Original Article

The impact of the new 2010 World Health Organization criteria for semen analyses on the diagnostics of male infertility

O impacto dos novos critérios da OMS (2010) para avaliação seminal no diagnóstico da infertilidade

Jaime Larach, M.D.ª, Dayalis González, D.O.ª, Saúl Barrera, M.D.ª, Roberto Epifanio, M.D.ª, Mayka Morgan, M.D.ª, Ana Palma D.O.ª

ªInstituto Valenciano de Infertilidad, Panamá City, Panamá.

Objective: To quantify the effect of the new 2010 World de referência, previamente abaixo dos valores em 1999. Health Organization (WHO) semen analysis reference Resultados: Um total de 255 amostras foram anali- values on reclassifying previous semen analysis parame- VDGDV D SDUWLU GDV TXDLV IRUDP UHFODVVL¿FDGDV WHUVDQGGH¿QLWLRQRISDWLHQWVZLWKPDOHIDFWRULQIHUWLOLW\ HP SHOR PHQRV XP SDUkPHWUR H IRUDP Method: A uni-institutional retrospective chart review. UHFODVVL¿FDGDV FRPR QRUPR]RRVSHUPLFRV 8VDQGR DV Men who consulted for infertility during 2012 at Panamá referências de 1999, houve uma maior prevalência de IVI Clinic. The news 2010 WHO criteria were aplied to achados anormais especialmente de teratozoospermia patients whose spermograms had been analyzed using TXH IRL GH HQTXDQWR D SUHYDOHQFLD GH QRUPR- WKHSUHYLRXVFULWHULDDIWHUZDUGVWKHUHFODVVL¿FDWLRQ ]RRVSHUPLD IRL GH &RP RV YDORUHV GH ZDV HYDOXDWHG &KDQJH RU 5HFODVVL¿FDWLRQ ZHUH GH¿QHG HVWHV HUDP H UHVSHFWLYDPHQWH $OpP GLVVR as the parameter being above the new reference values, com os critérios de 2010, houve uma maior varieda- previously being below that proposed by 1999 WHO. GH GH GLDJQyVWLFRV SDFLHQWHV IRUDP UHFODV- Result(s): A total of 255 samples were analyzed, from VL¿FDGRV SHOD PRUIRORJLD SHOD PRWLOLGD- ZKLFKZHUHUHFODVVL¿HGLQDWOHDVWRQHSDUDPHWHU GH HPYROXPHH QDFRQWDJHPGH DQG ZHUHUHFODVVL¿HGDVQRUPR]RRVSHUPLFV espermatozóides; asthenozoospermia foi o achado que Using the 1999 WHO values there was a higher preva- DSUHVHQWRX D PDLRU WD[D GH UHFODVVL¿FDomR OHQFHRIDEQRUPDO¿QGLQJVVSHFLDOO\RIWHUDWR]RRVSHUPLD Conclusão : Os novos valores de referência resultaram WKDW ZDV ZKLOH QRUPR]RRVSHUPLD SUHYDOHQFH ZDV em muitos de nossos pacientes, que tiveram um esper- :LWKWKHYDOXHVWKHVHZHUHDQG PRJUDPD DQRUPDO VHQGR UHFODVVL¿FDGR FRPR QRUPR- respectively. Also, with the criteria of 2010, a greater zoospermicos. Isto pode levar a uma nova perspectiva variety of diagnoses was evidenced. do seu diagnóstico e tratamento. SDWLHQWV ZHUHUHFODVVL¿HGE\PRUSKRORJ\ Palavras-chave: Andrologia, espermograma, critérios E\PRWLOLW\ E\YROXPHDQG E\ da OMS. VSHUPFRXQWDVWKHQR]RRVSHUPLDZDVWKH¿QGLQJZKLFK VKRZHGWKHKLJKHVWUHFODVVL¿FDWLRQUDWH INTRODUCTION Conclusion(s): The new reference values resulted in Clearly, the male and his semen quality is a key factor many of our patients, who had had an abnormal sper- in investigating and addressing infertility. As evidenced PRJUDP EHLQJ UHFODVVL¿HG DV QRUPR]RRVSHUPLFV 7KLV by Brugh, et al., 2004, male infertility accounts for the may lead to a different perspective on their diagnosis and LQIHUWLOLW\LQDOPRVWRIFRXSOHV treatment. Hence, the evaluation of the male partner is a crucial Key Words: Andrology, spermogram, WHO criteria, step in the diagnosis and treatment of couples atten- infertility. GLQJDQLQIHUWLOLW\¿UVWYLVLW2IFRXUVHZHQHHGDJHQHUDO medical history: anamnesis and physical examination, RESUMO DVLQDOO¿HOGVRIPHGLFLQHDUHSUHUHTXLVLWHV+RZHYHU Objetivo TXDQWL¿FDU R HIHLWR GRV QRYRV YDORUHV in andrology, performing at least one semen analysis, de referencia ( 2010) da Organização Mundial da ideally in a fertility center, is a mandatory step to esta- Saúde (OMS) para a análise do sêmen, em reclas- EOLVKWKHGH¿QLWLYHIHUWLOLW\PDQDJHPHQWIRURXUFRXSOH VL¿FDU SDUkPHWURV GH DQiOLVH GH VrPHQ DQWHULRUHV H D Like many other diagnostic tests, the minimum “normal” GH¿QLomR GH SDFLHQWHV FRP LQIHUWLOLGDGH PDVFXOLQD reference values have been changing over time. While Método: Estudo retrospectivo uni-institucional. Homens we can differentiate “normality” from “abnormality”, it que consultaram para infertilidade ao longo de 2012 na is important to note that having a parameter below a Clínica IVI Panamá. Os novos criterios de 2010 da OMS minimum normal reference value does not necessarily foram aplicados aos pacientes cujos spermograms foram mean being infertile, and males with values below these analisados usando os critérios anteriores (1999), e depois can still achieve pregnancies. At least two pathological DUHFODVVL¿FDomRIRLDYDOLDGD$OWHUDURX5HFODVVL¿FDUIRUDP spermograms, taken in a period of 15 days, is consi- GH¿QLGRVFRPRVHQGRSDUkPHWURDFLPDGRVQRYRVYDORUHV GHUHGDUHTXLUHPHQWWRGH¿QLWLYHO\HVWDEOLVK³DEQRUPD-

93 94 Original Article

lities” in male fertility. Other authors (Mortimer et al., RESULTS 1985, Castilla et al., 2006, Keel et al., 2006) recommend We reviewed the database for all spermogram samples 3 or 4 analyses in a period of 3 months, representing one analyzed during 2012 belonging to patients who consul- complete cycle of spermatogenesis. ted at the IVI Panama Clinic. In total 255 semen reports The semen analysis should be performed by using stan- were found for that period. dard techniques and criteria as described by the World The most frequently found diagnostic applying the 1999 Health Organization (WHO) and updated in 2002 by the SDUDPHWHUV ZDV LVRODWHG WHUDWR]RRVSHUPLD European Society of Human Reproduction and Embryo- followed by teratozoospermia associated with hyposper- logy (ESHRE). The reference values given by WHO are PLD 1RUPR]RRVSHUPLD IUHTXHQF\ ZDV approximate, and, in theory, each laboratory should esta- 7KHOHDVWIUHTXHQWZDVLVRODWHGK\SRVSHUPLD 6HH blish its own, but this task is almost impossible because Table 1. Teratozoospermia (isolated or associated) was RIWKHGLI¿FXOW\LQGH¿QLQJDQGREWDLQLQJDUHIHUHQFHIHUWL- WKH ¿QGLQJ ZKLFK SUHVHQWHG ZLWK WKH KLJKHVW IUHTXHQF\ le population. For this reason, most laboratories adopted IROORZHG E\ ROLJR]RRVSHUPLD K\SRVSHUPLD WHO criteria which come from a large fertile population, DVWKHQR]RRVSHUPLD DQG ¿QDOO\ FU\SWR]RRVSHUPLD 6HH EXWGRQRWLQWKHPVHOYHVFRQ¿UPIHUWLOLW\RULQIHUWLOLW\ Table 2. 6LQFH :+2 KDV SXEOLVKHG ¿YH HGLWLRQV RI ³:+2 Manual for the Examination of Human Semen and Table 1. 1999 WHO diagnostics and percentage of reclassi- Sperm-Cervical Mucus Interaction.” The latest of 2010 ¿FDWLRQ used a fertile population in 14 countries and decreased the normal minimum cutoffs of 1999 criteria. The main Diagnostics N: 255 5HFODVVL¿FDWLRQ objective (Cooper et al., 2011) was to improve the inci- Normozoospermia 0 dence of misdiagnosis and thereby improve the clinical Teratozoospermia: management of patients. Of course, using these para- PHWHUVWRGH¿QLWLYHO\HVWDEOLVKQRUPDOLW\ZRXOGEHYHU\ Oligoasthenoterato- risky: while WHO evaluated a large and varied population zoospermia: (all of them fertile) some biases can be found regarding Oligoteratozoospermia: population which might lie outside (underdiagnosed or Teratozoospermia/ overdiagnosed) the range used in 2010 WHO. A man hypospermia: VKRXOGQRWEHFODVVL¿HGDVIHUWLOHRULQIHUWLOHEDVHGRQO\ Oligoasthenoterato- on the spermogram or semen analysis. zoospermia/ Recently, Murray et al., 2012, published a study to assess hypospermia: the impact of the new 2010 WHO criteria on spermo- Astenoteratozoospermia: JUDPVDQGLQWHUSUHWLQJDQGGH¿QLQJWKHFKDQJHIURPWKH FXWRIIVRI:+27KH\IRXQGUHFODVVL¿FDWLRQLQVHPL- Astenoteratozoospermia/ hypospermia: nal volume, sperm concentration, motility and morpho- ORJ\ RI DQG UHVSHFWLYHO\ IRU Oligoteratozoospermia/ SDWLHQWVZLWKPXOWLSOHVHPHQVDPSOHVDQG hypospermia: DQGUHVSHFWLYHO\IRUSDWLHQWVZLWKDVLQJOH Cryptozoospermia 4/255 VHPHQ VDPSOH 7KHLU VWXG\ DOVR VKRZHG WKDW RI SDWLHQWVZHUHUHFODVVL¿HGRQDWOHDVWRQHSDUDPHWHU /HW Hypospermia: ò XVUHPHPEHUWKDWUHFODVVL¿FDWLRQZDVGH¿QHGDVDVHPHQ parameter changing from being below the old reference TOTAL: value to being above the new reference value.) As shown, the application of the current 2010 WHO criteria to the samples increases the incidence of normozoosper- Table 2.7RWDOIUHTXHQF\RI¿QGLQJV LVRODWHGRUDVVRFLD- mia principally because of morphology and sperm motility. ted), 1999 WHO. The objective of this study is to quantify at IVI Panama FINDING N: 255 clinic the magnitude of change in the interpretation of Teratozoospermia spermograms when we apply the new criteria of 2010 WHO criteria, in comparison to the 1999 WHO criteria. Oligozoospermia Hypospermia MATERIALS AND METHODS Asthenozoospermia We conducted a review of all spermogram reports made Normozoospermia during 2012 for patients consulting for infertility at IVI Panamá Clinic. All reports have data concerning moti- Cryptozoospermia lity, concentration, morphology and volume. First, we applied both 1999 and 2010 WHO reference values, establishing the respective diagnosis for each sample. RIVDPSOHVKDGUHFODVVL¿FDWLRQLQDWOHDVWRQHSDUD- :H WKHQ DQDO\]HG WKH SHUFHQWDJH RI UHFODVVL¿FDWLRQ RU meter, with astenoteratozoospermia associated with hypos- change and also other issues such as the frequency of SHUPLD EHLQJ WKH GLDJQRVWLF ZLWK WKH KLJKHVW UHFODVVL¿FD- GLDJQRVHV DQG ¿QGLQJV LVRODWHG RU DVVRFLDWHG WR HDFK WLRQUDWH $VZHDQWLFLSDWHGQRUPR]RRVSHUPLDDQG WHO interpretation, as well as the characteristics of the cryptozoospermia were the only diagnoses which were not UHFODVVL¿FDWLRQDQGWKHQHZHYLGHQFHDOLNH UHFODVVL¿HG6HH7DEOH The minimum reference values of 2010 WHO applied are: VDPSOHV ZHUH UHFODVVL¿HG E\ PRUSKRORJ\ volume of 1.5 ml, sperm concentration of 15 million/mL, E\ PRWLOLW\ E\ YROXPH DQG E\ PRWLOLW\RIDQGRIQRUPDOPRUSKRORJ\ .UXJHU VSHUP FRXQW $VWKHQR]RRVSHUPLD ZDV WKH ¿QGLQJ ZLWK WKH criteria). On the other hand, the 1999 WHO parameters KLJKHVWUHFODVVL¿FDWLRQUDWH 6HH7DEOHVDQG included: volume of 2.0 ml, concentration of 20 million/ $SSO\LQJ WKH SDUDPHWHUV SDWLHQWV ZHQW P/PRWLOLW\RIDQGRIPRUSKRORJ\ from having a spermogram abnormality to normozoosper-

JBRA Assist. Reprod. | V. 17 | nº2 | Mar-Apr / 2013 The impact of the new 2010 World Health Organization criteria - Larach, J. et al. 95 mic, which increased the total frequency of normozoos- Table 6. 2010 WHO diagnostics. SHUPLD WR DQG GLPLQLVKHG WKDW RI WHUDWR]RRVSHUPLD Diagnostic N:255 LVRODWHGRUDVVRFLDWHG WR)XUWKHUPRUHWKHGLDJQRVLV Normozoospermia most frequently found was normozoospermia, while the least Oligozoospermia frequent was astenoteratozoospermia. Moreover, we obser- Teratozoospermia ved the emergence of a variety of diagnostics which we did Asthenozoospermia not see with 1999 criteria, such as isolated oligozoospermia, isolated asthenozoospermia, as well as the association of Oligoasthenoteratozoospermia hypospermia with normozoospermia. Overall, with the 2010 Oligoasthenozoospermia parameters, we observed a higher frequency of normozoos- Oligoteratozoospermia permia, a lower prevalence of abnormalities, and a greater Teratozoospermia/hypospermia variety of diagnostics. See Tables 6 and 7. Oligoasthenoteratozoospermia/ hypospermia Table 3. )UHTXHQF\ RI ¿QGLQJV ZKLFK KDYH UHFODVVL¿FDWLRQ Normozoospermia/Hypospermia DFFRUGLQJWRWRWDORIVDPSOHVDQGUHFODVVL¿FDWLRQUDWHIRUHDFK Asthenoteratozoospermia one. Cryptozoospermia Diagnostic N: 255, 5HFODVVL¿FDWLRQ Asthenozoospermia/hypospermia Total Rate Teratozoospermia (245) Asthenozoospermia (49) Table 7. 7RWDOIUHTXHQF\ RI ¿QGLQJV LVRODWHG RU DVVRFLDWHG Hypospermia (54) 2010 WHO. Oligozoospermia (63) Diagnostic N:255 Cryptozoospermia (4) Teratozoospermia Oligozoospermia Asthenozoospermia Table 4. 0L[HG GLDJQRVWLFV IRU :+2 5HFODVVL¿HG SDUD- Hypospermia PHWHUHVSHUHDFKGLDJQRVWLFDQGE\:+2LQÀXHQFHRUGHU (+,++,+++). Normozoospermia Cryptozoospermia Diagnostic Moti- Morpho- Sperm Volu- lity logy Count me Oligoasthenoterato +++ + ++ )LQDOO\ NHHS LQ PLQG WKDW RI WKH VDPSOHV ZHUH zoospermia QRW UHFODVVL¿HG )URP WKRVH H[FHSW QRUPR]RRVSHUPLD Oligoterato- + + DQG FU\SWR]RRVSHUPLD FRQWL- zoospermia QXHGWRVKRZWKH:+2DEQRUPDO¿QGLQJVEXWZLWK Teratozoospermia/ ++ + values closer to normal minimum cutoff of 2010 WHO. hypospermia Oligoasthenoterato- + ++ DISCUSSION AND CONCLUSIONS zoospermia/ As mentioned, WHO has made changes to the spermo- hypospermia gram parameters in the last few years. Some authors Asthenoteratozoos- ++ + have previously suggested the need for change: Ombelet permia et al., 1997, showed a need for change in the interpre- Asthenoteratozoos- +++ ++ + tation of semen analysis, comparing fertile and sub-ferti- permia/ le population. Chia et al., 1998, applied the 1998 WHO hypospermia parameters to spermograms in a fertile population, and Oligoterato- + ++ VKRZHGWKDWRQO\RIIHUWLOHPHQKDGVSHUPPRUSKR- zoospermia/ logy within normal parameters. It is said that the predic- hypospermia

Table 5.:+2UHFODVVL¿HGGLDJQRVWLFVGLVWULEXWLRQE\SHUFHQWDJHRIWKHQHZ:+2GLDJQRVWLFVSHUHYHU\SUHYLRXV:+2 diagnostic. OMS 2010 N OT OA AT T O H OAT A T/H A/H OMS 1999 T OAT T/H OAT/H AT AT/H OT/H H OT

T: Teratozoospermia. AT: Asthenoteratozoospermia. A: Asthenozoospermia OAT: Oligoasthenoteratozoospermia. N: Normozoospermia. OT: Oligoteratozoospermia OA: Oligoasthenozoospermia. H: Hypospermia. O: Oligozoospermia.

JBRA Assist. Reprod. | V. 17 | nº2 | Mar-Apr / 2013 96 Original Article

tive power of the traditional reference values in semen Perhaps morphology is the most worrying parameter at parameters is not absolute and has a high degree of over- the time of making a decision about what kind of treat- lap between what is called normal and abnormal. Aziz et ment we should offer. While with the 2010 criteria, the al., 2008, and Niederberger et al., 2011. cutoff for other parameters decreased by about a quarter Murray and Cols argue that perhaps there is some bias in relation to the criteria of 1999, morphology decrea- in the 2010 WHO criteria, as some population might lie sed by two-thirds. In other words, the new 2010 criteria outside the range used in that (underdiagnosis or over- decreased the minimum normal cutoff in morphology to diagnosis), mainly because a spermogram does not have what was considered the limit for severe teratozoosper- DQ\XSSHUOLPLWDQGRQWKHRWKHUKDQGLWLVGLI¿FXOWWR mia in 1999. This type of change is a parallel discovery diagnose a man as infertile, having a parameter below to some debates which arise about fertility treatments the reference value, when only fertile population was prognosis as well as indications of high or low complexity. included in that study. Moreover, Jon et al., 2012, and Just to cite examples, some works argue that there is a Lamb et al., 2010, believe that some functional parame- VLJQL¿FDQWGHFUHDVHLQWKHUHVXOWVDQGRWKHUVQRWZKHQ ters which are not routinely evaluated in a spermogram SHUIRUPLQJ DUWL¿FLDO LQVHPLQDWLRQ ZLWK QRUPDO VSHUP FDQGH¿QLWO\LQÀXHQFHWKH¿QDOGLDJQRVLVRIIHUWLOLW\ PRUSKRORJ\OHVVWKDQ/HHHWDO9DQ:DDUWHW As we have seen, it is not easy to establish parameters al., 2001, Matorras et al., 1995. of normality or abnormality on a diagnostic test that 7KXVZHKDYHVHHQKRZFRPSOLFDWHGLWLVWRGH¿QHWKH provides only one variable in relation to a desired goal cutoffs, as the treatment results vary from study to (the pregnancy), and yet at the same time depends on study, even after applying the new 2010 criteria. Moreo- subjective and sometimes non-standard measures prone ver, many authors propose that semen parameters to change. VKRXOG QRW EH FODVVL¿HG DV QRUPDO RU DEQRUPDO EXW DV How much the interpretation of a spermogram could above or below the reference value. Perhaps, in terms of change by applying the new 2010 WHO criteria has alre- motility and concentration, we have a little less compli- ady been investigated by Murray et al. recently. They cation when indicating a treatment, taking into account IRXQG WKDW RI SDWLHQWV KDG UHFODVVL¿FDWLRQ LQ DW the current availability of the test for sperm capacitation least one parameter, mainly in morphology and motility; or motile sperm count (REM in Spanish), which nowadays WKDWEHWZHHQDQGRISDWLHQWVFKDQJHGLQ establishes clear breakpoints about how the prognosis PRUSKRORJ\DQGEHWZHHQDQGFKDQJHGLQ WHFKQLTXHVFKDQJHVVLJQL¿FDQWO\DERYHPLOOLRQWRRIIHU PRWLOLW\7KH\GH¿QHGWKHLUUHVXOWVDVVLJQL¿FDQWFKDQJHV low complexity treatments; above 1-1.5 million to offer considering that the parameter variations due to the new conventional IVF; and below 1 million to offer ICSI. 2010 WHO criteria were relatively small, being only: 5 Our study is a retrospective review that may have many PLOOLRQP/LQVSHUPFRQFHQWUDWLRQLQPRUSKRORJ\ OLPLWDWLRQV 7KH ¿UVW DQG SHUKDSV WKH PRVW LPSRUWDQW POLQYROXPHDQGLQSURJUHVVLYHPRWLOLW\ is that we only analyzed patients with a single spermo- 2XUUHYLHZVKRZHG¿QGLQJVHYHQPRUHVXUSULVLQJEHFDX- gram. Considering that within the current recommenda- se when we applied 2010 parameters, we passed from a tions aimed at optimizing the study and interpretation of bleak panorama where normality practically didn’t exist this test, and increasing diagnostic reliability, we should using 1999 criteria: from a normozoospermia prevalence ideally recommend at least two spermograms per patient. RIWRDSUHYDOHQFHRI7KLV¿QGLQJLVPRUH However, it’s worth noting that the objective of this study in line with what the literature has proposed, suggesting was not to analyze the evolution over time of one or more WKDWDURXQGRILQIHUWLOHFRXSOHVSUHVHQWVRPHGHJUHH patients, but to analyze with different reference values of male factor. We also observed a large impact on the a single spermogram. On the other hand, in the study RYHUDOOSUHYDOHQFHRIWHUDWR]RRVSHUPLDZKLFKZDV by Murray et al., 2012, which made a similar analysis ZLWKFULWHULDEXWRQO\ZLWKFULWHULD6R WRRXUVZHGLGQRWGHWHFWDVLJQL¿FDQWGLIIHUHQFHLQWKH we can say that the new criteria have balanced the scales UHFODVVL¿FDWLRQDPRQJSDWLHQWVZKHWKHUWKH\KDGRQHRU E\ UHVFXLQJ VSHUPRJUDPV ¿QGLQJ QRUPR]RRVSHUPLD DW two spermograms. the expense of a decrease mainly in the prevalence of The other limitation of this study is that we did not inclu- teratozoospermia and asthenozoospermia. de reproductive outcomes and patients’ progress, espe- Despite this, we hesitate to consider that we have the FLDOO\IURPWKRVHZKRSUHVHQWHGUHFODVVL¿FDWLRQLQRUGHU GH¿QLWLYH YHUVLRQ UHJDUGLQJ WKH ¿QDO GLDJQRVHV LQ PDOH to correlate and compare the probability of success in infertility, taking into account that some authors argue assisted reproduction treatments in relation to both 1999 that nowadays some functional problems can be missed and 2010 WHO criteria. In any case, we believe that this DQGEHSUHVHQWLQVSHUPRJUDPVZKLFKDUHFODVVL¿HGDV VWXG\FRXOGEHWKH¿UVWVWHSLQH[DPLQLQJWKHFRQVHTXHQ- normal, and instead we could be including patients with ces of the new 2010 WHO criteria on male fertility diag- abnormalities in the normozoospermics group. QRVLVDQGWRVWDUWLIQHFHVVDU\WRUHGH¿QHQHZUHIHUHQ- With This latter outcome many patients can lose the ce values. As Cooper et al., authors of the new publication advantages of further evaluation, as Kolletis and Cols on WHO criteria, pointed out, it is clear that the semen VDLG7KH\KDYHVKRZQWKDWXSWRRIPHQSUHVHQWLQJ and the current reference values, become a complemen- with infertility may have serious medical problems which tary tool to medical history, which is important to support are subsequently discovered, within the context of good our approach to, and management of, couples consul- medical practice, during the investigation into the cause ting for infertility, and working towards an optimization of their infertility. of their parameters. Also, with the appearance of new 7KHRWKHULVVXHWKDWDULVHVZKHQDSSO\LQJWKLVUHFODVVL¿- VSHFL¿FJHRJUDSKLFUHJLRQVWXGLHVIXUWKHUUH¿QHPHQWRI cation and adopting the 2010 WHO criteria is the thera- biases may avoid overlapping of normozoospermics with peutic approach derived from that. Normally, the basic altered spermograms. study of semen guides us towards the degree of comple- On our side, we feel that, with our simple study, we disco- xity in assisted reproductive treatments that a couple YHUHGDVXUSULVLQJFKDQJHLQUHFODVVL¿FDWLRQRIPDOHLQIHU- UHTXLUHVGHSHQGLQJRQWKHVHYHULW\RIWKH¿QGLQJVDQG tility diagnoses by applying the new 2010 WHO criteria, of course, also depending on the other variables which and the next step might be to try to discover whether play a role in achieving pregnancy. WKHVHFKDQJHVDUHDOVRUHÀHFWHGLQWKHUHVXOWVRIIHUWLOLW\

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