CoChat
Sign Up
Cited by 52Sperm and Testicular FunctionPrenatal Substance Exposure EffectsSmoking Behavior and Cessation

The impact of paternal and maternal smoking on semen quality of adolescent men

Open access
Axelsson, Jonatan, Rylander, Lars, Rignell-Hydbom, Anna, Silfver, Karl Ågren, Stenqvist, Amelie, Giwercman, Aleksander·2013·PLoS ONE
DOI 10.1371/journal.pone.0066766PMC PMC3694111
Open this paper in CoChat — free account

Abstract

BACKGROUND: Maternal smoking during pregnancy has been reported to negatively impact sperm counts of the sons. Sufficient data on the effect of paternal smoking is lacking. OBJECTIVES: We wished to elucidate the impact of maternal and paternal smoking during pregnancy and current own smoking on reproductive function of the male offspring. METHODS: Semen parameters including sperm DNA integrity were analyzed in 295 adolescents from the general population close to Malmö, Sweden, recruited for the study during 2008-2010. Information on maternal smoking was obtained from the Swedish Medical Birth Register, and regarding own and paternal smoking from questionnaires. The impacts of maternal, paternal and own smoking were evaluated in a multivariate regression model and by use of models including interaction terms. Totally, three exposures and five outcomes were evaluated. RESULTS: In maternally unexposed men, paternal smoking was associated with 46% lower total sperm count (95%CI: 21%, 64%) in maternally unexposed men. Both paternal and maternal smoking were associated with a lower sperm concentration (mean differences: 35%; 95%CI: 8.1%, 55% and 36%; 95%CI: 3.9%, 57%, respectively) if the other parent was a non-smoker. No statistically significant impact of own smoking on semen parameters was seen. CONCLUSIONS: Prenatal both maternal and paternal smoking were separately associated with some decrease in sperm count in men of whom the other parent was not reported to smoke.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1371/journal.pone.0066766

Cites

1 of 1 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Sperm concentration, semen volume, total sperm count, percent morphologically normal and progressively motile sperm were analysed according to WHO guidelines, and DNA fragmentation index was studied by the Sperm Chromatin Structure Assay.

    “Sperm concentration (millions/ml), semen volume (ml), total sperm count (millions of sperms), percent morphologically normal sperms (%) and percent progressively motile sperms (%) were analysed according to the WHO guidelines used at the time. 22 Furthermore, the sperm DNA fragmentation index was studied by use of the Sperm Chromatin Structure Assay, 23 as previously briefly described for the two”

    From Decreased sperm counts in Swedish users of oral tobacco (2022) · cites this paper as [24]

    The Materials and Methods section (‘Semen analysis’; page unavailable) says semen samples were analysed under the 1999 WHO guidelines and describes using SCSA to determine the DNA fragmentation index. The Statistical methods section lists concentration, volume, total count and progressive motility, but our copy does not establish that the percentage of morphologically normal sperm was analysed. (LLM, conf=0.85)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

  • A quality study of a medical birth registry

    Cnattingius, S., Ericson, A., Gunnarskog, J., & Källén, B. (1990) · Scandinavian Journal of Social Medicine · doi:10.1177/140349489001800209 · Cited by 972 · cited 1× · see citing works

    “In Sweden, information on maternal smoking in gestational week 8 to 12 can be derived from the Medical Birth Register (MBR) [12] which is missing in only 3–7% of cases and has a low error rate [13].”
    Background

Flagged first, then by citations

Research works printed but not linked: 61

  1. [1]Jensen TK, Jorgensen N, Punab M, Haugen TB, Suominen J, et al (2004) Association of in utero exposure to maternal smoking with reduced semen quality and testis size in adulthood: a cross-sectional study of 1,770 young men from the general population in five European countries. Am J Epidemiol 159: 49– 58. 14693659
  2. [2]Ramlau-Hansen CH, Thulstrup AM, Storgaard L, Toft G, Olsen J, et al (2007) Is prenatal exposure to tobacco smoking a cause of poor semen quality? A follow-up study. Am J Epidemiol 165: 1372– 1379. 17369608
  3. [3]Storgaard L, Bonde JP, Ernst E, Spano M, Andersen CY, et al (2003) Does smoking during pregnancy affect sons' sperm counts? Epidemiology 14: 278– 286. 12859027
  4. [4]Jensen MS, Mabeck LM, Toft G, Thulstrup AM, Bonde JP (2005) Lower sperm counts following prenatal tobacco exposure. Hum Reprod 20: 2559– 2566. 15919771
  5. [5]Paasch U, Salzbrunn A, Glander HJ, Plambeck K, Salzbrunn H, et al (2008) Semen quality in sub-fertile range for a significant proportion of young men from the general German population: a co-ordinated, controlled study of 791 men from Hamburg and Leipzig. Int J Androl 31: 93– 102. 18315714
  6. [6]Ravnborg TL, Jensen TK, Andersson AM, Toppari J, Skakkebaek NE, et al (2011) Prenatal and adult exposures to smoking are associated with adverse effects on reproductive hormones, semen quality, final height and body mass index. Hum Reprod 26: 1000– 1011. 21335416
  7. [7]Ratcliffe JM, Gladen BC, Wilcox AJ, Herbst AL (1992) Does early exposure to maternal smoking affect future fertility in adult males? Reprod Toxicol 6: 297– 307. 1521002
  8. [8]Richthoff J, Elzanaty S, Rylander L, Hagmar L, Giwercman A (2008) Association between tobacco exposure and reproductive parameters in adolescent males. Int J Androl 31: 31– 39. 17376217
  9. [9]Jorgensen N, Vierula M, Jacobsen R, Pukkala E, Perheentupa A, et al (2011) Recent adverse trends in semen quality and testis cancer incidence among Finnish men. Int J Androl 34: e37– 48. 21366607 PMC3170483
  10. [10]Virtanen HE, Sadov S, Toppari J (2012) Prenatal exposure to smoking and male reproductive health. Curr Opin Endocrinol Diabetes Obes 19: 228– 232. 22499223
  11. [11]Hughes IA (2001) Minireview: sex differentiation. Endocrinology 142: 3281– 3287. 11459768
  12. [14]Chen D, Tian T, Wang H, Liu H, Hu Z, et al (2009) Association of human aryl hydrocarbon receptor gene polymorphisms with risk of lung cancer among cigarette smokers in a Chinese population. Pharmacogenet Genomics 19: 25– 34. 18818557
  13. [15]Fraga CG, Motchnik PA, Wyrobek AJ, Rempel DM, Ames BN (1996) Smoking and low antioxidant levels increase oxidative damage to sperm DNA. Mutat Res 351: 199– 203. 8622715
  14. [16]Perrin J, Tassistro V, Mandon M, Grillo JM, Botta A, et al (2011) Tobacco consumption and benzo(a)pyrene-diol-epoxide-DNA adducts in spermatozoa: in smokers, swim-up procedure selects spermatozoa with decreased DNA damage. Fertil Steril 95: 2013– 2017. 21406302
  15. [17]Aitken RJ (1999) The Amoroso Lecture. The human spermatozoon–a cell in crisis? J Reprod Fertil 115: 1– 7. 10341716
  16. [18]Aitken RJ, Koopman P, Lewis SE (2004) Seeds of concern. Nature 432: 48– 52. 15525979
  17. [19]Zenzes MT, Puy LA, Bielecki R, Reed TE (1999) Detection of benzo[a]pyrene diol epoxide-DNA adducts in embryos from smoking couples: evidence for transmission by spermatozoa. Mol Hum Reprod 5: 125– 131. 10065867
  18. [20]Zenzes MT, Bielecki R, Reed TE (1999) Detection of benzo(a)pyrene diol epoxide-DNA adducts in sperm of men exposed to cigarette smoke. Fertil Steril 72: 330– 335. 10439006
  19. [21]Laubenthal J, Zlobinskaya O, Poterlowicz K, Baumgartner A, Gdula MR, et al (2012) Cigarette smoke-induced transgenerational alterations in genome stability in cord blood of human F1 offspring. FASEB J 22730438
  20. [22]Zitzmann M, Rolf C, Nordhoff V, Schrader G, Rickert-Fohring M, et al (2003) Male smokers have a decreased success rate for in vitro fertilization and intracytoplasmic sperm injection. Fertil Steril 79 Suppl 3: 1550– 1554. 12801558
  21. [23]Venners SA, Wang X, Chen C, Wang L, Chen D, et al (2004) Paternal smoking and pregnancy loss: a prospective study using a biomarker of pregnancy. Am J Epidemiol 159: 993– 1001. 15128612
  22. [24]Blanco-Munoz J, Torres-Sanchez L, Lopez-Carrillo L (2009) Exposure to maternal and paternal tobacco consumption and risk of spontaneous abortion. Public Health Rep 124: 317– 322. 19320374 PMC2646489
  23. [25]Cresci M, Foffa I, Ait-Ali L, Pulignani S, Gianicolo EA, et al (2011) Maternal and paternal environmental risk factors, metabolizing GSTM1 and GSTT1 polymorphisms, and congenital heart disease. Am J Cardiol 108: 1625– 1631. 21890078
  24. [26]Gianicolo EA, Cresci M, Ait-Ali L, Foffa I, Andreassi MG (2010) Smoking and congenital heart disease: the epidemiological and biological link. Curr Pharm Des 16: 2572– 2577. 20550501
  25. [27]Kuciene R, Dulskiene V (2010) Parental cigarette smoking and the risk of congenital heart septal defects. Medicina (Kaunas) 46: 635– 641. 21252599
  26. [28]Zhang B, Jiao X, Mao L, Xue J (2011) Maternal cigarette smoking and the associated risk of having a child with orofacial clefts in China: a case-control study. J Craniomaxillofac Surg 39: 313– 318. 20832329
  27. [29]Zhang J, Savitz DA, Schwingl PJ, Cai WW (1992) A case-control study of paternal smoking and birth defects. Int J Epidemiol 21: 273– 278. 1428480
  28. [30]Zwink N, Jenetzky E, Brenner H (2011) Parental risk factors and anorectal malformations: systematic review and meta-analysis. Orphanet J Rare Dis 6: 25. 21586115 PMC3121580
  29. [31]Liu R, Zhang L, McHale CM, Hammond SK (2011) Paternal smoking and risk of childhood acute lymphoblastic leukemia: systematic review and meta-analysis. J Oncol 2011: 854584. 21765828 PMC3132639
  30. [32]Milne E, Greenop KR, Scott RJ, Bailey HD, Attia J, et al (2012) Parental Prenatal Smoking and Risk of Childhood Acute Lymphoblastic Leukemia. Am J Epidemiol 175: 43– 53. 22143821
  31. [33]Chang JS (2009) Parental smoking and childhood leukemia. Methods Mol Biol 472: 103– 137. 19107431
  32. [34]Castro-Jimenez MA, Orozco-Vargas LC (2011) Parental exposure to carcinogens and risk for childhood acute lymphoblastic leukemia, Colombia, 2000–2005. Prev Chronic Dis 8: A106. 21843409 PMC3181179
  33. [35]Secretan B, Straif K, Baan R, Grosse Y, El Ghissassi F, et al (2009) A review of human carcinogens–Part E: tobacco, areca nut, alcohol, coal smoke, and salted fish. Lancet Oncol 10: 1033– 1034. 19891056
  34. [36]Edraki M, Rambod M (2011) Parental smoking and risk of childhood cancer: hospital-based case-control study in Shiraz. East Mediterr Health J 17: 303– 308. 22259888
  35. [37]Davis DL (1991) Paternal smoking and fetal health. Lancet 337: 123. 1670716
  36. [38]Somers CM, Yauk CL, White PA, Parfett CL, Quinn JS (2002) Air pollution induces heritable DNA mutations. Proc Natl Acad Sci U S A 99: 15904– 15907. 12473746 PMC138537
  37. [39]Richthoff J, Rylander L, Hagmar L, Malm J, Giwercman A (2002) Higher sperm counts in Southern Sweden compared with Denmark. Hum Reprod 17: 2468– 2473. 12202443
  38. [40]World Health Organization. (1999) WHO laboratory manual for the examination of human semen and sperm-cervical mucus interaction. Cambridge, UK; New York, NY: Published on behalf of the World Health Organization [by] Cambridge University Press. x, 128 p. p.
  39. [42]Bungum M, Bungum L, Giwercman A (2011) Sperm chromatin structure assay (SCSA): a tool in diagnosis and treatment of infertility. Asian J Androl 13: 69– 75. 21057512 PMC3739398
  40. [43]Andersen AG, Jensen TK, Carlsen E, Jorgensen N, Andersson AM, et al (2000) High frequency of sub-optimal semen quality in an unselected population of young men. Hum Reprod 15: 366– 372. 10655308
  41. [44]Sanchez-Pozo MC, Mendiola J, Serrano M, Mozas J, Bjorndahl L, et al (2013) Proposal of guidelines for the appraisal of SEMen QUAlity studies (SEMQUA). Hum Reprod 28: 10– 21. 23054068
  42. [45]Jensen MS, Toft G, Thulstrup AM, Bonde JP, Olsen J (2007) Cryptorchidism according to maternal gestational smoking. Epidemiology 18: 220– 225. 17202869
  43. [46]Kurahashi N, Kasai S, Shibata T, Kakizaki H, Nonomura K, et al (2005) Parental and neonatal risk factors for cryptorchidism. Med Sci Monit 11: CR274– 283. 15917718
  44. [48]Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33: 159– 174. 843571
  45. [49]Danielsson M, Berglund T, Forsberg M, Larsson M, Rogala C, et al (2012) Sexual and reproductive health: Health in Sweden: The National Public Health Report 2012. Chapter 9. Scand J Public Health 40: 176– 196. 23238407
  46. [50]Axelsson J, Rylander L, Rignell-Hydbom A, Giwercman A (2011) No secular trend over the last decade in sperm counts among Swedish men from the general population. Hum Reprod 26: 1012– 1016. 21382832
  47. [51]Jensen TK, Andersson AM, Hjollund NH, Scheike T, Kolstad H, et al (1997) Inhibin B as a serum marker of spermatogenesis: correlation to differences in sperm concentration and follicle-stimulating hormone levels. A study of 349 Danish men. J Clin Endocrinol Metab 82: 4059– 4063. 9398713
  48. [52]Aitken RJ, Krausz C (2001) Oxidative stress, DNA damage and the Y chromosome. Reproduction 122: 497– 506. 11570956
  49. [53]Rothman KJ, Greenland S, Lash TL (2008) Modern epidemiology. Philadelphia: Lippincott Williams & Wilkins. 758 s. p.
  50. [54]Fukuda M, Fukuda K, Shimizu T, Nobunaga M, Andersen EW, et al (2011) Paternal smoking habits affect the reproductive life span of daughters. Fertil Steril 95: 2542– 2544. 21575937
  51. [55]Pierik FH, Burdorf A, Deddens JA, Juttmann RE, Weber RF (2004) Maternal and paternal risk factors for cryptorchidism and hypospadias: a case-control study in newborn boys. Environ Health Perspect 112: 1570– 1576. 15531444 PMC1247623
  52. [56]Brouwers MM, van der Zanden LF, de Gier RP, Barten EJ, Zielhuis GA, et al (2010) Hypospadias: risk factor patterns and different phenotypes. BJU Int 105: 254– 262. 19751252
  53. [57]Brouwers MM, Feitz WF, Roelofs LA, Kiemeney LA, de Gier RP, et al (2007) Risk factors for hypospadias. Eur J Pediatr 166: 671– 678. 17103190
  54. [58]Carbone P, Giordano F, Nori F, Mantovani A, Taruscio D, et al (2007) The possible role of endocrine disrupting chemicals in the aetiology of cryptorchidism and hypospadias: a population-based case-control study in rural Sicily. Int J Androl 30: 3– 13. 16824044
  55. [59]Wagner-Mahler K, Kurzenne JY, Delattre I, Berard E, Mas JC, et al (2011) Prospective study on the prevalence and associated risk factors of cryptorchidism in 6246 newborn boys from Nice area, France. Int J Androl 34: e499– 510. 21831232
  56. [60]Shen HM, Chia SE, Ni ZY, New AL, Lee BL, et al (1997) Detection of oxidative DNA damage in human sperm and the association with cigarette smoking. Reprod Toxicol 11: 675– 680. 9311575
  57. [61]Wyrobek AJ (1993) Methods and concepts in detecting abnormal reproductive outcomes of paternal origin. Reprod Toxicol 7 Suppl 1: 3– 16. 8400638
  58. [62]Olsen AK, Lindeman B, Wiger R, Duale N, Brunborg G (2005) How do male germ cells handle DNA damage? Toxicol Appl Pharmacol 207: 521– 531. 16051290
  59. [63]Yauk CL, Berndt ML, Williams A, Rowan-Carroll A, Douglas GR, et al (2007) Mainstream tobacco smoke causes paternal germ-line DNA mutation. Cancer Res 67: 5103– 5106. 17545587
  60. [64]Yauk C, Polyzos A, Rowan-Carroll A, Somers CM, Godschalk RW, et al (2008) Germ-line mutations, DNA damage, and global hypermethylation in mice exposed to particulate air pollution in an urban/industrial location. Proc Natl Acad Sci U S A 105: 605– 610. 18195365 PMC2206583
  61. [65]Somers CM (2011) Ambient air pollution exposure and damage to male gametes: human studies and in situ ‘sentinel’ animal experiments. Syst Biol Reprod Med 57: 63– 71. 21208146

Cited by

Sorted by citations

Authors
Axelsson, J., Rylander, L., Rignell-Hydbom, A., Silfver, K. Å., Stenqvist, A., & Giwercman, A.
Affiliations
  • Lund University (SE)
  • Skåne University Hospital (SE)
Corresponding author
Axelsson, Jonatan
ORCID
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2013-06-26
Volume
8
Issue
6
Pages
e66766
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0066766
PMC
PMC3694111
OpenAlex
W2047978577
Cited by
52
References
1
Citations by year
2026: 2 · 2025: 1 · 2024: 4 · 2023: 3 · 2022: 7 · 2021: 5 · 2020: 4 · 2019: 3 · 2018: 7 · 2017: 4 · 2016: 4 · 2015: 6 · 2014: 1
FWCI
3.99
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Lund University Publications (Lund University) (submittedVersion, other-oa)
Funders
Cancerfonden (CAN 2012/661)
Topics
  • Health Sciences › Medicine › Reproductive Medicine › Sperm and Testicular Function
  • Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Prenatal Substance Exposure Effects
  • Health Sciences › Medicine › Physiology › Smoking Behavior and Cessation
Keywords
paternal smoking, maternal smoking, adolescent men, semen quality, sperm count, sperm concentration, sperm DNA integrity, prenatal tobacco exposure, male reproductive function, adolescent smoking
MeSH terms
Adolescent, Female, Humans, Male, Military Personnel, Pregnancy, Prenatal Exposure Delayed Effects, Surveys and Questionnaires, Smoking, Sperm Count, Sweden, Testis, Semen Analysis

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review