Cited by 82Effects and risks of endocrine disrupting chemicalsSexual Differentiation and DisordersReproductive biology and impacts on aquatic species

Androgens and environmental antiandrogens affect reproductive development and play behavior in the Sprague-Dawley rat.

Open access
Hotchkiss, A K, Ostby, J S, Vandenburgh, J G, Gray, L E·2002·Environmental Health Perspectives

Abstract

In mammals, exposure to androgens early in development is essential for masculinization of the male reproductive phenotype. Male fetuses exposed to antiandrogens during perinatal life are permanently demasculinized in their morphology and physiology, whereas exposure to exogenous androgens permanently masculinizes females. In some litter-bearing species, proximity(italic) in utero(/italic) of females to males can partially masculinize female siblings and alter their responsiveness to endocrine-disrupting compounds. However, in our strain of rat (CD-SD Charles River), intrauterine position does not significantly influence testosterone concentrations and anogenital distance of fetuses. In comparison, administration of testosterone propionate to pregnant females, at doses that doubled fetal female testosterone levels, did masculinize the reproductive system. Discovery of androgen-active chemicals in the environment has placed increased emphasis on describing the reproductive and behavioral effects of both natural and environmental androgens and antiandrogens. Recently, the effects of an antiandrogen, vinclozolin, on the brain and behavior were cited as a special concern by the U.S. Environmental Protection Agency in its risk assessment of this pesticide. In rats, one such behavior that is perinatally organized by androgens is social play. Males play more than females, and administration of exogenous androgens during the neonatal period alters the juvenile expression of this sexually dimorphic behavior. Vinclozolin is an androgen receptor antagonist that inhibits androgen-dependent tissue growth in vivo. We were interested in whether developmental exposure to vinclozolin could also alter androgen-dependent behaviors such as play. Neonatal male rats were injected on postnatal days (PNDs) 2 and 3 with corn oil, the pharmacologic antiandrogen flutamide (50 mg/kg), or vinclozolin (200 mg/kg). On PNDs 36-37 animals were observed for social play. Behaviors associated with general social activity such as sniffing and dorsal contact were unaffected by treatment. However, play behavior in males treated with flutamide or vinclozolin was significantly reduced, resembling levels of play characteristic of females rather than untreated males. Therefore, this study demonstrates that perinatal exposure to vinclozolin, an environmental antiandrogen, can alter androgen-dependent play behavior in the male rat.

AI snapshot

Written from the paper’s full text.

TL;DR

In Sprague-Dawley rats, neonatal exposure to the antiandrogens flutamide (50 mg/kg) or vinclozolin (200 mg/kg) significantly reduced male rough-and-tumble play, making it resemble female levels, while general social behaviors were unaffected. The paper also reviews evidence that intrauterine position does not significantly affect fetal testosterone or anogenital distance in this rat strain and proposes play as an androgen-organized assay for endocrine disruptors.

Key findings

  • Neonatal male rats injected on postnatal days (PNDs) 2 and 3 with corn oil, flutamide (50 mg/kg), or vinclozolin (200 mg/kg) showed significantly reduced play behavior on PNDs 36–37 after flutamide or vinclozolin, resembling female levels; sniffing and dorsal contact were unaffected.
  • In related work (Hotchkiss et al. 2001), female pups treated with testosterone propionate showed increased rough-and-tumble play without altered other social activities; males treated with flutamide (50 mg/kg/day) or vinclozolin (200 mg/kg/day) showed decreased play bouts.
  • In CD-SD Charles River rats, intrauterine position did not significantly influence fetal testosterone concentrations or anogenital distance; testosterone propionate to pregnant females at doses that doubled fetal female testosterone levels masculinized the reproductive system.
  • Vinclozolin is an androgen receptor antagonist; the U.S. EPA cited its effects on brain and behavior as a special concern in vinclozolin risk assessment.

Methods

  • The paper combines a review with original neonatal rat experiments in Sprague-Dawley/CD-SD Charles River rats.
  • Neonatal male rats were injected on PNDs 2 and 3 with corn oil, flutamide (50 mg/kg), or vinclozolin (200 mg/kg); social play was observed on PNDs 36–37. In a related study, female pups received corn oil or testosterone propionate (250 g/kg/day as stated) on PNDs 2 and 3; males received corn oil, flutamide (50 mg/kg/day), or vinclozolin (200 mg/kg/day); play was observed for pairs of same litter, sex, and treatment for 10 min, with a play bout defined as one animal pinned to the floor with another on top.
  • Analyses compared frequencies of social behaviors (e.g., sniffing, dorsal contact, rough-and-tumble play) and sex differences; intrauterine position effects were examined on testosterone concentrations in fetal carcass, reproductive tract, and amniotic fluid and on anogenital distance.

Limitations

  • Stated: the neonatal rodent subcutaneous injection route has limited applicability to primates; because CNS development timing differs, none of the standard routes (lactational, gavage, subcutaneous) precisely simulates human exposure. The paper calls for studies measuring active vinclozolin metabolites in the rat CNS during neonatal life and comparing them with primate transplacental exposures.
  • Stated: intrauterine position findings in rats are inconsistent, and one study estimated that intrauterine position explained less than 12% of variation in prenatal testosterone; effects may be subtle and easily overshadowed.
  • Stated/evident: protocol differences (lactational vs direct pup exposure, dose, and lighting during testing) may explain contradictory vinclozolin play results across studies; the text also notes some cited findings are from an abstract/unpublished data.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1289/ehp.02110s3435

Cites

60 of 60 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

4 of 84 cited sources checked · 2 supported · 0 flagged · accuracy not yet measured

  • Premisecitation
    § Natural Variation in Androgen Concentrations during Development

    In one study, the amount of variation in prenatal testosterone explained by intrauterine position was estimated to be less than 12%.

    “In addition, in one study the amount of variation in prenatal testosterone, which was explained by the IUP, was estimated to be less than 12% (Houtsmuller et al. 1995).”
    Quote in the paperNot a substantial claim1 of 1 sources checked
    • cites Houtsmuller et al. 1995 source

      The Discussion reports that the number of caudal males explained about 12% of the variation in testosterone among female rat fetuses on day 19 of gestation. The claim captures the small contribution of intrauterine position, but states it as less than 12% and omits the study’s restriction to female rat fetuses and caudal males. (LLM, conf=0.85)

      Experimental — accuracy not yet measured
  • Premisecitation
    § Natural Variation in Androgen Concentrations during Development

    Even during the critical window, developing female fetuses have significant testosterone concentrations in many tissues, including those critical for the developing reproductive system.

    “However, even during this critical window, developing female fetuses have significant testosterone concentrations in many differ- ent tissues, including those critical for the developing reproductive system (Baum et al. 1991; Houtsmuller et al. 1995; Weisz and Ward 1980).”
    Quote in the paperNot a substantial claim1 of 3 sources checked
    • cites Baum et al. 1991

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

    • cites Houtsmuller et al. 1995 source

      Table 1 (p. 496) reports measurable plasma testosterone in female rat fetuses on day 19 of gestation, within the critical window described in the Introduction. The Hormone Measurements section says testosterone was measured in plasma; the paper does not establish concentrations in many tissues, including reproductive tissues. (LLM, conf=0.87)

      Experimental — accuracy not yet measured
    • cites Weisz and Ward 1980 source
  • Findingown data
    § Abstract

    Administration of testosterone propionate to pregnant females at doses that doubled fetal female testosterone levels masculinized the reproductive system.

    “In comparison, administration of testosterone propionate to pregnant females, at doses that doubled fetal female testosterone levels, did masculinize the reproductive system.”
    Quote in the paperSubstantial claim
  • Findingown data
    § Abstract

    In CD-SD Charles River rats, intrauterine position does not significantly influence fetal anogenital distance.

    “However, in our strain of rat (CD-SD Charles River), intrauterine position does not significantly influence testosterone concentrations and anogenital distance of fetuses.”
    Quote in the paperSubstantial claim
  • Findingown data
    § Abstract

    In CD-SD Charles River rats, intrauterine position does not significantly influence fetal testosterone concentrations.

    “However, in our strain of rat (CD-SD Charles River), intrauterine position does not significantly influence testosterone concentrations and anogenital distance of fetuses.”
    Quote in the paperSubstantial claim
  • Classified as probably not a substantial claim. 19
  • The quote only partly states this claim. 1
  • May combine two claims. 15
  • Classified as probably not a substantial claim.

    Premisecitation
    § Discussion

    Recent reports have identified androgenic chemicals in the environment.

    “In addition, recent reports (Gray et al. 2001b; Parks et al. 2001; Schiffer et al. 2001) of androgenic chemicals in the environment necessitate development of behavioral tests for assess- ing organizational effects of these chemicals on females.”
    Quote in the paperSubstantial claim1 of 3 sources checked
    • cites Gray et al. 2001b

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

    • cites Parks et al. 2001

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

    • cites Schiffer et al. 2001 source
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation
    § Discussion

    A cohort of women between 20 and 40 years of age had measurable amounts of endocrine-active chemicals in their urine.

    “Blount et al. (2000) showed that a cohort of women between 20 and 40 years of age had measurable amounts of endocrine-active chemicals in their urine.”
    Quote in the paperNot a substantial claim1 of 1 sources checked
    • cites Blount et al. (2000) source
  • The quote only partly states this claim.

    Findingown data
    § Abstract

    Behaviors associated with general social activity such as sniffing and dorsal contact were unaffected by treatment with flutamide or vinclozolin.

    “Behaviors associated with general social activity such as sniffing and dorsal contact were unaffected by treatment.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation
    § Abstract

    In some litter-bearing species, proximity in utero of females to males can partially masculinize female siblings and alter their responsiveness to endocrine-disrupting compounds.

    “In some litter-bearing species, proximity in utero of females to males can partially masculinize female siblings and alter their responsiveness to endocrine-disrupting compounds.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Clark et al. 1993 source
    • cites Howdeshell et al. 1999 source
  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Premisenone given
    § Effect of Androgen-Active Chemicals on Behavior

    In rodents, many behaviors are masculinized by the conversion of testosterone into estradiol in the brain.

    “In rodents, many behaviors are masculinized by the conversion of testosterone into estra- diol in the brain.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation
    § Natural Variation in Androgen Concentrations during Development

    In both gerbils and mice, intrauterine position of females has significant influence on subsequent litter sex ratios.

    “Interestingly, in both gerbils and mice, the intrauterine position of females has signifi- cant influence on their subsequent litter sex ratios.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Clark and Galef 1995 source
    • cites Vandenbergh and Huggett 1994

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • May combine two claims.

    Premisecitation
    § Role of Androgens in Reproductive and Behavioral Development

    Testosterone is important for differentiation of the Wolffian ducts, associated sex accessory tissues, and testicular descent.

    “Whereas MIS is critical for the inhibition of the Mullerian system, testosterone is important for differenti- ation of the Wolffian ducts, associated sex accessory tissues, and testicular descent (Jost 1970).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Jost 1970 source
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation
    § Natural Variation in Androgen Concentrations during Development

    Brief exposure to elevated androgens late in gestation sensitizes the developing male to androgen exposure during the neonatal period.

    “Several studies have suggested that this brief expo- sure to elevated androgens late in gestation sensitizes the developing male to androgen exposure during the neonatal period (Baum et al. 1990; Hoepfner and Ward 1988; Tobet and Baum 1987).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Baum et al. 1990

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

    • cites Hoepfner and Ward 1988 source
    • cites Tobet and Baum 1987 source
  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Premisenone given
    § Natural Variation in Androgen Concentrations during Development

    In several other litter-bearing species, variation in prenatal androgens can be largely attributed to the intrauterine position phenomenon.

    “In several other litter-bearing species, vari- ation in prenatal androgens can be largely attributed to the intrauterine position (IUP) phenomenon.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Premisecitation
    § Effect of Androgen-Active Chemicals on Behavior

    The critical time in the rat for organization of play is the early neonatal period, when interactions of androgens with the androgen receptor set up the sex difference observed in juveniles.

    “The critical time in the rat for organization of play is the early neonatal period, when interactions of androgens with the AR set up the sex differ- ence observed in juveniles (Meaney et al. 1983; Meaney and McEwen 1986; Pellis and Pellis 1997).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Meaney et al. 1983

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

    • cites Meaney and McEwen 1986 source
    • cites Pellis and Pellis 1997

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • May combine two claims.

    Premisecitation
    § Abstract

    Vinclozolin is an androgen receptor antagonist that inhibits androgen-dependent tissue growth in vivo.

    “Vinclozolin is an androgen receptor antagonist that inhibits androgen-dependent tissue growth in vivo.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Kelce et al. 1997 source
    • cites Waller et al. 1996 source
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationcitation
    § Natural Variation in Androgen Concentrations during Development

    Failure to account for intrauterine position in EDC toxicology studies could lead to false negative results, especially when adverse alterations are produced by low doses in fetuses from only one IUP.

    “In this regard, failure to account for IUP in EDC toxicology studies could lead to false negative results, especially when adverse alterations are produced by low doses in fetuses from only one IUP (Howdeshell et al. 1999; Welshons et al. 1999).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Howdeshell et al. 1999 source
    • cites Welshons et al. 1999

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation
    § Natural Variation in Androgen Concentrations during Development

    Females that develop in utero between two males produce more males in their litters than do females gestated between two females.

    “Females that develop in utero between two males produce more males in their litters than do females gestated between two females (Clark and Galef 1995; Vandenbergh and Huggett 1994).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Clark and Galef 1995 source
    • cites Vandenbergh and Huggett 1994

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • Classified as probably not a substantial claim.

    Premisecitation
    § Summary

    Several useful biomarkers have been suggested for characterizing the prenatal androgen environment.

    “Regardless of the sources of variation in prenatal androgens, several use- ful biomarkers have been suggested for char- acterizing the prenatal androgen environment (Gray et al. 1999; Vandenbergh and Huggett 1995).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Gray et al. 1999

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

    • cites Vandenbergh and Huggett 1995

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • Classified as probably not a substantial claim. May combine two claims.

    Premisecitation
    § Summary

    Discovery of novel antiandrogens and reports of androgenic chemicals in the environment has renewed interest in describing the role of androgens in reproductive and behavioral development.

    “Discovery of novel antiandrogens (Mylchreest et al. 1998; Parks et al. 2000) and reports of androgenic chemicals (Gray et al. 2001a; Parks et al. 2001; Schiffer et al. 2001) in the environment has renewed interest in describing the role of androgens in reproductive and behavioral develop- ment.”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Mylchreest et al. 1998

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

    • cites Parks et al. 2000

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

    • cites Gray et al. 2001a

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation
    § Discussion

    A recent report by the U.S. Environmental Protection Agency calls for studies of the developmental neurotoxicity of vinclozolin.

    “a recent report by the U.S. Environmental Protection Agency (U.S. EPA) calls for studies of the developmental neurotoxicity of vinclozolin (U.S. EPA 2000).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites U.S. EPA 2000

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • May combine two claims.

    Premisecitation
    § Effect of Androgen-Active Chemicals on Behavior

    The dose used in the Flynn study was lower (up to 60 mg/kg/day to pregnant female) than that used in the Hotchkiss et al. (200 mg/kg/day to neonatal pup) and Gray and Ostby studies (200 mg/kg/day to pregnant female).

    “Second, the dose used in the Flynn study was lower (up to 60 mg/kg/day to pregnant female) than that used in the Hotchkiss et al. (200 mg/kg/day to neonatal pup) and Gray and Ostby studies (200 mg/kg/day to pregnant female).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Flynn et al. 2001 source
    • cites Hotchkiss et al. 2001

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

    • cites Gray and Ostby 1998 source
  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Premisenone given
    § Discussion

    Antiandrogenicity of vinclozolin has been established since 1994.

    “Although antiandrogenicity of vinclozolin has been established since 1994”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Interpretationcitation
    § Summary

    Both of these indicators reflect the prenatal androgen environment and can be used for characterizing early developmental exposure to androgenic or antiandrogenic chemicals.

    “Both of these indicators reflect the prenatal andro- gen environment and can be used for char- acterizing early developmental exposure to androgenic or antiandrogenic chemicals.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S2 (checkable). May combine two claims.

    Interpretationreasoning
    § Discussion

    This study has implications both for risk assessment of known antiandrogens, such as vinclozolin, and for testing of novel chemicals.

    “This study has implications both for risk assessment of known antiandrogens, such as vinclozolin, and for testing of novel chemicals.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Interpretationnone given
    § Summary

    Social play is an androgen-organized behavior in rats that can be used to test for environmental androgens and antiandrogens.

    “Finally, social play is an androgen- organized behavior in rats that can be used to test for environmental androgens and antiandrogens.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Premisecitation
    § Effect of Androgen-Active Chemicals on Behavior

    In studies by Flynn et al. (2001) and Gray and Ostby (1998), neonatal exposure to the AR antagonist was through lactational exposure, whereas in Hotchkiss et al. (2001) the compound was administered directly to the pup.

    “First, in studies conducted by Flynn et al. (2001) and Gray and Ostby (1998), neonatal exposure to the AR antagonist was through lactational exposure. In the Hotchkiss et al. study (2001), the compound was administered directly to the pup.”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Flynn et al. 2001 source
    • cites Gray and Ostby 1998 source
    • cites Hotchkiss et al. 2001

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Premisenone given
    § Summary

    IUP has been shown to explain much of the variability in prenatal androgens in the mouse and gerbil.

    “Although IUP has been shown to explain much of the variability in prenatal androgens in the mouse and gerbil”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based). May combine two claims.

    Interpretationreasoning
    § Discussion

    If concentrations of active metabolites are comparable between these species, then injections of endocrine-active chemicals into neonatal rats could constitute a meaningful route of exposure at the appropriate developmental period.

    “If concentrations of active metabolites are comparable between these species, then injections of endocrine- active chemicals into neonatal rats could constitute a meaningful route of exposure at the appropriate developmental period.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing), S4 (based).

    Interpretationnone given
    § Discussion

    This lag in behavioral data on vinclozolin likely results from the limited numbers of behaviors masculinized by androgens, rather than estradiol, in the rodent.

    “This lag in behavioral data on vinclozolin likely results from the limited numbers of behaviors masculinized by androgens, rather than estradiol, in the rodent.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Premisecitation
    § Effect of Androgen-Active Chemicals on Behavior

    In both Flynn et al. (2001) and Gray and Ostby (1998) studies, no effect of perinatal vinclozolin was found on male play behavior.

    “In both of these studies, no effect of perinatal vinclo- zolin was found on male play behavior.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Flynn et al. 2001 source
    • cites Gray and Ostby 1998 source
  • May combine two claims.

    Premisecitation
    § Effect of Androgen-Active Chemicals on Behavior

    In that study, females treated with testosterone propionate had increased levels of rough-and-tumble play without alteration in the frequency of other social activities.

    “Females treated with testosterone pro- pionate had increased levels of rough-and- tumble play without alteration in the frequency of other social activities.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Hotchkiss et al. 2001

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • Probably not a substantial claim: may not pass S2 (checkable).

    Interpretationreasoning
    § Discussion

    Play behavior could be developed into a rodent behavioral test for chemicals with androgenic or antiandrogenic activity.

    “Considering the utility of this assay for testing behavioral effects of these EDCs, play behavior could be developed into a rodent behavioral test for chemicals with androgenic or antiandrogenic activity.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation
    § Effect of Androgen-Active Chemicals on Behavior

    The two other studies observed higher levels of play behaviors in males than in females during lights out when activity levels are higher in nocturnal animals such as the rat.

    “This is in contrast to the two other studies that observed higher levels of play behaviors in males than in females during lights out when activity levels are higher in nocturnal animals such as the rat.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Interpretationcitation
    § Effect of Androgen-Active Chemicals on Behavior

    Rat rough-and-tumble play is clearly organized by androgens themselves during the neonatal period and is not influenced by activational effects of other steroid hormones.

    “Therefore, rat rough-and- tumble play is unique in that it is clearly organized by androgens themselves during the neonatal period and is not influenced by activational effects of other steroid hormones.”
    Quote in the paperSubstantial claim
30 of 30
  • The paper relies on this without support.

    Few studies have used play as a behavioral assay for androgen-active environmental chemicals.

    “Although Meaney and Stewart (1981) showed that neonatal exposure to testosterone increased play in juvenile female rats, few studies have used play as a behavioral assay for androgen-active environmental chemi- cals.”
  • The paper relies on this without support.

    Toxicants present in pregnant females can be transferred to their offspring.

    “Therefore, toxicants present in pregnant females potentially could be transferred to their offspring.”
2 of 2

Self-check

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

Each contradiction between two passages listed here was confirmed by an independent check.

  • Rat example cites a hamster study

    Minor

    The text presents Paup et al. (1972) as an example concerning rats, but the paper's reference list identifies that study as being about female golden hamsters.

1 of 1

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Authors
Hotchkiss, A. K., Ostby, J. S., Vandenburgh, J. G., & Gray, L. E.
Affiliations
North Carolina State University (US)
Venue
Environmental Health Perspectives
Published
2002-06-01
Volume
110
Issue
suppl 3
Pages
435-439
ISSN
  • 0091-6765 (ISSN-L)
  • 1552-9924
OpenAlex
W2038040689
Cited by
82
References
60
Citations by year
2024: 2 · 2023: 3 · 2022: 4 · 2021: 2 · 2020: 3 · 2019: 4 · 2018: 1 · 2017: 2 · 2016: 3 · 2015: 3 · 2014: 5 · 2012: 3
FWCI
4.48
Type
journal article
Language
en
Open access
Locations
  • Environmental Health Perspectives (publishedVersion, public-domain)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (submittedVersion)
  • PubMed Central (submittedVersion)
Topics
  • Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Effects and risks of endocrine disrupting chemicals
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Sexual Differentiation and Disorders
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Reproductive biology and impacts on aquatic species
Keywords
androgens, androgen receptor antagonists, vinclozolin, flutamide, social play, masculinization, perinatal exposure, prenatal androgen exposure, sexual differentiation, reproductive development, anogenital distance, endocrine disruptors, Sprague-Dawley rats
MeSH terms
Androgen Antagonists, Androgens, Animals, Animals, Newborn, Environmental Exposure, Female, Gonads, Male, Oxazoles, Play and Playthings, Reproduction, Social Behavior, Rats, Sprague-Dawley, Risk Assessment, Rats

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