Dioxin exposure, from infancy through puberty, produces endocrine disruption and affects human semen quality

Paolo Mocarelli, Pier Mario Gerthoux, Donald G. Patterson, Silvano Milani, Giuseppe Limonta, Maria Bertona, Stefano Signorini, Pierluigi Tramacere, Laura Colombo, Carla Crespi, Paolo Brambilla, Cecilia Sarto, Vittorio Carreri, Eric J. Sampson, Wayman E. Turner, Larry L. Needham

Research output: Contribution to journalArticle

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Abstract

Background: Environmental toxicants are allegedly involved in decreasing semen quality in recent decades; however, definitive proof is not yet available. In 1976 an accident exposed residents in Seveso, Italy, to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Objective: The purpose of this study was to investigate reproductive hormones and sperm quality in exposed males. Methods: We studied 135 males exposed to TCDD at three age groups, infancy/prepuberty (1-9 years), puberty (10-17 years), and adulthood (18-26 years), and 184 healthy male comparisons using 1976 serum TCDD levels and semen quality and reproductive hormones from samples collected 22 years later. Results: Relative to comparisons, 71 men (mean age at exposure, 6.2 years; median serum TCDD, 210 ppt) at 22-31 years of age showed reductions in sperm concentration (53.6 vs. 72.5 million/mL; p = 0.025); percent progressive motility (33.2% vs. 40.8%; p < 0.001); total motile sperm count (44.2 vs. 77.5 × 106; p = 0.018); estradiol (76.2 vs. 95.9 pmol/L; p = 0.001); and an increase in follicle-stimulating hormone (FSH; 3.58 vs. 2.98 IU/L; p = 0.055). Forty-four men (mean age at exposure, 13.2 years; median serum TCDD, 164 ppt) at 32-39 years of age showed increased total sperm count (272 vs. 191.9 × 1066; p = 0.042), total motile sperm count (105 vs. 64.9 × 106; p = 0.036), FSH (4.1 vs. 3.2 UI/L; p = 0.038), and reduced estradiol (74.4 vs. 92.9 pmol/L; p < 0.001). No effects were observed in 20 men, 40-47 years of age, who were exposed to TCDD (median, 123 ppt) as adults (mean age at exposure, 21.5 years). Conclusions: Exposure to TCDD in infancy reduces sperm concentration and motility, and an opposite effect is seen with exposure during puberty. Exposure in either period leads to permanent reduction of estradiol and increased FSH. These effects are permanent and occur at TCDD concentrations < 68 ppt, which is within one order of magnitude of those in the industrialized world in the 1970s and 1980s and may be responsible at least in part for the reported decrease in sperm quality, especially in younger men.

Original languageEnglish (US)
Pages (from-to)70-77
Number of pages8
JournalEnvironmental health perspectives
Volume116
Issue number1
DOIs
StatePublished - Jan 1 2008

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Dioxins
Semen Analysis
Puberty
Sperm Count
Spermatozoa
Estradiol
Serum
Hormones
Polychlorinated Dibenzodioxins
Sperm Motility
Follicle Stimulating Hormone
Italy
Accidents
Age Groups

All Science Journal Classification (ASJC) codes

  • Public Health, Environmental and Occupational Health
  • Health, Toxicology and Mutagenesis

Cite this

Mocarelli, P., Gerthoux, P. M., Patterson, D. G., Milani, S., Limonta, G., Bertona, M., ... Needham, L. L. (2008). Dioxin exposure, from infancy through puberty, produces endocrine disruption and affects human semen quality. Environmental health perspectives, 116(1), 70-77. https://doi.org/10.1289/ehp.10399
Mocarelli, Paolo ; Gerthoux, Pier Mario ; Patterson, Donald G. ; Milani, Silvano ; Limonta, Giuseppe ; Bertona, Maria ; Signorini, Stefano ; Tramacere, Pierluigi ; Colombo, Laura ; Crespi, Carla ; Brambilla, Paolo ; Sarto, Cecilia ; Carreri, Vittorio ; Sampson, Eric J. ; Turner, Wayman E. ; Needham, Larry L. / Dioxin exposure, from infancy through puberty, produces endocrine disruption and affects human semen quality. In: Environmental health perspectives. 2008 ; Vol. 116, No. 1. pp. 70-77.
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title = "Dioxin exposure, from infancy through puberty, produces endocrine disruption and affects human semen quality",
abstract = "Background: Environmental toxicants are allegedly involved in decreasing semen quality in recent decades; however, definitive proof is not yet available. In 1976 an accident exposed residents in Seveso, Italy, to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Objective: The purpose of this study was to investigate reproductive hormones and sperm quality in exposed males. Methods: We studied 135 males exposed to TCDD at three age groups, infancy/prepuberty (1-9 years), puberty (10-17 years), and adulthood (18-26 years), and 184 healthy male comparisons using 1976 serum TCDD levels and semen quality and reproductive hormones from samples collected 22 years later. Results: Relative to comparisons, 71 men (mean age at exposure, 6.2 years; median serum TCDD, 210 ppt) at 22-31 years of age showed reductions in sperm concentration (53.6 vs. 72.5 million/mL; p = 0.025); percent progressive motility (33.2{\%} vs. 40.8{\%}; p < 0.001); total motile sperm count (44.2 vs. 77.5 × 106; p = 0.018); estradiol (76.2 vs. 95.9 pmol/L; p = 0.001); and an increase in follicle-stimulating hormone (FSH; 3.58 vs. 2.98 IU/L; p = 0.055). Forty-four men (mean age at exposure, 13.2 years; median serum TCDD, 164 ppt) at 32-39 years of age showed increased total sperm count (272 vs. 191.9 × 1066; p = 0.042), total motile sperm count (105 vs. 64.9 × 106; p = 0.036), FSH (4.1 vs. 3.2 UI/L; p = 0.038), and reduced estradiol (74.4 vs. 92.9 pmol/L; p < 0.001). No effects were observed in 20 men, 40-47 years of age, who were exposed to TCDD (median, 123 ppt) as adults (mean age at exposure, 21.5 years). Conclusions: Exposure to TCDD in infancy reduces sperm concentration and motility, and an opposite effect is seen with exposure during puberty. Exposure in either period leads to permanent reduction of estradiol and increased FSH. These effects are permanent and occur at TCDD concentrations < 68 ppt, which is within one order of magnitude of those in the industrialized world in the 1970s and 1980s and may be responsible at least in part for the reported decrease in sperm quality, especially in younger men.",
author = "Paolo Mocarelli and Gerthoux, {Pier Mario} and Patterson, {Donald G.} and Silvano Milani and Giuseppe Limonta and Maria Bertona and Stefano Signorini and Pierluigi Tramacere and Laura Colombo and Carla Crespi and Paolo Brambilla and Cecilia Sarto and Vittorio Carreri and Sampson, {Eric J.} and Turner, {Wayman E.} and Needham, {Larry L.}",
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Mocarelli, P, Gerthoux, PM, Patterson, DG, Milani, S, Limonta, G, Bertona, M, Signorini, S, Tramacere, P, Colombo, L, Crespi, C, Brambilla, P, Sarto, C, Carreri, V, Sampson, EJ, Turner, WE & Needham, LL 2008, 'Dioxin exposure, from infancy through puberty, produces endocrine disruption and affects human semen quality', Environmental health perspectives, vol. 116, no. 1, pp. 70-77. https://doi.org/10.1289/ehp.10399

Dioxin exposure, from infancy through puberty, produces endocrine disruption and affects human semen quality. / Mocarelli, Paolo; Gerthoux, Pier Mario; Patterson, Donald G.; Milani, Silvano; Limonta, Giuseppe; Bertona, Maria; Signorini, Stefano; Tramacere, Pierluigi; Colombo, Laura; Crespi, Carla; Brambilla, Paolo; Sarto, Cecilia; Carreri, Vittorio; Sampson, Eric J.; Turner, Wayman E.; Needham, Larry L.

In: Environmental health perspectives, Vol. 116, No. 1, 01.01.2008, p. 70-77.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Dioxin exposure, from infancy through puberty, produces endocrine disruption and affects human semen quality

AU - Mocarelli, Paolo

AU - Gerthoux, Pier Mario

AU - Patterson, Donald G.

AU - Milani, Silvano

AU - Limonta, Giuseppe

AU - Bertona, Maria

AU - Signorini, Stefano

AU - Tramacere, Pierluigi

AU - Colombo, Laura

AU - Crespi, Carla

AU - Brambilla, Paolo

AU - Sarto, Cecilia

AU - Carreri, Vittorio

AU - Sampson, Eric J.

AU - Turner, Wayman E.

AU - Needham, Larry L.

PY - 2008/1/1

Y1 - 2008/1/1

N2 - Background: Environmental toxicants are allegedly involved in decreasing semen quality in recent decades; however, definitive proof is not yet available. In 1976 an accident exposed residents in Seveso, Italy, to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Objective: The purpose of this study was to investigate reproductive hormones and sperm quality in exposed males. Methods: We studied 135 males exposed to TCDD at three age groups, infancy/prepuberty (1-9 years), puberty (10-17 years), and adulthood (18-26 years), and 184 healthy male comparisons using 1976 serum TCDD levels and semen quality and reproductive hormones from samples collected 22 years later. Results: Relative to comparisons, 71 men (mean age at exposure, 6.2 years; median serum TCDD, 210 ppt) at 22-31 years of age showed reductions in sperm concentration (53.6 vs. 72.5 million/mL; p = 0.025); percent progressive motility (33.2% vs. 40.8%; p < 0.001); total motile sperm count (44.2 vs. 77.5 × 106; p = 0.018); estradiol (76.2 vs. 95.9 pmol/L; p = 0.001); and an increase in follicle-stimulating hormone (FSH; 3.58 vs. 2.98 IU/L; p = 0.055). Forty-four men (mean age at exposure, 13.2 years; median serum TCDD, 164 ppt) at 32-39 years of age showed increased total sperm count (272 vs. 191.9 × 1066; p = 0.042), total motile sperm count (105 vs. 64.9 × 106; p = 0.036), FSH (4.1 vs. 3.2 UI/L; p = 0.038), and reduced estradiol (74.4 vs. 92.9 pmol/L; p < 0.001). No effects were observed in 20 men, 40-47 years of age, who were exposed to TCDD (median, 123 ppt) as adults (mean age at exposure, 21.5 years). Conclusions: Exposure to TCDD in infancy reduces sperm concentration and motility, and an opposite effect is seen with exposure during puberty. Exposure in either period leads to permanent reduction of estradiol and increased FSH. These effects are permanent and occur at TCDD concentrations < 68 ppt, which is within one order of magnitude of those in the industrialized world in the 1970s and 1980s and may be responsible at least in part for the reported decrease in sperm quality, especially in younger men.

AB - Background: Environmental toxicants are allegedly involved in decreasing semen quality in recent decades; however, definitive proof is not yet available. In 1976 an accident exposed residents in Seveso, Italy, to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Objective: The purpose of this study was to investigate reproductive hormones and sperm quality in exposed males. Methods: We studied 135 males exposed to TCDD at three age groups, infancy/prepuberty (1-9 years), puberty (10-17 years), and adulthood (18-26 years), and 184 healthy male comparisons using 1976 serum TCDD levels and semen quality and reproductive hormones from samples collected 22 years later. Results: Relative to comparisons, 71 men (mean age at exposure, 6.2 years; median serum TCDD, 210 ppt) at 22-31 years of age showed reductions in sperm concentration (53.6 vs. 72.5 million/mL; p = 0.025); percent progressive motility (33.2% vs. 40.8%; p < 0.001); total motile sperm count (44.2 vs. 77.5 × 106; p = 0.018); estradiol (76.2 vs. 95.9 pmol/L; p = 0.001); and an increase in follicle-stimulating hormone (FSH; 3.58 vs. 2.98 IU/L; p = 0.055). Forty-four men (mean age at exposure, 13.2 years; median serum TCDD, 164 ppt) at 32-39 years of age showed increased total sperm count (272 vs. 191.9 × 1066; p = 0.042), total motile sperm count (105 vs. 64.9 × 106; p = 0.036), FSH (4.1 vs. 3.2 UI/L; p = 0.038), and reduced estradiol (74.4 vs. 92.9 pmol/L; p < 0.001). No effects were observed in 20 men, 40-47 years of age, who were exposed to TCDD (median, 123 ppt) as adults (mean age at exposure, 21.5 years). Conclusions: Exposure to TCDD in infancy reduces sperm concentration and motility, and an opposite effect is seen with exposure during puberty. Exposure in either period leads to permanent reduction of estradiol and increased FSH. These effects are permanent and occur at TCDD concentrations < 68 ppt, which is within one order of magnitude of those in the industrialized world in the 1970s and 1980s and may be responsible at least in part for the reported decrease in sperm quality, especially in younger men.

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