Professional Documents
Culture Documents
ISSN: 2047-2919
ORIGINAL ARTICLE
Correspondence:
Usha Punjabi, Centre for Reproductive Medicine,
Antwerp University Hospital, Wilrijkstraat 10, 2650
Edegem, Belgium.
E-mail: usha.punjabi@uza.be
Keywords:
quality control, sperm concentration, sperm
morphology, sperm motility, sperm quality
parameters
Received: 28-Mar-2016
Revised: 2-May-2016
Accepted: 6-May-2016
Centre for Reproductive Medicine, Antwerp University Hospital, Edegem, 2Cliniques Universitaires
Saint Luc, Brussels, 3University Hospital of Ghent, Ghent, 4Scientific Institute of Public Health,
Brussels, and 5Centre for Reproductive Medicine, UZ Brussel, Brussels, Belgium
doi: 10.1111/andr.12230
SUMMARY
Semen analysis is difficult to standardize, quality control and quality assurance are necessary to ensure that results are accurate
and precise. This Belgian EQA survey over a 15-year period, involving 121 laboratories, attempted to reduce interlaboratory variability
and at the same time, encouraged participating laboratories to implement correct techniques as advised by the WHO. Over the total
period, the median coefficient of variation (CV) for sperm count, irrespective of the method used was 19.2%, while using improved
Neubauer chamber resulted in a significantly (p < 0.001) lower median CV (14.4%). The overall median CV for rapid progressive
motility was high (37.1%), but progressive motility (15.1%) and total motility (13.8%) were acceptable. Sperm morphology revealed a
large variability in 79.4% irrespective of the staining procedures or evaluation criteria used. Participation in the Belgian EQA is on voluntary basis. Both, participation and implementation of the correct techniques should be made mandatory for accreditation and
benefit of patient treatment. The existing Belgian EQA program should now be harmonized with other existing EQA schemes in
Europe.
INTRODUCTION
Accurate semen analysis is the cornerstone of male infertility
evaluation. However, the large variations in the analysis data
obtained within and between laboratories (Jequier & Ukombe,
1983; Ayodeji & Baker, 1986; Neuwinger et al., 1990; Walker,
1992; Matson, 1995; Keel et al., 2000) have made semen analysis
inaccurate and unreliable (Chong et al., 1983; Mortimer et al.,
1986; Ombelet et al., 1997).
In response to the growing need for standardization of procedures, the World Health Organization (WHO) has published a
series of laboratory manuals to encourage this (WHO, 1980,
1987, 1992, 1999, 2010). Later on, the Nordic Association for
Andrology (NAFA) and the Special Interest Group Andrology
(SIGA) of the European Society of Human Reproduction and
Embryology (ESHRE) have provided more detailed instructions
rnfor the techniques recommended by the WHO (Kvist & Bjo
dahl, 2002).
Although these manuals are widely recognized as the golden
standard for semen testing worldwide, not all laboratories have
implemented the recommended techniques and the repeatedly
updated normal or reference values. Cut-off values (normal vs.
2016 American Society of Andrology and European Academy of Andrology
abnormal) are still highly variable between laboratories, and differences in assessment procedures between laboratories jeopardize the comparability of test results and conclusions regarding
the male fertility status.
As semen analysis is difficult to standardize, quality control is
essential to detect and correct systematic errors and an internal
quality assurance program should ensure that results are both
accurate and precise. Mortimer et al. (1986) introduced the concept of quality assurance in semen analysis, which was included
only from the fourth edition of the WHO manual (1999) and further emphasized in the last edition (WHO, 2010). Quality control
and quality assurance should be an integral part both within [internal quality control (IQC)] and between [external quality control (EQC)] laboratories. While IQC monitors precision, EQC
monitors the accuracy and stability of the methods (Plaut &
Westgard, 2002), thus both are complementary processes.
At present, EQC for the determination of sperm concentration,
motility, and morphology is being widely appreciated in Europe
(Neuwinger et al., 1990; Cooper, 1996; Jrgensen et al., 1997;
Ochsendorf & Beschmann, 1998; Auger et al., 2000; Alvarez
et al., 2005; Mallidis et al., 2012; Jedrzejczak et al., 2012;
Andrology, 110
U. Punjabi et al.
Filimberti et al., 2012) and other parts of the world (Keel et al.,
2000; Brazil et al., 2004; Zuvela et al., 2011).
In 1997, the Scientific Institute of Public Health (IPH) of
the Belgian Ministry became aware of the need for an EQC in
semen analysis because of the large costs ( 116509.92 for
41260 concentration/motility tests and 69410.17 for 26631
morphology tests on yearly basis) covering these analyses and
the lack of standardization in the semen parameters analyzed.
This led to the establishment of an EQC program to monitor
interlaboratory proficiency, aiming for a growing awareness of
the need to implement the correct procedures by participating laboratories. In 1999, the IPH was officially mandated for
the organization of EQC in clinical biology laboratories in Belgium (Demotte, 1999). The IPH was accredited under the
International Organization for Standardization (ISO) guide 43
(Proficiency testing by interlaboratory comparisons, 1997.
Geneva, Switzerland) and The International Accreditation
cooperation (ILAC) G13 (Guidelines for the requirements for
the competence of provider of proficiency testing schemes,
2000. Silverwater, Australia) and since 2011 under ISO17043
(Conformity assessment General requirements for proficiency testing, 2010. Geneva, Switzerland) standard for the
organization of EQC in human semen quality. The present
paper describes 15 years of Belgian experience with external
quality assessment of semen analysis.
Andrology, 110
ANDROLOGY
The results of the participants were analyzed by the IPH and
discussed with the CC. Feedback to the participating laboratories based on WHO recommendations was provided as well as
advice for improvement, with possibility of specific training
when available (Basic semen analysis course in collaboration
with the ESHRE SIGA). Upon request, laboratory technicians
from participating centers could benefit from onsite training in
the laboratories of the members of the CC.
Sample preparation and distribution
One single Andrology laboratory prepared all the samples for
concentration and morphology for each scheme. For sperm
count, human semen for two different pools was collected, fixed
in formalin, and aliquots of 500 lL were prepared. The participating laboratories were instructed to mix the samples gently by
a few aspirations with a glass pipette or using a vortex at low
speed. Spermatozoa were counted according to the laboratorys
routine procedure. Results were recorded as 9106 spermatozoa/
mL. The laboratory was requested to indicate the type of counting chamber used. Since 2007, the use of positive displacement
pipette was also reported.
For morphology, semen smears were prepared from two different pools of semen and air-dried. Two air-dried smears were
distributed per scheme. The participants were instructed to fix
and stain the smears and perform morphological analysis adopting their routine methods. Results were reported as percentage
of normal forms and the morphology smears were as such also
scored as normal or abnormal. The participants were requested
to indicate the type of stain and the criteria used to evaluate
sperm morphology.
For sperm motility, a series of video/DVDs containing four different samples were prepared. Participating laboratories
reported the four motility grades (rapid progressive, slow progressive, non-progressive, and immotile, WHO, 1999) or three
motility grades (progressive, non-progressive, and immotile,
WHO, 2010). Only one video/DVD was distributed per year.
After preparation, the samples were distributed to the participating laboratories by the IPH. The laboratories were asked to
perform the analyses and return the results within 2 weeks of
reception.
Data processing for each survey
Results were received by the IPH and each laboratory was
coded before data processing by the IPH. After data processing,
the results of the survey were discussed with the CC and recommendations were formulated. Per scheme, the results for each
parameter were reported as the overall mean, median, standard
deviation, p10p90, p25p75, minimum and the maximum
value, and the coefficient of variation (CV) of all the participating
laboratories and of those performing the analysis with the same
method. In addition, box and whisker plots were included for
concentration, motility, and morphology. For morphology, in
addition to the percentile ranges, an overall score as normal/abnormal was given to each smear based on the classification used
by each laboratory.
Statistical analyses
Over the total period of 15 years, the evolution of the coefficients of variation for each parameter were presented in figures.
For each parameter, for the whole period (19982012), the
2016 American Society of Andrology and European Academy of Andrology
ANDROLOGY
RESULTS
Participating laboratories
Out of the 200 replies (50%) to the initial 1997 questionnaire,
181 laboratories (90.5%) were performing diagnostic semen
analysis and were in favor of participating in an EQC scheme
Table I Answers to the questionnaire in 2006 regarding the type of laboratories, number of samples analyzed, number of technicians involved and
training undertaken by the laboratory staff
Type of laboratories involved
General Clinical laboratories in a hospital set-up
Laboratories linked to an IVF Centre in a hospital set-up
General Clinical laboratory in a private set-up
Specialized andrology laboratories
Mean number of samples analyzed/month (range)
Sperm concentration
Sperm motility
Sperm morphology
Number of technicians involved in semen analysis
Laboratories were analysis was performed by dedicated
technicians
Laboratories were analysis was performed by technicians
involved in other clinical tests
Information unavailable
Training undertaken by the laboratory staff
Laboratory technicians only performing semen analyses after
training
Laboratory technicians combining semen analysis and other
clinical tests after training
Head of the laboratories (Clinicians/Clinical biologists/
embryologists) with training
72/121 (59.5%)
14/121 (11.6%)
29/121 (24.0%)
6/121 (5.0%)
15 (1250)
10 (1250)
10 (1250)
20/121 (16.5%)
Sperm count
Regarding the 87 samples for sperm count, the median CV
over the whole period (19982012) was 19.2% (Q1Q3: 16.2
22.6), irrespective of the method used (Fig. 2). The use of the
improved Neubauer chamber resulted in a significantly
(p < 0.001) lower median CV of 14.4% (Q1Q3: 12.218.3; Fig. 3)
compared with the global results (Fig. 4).
There was a clear evolution in the use of the different counting
chambers (Fig. 5). The use of the improved Neubauer increased
83/121 (68.6%)
18/121 (14.9%)
26/65 (40.0%)
83/401 (20.7%)
60/88 (68.2%)
Figure 1 Evolution in the number of participants for sperm concentration, motility, and morphology over the whole period (19982012).
160
Number of participants
140
120
100
80
60
12
20
11
20
10
20
09
20
07
08
20
06
20
05
20
03
02
01
00
99
04
20
20
20
20
20
20
98
19
19
19
97
40
Year
Concentration
Morphology
Motility
Andrology, 110
ANDROLOGY
U. Punjabi et al.
Figure 2 Evolution in the mean coefficient of variation (CV) of sperm concentration over the whole period (19982012) using all types of counting
chambers.
90
80
70
CV (%)
60
50
40
30
20
10
20
13
20
12
20
11
20
10
20
09
20
08
20
07
20
06
20
05
20
04
20
03
20
02
20
01
20
00
19
99
19
98
19
97
Year
Figure 3 Evolution in the mean coefficient of variation (CV) of sperm concentration over the whole period (19982012) using the improved Neubauer
counting chamber.
90
80
70
CV (%)
60
50
40
30
20
10
13
20
12
20
11
20
10
20
09
20
08
20
07
20
06
20
05
20
04
20
03
20
02
20
01
20
00
20
99
19
98
19
19
97
Year
from 32 to 68%, whereas the Burker chamber and Makler chamber decreased from 29 to 10% and 12 to 5%, respectively. The
number of participants using the Thoma chamber (8%) and the
Fuchs-Rosenthal chamber (6%) remained stable. The combined
use of the improved Neubauer chamber with a positive displacement pipette (recorded since 2007) is still increasing.
Sperm motility
For sperm motility analysis of the 59 recordings, the overall
median CV was 37.1% for rapid progressive motility grade a (Q1
Q3: 28.259.8), 15.1% for progressive motility grade a + b (Q1Q3:
12.120.4), 13.8% for total motility, grade a + b + c (Q1Q3:
4
Andrology, 110
ANDROLOGY
n = 87
p < 0.001
Figure 5 Evolution in the use of different counting chambers for sperm concentration during the whole period (19982012).
80
70
Number of participants
60
50
40
30
20
10
0
1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008
Year
Improved Neubauer + positive displacement pipette
Burker
Makler
2016 American Society of Andrology and European Academy of Andrology
Improved Neubauer
Thoma
Fuchs Rosenthal
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ANDROLOGY
U. Punjabi et al.
Figure 7 Evolution in the coefficient of variation (CV) of sperm morphology during the whole period (19982012).
250
CV (%)
200
150
100
50
19
97
19
98
19
99
20
00
20
01
20
02
20
03
20
04
20
05
20
06
20
07
20
08
20
09
20
10
20
11
20
12
20
13
Year
Figure 8 Evolution in the use of different staining procedures for sperm morphology during the whole period (19982012).
70
Number of participants
60
50
40
30
20
10
0
1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012
Year
Papanicolaou
GIEMSA
(Fig. 9). In 2012, 89% of the laboratories had adopted the WHO
2010 or the equivalent Strict criteria (Menkveld et al., 1990).
Irrespective of the staining procedures or the criteria used,
there was consensus between the participants in morphology
scoring as normal/abnormal for 69/87 smears (79.3%). In 14/87
(16.1%) smears, there was no agreement and in 4/87 (4.6%)
smears, the borderline score was adopted as consensus.
DISCUSSION
In spite of the clear laboratory guidelines addressing the techniques and quality control procedures for semen analysis, as
published by the WHO and NAFA-ESHRE, the results of the Belgian EQC program reveal a large variability, as also observed by
the other groups (Neuwinger et al., 1990; Matson, 1995; Cooper
6
Andrology, 110
SHORR
Spermac
Diff quick
et al., 1999; Auger et al., 2000; Gandini et al., 2000; Keel, 2004;
Alvarez et al., 2005; Mallidis et al., 2012; Filimberti et al., 2012).
However, the variability observed among the Belgian participants was much more acceptable than what has reported in literature as far as concentration and motility are concerned.
For the first time, we present here the results of an EQC program over an extended period (15 years), including a large number of participating laboratories, and involving a substantial
number of distributions. Over this period, participants were continuously advised by the CC to adopt the latest WHO recommended procedures. Moreover, an additional step toward
standardization was teaching the right procedures during basic
semen analysis courses organized by members of the CC (Pun rndahl et al.,
jabi & Spiessens, 1998; Vreeburg & Weber, 1998; Bjo
2016 American Society of Andrology and European Academy of Andrology
ANDROLOGY
CV (%)
70
60
50
40
30
20
10
0
1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012
Year
WHO 1987
WHO 1992
WHO 1999
U. Punjabi et al.
Andrology, 110
ANDROLOGY
The changes in assessment criteria as well as changes in cut-off
normal values in the consecutive editions of the WHO manual,
have undoubtedly contributed to this problem. In the initial
years of our EQC program, large CVs were observed. In the later
years, there was a tendency toward improvement, although the
CV was still unacceptably high. Different authors ascribed these
variations to a lack of standardization (Chong et al., 1983; Dunphy et al., 1989), to a difference in techniques of smear preparation and staining procedures (Davis & Gravance, 1993) and to
the level of technical expertize (Dunphy et al., 1989; Neuwinger
et al., 1990).
Keel et al. (2000) reported a wide variation in the CV of percent
normal morphology ranging from 15 to 93%. These authors
claimed that premade semen smears eliminate the potential variation associated with individual slide preparation, thereby excluding its potential effect on individual laboratory performance.
Results of Filimberti et al. (2012) suggest that the variability
concerning morphology is independent of the staining procedure as mean CV values for the various methods employed by
their participating laboratories were not different. However, the
mean CV noted in three trials was very high and ranged between
88.6 and 105.6%. Moreover, the participating laboratories
adopted staining procedures not recommended by the WHO
(Haematoxilin-Eosin, May-Grunwald and use of Test Simplets).
According to Filimberti et al. (2012), sperm morphology teaching courses may offer the solution to decrease the variability in
rndahl et al.
the results, confirming the observations of Bjo
(2002). The same authors, however, finally observed that teaching was insufficient to limit variability in the morphology results
at the end of their study period.
In our scheme, we observed a trend toward a reduced variability over the period of 15 years, which might mainly be explained
by the adoption of the WHO 2010 or Strict criteria by most of the
laboratories.
Keel et al. (2000) pointed out that one must be cautious when
computing and comparing CVs among morphology criteria with
different cutoffs for normality. During one of our surveys in
2003, participating laboratories were asked to provide the cut-off
values used to define normality for the specific morphology criteria adopted by them. The laboratories using WHO 1992 criteria
handled a cutoff for normality ranging between 25 and 60%.
Those using WHO-1999 criteria had a cutoff between 10 and
70%, and for the strict criteria cutoffs ranged between 5 and
25%. The change in the normal morphology cutoff of 50% in the
WHO 1987 edition to 30% in the WHO 1992 edition, and the
omission of a normal value in the WHO 1999 edition has certainly added to the ambiguity regarding morphology assessment
and to the increased confusion regarding its clinical relevance
(Riddell et al., 2005). These authors also note that only 5% of the
laboratories who participated in their survey were compliant
with all current WHO guidelines regarding sperm morphology.
Alvarez et al. (2005) also believe that differences in the application of morphologic criteria are the main cause of variations
between laboratories (CV 33.575.0%). The authors, however,
believe that the use of micrometers, as recommended in the
1999 WHO manual, could help to reduce this difference.
In our program, participants were asked to specify the staining
procedure and assessment criteria for sperm morphology at
each survey. However, other sources of error were beyond our
control.
2016 American Society of Andrology and European Academy of Andrology
It is critical to keep in mind that semen analysis is a diagnostic tool, and as such, the results are used to guide
patients treatment. Inappropriate material and procedures
may undoubtedly lead to the wrong diagnosis and inappropriate therapy. In addition, in Belgium, semen analysis costs are
reimbursed by the Health Care System, possible errors in the
procedures arising from incorrect semen analysis may result
in a great waste of public money. Quality survey should meet
the needs of all disciplines that are involved in semen analysis. Participation in an EQC survey should be made mandatory in order to fulfill the requirements for accreditation and
for the benefit of patient treatment. This Belgian EQC survey
over a 15-year period has attempted to reduce interlaboratory
variability. At the same time, participating laboratories have
been encouraged to implement correct techniques as advised
by the WHO. While an overall trend to improve standardization over the years was observed, continuous efforts and new
initiatives should aim to further harmonize the procedures
among the laboratories. This unique long-term EQA program
emphasizes that quality assessment must be a continuous
process paving the way to semen analysis standardization.
The next step toward standardization is to harmonize the Belgian EQC program with an existing EQC scheme of other
European countries or societies.
ACKNOWLEDGEMENTS
The authors acknowledge Jean Claude Libeer (past member of
the IPH), Frank Comhaire and Bernard Van Abelle (past members of the CC).
DECLARATION OF INTEREST
The authors declare no conflict of interest.
FUNDING
IPH departmental funds were used to support the authors
throughout the study period in sample preparation and
distribution.
AUTHOR CONTRIBUTIONS
U.P. substantial contribution to conception, acquisition of
data, analysis and interpretation of data, and drafting the article.
G.V., C.W. revising it critically for important intellectual content.
A.M. involved in sample collection and preparation, contributed
toward the critical discussion of the manuscript. K.V., B.C.
involved in coordinating the scheme distributions, making global reports, critical discussion of the manuscript. All authors
approved the final version of the manuscript.
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