal morphology (7% versus 6%, P < 0.001). The median non-progressive spermatozoa (Grade C) were significantly lower in the consecutive sample compared with the initial sample (0% versus 5%, P < 0.01). Similarly, the medians for slow motility (Grade B) and immotile spermatozoa (Grade D) were lower in the consecutive samples (13% versus 20%, P < 0.01, and 50% versus 60%, P < 0.001, respectively). The median for rapid motility (Grade A) was significantly higher in the consecutive sample compared with the initial ejaculate (30% versus 5%, P < 0.001).
The overall median of progressive motility (Grade A + B) as benchmarked by the
WHO, 2010
criteria was higher in the consecutive sample (43% versus 25%, P < 0.001).There were no differences observed in antisperm antibody concentrations between the two samples.
Discussion
This study found that there was a significant improvement in the sperm motility, progression and morphology associations with no detriment to the sperm concentration. However, a drop in the semen volume was observed and there was a significant difference between the proportion of high viscosities in the initial and consecutive ejaculates: 25% and 39%, respectively (Fisher's exact test, P < 0.001). The consecutive sample had a higher median normal morphology (7% versus 6%, P < 0.001). The main parameters from this study that showed a significant improvement in the consecutive ejaculate sample were the rapid motility (Grade A) 30% (consecutive) versus 5% (initial) and the progressive motility (Grade A + B) 43% (consecutive) 25% (initial).
Reports on semen produced with short abstinence times are embedded within treatment settings to improve outcomes, and as such specific data on diagnostic semen analyses are either lacking in completeness or the methodology is non-compliant with the fifth WHO standards (
WHO, 2010
). Consecutive ejaculates have been utilized in clinical settings for human semen preparation for IVF (Barash et al, 1995
) and IUI (Küçük et al, 2008
). Pooled consecutive ejaculates have been used as a method to increase the total number of motile spermatozoa from men with oligozoospermia (Tur-Kaspa et al, 1990
). A study on the frequency of ejaculation on semen parameters in men with impaired fertility supported the benefit of pooling two ejaculates in a subset of patients (Maj et al, 1998
).The effect of varying abstinence times in single individuals has been previously reported (
Magnus et al, 1991
). Another study analysed the semen characteristics of 57 samples obtained within 1 day of abstinence, but the study did not have a breakdown within the 0–1 day period and the authors suggested that in order to obtain the best characteristics in semen samples, patients with male factor infertility should provide a semen sample after just 1 day of sexual abstinence (Levitas et al, 2005
). This study relates to much shorter abstinence times of less than 40 min compared with the above studies. The closest agreement to the findings from this study were data collected over 11 years for 22 couples who previously exhibited oligoasthenozoospermia from an IVF–embryo transfer setting. This study reported that the consecutive ejaculate collected 30–60 min after the first showed an improved sperm quality in oligoasthenozoospermic patients. The improvement was in motility and motile sperm concentration, but no improvement was shown in sperm cell count. The volume of the consecutive ejaculate was significantly decreased in comparison with the first (Sugiyam et al, 2008
). Data from this study suggest the use of an abstinence period of up to 40 min, which would allow for a practical processing time of both ejaculates for treatment purpose.One of the potential benefits of using a consecutive ejaculate sample is in the context of IUI. An ejaculatory abstinence period of less than 2 days before IUI has shown the highest pregnancy rates per cycle compared with longer intervals of abstinence (
Marshburn et al, 2010
). The processed motile sperm count correlates with pregnancy outcome after IUI (Miller et al, 2002
, Wainer et al, 2004
). An attempt was made to unravel the optimal interval for ejaculatory abstinence in couples undergoing IUI and treatment with clomiphene citrate (Jurema et al, 2005
). Abstinence correlated positively with the sperm count but negatively with motility. The highest pregnancy rate was observed with an abstinence interval of 3 days or less (14%) and the lowest pregnancy rate seen with an abstinence interval of 10 days or more (3%).In an IVF setting improved clinical pregnancy rates could be achieved by requesting a consecutive sperm ejaculate on the day of oocyte retrieval in order to collect more spermatozoa and/or increase the total number of motile spermatozoa for assisted reproduction treatments, while recognizing that this method can avoid other invasive sperm processing techniques and the need of unnecessary micromanipulative fertilization. (
Zhai et al, 2011
). For a group of infertile men with oligoasthenozoospermia whose partners were scheduled for IVF–embryo transfer, it was suggested that if on the day of retrieved oocytes insemination, the ejaculate had unacceptable characteristics, a consecutive ejaculate collected 2 h after collection of the initial ejaculate may produce a sample that exhibits improvements in both semen parameters and reproductive potential. In this study, 28.2% of the individuals the semen analysis of the first ejaculate precluded proceeding with IVF (Barash et al, 1995
), thereby highlighting the potential application of consecutive ejaculates.Previous reports have also investigated the use of consecutive ejaculates (
Bar-Hava et al, 2000
, Küçük et al, 2008
). Men in a study group were asked to produce a consecutive semen sample within 2 h of the first sample on the day of insemination (Küçük et al, 2008
). This group concluded that obtaining a consecutive semen sample when the motile sperm yield of the initial semen sample is 1–5 million significantly increased the total motile sperm count in the final inseminate. In a further study, a consecutive semen sample within 1 h of the initial sample in cases of unacceptable ejaculate characteristics (compared with previous occasions) or very poor semen characteristics was utilized (Bar-Hava et al, 2000
). Differences in sperm parameters between the consecutive samples determined by paired t-test showed in 36 cases (33% of cohort) the consecutive sample to be superior in characteristics to the initial sample and was therefore used for fertilization. They concluded that a request for a consecutive ejaculate immediately after the initial sample in men with poor semen characteristics or no detectable motile sperm could yield a better sample in a significant percentage of cases. Clinicians could avoid micromanipulative techniques to retrieve spermatozoa if consecutive ejaculates were investigated initially and in one study epididymal necrospermia was overcome by frequent ejaculation (two ejaculates per day for 4 or 5 days) to gain motile spermatozoa (Wilton et al, 1988
).The mechanism of improvement in sperm quality for the consecutive ejaculate collected in a short interval is unclear. Shorter periods of abstinence may improve sperm quality by protecting from reactive oxygen species damage. It is possible that the period of ejaculatory abstinence influences the total antioxidant capacity (TAC) of semen, and lipid peroxidation (LPO) of sperm membranes has been investigated over abstinence periods of 1–4 days (
Gosálvez et al, 2011
, - Gosálvez J.
- González-Martínez M.
- López-Fernández C.
- Fernández J.L.
- Sánchez-Martín P.
Shorter abstinence decreases sperm deoxyribonucleic acid fragmentation in ejaculate.
Fertil. Steril. 2011; 96 (Epub 2011 Sep 15): 1083-1086https://doi.org/10.1016/j.fertnstert.2011.08.027
Marshburn et al, 2014
, Pons et al, 2013
, Sánchez-Martín et al, 2013
). Markedly less DNA fragmentation was associated with shorter abstinence periods and lower baseline levels of sperm DNA fragmentation were observed after shorter periods of abstinence between ejaculations (24 h and 3 h) than those recommended (Gosálvez et al, 2011
). One abstinence day decreased sperm DNA fragmentation in 90% of selected patients (- Gosálvez J.
- González-Martínez M.
- López-Fernández C.
- Fernández J.L.
- Sánchez-Martín P.
Shorter abstinence decreases sperm deoxyribonucleic acid fragmentation in ejaculate.
Fertil. Steril. 2011; 96 (Epub 2011 Sep 15): 1083-1086https://doi.org/10.1016/j.fertnstert.2011.08.027
Pons et al, 2013
). There is also a correlation between sperm DNA damage and progressive motility, and both are possible predictors of fertilization (Simon, Lewis, 2011
).- Simon L.
- Lewis S.E.
Sperm DNA damage or progressive motility: which one is the better predictor of fertilization in vitro?.
Syst. Biol. Reprod. Med. 2011; 57 (Epub 2011 Feb 8): 133-138https://doi.org/10.3109/19396368.2011.553984
Surprisingly little is known about the regulation of sperm motility, which is an important predictor of male fertility. Improvement in motility with shorter abstinence times has a more complex explanation, and the impact of epididymal and accessory sex gland function on sperm motility has been considered (
Elzanaty et al, 2002
). Sperm motility correlated with seminal concentrations of neutral alpha-glucosidase (NAG), prostate-specific antigen (PSA), zinc and fructose (Elzanaty et al, 2005
), while sperm motility regulation is associated with Ca2+ signals generated by CatSper and Ca2+ stores which regulate different behaviours in human spermatozoa (Alasmari et al, 2013
). Therefore biochemical changes between first and consecutive ejaculates could help explain sperm motility changes. Similarly, biochemical changes such acidic pH and micromolar concentrations of Ca2+ affect dynein-ATPase activities and therefore decrease sperm motility (Peralta-Arias et al, 2015
) and this provides another possible explanation for observed differences between the two consecutive ejaculates.There is therefore a collective body of evidence within this manuscript associated with the positive effects on semen characteristics with short abstinence periods, not just at a molecular level but also on sperm motility and progression. Combining the initial and consecutive ejaculates allows for a potential shift of severe and oligozoospermia patients towards the normospermia range. The use of consecutive ejaculates in first-line fertility treatments needs to be validated in large prospective randomized controlled trials studies to overcome any confounding factors in order to establish whether this approach can improve pregnancy and live birth rates.
In conclusion, there was a significant improvement in the sperm motility, progression and morphology associations with no detriment to the sperm concentration in the consecutive ejaculate. Concentrations of rapid grade (Grade A) spermatozoa were significantly higher in the consecutive ejaculate. While consensus on optimal abstinence for subfertile men is lacking, it is clear from our work that the consecutive ejaculate produced within 40 min (mean of 30 min) of the initial ejaculate is pragmatic. Favourable semen characteristics in consecutive ejaculates with short abstinence in subfertile men suggests this needs to be routinely investigated, as it could have a profound alteration in the management of the couple's subfertility investigation.
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Biography
Dr Gulam Bahadur is a past member of the HFEA. His main involvement is in andrology with special emphasis on diagnostic analyses, male cancer patients, counselling, sperm donor recruitment and sperm freezing, and recovery rates following cryopreservation. Important ways to optimize pregnancy rates in simple first-line treatment intrauterine insemination is being researched and applied within a number of UK NHS Trust Hospitals. Dr Bahadur has made significant contributions to the understanding of semen qualities in subfertile males, cancer patients, adolescent cancer patients and produced one of the first reports on ovarian tissue freezing for cancer patients.
Article info
Publication history
Published online: December 30, 2015
Accepted:
November 25,
2015
Received in revised form:
November 13,
2015
Received:
August 12,
2015
Identification
Copyright
© 2015 Reproductive Healthcare Ltd. Published by Elsevier Inc. All rights reserved.
