References | Methods | Results |
---|---|---|
Animal Data | ||
Matikainen et al., 2001 [63] | Adult mouse exposure to a single intraperitoneal injection of 9,10-dimethylbenz[a]anthracene (DMBA) 50 mg/kg, a typical PAH | Activation of the aromatic hydrocarbon receptor (Ahr) driving Bax expression in oocytes, a pro-apoptosis factor |
Jurisicova et al., 2007 [78] | Exposure of mice to 2 PAHs (DMBA and BaP) 3 weeks before gestation and during lactation | ⇘ by one third of the ovarian follicle pool in F1 compared to unexposed offspring |
Paixão et al., 2012 [79] | Exposure of 10 mice to cigarette smoke 8 h/day, 7 days/week for 15 days. Euthanized at the end of exposure or 30 days after. | Alteration in follicular growth even after discontinuing the exposure. ⇘ Number of granulosa cells in the exposed group |
Kilic et al., 2012 [76] | Prospective randomized study, 25 pregnant rats exposed or unexposed to cigarette smoke. | significant ⇗ in DNA anomalies and the apoptotic index in the ovaries of exposed group ⇘ offspring ovarian reserve |
Gannon et al., 2012 [77] | Mice exposed to tobacco smoke 5 day/week, for 4, 8, 9 or 17 weeks. | ⇘ ovary weight and number of primordial follicles. ⇗ oxidative stress. Bcl-2 expression ⇘ but apoptosis was not induced |
Sobinoff et al., 2013 [65] | Nasal exposure of mice to cigarette smoke. Ovarian toxicity analysis | ⇗ Depletion of primordial and antral follicular stock via, mechanisms of apoptosis and oxidative stress |
Lim et al., 2013 [89] | Mouse exposed by gavage to B[a]P at 0.2 or 10 mg/kg/d from the 7th to 16th gestational day. Effect of polymorphism of glutamate cysteine ligase | Prenatal exposure to BaP induced POI. Deletion of glutamate cysteine ligase increased the sensitivity of these ovarian effects |
Camlin et al., 2016 [82] | Nasal exposure of pregnant mice to cigarette smoke for 12 weeks. Analysis of F1 ovary and oocyte quality | Abnormal proliferation of neonatal somatic cells, ⇗ apoptosis, ⇘ follicles at birth and at the adult age. ⇗ oxidative stress |
Human Data | ||
Progetto Menopausa Italia Study Group, 2003 [74] | Cross-sectional study between 1997 and 1999. Inclusion of patients between ages 45 to 75 making a 1st consultation in a specialized center for menopause in Italy | No significant association between the risk of POI and smoking |
Chang et al., 2007 [72] | Study of risk factors in 137 menopausal patients < 40 years, 281 between 40 and 4 years, and 1318 between 45 and 60 years | Smoking ⇗ the idiopathic risk of POI: OR = 1.82 [1.03–3.23] |
Kinney et al., 2007 [110] | Effect of cigarette smoking on antral follicle count and FSH in 188 patients aged 22 to 49 years | Chronic cigarette smoking is associated with higher rates of FSH β = 0.21, 95% CI = 0.04, 0.39, but there is no significant difference on the AFC |
Strohsnitter et al., 2008 [84] | Epidemiological study on 4025 women. Association between prenatal exposure to cigarette smoking and age at menopause | An association between prenatal exposure and age at menopause for patients who have never smoked (HR = 1.38, 95% CI: 1.10, 1.74). Not found in patients who smoke (HR = 1.03, 95% CI: 0.81, 1.31) |
Fleming et al., 2008 [70] | Epidemiological study on 7596 women. Cotinine and FSH levels in the blood | Average age at menopause = 47.17 years for smokers compared to 48.59 years for non-smokers. |
Freour et al., 2008 [81] | Analysis of 111 patients treated for infertility | Significant ⇘ of AMH levels in patients who smoke 3.06 +/− 1.68 mg/L, compared to 3.86 +/− 1.92 |
Lutterodt et al., 2009 [87] | Ovary analysis of 29 fetuses in the 1st trimester. Ovary analysis, compared to maternal cigarette smoking exposure | ⇘ number of somatic cells (P ≤ 0.01). Number of oogonia not associated with prenatal exposure to maternal cigarette smoking (P ≤ 0.09). |
Ernst et al., 2012 [86] | Prospective study on 965 pregnant women at 30 weeks amenorrhea. Evaluation of maternal cigarette smoking and study in 2008 on the fertility of their daughter (n = 438) | No significant association between in utero cigarette smoking exposure and the number of follicles |
(Yasui et al., 2012) | Transversal study of a cohort of 24,152 Japanese nurses, research on factors associated with POI | Cigarette smoking is associated with an earlier age at menopause |
Fraser et al., 2013 [83] | Analysis of a cohort of 1399 adolescents between 1991 and 2008. Study on AMH levels depending on parental exposure to cigarette smoking | Paternal, and not maternal, cigarette smoking before and during pregnancy is associated with a decrease in AMH levels. |
Caserta et al., 2013 [80] | Analysis of the antral follicle count and FSH levels in 296 women, including 102 smokers | ⇘ Antral follicle count and ⇗ FSH in cigarette smokers correlated to the number of pack- years. |
Fowler et al., 2014 [85] | Analysis of 105 fetuses resulting from elective terminations in the 2nd trimester, 56 exposed, 49 unexposed. | Dysregulation of fetal ovarian signaling pathways |
Butts et al., 2014 [88] | Survival analysis for a cohort of 410 patients. Nucleotide polymorphism study | Risk of early menopause in cigarette smokers depends on genetic polymorphism. |
Tawfik et al., 2015 [71] | Cohort study of 1001 women aged 39 to 49 years. Evaluation of the association between exposure to cigarette smoke throughout the lifetime (prenatal, childhood, adulthood) and menopause status | Prenatal exposure and current cigarette smoking: 3 times more risk of early menopause (3.4; 95% CI, 1.1–10.3). Long-term exposure (>26 years) is associated to the age at menopause. |
Peck et al., 2016 [73] | Analysis of primordial follicle stock in 133 patients having underwent hysterectomy for a benign pathology. | No association between follicle count and cigarette smoking |
Meta-Analysis | ||
Sun et al., 2012 [66] | Analysis of 11 studies Effect of cigarette smoking on age at menopause | Dichotomous studies: OR = 0.67 (CI 95%, 0.61 to 0.73, P <0.01). Continuous studies: OR = −0.90 (CI 95%, −1.58 to −0.21, P <0.01) Cigarette smoking = independent factor in early age at menopause |