Semen quality
Semen quality is a measure of male fertility, a measure of the ability of sperm in semen to accomplish fertilization. Semen quality involves both sperm quantity and quality. Semen quality is a major factor for fertility.
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.
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, maternal smoking during prenatal development, pesticide exposure, or lifestyle changes during adulthood.[1]
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.[2] 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 found that, with confounding variables controlled, the risk of autism increased with increasing paternal age.[3]
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.[4] 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.[5]
Heat
Sperm are heat-sensitive, and cannot endure high temperatures. Increases of 2–3 °C are associated with increased DNA fragmentation.[6] 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:
- sauna sessions
- bathing for a long time in hot water
- Long-time tanning bed sessions
- Placement of a laptop computer over the groin for extended use
Fever raises the body temperature, which can strike sperm quality.
Contrary to widely held beliefs, no evidence supports that wearing tight underpants 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.[7][dubious – discuss]
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. 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.[8]
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.[9] Ninety-nine percent of over 100,000 recently introduced chemicals[vague] are poorly regulated.[9]
At least three types of synthetic toxins have been found in the semen of student volunteers: polychlorinated biphenyls (PCBs), DDT, and hexachlorobenzene.[10] DDT and hexachlorobenzene are associated with decreased semen quality, while PCBs are associated with decreased fertility overall.[8] Leaks of dibromochloropropane (DBCP) have caused sterility in men.[10] 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.[10]
Phthalates, a ubiquitous pollutant, may cause decreased sperm production when having been exposed to it during prenatal development.[8][11]
Other potential xenoestrogens that have been associated with decreased sperm quality in some studies are bisphenol A, nonylphenol and octylphenol.[8]
Medication
- Depo-Provera, Adjudin, and gossypol are examples of substances used as male contraceptives or in chemical castration. Recent studies have found that THC present in cannabis can confuse the movements of intact sperm, reducing their ability to achieve fertilization.[12][13]
- Selective serotonin reuptake inhibitors (SSRI) may cause low sperm count.[14]
- Many antibiotics, e.g., penicillin and tetracycline, suppress sperm production.[10]
In addition, in vitro studies have observed altered sperm function by the following medications:
- Many psychoactive drugs, including many antidepressants, many antiepileptics (e.g., lithium), and propranolol[8]
- Opioid analgesics[8]
- Calcium channel blockers[8]
- Phosphodiesterase inhibitors (e.g., caffeine, theophylline, pentoxifylline)[8]
- Statins[8]
- Calcium chelators (e.g., EDTA)[8]
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.[8]
Hormones
- Anabolic steroids use and use of other hormones can reduce sperm quality. Changes in hormone homeostasis affect the spermatogenesis.
The body also has natural variations in hormone concentrations, giving sperm quality natural fluctuations as well.[citation needed]
Diet
- Drinking over 1 litre of cola a day might decrease sperm quality by up to 30%[15] (study claims there is correlation, but not causation)
- Soy products decrease sperm quality due to the high content of a type of phytoestrogen called isoflavones.[16][17] Theoretically, this exposure to high levels of phytoestrogen in men may alter the hypothalamic-pituitary-gonadal axis. A few studies on animals have shown that such a hormonal effect may be significant and decrease fertility.[18] On the other hand, most studies have shown that isoflavone supplements have little to no effect on sperm concentration, count, or mobility, and cause no changes in testicular or ejaculate volume.[19][20]
- A review in 2010 concluded that there is little evidence for a relationship with semen parameters and increased BMI.[21]
- Folate (vitamin B9) may protect sperm cells from aneuploidy.[22]
- Gossypol has been associated with reduced sperm production. It is present in crude cottonseed oil, and potentially the organ meats from animals poisoned with it[23]
- Recently, a review of epidemiological/observational studies provided the most comprehensive analysis to date of the associations between diet or nutrient intake and the risk of infertility. It suggests that diet modifications may be useful in modulating male fertility and fecundability. Healthy diets (i.e. the Mediterranean diet) rich in such nutrients as omega-3 fatty acids, some antioxidants and vitamins, and low in saturated fatty acids (SFAs) and trans-fatty acids (TFAs) are associated with high semen quality parameters. In terms of food groups, fruit, seafood, poultry, eggs, cereals, leafy vegetables, dark chocolate, and low-fat dairy products have been positively related to sperm quality. However, diets rich in processed meat, fried foods, potatoes, full-fat dairy products, caffeine, alcohol and sugar-sweetened beverages have been inversely associated with the quality of semen in some studies. The few studies relating male nutrient or food intake and fecundability also suggest that diets rich in red meat, processed meat, tea and caffeine are associated with a lower rate of fecundability. This association is only controversial in the case of coffee, because a little bit of coffee, two to three cups a day, has been shown to help improving sperm motility, but more than three cups a day have been shown to have impaired fertility.[24] The potential biological mechanisms linking diet with sperm function and fertility are largely unknown and require further study.[25]
- One study found that following a diet rich in fruits, vegetables, potatoes, meat, full-fat dairy products, seafood and pastries increased sperm count by 50%. Men who consume such diet have sperm counts nearly twice as high as men who do not.[26]
Other chemicals
Environmental mutagens that are associated with decreased semen quality include the following:
- Plutonium, widely spread from nuclear weapon tests, accumulates in the testes, where it disrupts zinc metabolism, in turn causing genetic damage.[10]
- Ethylene oxide, a chemical sterilizer, is associated with decreased semen quality.[8]
Other environmental agents associated with decreased semen quality include:
- Cadmium, causing damage to Sertoli cells, thereby impeding spermatogenesis.[8]
- Lead, causing reduced spermatogenesis and abnormal spermatozoa.[8]
- Mercury, being highly damaging to spermatogenesis.[8]
- Many pesticides, causing decreased semen quality as well as sperm chromosome anomalies.[8]
- Polybrominated diphenyl ethers (PBDEs).[8]
- Many solvents, such as benzene, toluene, xylene, styrene, 1-bromopropane, 2-bromopropane, perchloroethylene, trichloroethylene.[8]
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%.[27]
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.[28] This increase in pregnancy rate occurs despite a lower value of total motile spermatozoa.[28] 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.[29]
Masturbation vs intercourse
Semen samples obtained via sexual intercourse contain 70[30]–120[31]% more sperm, with sperm having a slightly higher[32] motility and slightly more normal[32] morphology, compared with semen samples obtained via masturbation. Sexual intercourse also generates a 25–45%[32] increase in ejaculate volume, mainly by increased prostate[33] secretion.
This intercourse advantage is even greater for men with oligospermia.[32]
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,[32][34] although there may be a slight correlation.[35] Neither do any substantial fluctuations in sex hormones explain the intercourse advantage.[33] It is hypothesized that sexual intercourse subdues an inhibition from the central nervous system,[32] but what, in turn, is the subduing factor is still not completely known.
Home or in clinic
Sperm quality is higher when a sample is collected at home than in a clinic.[36] Collecting the sperm at home gives a higher sperm concentration, sperm count and motility, particularly if the sperm is collected via sexual intercourse.[36] If the semen sample is to be collected by masturbation, a specimen from the early stages of the ejaculate should be into a clean, 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.[citation needed]
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.[citation needed] 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.[37]
In a non-harmful environment outside the body, such as in a sterile glass container[32] the number of motile sperm decreases by approximately 5–10%[32] per hour. In contrast, in a latex condom, the quality decreases by 60–80%[32] per hour, rendering the sample unusable in a relatively short time.
In female
The environment in the uterus and fallopian tubes is advantageous. A pregnancy resulting from sperm life of eight days has been documented.[38][39][40]
Others
Tobacco smoking lowers the sperm quality,[10] perhaps by decreased ability to attach to hyaluronan on the egg cell.[41] Wright et al.[6] have reviewed evidence that smoking is associated with increased sperm DNA damage and male infertility. Smoking cannabis can decrease sperm quantity.[10]
Long-term stress is also suggested. The practise of tucking can reduce both the sperm count and sperm quality.[42] Meta-analysis indicates that mobile phone exposure affects sperm quality negatively.[43]
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.[44] Adrenaline-levels are higher during awakening (~06.00 to noon),[45] 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.[46]
A longer duration of sexual stimulation before ejaculation slightly increases sperm quality.[47]
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.[48]
Testicular cancer, Leydig cell tumours and Sertoli cell tumours are also associated with reduced sperm count and quality.[49]
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.[50][51]
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.[52] 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.[53] However, a negative result on the hamster test correlates with a lower probability of the man's partner becoming pregnant.[54]
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).[55]
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.[55]
Other tests
- PCR-based detection of the pathogens in the semen of patients with asymptomatic genital infection.[55]
- Biochemical markers like creatine kinase, Reactive oxygen species.[55]
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.
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.[56]
Bad freezers
In 10–20% of all men, the semen does not endure cryopreservation. 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.
See also
References
- ^ 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. 23 (6): 646–659. doi:10.1093/humupd/dmx022. PMC 6455044. PMID 28981654.
- ^ Gurevich, Rachel (6 October 2008). "Does Age Affect Male Fertility?". About.com:Fertility. About.com. Archived from the original on 28 September 2015. Retrieved 14 February 2010.
- ^ 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. doi:10.1111/j.1469-7610.2004.00391.x. PMID 16108999. Archived from the original on 2012-06-20.
- ^ 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. doi:10.1016/j.fertnstert.2014.02.006. PMID 24690240.
- ^ McIntosh, GC; Olshan, AF; Baird, PA (May 1995). "Paternal age and the risk of birth defects in offspring". Epidemiology. 6 (3): 282–8. doi:10.1097/00001648-199505000-00016. PMID 7619937. S2CID 21478909.
- ^ a b 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. doi:10.1016/j.rbmo.2014.02.004. PMID 24745838.
- ^ 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]
- ^ a b c d e f g h i j k l m n o p q r 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: i1–45. doi:10.1093/humupd/dmt008. hdl:2263/21332. PMID 23552271.
- ^ a b <Please add first missing authors to populate metadata.> (7 December 2008). "It's official: Men really are the weaker sex". The Independent. Archived from the original on December 8, 2008.
- ^ a b c d e f g "The Male Fertility Crisis - Natural Health - MOTHER EARTH NEWS".
- ^ [sciencenews.org: EPA should test demasculinizing pollutants collectively, NRC says] By Janet Raloff. Web edition : Thursday, December 18th, 2008
- ^ 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. doi:10.1016/j.fertnstert.2005.08.027. PMID 16500334.
- ^ "Smoking Marijuana Lowers Fertility". WebMD. Retrieved 2018-05-16.
- ^ 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. doi:10.1016/j.juro.2008.07.034. PMID 18804223. (This paper currently has an expression of concern, see doi:10.1097/JU.0000000000003115, PMID 36626339 )
- ^ Jensen TK; Swan SH; Skakkebaek NE; Rasmussen S; Jørgensen N. (April 2010). "Caffeine intake and semen quality in a population of 2,554 young Danish men". American Journal of Epidemiology. 171 (8): 883–91. doi:10.1093/aje/kwq007. PMID 20338976.
- ^ "Domain parked by OnlyDomains". Archived from the original on 2005-12-15.
- ^ "Beer, coffee, wine and nuts may lower male fertility - Health Jockey". www.healthjockey.com. Archived from the original on 2011-07-19. Retrieved 2018-05-16.
- ^ "Rats, Mice, Birds & Cattle". Archived from the original on 2006-05-02.
- ^ Dabrowski, Waldemar M. (2004). Toxins in Food. CRC Press Inc. p. 95. ISBN 978-0-8493-1904-4.
- ^ Mitchell JH; Cawood E; Kinniburgh D; Provan A; Collins AR; Irvine DS (June 2001). "Effect of a phytoestrogen food supplement on reproductive health in normal males". Clinical Science. 100 (6): 613–8. doi:10.1042/CS20000212. PMID 11352776.
- ^ MacDonald AA; Herbison GP; Showell M; Farquhar CM (2010). "The impact of body mass index on semen parameters and reproductive hormones in human males: a systematic review with meta-analysis". Hum. Reprod. Update. 16 (3): 293–311. doi:10.1093/humupd/dmp047. PMID 19889752.
- ^ Folate 'may keep sperm healthy' BBC News. Last Updated: Thursday, 20 March 2008, 04:39 GMT
- ^ "Merck Veterinary Manual". Retrieved 2018-05-16.
- ^ "MillsHealthySpermTips" (PDF). 5-Tips-To-Ensure-Healthy-Sperm.pdf - UCLA Health. David Geffen. Retrieved 9 January 2022.
- ^ Albert Salas-Huetos, Mònica Bulló, Jordi Salas-Salvadó; Dietary patterns, foods and nutrients in male fertility parameters and fecundability: a systematic review of observational studies, Human Reproduction Update, Volume 23, Issue 4, 1 July 2017, Pages 371–389, https://doi.org/10.1093/humupd/dmx006
- ^ "Improving Male Fertility — Research Suggests a Nutrient-Dense Diet May Play an Integral Role".
- ^ 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.
- ^ a b 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. doi:10.1016/j.fertnstert.2009.07.972. PMID 19732887.
- ^ Study: Daily sex helps to reduce sperm DNA damage and improve fertility Archived 2011-09-18 at the Wayback Machine the European Society of Human Reproduction and Embryology (ESHRE). Press releases ESHRE 2009, Tuesday 30 June 2009
- ^ Gerris citing Zavos, 1995: Gerris J (May 1999). "Methods of semen collection not based on masturbation or surgical sperm retrieval". Human Reproduction Update. 5 (3): 211–5. doi:10.1093/humupd/5.3.211. PMID 10438105.
- ^ Gerris citing Sofikitis and Miyagawa, 1993: Gerris J (May 1999). "Methods of semen collection not based on masturbation or surgical sperm retrieval". Human Reproduction Update. 5 (3): 211–5. doi:10.1093/humupd/5.3.211. PMID 10438105.
- ^ a b c d e f g h i Gerris J (May 1999). "Methods of semen collection not based on masturbation or surgical sperm retrieval". Human Reproduction Update. 5 (3): 211–5. doi:10.1093/humupd/5.3.211. PMID 10438105.
- ^ a b Sofikitis NV; Miyagawa I (September–October 1993). "Endocrinological, biophysical, and biochemical parameters of semen collected via masturbation versus sexual intercourse". J. Androl. 14 (5): 366–73. doi:10.1002/j.1939-4640.1993.tb00402.x. PMID 8288490.
- ^ 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. doi:10.1093/oxfordjournals.humrep.a019008. PMID 8671177.
- ^ 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. doi:10.1046/j.1439-0272.2000.00353.x. PMID 10863967. S2CID 23972414.
- ^ a b 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. doi:10.1016/j.fertnstert.2007.05.044. PMID 17658521.
- ^ "Sahlgrenska University Hospital (SU) - reproduction medicine". Archived from the original on 2006-02-23. Retrieved 2007-08-07.
- ^ 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. doi:10.1016/0028-2243(76)90004-6. PMID 985763.
- ^ Evelyn Billings & Ann Westmore (2005). "Trials of The Billings Ovulation Method". Archived from the original on 2005-11-05. Retrieved 2005-11-03.
- ^ 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.
- ^ 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. doi:10.1016/j.fertnstert.2009.07.970. PMID 19733846.
- ^ Dickey, Lore m; Ducheny, Kelly M; Ehrbar, Randall D (2016). "Family creation options for transgender and gender nonconforming people". Psychology of Sexual Orientation and Gender Diversity. 3 (2): 173. doi:10.1037/sgd0000178.
- ^ Adams, Jessica A; Galloway, Tamara S; Mondal, Debapriya; Esteves, Sandro C; Mathews, Fiona (2014). "Effect of mobile telephones on sperm quality: A systematic review and meta-analysis". Environment International. 70: 106–12. Bibcode:2014EnInt..70..106A. doi:10.1016/j.envint.2014.04.015. hdl:10871/15088. PMID 24927498.
- ^ Cagnacci A; Maxia N; Volpe A (1999). "Diurnal variation of semen quality in human males". Hum. Reprod. 14 (1): 106–9. doi:10.1093/humrep/14.1.106. PMID 10374104.
- ^ Mitchell, Richard Sheppard; Kumar, Vinay; Abbas, Abul K.; Fausto, Nelson (2007). Robbins Basic Pathology: With STUDENT CONSULT Online Access (8th ed.). Philadelphia: Saunders. p. 389. ISBN 978-1-4160-2973-1.
- ^ 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. doi:10.1016/j.fertnstert.2008.09.010. hdl:10553/76413. PMID 19013565.
- ^ 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. doi:10.1016/S0031-9384(02)00803-X. PMID 12127009. S2CID 37524348.
- ^ 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. doi:10.1093/humrep/deq113. PMID 20472914.
- ^ Negri L, et al. (May 2008). "Cancer Risk in Male Factor-infertility". Placenta. 29: 178–183. doi:10.1016/j.placenta.2008.07.014. PMID 18755508.
- ^ "Understanding Semen Analysis". Stonybrook, State University of New York. 1999. Archived from the original on 2007-10-17. Retrieved 2007-08-05.
- ^ Essig, Maria G. (2007-02-20). Susan Van Houten; Tracy Landauer (eds.). "Semen Analysis". Healthwise. WebMD. Retrieved 2007-08-05.
- ^ 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. Archived from the original (PDF) on 2016-03-03. Retrieved 2007-08-08.
- ^ 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.
- ^ Koulischer L; Debry JM (1989). "The hamster test. Practical consequences". Acta Urologica Belgica (in French). 57 (1): 77–81. PMID 2718849.
- ^ a b c d "Understanding Semen Analysis". University Hospital & Medical Center at Stony Brook Male Infertility Program. Archived from the original on 17 October 2007. Retrieved 4 May 2013.
- ^ 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. doi:10.1016/S0015-0282(16)58515-X. PMID 8751744.