Semen quality

Semen quality is a measure of the ability of semen to accomplish fertilization. Thus, it is a measure of fertility in a man. It is the sperm in the semen that are of importance, and therefore semen quality involves both sperm quantity and quality. Decreased semen quality is a major factor of male infertility.

Cryptorchidism, Hypospadias, Testicular cancer and poor Semen quality make up the syndrome known as Testicular dysgenesis syndrome.

Factors

There are many factors that influence the sperm quality. Exposure to any of the temporary factors can cause up to a three-month delay before sperm quality returns to normal, due to spermiogenesis.[1]

General decline

A 2017 review and meta-analysis found sperm counts among Western men (i.e. men in Australia, Europe, New Zealand, and North America) declined 50—60% between 1973 and 2011, with an average decline of 1.4% per year. The meta-analysis found no indication the decline is leveling off. The amount of decline among men in North America and men in Australia/Europe is similar. The decline in sperm count among men in South America, Asia, and Africa is less than men in Western countries, though the amount of decline in these regions is uncertain. Reasons for the decline are not known with certainty, but it may be associated with chemical exposure or maternal smoking during prenatal development or pesticide exposure or lifestyle changes during adulthood.[2]

Age

Although it is possible for men to father children into old age, the genetic quality of sperm, as well as its volume and motility, all typically decrease with age.[3] In other words, older sperm are less likely to result in a successful pregnancy and, moreover, the cumulative fragmentation of sperm DNA over time[4] increases the likelihood that a small fraction of men will pass on achondroplasia and transmit multiple genetic and chromosomal defects.[5] For example, the percentage of sperm with highly damaged DNA, comet extent, DNA break number, and other comet measures has been found to be significantly higher in men aged 36–57 years than in those aged 20–35 years.[6] Advancing paternal age has been implicated in a number of possible health effects. One particularly well-studied connection is the link between advancing age and autism. For example, one study of 943,664 children less than 10 years old,[7] found that, with confounding variables controlled, the risk of autism increased with increasing paternal age.[7] In men with a normal level of sperm production (normozoospermia), the percentage of sperm DNA fragmentation is positively correlated with age, and inversely correlated with progressive sperm motility.[8] No age related effects on sperm were noted in separate control groups recruited in different geographical locations, indicating that dietary habits, lifestyle or ethnicity could play a part in the quality of sperm.

While advanced age can be a possible factor in sperm motility and health, the sperm of men below 20 years of age has likewise been linked to an increase in birth defects such as neural tube defects, hypospadias, cystic kidney, and Down syndrome.[9]

Prospective fathers should take up age-related fertility issues with a qualified fertility specialist such as a reproductive endocrinologist.

Heat

Sperm are heat-sensitive, and cannot endure high temperatures. Increases of 2-3°C are associated with increased DNA fragmentation.[10] The body has compensatory mechanisms, like the cremaster muscle relaxing and letting the testicle hang further away from the warm body, sweating and a countercurrent exchange of blood cooling inflowing blood. However, despite these compensations, there are activities that should not be performed too often, in order to prevent infertility due to heat;

Fever raises the body temperature, which can strike sperm quality. In the same way, sperm quality can be lower in the summer.[1]

Contrary to widely held beliefs, no evidence supports that wearing constrictive underwear, or "briefs," decreases fertility. Even with an elevation in temperature of 0.8-1° caused by wearing constrictive underwear, no changes in sperm parameters, no decrease in spermatogenesis, and no changes in sperm function are observed [11]

Physical trauma

A blow from outside does not affect the sperm quality of already produced sperm cells. Furthermore, the testes are well protected in the scrotum, for example by the tunica vaginalis, making the testes slide away from external pressure rather than being malformed from it; however, a hard enough hit can close or crush the capillaries that supply the sperm producing tissue, resulting in permanent or temporary and partial or total inability to produce sperm in the affected testicle.

Chemicals

There is suspicion that many toxic substances, including several types of medication and hormones, and also constituents of the diet, influence sperm quality.[1] While a few chemicals with known effects on fertility have been excluded from human consumption, we cannot know if others remain undiscovered. Many products that come into direct contact with spermatozoa lack adequate testing for any adverse effect on semen quality.[12]

Endocrine disruptors

Endocrine disruptors are chemicals that interfere with the endocrine (hormone) system.

A 2008 report demonstrated evidence of the effects of feminizing chemicals on male development in each class of vertebrate species as a worldwide phenomenon; these chemical are suspected of reducing the sex ratio and sperm counts in humans.[13] Ninety-nine percent of over 100,000 recently introduced chemicals are poorly regulated.[13]

At least three types of synthetic toxins have been found in the semen of student volunteers: polychlorinated biphenyls (PCBs), DDT, and hexachlorobenzene.[14] DDT and hexachlorobenzene are associated with decreased semen quality, while PCBs are associated with decreased fertility overall.[12] Leaks of dibromochloropropane (DBCP) have caused sterility in men.[14] Soldiers that were exposed to dioxins and dioxin-like compounds during the Vietnam war have given rise to children with an increased rate of birth defects.[14]

Phthalates, a ubiquitous pollutant, may cause decreased sperm production when having been exposed to it during prenatal development.[12][15]

Other potential xenoestrogens that have been associated with decreased sperm quality in some studies are bisphenol A, nonylphenol and octylphenol.[12]

Medication

In addition, in vitro studies have observed altered sperm function by the following medications:

Also, numerous products that are intended for exposure to spermatozoa have only a general assumption of safety based on the absence of evidence of actual harm.[12]

Hormones

The body also has natural variations in hormone concentrations, giving sperm quality natural fluctuations as well.[1]

Diet

Other chemicals

Environmental mutagens that are associated with decreased semen quality include the following:

Other environmental agents associated with decreased semen quality include:

Last ejaculation

How long the man has abstained prior to providing a semen sample correlates with the results of semen analysis and also with success rates in assisted reproductive technology (ART).

Both a too short period of time since last ejaculation and a too long one reduce semen quality.

A period of time of less than one day reduces sperm count by at least 20%.[28]

Longer periods of abstinence correlate with poorer results – one study found that couples where the man had abstained for more than 10 days before an intrauterine insemination (IUI) had only a 3% pregnancy rate. An abstinence period of only 1 or 2 days produce the highest pregnancy rates per IUI cycle compared with longer intervals of ejaculatory abstinence.[29] This increase in pregnancy rate occurs despite a lower value of total motile spermatozoa.[29] Daily sexual activity increases sperm quality in men minimizing DNA damage in the sperm -because it is speculated to result in less storage time where damage may accumulate.[30]

Masturbation vs intercourse

Semen samples obtained via sexual intercourse contain 70[31]-120[32]% more sperm, with sperm having a slightly higher[33] motility and slightly more normal[33] morphology, compared with semen samples obtained via masturbation. Sexual intercourse also generates a 25–45%[33] increase in ejaculate volume, mainly by increased prostate[34] secretion.

This intercourse advantage is even greater for men with oligospermia.[33]

However, the single factor or factors for the intercourse advantage have not yet been isolated. It cannot be explained by presence of visual perception of physical attractiveness alone during stimulation,[33][35] although there may be a slight correlation.[36] Neither do any substantial fluctuations in sex hormones explain the intercourse advantage.[34] It is hypothesized that sexual intercourse subdues an inhibition from the central nervous system,[33] but what, in turn, is the subduing factor is still not completely known.

Home or in clinic

The sperm quality is better if the sample is collected at home than in the clinics.[37] Collecting the sperm at home gives a higher sperm concentration, sperm count and motility particularly if the sperm is collected via sexual intercourse.[37] If the semen sample is to be collected by masturbation, a specimen from the early stages of the ejaculate should be into a clean new and unused, sealed collection cup.

Environment

For semen that has been ejaculated, the quality deteriorates with time. However, this lifetime can be shortened or prolonged, depending on the environment.

Outside body

Sperm outside the body generally has a life expectancy which is considered to depend on pH, temperature, presence of air and other factors, and is unpredictable but smaller than the life expectancy inside the human body. For instance, sperm donors who collect the sample outside the clinic are advised to have handed in the sample no more than one hour from collection, and to keep it, if not at body temperature, then at least at room temperature.[38]

In a non-harmful environment outside the body, such as in a sterile glass container[33] the number of motile sperm decreases by approximately 5-10%[33] per hour. In contrast, in a latex condom, the quality decreases by 60-80%[33] per hour, rendering the sample unusable in a relatively short time.

In female

The environment in the uterus and fallopian tubes are advantageous. A pregnancy resulting from sperm life of eight days has been documented.[39][40][41]

Others

Tobacco smoking lowers the sperm quality,[14] perhaps by decreased ability to attach to hyaluronan on the egg cell.[42] Wright et al.[10] have reviewed evidence that smoking is associated with increased sperm DNA damage and male infertility. Smoking cannabis can decrease sperm quantity.[14]

Long-term stress is also suggested.[1]

Higher levels of intelligence are also correlated with higher levels of sperm quality in three key indicators: sperm concentration, sperm count and sperm motility. Men who scored high on a battery of intelligence tests tended to have higher counts of healthy sperm, while low scorers tended to have fewer and more sickly sperm. It is conceivable that intelligence might tip off a man's overall health to women looking for a mate with healthy genes, explained University of New Mexico evolutionary psychologist Geoffrey Miller at a talk at Harvard University. "Though the connections between brains and sperm were 'not awesome, they're there and highly significant,' Miller said. All things held equal, good sperm and good brains go together."[43][44]

Regarding diet, malnutrition or an unhealthy diet can lead to e.g. Zinc deficiency, lowering sperm quality.

Sperm quality is better in the afternoon than in the morning.[45] Adrenaline-levels are higher during awakening (~06.00 to noon),[46] which may contribute similarly to general stress.

Lack of exercise, as well as excessive exercise, are minor factors. In professional sports, semen quality parameters tend to decrease as training requirements increase. The effect differs substantially between different professional sport types. For example, water polo appears substantially less harmful to semen quality than triathlon.[47]

A longer duration of sexual stimulation before ejaculation slightly increases sperm quality.[48]

Males carrying Robertsonian translocations in their chromosomes have significantly higher degree of sperm cell apoptosis and lower concentration. Sperm cells also have decreased forward motility, but normal morphology.[49]

Testicular cancer, Leydig cell tumours and Sertoli cell tumours are also associated with reduced sperm count and quality.[50]

Tests

Semen analysis

A semen analysis typically measures the number of sperm per millilitre of ejaculate, and analyzes the morphology (shape) and motility (ability to swim forward) of the sperm (the typical ejaculate of a healthy, physically mature young adult male of reproductive age with no fertility-related problems usually contains 300–500 million spermatozoa, though only a couple of hundred survive in the acidic environment of the vagina to be candidates for successful fertilization). Also usually measured are the concentration of white blood cells, the level of fructose in the semen, and the volume, pH, and liquefaction time of the ejaculate.[51][52]

A number of factors may influence the accuracy of semen analysis results, and results for a single man may have a large amount of natural variation over time.[53] For this reason, a subfertile result must be confirmed with at least two further analyses.[54]

Hamster zona-free ovum test

A man's sperm are mixed with hamster eggs that have had the zona pellucida (outer membranes) removed, and the number of sperm penetrations per egg is measured.[55] No strong correlation has been found between hamster egg penetration rates and the various semen parameters and the role of the hamster egg penetration test in the investigation of the causes of infertility should be evaluated further.[56] However, a negative result on the hamster test correlates with a lower probability of the man's partner becoming pregnant.[57]

Antisperm antibodies test

Presence of antisperm antibodies may be responsible for sperm agglutination, reduced sperm motility, abnormal postcoital test. Several tests are presently available including Sperm Immobilization test, Sperm Agglutination tests, Indirect immunofluorescence test, Enzyme-linked immunosorbent assay, Radiolabelled Antiglobulin Assay. One of the most informative and specific tests is Immunobead Rosette Test which can identify different antibody classes involved (IgG, IgA, IgM) and location on the sperm cell (head, body or tail).[58]

Hemizona test

Hemizona test is a test to evaluate sperm zona-binding capacity. In this test, the two halves of human zona pellucida is incubated with patient's capacitated sperm and control fertile donor's sperm.[58]

Other tests

Cryopreservation

When performing cryopreservation of semen, it is the sperm quality after reviving the sample that is of importance, because many sperm cells die in the process.

To be of use in assisted reproductive technology, the sample should after thawing have more than 5 million motile sperm cells per ml with a good grade of mobility. If the grade of mobility is poor, 10 million motile cells per ml is required.[1]

Home insemination of previously frozen sperm can be accomplished with the use of a cervical cap conception device as a delivery system for the sperm.[59]

Bad freezers

In 10–20% of all men, the semen does not endure cryopreservation.[1] The cause is unknown. It does not necessarily mean an otherwise bad semen quality.

Sperm washing

When a sperm sample is prepared for intrauterine insemination, it is washed at a facility such as a fertility clinic or a sperm bank. Some sperm does not survive the washing process, as is also the case when freezing the sperm.[60]

References

  1. 1 2 3 4 5 6 7 8 9 10 11 Cryos International - Denmark(Danish)
  2. ↑ Levine, Hagai; Jørgensen, Niels; Martino-Andrade, Anderson; Mendiola, Jaime; Weksler-Derri, Dan; Mindlis, Irina; Pinotti, Rachel; Swan, Shanna H. (25 July 2017). "Temporal trends in sperm count: a systematic review and meta-regression analysis". Human Reproduction Update: 1–14. doi:10.1093/humupd/dmx022.
  3. ↑ Gurevich, Rachel (06-10-2008). "Does Age Affect Male Fertility?". About.com:Fertility. About.com. Retrieved 14 February 2010. Check date values in: |date= (help)
  4. ↑ Herbert, MD, Dr. Carl M. (01-02-2007). "Sperm Quality and Age". Healthline: Infertility Insights. Healthline Networks, Inc. p. 1. Retrieved 15 February 2010. Check date values in: |date= (help)
  5. ↑ Osolin, Charlie (06-05-2006). "Study shows that genetic quality of sperm deteriorates as men age". LLNL Public Affairs Office News Release. Lawrence Livermore National Laboratory. Retrieved 14 February 2010. Check date values in: |date= (help)
  6. ↑ Singh NP; Muller CH; Berger RE (2003). "Effects of age on DNA double-strand breaks and apoptosis in human sperm" (PDF). Fertil Steril. 80 (6): 1420–30. PMID 14667878. doi:10.1016/j.fertnstert.2003.04.002.
  7. 1 2 Lauritsen MB; Pedersen CB; Mortensen PB (2005). "Effects of familial risk factors and place of birth on the risk of autism: a nationwide register-based study". J Child Psychol Psychiatry. 46 (9): 963–71. PMID 16108999. doi:10.1111/j.1469-7610.2004.00391.x.
  8. ↑ Belloc S, Benkhalifa M, Cohen-Bacrie M, Dalleac A, Amar E, Zini A (2014). "Sperm deoxyribonucleic acid damage in normozoospermic men is related to age and sperm progressive motility". Fertil. Steril. 101 (6): 1588–93. PMID 24690240. doi:10.1016/j.fertnstert.2014.02.006.
  9. ↑ McIntosh, GC; Olshan, AF; Baird, PA (May 1995). "Paternal age and the risk of birth defects in offspring.". Epidemiology (Cambridge, Mass.). 6 (3): 282–8. PMID 7619937. doi:10.1097/00001648-199505000-00016.
  10. 1 2 Wright C, Milne S, Leeson H (2014). "Sperm DNA damage caused by oxidative stress: modifiable clinical, lifestyle and nutritional factors in male infertility". Reprod. Biomed. Online. 28 (6): 684–703. PMID 24745838. doi:10.1016/j.rbmo.2014.02.004.
  11. ↑ Wang C, McDonald V, Leung A, Superlano L, Berman N, Hull L, et al. Effect of increased scrotal temperature on sperm production in normal men. Fertil Steril. Aug 1997;68(2):334-9. [Medline]
  12. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 Mortimer, D.; Barratt, C. L. R.; Bjorndahl, L.; De Jager, C.; Jequier, A. M.; Muller, C. H. (2013). "What should it take to describe a substance or product as 'sperm-safe'". Human Reproduction Update. 19: i1. doi:10.1093/humupd/dmt008.
  13. 1 2 <Please add first missing authors to populate metadata.> (07/12/2008). "It's official: Men really are the weaker sex". The Independent. Check date values in: |date= (help)
  14. 1 2 3 4 5 6 7 motherearthnews.com - THE SPERM CRISIS.
  15. ↑ [sciencenews.org: EPA should test demasculinizing pollutants collectively, NRC says] By Janet Raloff. Web edition : Thursday, December 18th, 2008
  16. ↑ "WebMD: Smoking marijuana lowers fertility".
  17. ↑ Whan LB; West MC; McClure N; Lewis SE (March 2006). "Effects of delta-9-tetrahydrocannabinol, the primary psychoactive cannabinoid in marijuana, on human sperm function in vitro". Fertility and Sterility. 85 (3): 653–60. PMID 16500334. doi:10.1016/j.fertnstert.2005.08.027.
  18. ↑ Safarinejad MR (November 2008). "Sperm DNA damage and semen quality impairment after treatment with selective serotonin reuptake inhibitors detected using semen analysis and sperm chromatin structure assay". The Journal of Urology. 180 (5): 2124–8. PMID 18804223. doi:10.1016/j.juro.2008.07.034.
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  21. ↑ http://www.healthjockey.com/2008/09/17/beer-coffee-wine-and-nuts-may-lower-male-fertility
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  26. ↑ Folate 'may keep sperm healthy' BBC News. Last Updated: Thursday, 20 March 2008, 04:39 GMT
  27. ↑ "Merck Veterinary Manual".
  28. ↑ Nnatu SN; Giwa-Osagie OF; Essien EE (1991). "Effect of repeated semen ejaculation on sperm quality". Clinical and Experimental Obstetrics & Gynecology. 18 (1): 39–42. PMID 2054949.
  29. 1 2 Marshburn PB, Alanis M, Matthews ML, et al. (September 2009). "A short period of ejaculatory abstinence before intrauterine insemination is associated with higher pregnancy rates". Fertil. Steril. 93 (1): 286–8. PMID 19732887. doi:10.1016/j.fertnstert.2009.07.972.
  30. ↑ Study: Daily sex helps to reduce sperm DNA damage and improve fertility the European Society of Human Reproduction and Embryology (ESHRE). Press releases ESHRE 2009, Tuesday 30 June 2009
  31. ↑ Gerris citing Zavos, 1995: Gerris J (1999). "Methods of semen collection not based on masturbation or surgical sperm retrieval". Human Reproduction Update. 5 (3): 211–5. PMID 10438105. doi:10.1093/humupd/5.3.211.
  32. ↑ Gerris citing Sofikitis and Miyagawa, 1993: Gerris J (1999). "Methods of semen collection not based on masturbation or surgical sperm retrieval". Human Reproduction Update. 5 (3): 211–5. PMID 10438105. doi:10.1093/humupd/5.3.211.
  33. 1 2 3 4 5 6 7 8 9 Gerris J (1999). "Methods of semen collection not based on masturbation or surgical sperm retrieval". Human Reproduction Update. 5 (3): 211–5. PMID 10438105. doi:10.1093/humupd/5.3.211.
  34. 1 2 Sofikitis NV; Miyagawa I (1993). "Endocrinological, biophysical, and biochemical parameters of semen collected via masturbation versus sexual intercourse". J. Androl. 14 (5): 366–73. PMID 8288490.
  35. ↑ van Roijen JH, Slob AK, Gianotten WL, et al. (January 1996). "Sexual arousal and the quality of semen produced by masturbation". Human Reproduction. 11 (1): 147–51. PMID 8671177. doi:10.1093/oxfordjournals.humrep.a019008.
  36. ↑ Yamamoto Y; Sofikitis N; Mio Y; Miyagawa I (May 2000). "Influence of sexual stimulation on sperm parameters in semen samples collected via masturbation from normozoospermic men or cryptozoospermic men participating in an assisted reproduction programme". Andrologia. 32 (3): 131–8. PMID 10863967. doi:10.1046/j.1439-0272.2000.00353.x.
  37. 1 2 Elzanaty S; Malm J (June 2008). "Comparison of semen parameters in samples collected by masturbation at a clinic and at home". Fertility and Sterility. 89 (6): 1718–22. PMID 17658521. doi:10.1016/j.fertnstert.2007.05.044.
  38. ↑ Sahlgrenska University Hospital (SU) - reproduction medicine
  39. ↑ Ball M (1976). "A prospective field trial of the "ovulation method" of avoiding conception". European Journal of Obstetrics, Gynecology, and Reproductive Biology. 6 (2): 63–6. PMID 985763. doi:10.1016/0028-2243(76)90004-6.
  40. ↑ Evelyn Billings & Ann Westmore (2005). "Trials of The Billings Ovulation Method". Retrieved 2005-11-03.
  41. ↑ Sinha G; Sinha A (October 1993). "A field trial of Billings' ovulation method for spacing and limitation of birth". Journal of the Indian Medical Association. 91 (10): 255–6. PMID 8308307.
  42. ↑ Wegner CC; Clifford AL; Jilbert PM; Henry MA; Gentry WL (September 2009). "Abnormally high body mass index and tobacco use are associated with poor sperm quality as revealed by reduced sperm binding to hyaluronan-coated slides". Fertil. Steril. 93 (1): 332–4. PMID 19733846. doi:10.1016/j.fertnstert.2009.07.970.
  43. ↑ http://www.newscientist.com/blogs/shortsharpscience/2008/10/do-intelligent-men-have-better.html
  44. ↑ Semen Quality Linked to Intelligence at the Wayback Machine (archived December 17, 2008)
  45. ↑ Cagnacci A; Maxia N; Volpe A (1999). "Diurnal variation of semen quality in human males". Hum. Reprod. 14 (1): 106–9. PMID 10374104. doi:10.1093/humrep/14.1.106.
  46. ↑ Mitchell, Richard Sheppard; Kumar, Vinay; Abbas, Abul K.; Fausto, Nelson (2007). Robbins Basic Pathology: With STUDENT CONSULT Online Access. Philadelphia: Saunders. p. 389. ISBN 1-4160-2973-7. 8th edition.
  47. ↑ Vaamonde D; Da Silva-Grigoletto ME; García-Manso JM; Vaamonde-Lemos R; Swanson RJ; Oehninger SC (November 2008). "Response of semen parameters to three training modalities". Fertil. Steril. 92 (6): 1941–6. PMID 19013565. doi:10.1016/j.fertnstert.2008.09.010.
  48. ↑ Pound N; Javed MH; Ruberto C; Shaikh MA; Del Valle AP (August 2002). "Duration of sexual arousal predicts semen parameters for masturbatory ejaculates". Physiology & Behavior. 76 (4–5): 685–9. PMID 12127009. doi:10.1016/S0031-9384(02)00803-X.
  49. ↑ Brugnon F, Janny L, Communal Y, et al. (May 2010). "Apoptosis and meiotic segregation in ejaculated sperm from Robertsonian translocation carrier patients". Hum Reprod. 25 (7): 1631–42. PMID 20472914. doi:10.1093/humrep/deq113.
  50. ↑ Negri L, et al. (May 2008). "Cancer Risk in Male Factor-infertility". Placenta. 29: 178–183. doi:10.1016/j.placenta.2008.07.014.
  51. ↑ "Understanding Semen Analysis". Stonybrook, State University of New York. 1999. Retrieved 2007-08-05.
  52. ↑ Essig, Maria G. (2007-02-20). Susan Van Houten; Tracy Landauer, eds. "Semen Analysis". Healthwise. WebMD. Retrieved 2007-08-05.
  53. ↑ "Adequate Analysis Frequency". Kokopelli Technologies. 2007. Retrieved 2007-08-11.
  54. ↑ Weschler, Toni (2002). Taking Charge of Your Fertility (Revised ed.). New York: HarperCollins. p. 189. ISBN 0-06-093764-5.
  55. ↑ C. Matthew Peterson; Kirtly Parker Jones; Harry H. Hatasaka & Kenneth H. H. Wong (October 2002). "Hamster Egg Penetration Test" (PDF). Utah Center for Reproductive Medicine. Retrieved 2007-08-08.
  56. ↑ Osser, S; Wramsby, H; Liedholm, P (May–Jun 1988). "A comparison between the hamster egg penetration test and the seminal parameters in men of infertile couples.". International journal of fertility. 33 (3): 207–11. PMID 2899568.
  57. ↑ Koulischer L; Debry JM (1989). "The hamster test. Practical consequences". Acta urologica Belgica (in French). 57 (1): 77–81. PMID 2718849.
  58. 1 2 3 4 "Understanding Semen Analysis". University Hospital & Medical Center at Stony Brook Male Infertility Program. Retrieved 4 May 2013.
  59. ↑ Meyer WR; Smith PM; Clark MR; Cusmano LL; Fritz MA (September 1996). "Therapeutic cup insemination with cryopreserved donor sperm: prognostic value of cervical mucus score at insemination and the number of motile sperm in mucus at 24 hours". Fertility and Sterility. 66 (3): 435–9. PMID 8751744.
  60. ↑ Cryos International - Denmark
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