- Email: [email protected]
Hypothesis: Smoking decreases breast feeding duration by suppressing prolactin secretion
Medical Hypotheses 81 (2013) 582–586
Contents lists available at ScienceDirect
Medical Hypotheses journal homepage: www.elsevier.com/locate/mehy
Hypothesis: Smoking decreases breast feeding duration by suppressing prolactin secretion q Babak Bahadori a,⇑, Natalie D. Riediger b,c, Sharla M. Farrell b, Elisabeth Uitz a, Mohammed F. Moghadasian b,c a b c
State Clinic St. Poelten, Department of Internal Medicine 2, St. Poelten, Austria University of Manitoba, Department of Human Nutritional Sciences, Winnipeg, Manitoba, Canada Canadian Centre for Agri-food Research in Health and Medicine, St. Boniface Hospital Research Centre, Winnipeg, Manitoba, Canada
a r t i c l e
i n f o
Article history: Received 28 April 2012 Accepted 3 July 2013
a b s t r a c t A number of studies, including new data summarized here, conclude that breast feeding duration is lower in smoking mothers. Although some have suggested that this merely reflects poor health motivation in those prone to smoke, several lines of evidence support the view that chronic smoking does indeed compromise breast feeding by suppressing prolactin secretion and thereby lowering breast milk volume. Moreover, a recent clinical trial shows that an effective smoking cessation program can boost breast feeding duration in smokers. An analysis of pertinent rodents studies suggests that chronic nicotine administration boosts dopaminergic activity in the tuberoinfundibular tract which functions to inhibit prolactin release; this increase in dopaminergic activity, in turn, may reflect a nicotine-mediated suppression of hypothalamic opioid activity. Ó 2013 Elsevier Ltd. All rights reserved.
Breast feeding duration is low in smokers A number of previous studies have found that duration of breast feeding tends to be lower in women who smoke during the postpartum period, as compared to non-smokers; our own recent study, reported in an appendix, supports these findings [1–14]. In China, where maternal smoking is quite rare, but paternal smoking common, paternal smoking has recently been linked to shorter breast feeding duration, possibly indicative of an adverse effect of side-stream smoke [15]. A negative impact of smoking on initiation of breast feeding is less consistently observed. If smoking does indeed suppress breast feeding duration, this could be expected to have important health implications both for the infant and the mother; prolonged breast feeding is associated with decreased maternal risk for breast and ovarian cancer, and possibly metabolic syndrome, and breast-fed infants are at lower risk for a number of types of infections [16–19]. Nevertheless, some commentators have suggested that smoking per se does not notably influence lactation, but rather that motivational factors can account for lesser breast feeding duration in smokers [20–24]. In other words, women who do not smoke, or who are willing and able to quit smoking post-natally, simply have q The work was done in a cooperation of all the three institution mentioned above. ⇑ Corresponding author. Address: State Clinic St. Poelten, Department of Internal Medicine 2, Propst-Führer Straße 4, 3100 St. Poelten, Austria. Tel.: +43 6644304061; fax: +43 274230019009. E-mail address: [email protected] (B. Bahadori).
0306-9877/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.mehy.2013.07.007
better self-control and a more intelligent regard for their own welfare and that of their infant which translates into a greater willingness to commit to long-term breast feeding. By way of analogy, a recent study has found that the chances of a mother breast feeding for 6 months or more varied directly with the extent to which she included fruits and vegetables in her diet; the authors of this study argue credibly that typical variations in fruit and vegetable consumption would not have such a major impact on capacity for lactation as to account for these findings [24]. It does indeed seem likely that psychological predispositions are playing some role in the shorter breast feeding durations observed in smoking mothers. If such predispositions were the sole reason for decreased duration of breast feeding in smokers, then it could be concluded that post-partum smoking cessation programs would have little real impact on breast feeding duration. But in fact there is good reason to suspect that the physiological effects of nicotine addiction do indeed negatively impact capacity for lactation, and that achieving postpartum smoking abstinence will indeed favorably influence breast feeding duration: 1. Two studies have found that breast milk volumes are lower in smokers than non-smokers [25,26]. 2. There are several reports that maternal prolactin levels are lower in smoking women both during pregnancy and postpartum; low prolactin has also been noted in smoking women outside of pregnancy [27–34]. As is well known, prolactin is a major hormonal stimulant to breast milk production [35,36].
583
B. Bahadori et al. / Medical Hypotheses 81 (2013) 582–586
3. Passive smoking by non-smoking women, as assessed by blood cotinine levels at delivery, was associated with lesser duration of breast feeding in one recent study [37]. This finding is evidently consistent with a negative impact of nicotine or other tobacco toxins on breast feeding duration and it accords well with recent evidence that paternal smoking adversely influences breast feeding duration [15]. 4. A recent study provides cogent evidence that smoking cessation per se can improve breast feeding duration [11]. Post-partum women were randomized to an incentive program which provided reward vouchers for demonstrable abstinence from smoking, or to a control program that provided the these vouchers without requirements. Breast feeding was found to be greater at 8 and 12 weeks postpartum in the first group, as opposed to the latter. Since there is no reason to suspect that women randomized to the first group had greater motivation for breast feeding, the results suggest that smoking cessation per se was beneficial for breast feeding duration. Moreover, analysis of the data from both groups combined showed that those women in either group who achieved smoking cessation tended to achieve greater breast feeding duration; and a multiple regression analysis showed that, within the first group, smoking cessation entirely explained the observed increase in breast feeding duration. Of related interest is a recent controlled study which encouraged postpartum smoking abstinence indirectly by instruction in infant bonding [13]. Smoking mothers who had ceased smoking during pregnancy all received postpartum advice regarding the importance of continuing smoking abstinence, but some were randomly selected to receive various books, handouts, and DVDs intended to encourage bonding with their infants. On follow-up evaluation 8 weeks postpartum, 81% of the bonding-instructed mothers were smoking abstinent and 86% were still breast feeding; in the control group, 46% were smoking abstinent and 21% still breast feeding at this time. Although in contrast to the previously cited study it is not clear to what extent smoking abstinence per se was responsible for longer breast feeding duration in the intervention group, this study offers suggestive evidence that childbonding instruction soon after birth may be quite useful for promoting both smoking abstinence and prolonged breast feeding. We therefore suggest that smoking does indeed impair breast feeding duration in the post-partum period, most probably by suppressing prolactin secretion, and that effective smoking cessation programs following childbirth, particularly those which stress infant bonding, can be expected to have a favorable impact on breast feeding duration.
Nicotine addiction suppresses prolactin by up-regulating tuberoinfundibular dopamine How then does smoking suppress prolactin secretion? In rats, a single dose of nicotine typically provokes prolactin secretion; however, this response is substantially blunted if subsequent doses are given [38–42]. Studies in rats chronically treated with nicotine show a decrease in blood prolactin levels [43–45]. In one provocative study, pregnant rats were injected with 2 mg nicotine daily from day 5 of gestation until the pups were weaned. Although their litter sizes and weights were near–normal at birth, the pups failed to gain weight normally, and about 70% died prior to weaning; the nicotine had blocked the normal post-partum rise in maternal prolactin, milk volumes were grossly subnormal, and most of the pups died from starvation [43].
Dopamine secreted by hypothalamic tuberoinfundibular dopaminergic neurons is known to suppress pituitary secretion of prolactin, and indeed is one of the major determinants of prolactin activity [46]. Whereas an acute administration of nicotine is reported to suppress this dopaminergic activity, chronic administration boosts it, resulting in a suppression of prolactin release [45,47–49]. There is reason to suspect as postulated by Rasmussen [45] that this chronic up-regulation tuberoinfundibular dopaminergic activity might be attributable, at least in part, to a concurrent suppression of opioid activity in the mediobasal hypothalamus (MBH), as has been observed in rodents treated chronically with nicotine [45,50]. Chronic nicotine administration in rats leads to a reduction in expression of proopiomelanocortin mRNA in the MBH (presumably a marker for opioid activity), accompanied by an up-regulation of tyrosine hydroxylase expression in this region [45]. Tuberoinfundibular dopaminergic activity is suppressed by opioids [47,51]; indeed, the acute stimulatory effect of a single dose of nicotine on prolactin release appears to be mediated by an increase in opioid activity that inhibits hypothalamic dopamine release [47]. Hence, the suppression of hypothalamic opioid production associated with nicotine addiction an effect which likely motivates the addiction, as nicotine acutely boosts opioid activity [45,52] may be largely responsible for the increased dopaminergic tone which inhibits prolactin release in smokers. However, this model is difficult to square with a recent clinical study in which the impact of naltrexone administration on prolactin levels was assessed in smokers and non-smokers [53]. While the smokers showed less responsiveness to naltrexone than nonsmokers – as would be expected from a predicted down-regulation of opioid activity in smokers prolactin rose in response to the naltrexone, a response opposite in direction to that predicted from the model. Perhaps this reflects an impact of naltrexone on some part of the brain other than the hypothalamus or perhaps rodent models of nicotine addiction are less than perfect guides to the Table 1 Characteristics of study cohort of Canadian women who gave birth (n = 3485). Characteristic
Proportion of sample sizea
Age 15-19 20-24 25-29 30-34 35-39 40-44 45-49
1.9 11.6 26.1 32.7 21.2 5.7 0.8
Income <$15000 $15000-$29999 $30000-$49999 $50000-$79999 >$80000
9.9 14.5 21.5 29.2 25.0
Education Less than secondary school graduation Secondary school graduation Some post-secondary education Post-secondary graduation
7.8 13.0 6.6 72.6
Marital status Married Common-law Single (never married) Widowed/divorced/separated
62.2 17.5 13.2 7.1
Racial origin White Visible minorityb
84.4 15.6
a Percentages may not add up to 100% due to rounding; participants who did not respond to a question were not included in the analysis of that question. b In Canada, ‘‘visible minority’’ is defined as non-Caucasian people.
584
B. Bahadori et al. / Medical Hypotheses 81 (2013) 582–586
physiology of smoking humans. Further research will be required to clarify the role of hypothalamic opioids in the chronic up-regulation of MBH dopaminergic activity that characterizes nicotine addiction. Also of interest is a report that nicotine can act directly on prolactin-secreting GH3 cells to inhibit transcription of the prolactin gene; if valid, this effect evidently could complement the suppressive impact of increased dopaminergic activity on prolactin secretion [54].
established by using three frames: (1) an area frame (48% of respondents), (2) a telephone number frame (50% of respondents) and a random digit–dialing frame (2% of respondents). The survey was distributed to 1,30,000 people aged above 12 years in all provinces and territories in Canada, excluding Canadian Forces Bases and aboriginal reserves/Crown Lands. From this survey a sub-sample of women aged 15–49 years old who gave birth in the past five years was analyzed in the present study. A.2. Variables
Conflict of interest statement None. Appendix A. An observational study on breast feeding duration in smokers A.1. Data source Data source for the present study was the Canadian Community Health Survey cycle 2.1 Public Use File, conducted by Statistics Canada (2003). The use of the data obtained from this survey was approved by the University of Manitoba and Statistics Canada. The survey provides cross-sectional estimates of health status, health system utilization and health determinants and was conducted from January 2003 to December 2003. The survey was
The main outcome measure was the duration of breastfeeding. The participants reported duration of breastfeeding for their last child as either up to 12 weeks (3 months) or greater than 3 months. Fifteen questions were examined concerning information on the use and frequency of cigarettes, alcohol and illicit drugs. The questions pertaining to cigarette smoking habits aimed to determine the frequency of smoking as daily, occasional or never during pregnancy and lactation. For both daily and occasional smokers, the frequency of smoking during pregnancy and lactation was further assessed. A.3. Statistical analysis Data were analyzed using SPSS version 11.5 for windows. Methods described by Riediger et al., were used to partially account for
Table 2 Association of smoking status and duration of breastfeeding. Duration of breastfeeding (% sample size) Adverse behaviour (n)
< 3 months
3 months to > 1 year
p-valuea
p-valueb
Odds Ratio (95% CI)b
Type of smoker (n = 2451) Daily Occasional Not at all
46.7 36.2 29.6
53.3 63.8 70.4
p <0.001
p <0.05
1.229 (1.002, 1.508)
Type of smoker while pregnant (n=1601) Daily Occasionally Not at all Number of cigarettes smoked daily while pregnant (daily smokers) (n = 224) 1 to 5 6 to 10 >10 Number of cigarettes smoked daily while pregnant (occasional smokers) (n = 212) 61 2 to 4 >4
52.7 44.9 30.7
47.3 55.1 69.3
p <0.001
p <0.01
1.638 (1.232, 2.178)
40.9 53.9 62.2
59.1 46.1 37.8
p = 0.245
p=0.558
52.1 39.4 50.9
47.9 60.6 49.1
p = 0.697
p = 0.558
0.909 (0.659, 1.252)
47.1 34.9 33.9
52.9 65.1 66.1
p <0.001
p <0.05
1.439 (1.075, 1.926)
Number of cigarettes smoked daily while breastfeeding of daily smokers (n=224) 2 to 5 6 to 10 >10 Number of cigarettes smoked daily while breastfeeding of occasional smokers (n = 187)
41.1 42.7 55.8
58.9 57.3 44.2
p = 0.341
p = 0.115
0.718 (0.475, 1.084)
61 2 to 4 >4
31.4 29.9 48.9
68.6 70.1 51.1
p = 0.156
p = 0.057
0.652 (0.420, 1.012)
Type of smoker while breastfeeding(n=1601) Daily Occasionally Not at all
a
0.568 (0.369, 0.874)4
p-value according to chi-square test to detect differences in duration of breastfeeding among different types of smokers and their frequency of smoking p-value and odds ratio according to binary logistic regression after adjusting for age, total household income, education, province of residency, marital status, and ethnicity
b
B. Bahadori et al. / Medical Hypotheses 81 (2013) 582–586
survey design when conducting statistical analysis.[55] Chi-square test was used to determine significance of test variables. P-values <0.05 were considered statistically significant. Binary logistic regression was used to generate odds ratios (OR) and 95% confidence intervals (CI). Binary logistic regression analyses were adjusted for age, total household income, educational level, geographic location, marital status and ethnic origin. A.4. Results Characteristics of study participants, including age, income, educational level, marital status and racial origin are given in Table 1. In detail, 3485 women reported a birth between 1998 and 2003 and were included in the presented study. Of these 3485 women, 33.5% reported breastfeeding up to 3 months and 66.5% reported to breastfed over 3 months. A.5. Associations between duration of breastfeeding and smoking Smoking behavior of study participants is given in Table 2. In detail, 20.4% of the women who gave birth reported themselves as daily smokers, while 6.2% were occasional smokers, and 73.4% reported not smoking at all. During pregnancy, 14.9% of women were self-reported daily smokers, 13.5% occasional smokers, and 71.6% reported not to smoke at all. Similarly, 14.1% of lactating mothers reported daily smoking, 11.8% were occasional smokers, and 74.1% non-smokers. Of those women who reported daily smoking during pregnancy, 27.8% claimed to smoke 1–5 cigarettes/day, 37.6% smoked 6–10 cigarettes/day, and 34.6% smoked more than 10 cigarettes/day. Of the women that were self-reported occasional smokers during pregnancy, 22.6% smoked one or less cigarettes/day, 51.4% smoked 2–4 cigarettes/day, and 25.9% smoked greater than four cigarettes/day. Of those women that reported daily smoking during breastfeeding, 25% smoked between 2–5 cigarettes/day, 36.6% smoked 6–10 cigarettes/day, and 38.4% smoked more than 10 cigarettes/day. Of the women that reported occasional smoking during breastfeeding, 18.7% reported having less than or equal to one cigarette/day, 57.2% had 2–4 cigarettes/ day, and 24.1% smoked more than 4 cigarettes/day. Analyses of smoking status and frequency of smoking during pregnancy and breastfeeding are outlined in Table 2. In detail, the type of smoker (p < 0.001), type of smoker while pregnant (p < 0.001) and type of smoker while breastfeeding (p < 0.001) were all significantly associated with duration of breastfeeding. Occasional and daily smokers were less likely to breastfeed greater than 3 months compared to women that never smoked. Associations remained significant in binary logistic regression analyses after adjustment for various socio-demographic factors listed above with odds ratios of 1.229 (95%CI: 1.002–1.508) for type of smoker, 1.638 (95%CI: 1.232, 2.178) for type of smoker while pregnant and 1.439 (95%CI 1.075, 1.926) for type of smoker while breastfeeding. The number of cigarettes smoked during pregnancy and breastfeeding did not show a significant association with duration of breastfeeding. References [1] Horta BL, Kramer MS, Platt RW. Maternal smoking and the risk of early weaning: a meta-analysis. Am J Public Health 2001;91(2):304–7. [2] Mansbach IK, Greenbaum CW, Sulkes J. Onset and duration of breast feeding among Israeli mothers: relationships with smoking and type of delivery. Soc Sci Med 1991;33(12):1391–7. [3] Ratner PA, Johnson JL, Bottorff JL. Smoking relapse and early weaning among postpartum women: is there an association ? Birth 1999;26(2):76–82. [4] Knudsen A, Pedersen H, Klebe JG. Impact of smoking on the duration of breastfeeding in mothers with insulin-dependent diabetes mellitus. Acta Paediatr 2001;90(8):926–30.
585
[5] Scott JA, Binns CW, Oddy WH, Graham KI. Predictors of breastfeeding duration: evidence from a cohort study. Pediatrics 2006;117(4):e646–55. [6] Liu J, Rosenberg KD, Sandoval AP. Breastfeeding duration and perinatal cigarette smoking in a population-based cohort. Am J Public Health 2006;96(2):309–14. [7] Giglia R, Binns CW, Alfonso H. Maternal cigarette smoking and breastfeeding duration. Acta Paediatr 2006;95(11):1370–4. [8] Baxter J, Cooklin AR, Smith J. Which mothers wean their babies prematurely from full breastfeeding? An Australian cohort study. Acta Paediatr 2009;98(8):1274–7. [9] Thulier D, Mercer J. Variables associated with breastfeeding duration. J Obstet Gynecol Neonatal Nurs 2009;38(3):259–68. [10] Weiser TM, Lin M, Garikapaty V, Feyerharm RW, Bensyl DM, Zhu BP. Association of maternal smoking status with breastfeeding practices: Missouri, 2005. Pediatrics 2009;124(6):1603–10. [11] Higgins TM, Higgins ST, Heil SH, et al. Effects of cigarette smoking cessation on breastfeeding duration. Nicotine Tob Res 2010;12(5):483–8. [12] Collins BN, DiSantis KI, Nair US. Longer previous smoking abstinence relates to successful breastfeeding initiation among underserved smokers. Breastfeed Med 2011;6(6):385–91. [13] Phillips RM, Merritt TA, Goldstein MR, Deming DD, Slater LE, Angeles DM. Prevention of postpartum smoking relapse in mothers of infants in the neonatal intensive care unit. J Perinatol 2012;32(5):374–80. [14] Dennis CL, Gagnon A, Van HA, Dougherty G, Wahoush O. Prediction of duration of breastfeeding among migrant and Canadian-born women: results from a multi-center study. J Pediatr 2013;162(1):72–9. [15] Xu F, Binns C, Zhang H, Yang G, Zhao Y. Paternal smoking and breastfeeding in Xinjiang, PR China. J Hum Lact 2010;26(3):242–7. [16] Ma H, Bernstein L, Pike MC, Ursin G. Reproductive factors and breast cancer risk according to joint estrogen and progesterone receptor status: a meta-analysis of epidemiological studies. Breast Cancer Res 2006;8(4):R43. [17] Jordan SJ, Cushing-Haugen KL, Wicklund KG, Doherty JA, Rossing MA. Breast-feeding and risk of epithelial ovarian cancer. Cancer Causes Control 2012 June;23(6):919–27. [18] Gouveri E, Papanas N, Hatzitolios AI, Maltezos E. Breastfeeding and diabetes. Curr Diabetes Rev 2011 March;7(2):135–42. [19] Duijts L, Ramadhani MK, Moll HA. Breastfeeding protects against infectious diseases during infancy in industrialized countries. A systematic review. Matern Child Nutr 2009;5(3):199–210. [20] Amir LH. Maternal smoking and reduced duration of breastfeeding: a review of possible mechanisms. Early Hum Dev 2001;64(1):45–67. [21] Amir LH, Donath SM. Does maternal smoking have a negative physiological effect on breastfeeding? The epidemiological evidence. Birth 2002;29(2):112–23. [22] Donath SM, Amir LH. The relationship between maternal smoking and breastfeeding duration after adjustment for maternal infant feeding intention. Acta Paediatr 2004;93(11):1514–8. [23] Amir LH, Donath SM. Does maternal smoking have a negative physiological effect on breastfeeding? The epidemiological evidence. Breastfeed Rev 2003;11(2):19–29. [24] Amir LH, Donath SM. Maternal diet and breastfeeding: a case for rethinking physiological explanations for breastfeeding determinants. Early Hum Dev 2012;88(7):467–71. [25] Vio F, Salazar G, Infante C. Smoking during pregnancy and lactation and its effects on breast-milk volume. Am J Clin Nutr 1991;54(6):1011–6. [26] Hopkinson JM, Schanler RJ, Fraley JK, Garza C. Milk production by mothers of premature infants: influence of cigarette smoking. Pediatrics 1992;90(6):934–8. [27] Andersen AN, Lund-Andersen C, Larsen JF, et al. Suppressed prolactin but normal neurophysin levels in cigarette smoking breast-feeding women. Clin Endocrinol (Oxf) 1982;17(4):363–8. [28] Andersen AN, Ronn B, Tjonneland A, Djursing H, Schioler V. Low maternal but normal fetal prolactin levels in cigarette smoking pregnant women. Acta Obstet Gynecol Scand 1984;63(3):237–9. [29] Bremme K, Lagerstrom M, Andersson O, Johansson S, Eneroth P. Influences of maternal smoking and fetal sex on maternal serum oestriol, prolactin, hCG, and hPI levels. Arch Gynecol Obstet 1990;247(2):95–103. [30] Andersen AN, Semczuk M, Tabor A. Prolactin and pituitary-gonadal function in cigarette smoking infertile patients. Andrologia 1984;16(5):391–6. [31] Baron JA, Bulbrook RD, Wang DY, Kwa HG. Cigarette smoking and prolactin in women. Br Med J (Clin Res Ed) 1986;293(6545):482–3. [32] Berta L, Frairia R, Fortunati N, Fazzari A, Gaidano G. Smoking effects on the hormonal balance of fertile women. Horm Res 1992;37(1–2):45–8. [33] Glintborg D, Mumm H, Hougaard DM, Ravn P, Andersen M. Smoking is associated with increased adrenal responsiveness, decreased prolactin levels and a more adverse lipid profile in 650 white patients with polycystic ovary syndrome. Gynecol Endocrinol 2012;28(3):170–4. [34] Weigert M, Hofstetter G, Kaipl D, et al. The effect of smoking on oocyte quality and hormonal parameters of patients undergoing in vitro fertilization-embryo transfer. J Assist Reprod Genet 1999;16(6):287–93. [35] Ben-Jonathan N, Hugo ER, Brandebourg TD, LaPensee CR. Focus on prolactin as a metabolic hormone. Trends Endocrinol Metab 2006;17(3):110–6. [36] Gabay MP. Galactogogues: medications that induce lactation. J Hum Lact 2002;18(3):274–9. [37] Jedrychowski W, Perera F, Mroz E, et al. Prenatal exposure to passive smoking
586
[38]
[39]
[40]
[41]
[42]
[43] [44]
[45]
B. Bahadori et al. / Medical Hypotheses 81 (2013) 582–586 and duration of breastfeeding in nonsmoking women: krakow inner city prospective cohort study. Arch Gynecol Obstet 2008;278(5):411–7. Sharp BM, Beyer HS. Rapid desensitization of the acute stimulatory effects of nicotine on rat plasma adrenocorticotropin and prolactin. J Pharmacol Exp Ther 1986;238(2):486–91. Sharp BM, Beyer HS, Levine AS, Morley JE, McAllen KM. Attenuation of the plasma prolactin response to restraint stress after acute and chronic administration of nicotine to rats. J Pharmacol Exp Ther 1987;241(2):438–42. Hulihan-Giblin BA, Lumpkin MD, Kellar KJ. Acute effects of nicotine on prolactin release in the rat: agonist and antagonist effects of a single injection of nicotine. J Pharmacol Exp Ther 1990;252(1):15–20. Hulihan-Giblin BA, Lumpkin MD, Kellar KJ. Effects of chronic administration of nicotine on prolactin release in the rat: inactivation of prolactin response by repeated injections of nicotine. J Pharmacol Exp Ther 1990;252(1):21–5. Matta SG, Sharp BM. The role of the fourth cerebroventricle in nicotinestimulated prolactin release in the rat: involvement of catecholamines. J Pharmacol Exp Ther 1992;260(3):1285–91. Terkel J, Blake CA, Hoover V, Sawyer CH. Pup survival and prolactin levels in nicotine-treated lactating rats. Proc Soc Exp Biol Med 1973;143(4):1131–5. Fuxe K, Janson AM, Jansson A, Andersson K, Eneroth P, Agnati LF. Chronic nicotine treatment increases dopamine levels and reduces dopamine utilization in substantia nigra and in surviving forebrain dopamine nerve terminal systems after a partial di-mesencephalic hemitransection. Naunyn Schmiedebergs Arch Pharmacol 1990;341(3):171–81. Rasmussen DD. Effects of chronic nicotine treatment and withdrawal on hypothalamic proopiomelanocortin gene expression and neuroendocrine regulation. Psychoneuroendocrinology 1998 April;23(3):245–59.
[46] Reymond MJ, Porter JC. Involvement of hypothalamic dopamine in the regulation of prolactin secretion. Horm Res 1985;22(3):142–52. [47] Shieh KR, Pan JT. Nicotinic control of tuberoinfundibular dopaminergic neuron activity and prolactin secretion: diurnal rhythm and involvement of endogenous opioidergic system. Brain Res 1997;756(1–2):266–72. [48] Andersson K, Eneroth P, Fuxe K, Mascagni F, Agnati LF. Effects of chronic exposure to cigarette smoke on amine levels and turnover in various hypothalamic catecholamine nerve terminal systems and on the secretion of pituitary hormones in the male rat. Neuroendocrinology 1985;41(6):462–6. [49] Fuxe K, Andersson K, Eneroth P, Harfstrand A, Agnati LF. Neuroendocrine actions of nicotine and of exposure to cigarette smoke: medical implications. Psychoneuroendocrinology 1989;14(1–2):19–41. [50] Rosecrans JA, Hendry JS, Hong JS. Biphasic effects of chronic nicotine treatment on hypothalamic immunoreactive beta-endorphin in the mouse. Pharmacol Biochem Behav 1985;23(1):141–3. [51] Deyo SN, Swift RM, Miller RJ. Morphine and endorphins modulate dopamine turnover in rat median eminence. Proc Natl Acad Sci USA 1979;76(6):3006–9. [52] Mineur YS, Abizaid A, Rao Y, et al. Nicotine decreases food intake through activation of POMC neurons. Science 2011;332(6035):1330–2. [53] Shaw D, Al’Absi M. Blunted opiate modulation of prolactin response in smoking men and women. Pharmacol Biochem Behav 2010;95(1):1–5. [54] Coleman DT, Bancroft C. Nicotine acts directly on pituitary GH3 cells to inhibit prolactin promoter activity. J Neuroendocrinol 1995;7(10):785–9. [55] Riediger ND, Shooshtari S, Moghadasian MH. The influence of sociodemographic factors on patterns of fruit and vegetable consumption in Canadian adolescents. J Am Diet Assoc 2007;107(9):1511–8.
Contents lists available at ScienceDirect
Medical Hypotheses journal homepage: www.elsevier.com/locate/mehy
Hypothesis: Smoking decreases breast feeding duration by suppressing prolactin secretion q Babak Bahadori a,⇑, Natalie D. Riediger b,c, Sharla M. Farrell b, Elisabeth Uitz a, Mohammed F. Moghadasian b,c a b c
State Clinic St. Poelten, Department of Internal Medicine 2, St. Poelten, Austria University of Manitoba, Department of Human Nutritional Sciences, Winnipeg, Manitoba, Canada Canadian Centre for Agri-food Research in Health and Medicine, St. Boniface Hospital Research Centre, Winnipeg, Manitoba, Canada
a r t i c l e
i n f o
Article history: Received 28 April 2012 Accepted 3 July 2013
a b s t r a c t A number of studies, including new data summarized here, conclude that breast feeding duration is lower in smoking mothers. Although some have suggested that this merely reflects poor health motivation in those prone to smoke, several lines of evidence support the view that chronic smoking does indeed compromise breast feeding by suppressing prolactin secretion and thereby lowering breast milk volume. Moreover, a recent clinical trial shows that an effective smoking cessation program can boost breast feeding duration in smokers. An analysis of pertinent rodents studies suggests that chronic nicotine administration boosts dopaminergic activity in the tuberoinfundibular tract which functions to inhibit prolactin release; this increase in dopaminergic activity, in turn, may reflect a nicotine-mediated suppression of hypothalamic opioid activity. Ó 2013 Elsevier Ltd. All rights reserved.
Breast feeding duration is low in smokers A number of previous studies have found that duration of breast feeding tends to be lower in women who smoke during the postpartum period, as compared to non-smokers; our own recent study, reported in an appendix, supports these findings [1–14]. In China, where maternal smoking is quite rare, but paternal smoking common, paternal smoking has recently been linked to shorter breast feeding duration, possibly indicative of an adverse effect of side-stream smoke [15]. A negative impact of smoking on initiation of breast feeding is less consistently observed. If smoking does indeed suppress breast feeding duration, this could be expected to have important health implications both for the infant and the mother; prolonged breast feeding is associated with decreased maternal risk for breast and ovarian cancer, and possibly metabolic syndrome, and breast-fed infants are at lower risk for a number of types of infections [16–19]. Nevertheless, some commentators have suggested that smoking per se does not notably influence lactation, but rather that motivational factors can account for lesser breast feeding duration in smokers [20–24]. In other words, women who do not smoke, or who are willing and able to quit smoking post-natally, simply have q The work was done in a cooperation of all the three institution mentioned above. ⇑ Corresponding author. Address: State Clinic St. Poelten, Department of Internal Medicine 2, Propst-Führer Straße 4, 3100 St. Poelten, Austria. Tel.: +43 6644304061; fax: +43 274230019009. E-mail address: [email protected] (B. Bahadori).
0306-9877/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.mehy.2013.07.007
better self-control and a more intelligent regard for their own welfare and that of their infant which translates into a greater willingness to commit to long-term breast feeding. By way of analogy, a recent study has found that the chances of a mother breast feeding for 6 months or more varied directly with the extent to which she included fruits and vegetables in her diet; the authors of this study argue credibly that typical variations in fruit and vegetable consumption would not have such a major impact on capacity for lactation as to account for these findings [24]. It does indeed seem likely that psychological predispositions are playing some role in the shorter breast feeding durations observed in smoking mothers. If such predispositions were the sole reason for decreased duration of breast feeding in smokers, then it could be concluded that post-partum smoking cessation programs would have little real impact on breast feeding duration. But in fact there is good reason to suspect that the physiological effects of nicotine addiction do indeed negatively impact capacity for lactation, and that achieving postpartum smoking abstinence will indeed favorably influence breast feeding duration: 1. Two studies have found that breast milk volumes are lower in smokers than non-smokers [25,26]. 2. There are several reports that maternal prolactin levels are lower in smoking women both during pregnancy and postpartum; low prolactin has also been noted in smoking women outside of pregnancy [27–34]. As is well known, prolactin is a major hormonal stimulant to breast milk production [35,36].
583
B. Bahadori et al. / Medical Hypotheses 81 (2013) 582–586
3. Passive smoking by non-smoking women, as assessed by blood cotinine levels at delivery, was associated with lesser duration of breast feeding in one recent study [37]. This finding is evidently consistent with a negative impact of nicotine or other tobacco toxins on breast feeding duration and it accords well with recent evidence that paternal smoking adversely influences breast feeding duration [15]. 4. A recent study provides cogent evidence that smoking cessation per se can improve breast feeding duration [11]. Post-partum women were randomized to an incentive program which provided reward vouchers for demonstrable abstinence from smoking, or to a control program that provided the these vouchers without requirements. Breast feeding was found to be greater at 8 and 12 weeks postpartum in the first group, as opposed to the latter. Since there is no reason to suspect that women randomized to the first group had greater motivation for breast feeding, the results suggest that smoking cessation per se was beneficial for breast feeding duration. Moreover, analysis of the data from both groups combined showed that those women in either group who achieved smoking cessation tended to achieve greater breast feeding duration; and a multiple regression analysis showed that, within the first group, smoking cessation entirely explained the observed increase in breast feeding duration. Of related interest is a recent controlled study which encouraged postpartum smoking abstinence indirectly by instruction in infant bonding [13]. Smoking mothers who had ceased smoking during pregnancy all received postpartum advice regarding the importance of continuing smoking abstinence, but some were randomly selected to receive various books, handouts, and DVDs intended to encourage bonding with their infants. On follow-up evaluation 8 weeks postpartum, 81% of the bonding-instructed mothers were smoking abstinent and 86% were still breast feeding; in the control group, 46% were smoking abstinent and 21% still breast feeding at this time. Although in contrast to the previously cited study it is not clear to what extent smoking abstinence per se was responsible for longer breast feeding duration in the intervention group, this study offers suggestive evidence that childbonding instruction soon after birth may be quite useful for promoting both smoking abstinence and prolonged breast feeding. We therefore suggest that smoking does indeed impair breast feeding duration in the post-partum period, most probably by suppressing prolactin secretion, and that effective smoking cessation programs following childbirth, particularly those which stress infant bonding, can be expected to have a favorable impact on breast feeding duration.
Nicotine addiction suppresses prolactin by up-regulating tuberoinfundibular dopamine How then does smoking suppress prolactin secretion? In rats, a single dose of nicotine typically provokes prolactin secretion; however, this response is substantially blunted if subsequent doses are given [38–42]. Studies in rats chronically treated with nicotine show a decrease in blood prolactin levels [43–45]. In one provocative study, pregnant rats were injected with 2 mg nicotine daily from day 5 of gestation until the pups were weaned. Although their litter sizes and weights were near–normal at birth, the pups failed to gain weight normally, and about 70% died prior to weaning; the nicotine had blocked the normal post-partum rise in maternal prolactin, milk volumes were grossly subnormal, and most of the pups died from starvation [43].
Dopamine secreted by hypothalamic tuberoinfundibular dopaminergic neurons is known to suppress pituitary secretion of prolactin, and indeed is one of the major determinants of prolactin activity [46]. Whereas an acute administration of nicotine is reported to suppress this dopaminergic activity, chronic administration boosts it, resulting in a suppression of prolactin release [45,47–49]. There is reason to suspect as postulated by Rasmussen [45] that this chronic up-regulation tuberoinfundibular dopaminergic activity might be attributable, at least in part, to a concurrent suppression of opioid activity in the mediobasal hypothalamus (MBH), as has been observed in rodents treated chronically with nicotine [45,50]. Chronic nicotine administration in rats leads to a reduction in expression of proopiomelanocortin mRNA in the MBH (presumably a marker for opioid activity), accompanied by an up-regulation of tyrosine hydroxylase expression in this region [45]. Tuberoinfundibular dopaminergic activity is suppressed by opioids [47,51]; indeed, the acute stimulatory effect of a single dose of nicotine on prolactin release appears to be mediated by an increase in opioid activity that inhibits hypothalamic dopamine release [47]. Hence, the suppression of hypothalamic opioid production associated with nicotine addiction an effect which likely motivates the addiction, as nicotine acutely boosts opioid activity [45,52] may be largely responsible for the increased dopaminergic tone which inhibits prolactin release in smokers. However, this model is difficult to square with a recent clinical study in which the impact of naltrexone administration on prolactin levels was assessed in smokers and non-smokers [53]. While the smokers showed less responsiveness to naltrexone than nonsmokers – as would be expected from a predicted down-regulation of opioid activity in smokers prolactin rose in response to the naltrexone, a response opposite in direction to that predicted from the model. Perhaps this reflects an impact of naltrexone on some part of the brain other than the hypothalamus or perhaps rodent models of nicotine addiction are less than perfect guides to the Table 1 Characteristics of study cohort of Canadian women who gave birth (n = 3485). Characteristic
Proportion of sample sizea
Age 15-19 20-24 25-29 30-34 35-39 40-44 45-49
1.9 11.6 26.1 32.7 21.2 5.7 0.8
Income <$15000 $15000-$29999 $30000-$49999 $50000-$79999 >$80000
9.9 14.5 21.5 29.2 25.0
Education Less than secondary school graduation Secondary school graduation Some post-secondary education Post-secondary graduation
7.8 13.0 6.6 72.6
Marital status Married Common-law Single (never married) Widowed/divorced/separated
62.2 17.5 13.2 7.1
Racial origin White Visible minorityb
84.4 15.6
a Percentages may not add up to 100% due to rounding; participants who did not respond to a question were not included in the analysis of that question. b In Canada, ‘‘visible minority’’ is defined as non-Caucasian people.
584
B. Bahadori et al. / Medical Hypotheses 81 (2013) 582–586
physiology of smoking humans. Further research will be required to clarify the role of hypothalamic opioids in the chronic up-regulation of MBH dopaminergic activity that characterizes nicotine addiction. Also of interest is a report that nicotine can act directly on prolactin-secreting GH3 cells to inhibit transcription of the prolactin gene; if valid, this effect evidently could complement the suppressive impact of increased dopaminergic activity on prolactin secretion [54].
established by using three frames: (1) an area frame (48% of respondents), (2) a telephone number frame (50% of respondents) and a random digit–dialing frame (2% of respondents). The survey was distributed to 1,30,000 people aged above 12 years in all provinces and territories in Canada, excluding Canadian Forces Bases and aboriginal reserves/Crown Lands. From this survey a sub-sample of women aged 15–49 years old who gave birth in the past five years was analyzed in the present study. A.2. Variables
Conflict of interest statement None. Appendix A. An observational study on breast feeding duration in smokers A.1. Data source Data source for the present study was the Canadian Community Health Survey cycle 2.1 Public Use File, conducted by Statistics Canada (2003). The use of the data obtained from this survey was approved by the University of Manitoba and Statistics Canada. The survey provides cross-sectional estimates of health status, health system utilization and health determinants and was conducted from January 2003 to December 2003. The survey was
The main outcome measure was the duration of breastfeeding. The participants reported duration of breastfeeding for their last child as either up to 12 weeks (3 months) or greater than 3 months. Fifteen questions were examined concerning information on the use and frequency of cigarettes, alcohol and illicit drugs. The questions pertaining to cigarette smoking habits aimed to determine the frequency of smoking as daily, occasional or never during pregnancy and lactation. For both daily and occasional smokers, the frequency of smoking during pregnancy and lactation was further assessed. A.3. Statistical analysis Data were analyzed using SPSS version 11.5 for windows. Methods described by Riediger et al., were used to partially account for
Table 2 Association of smoking status and duration of breastfeeding. Duration of breastfeeding (% sample size) Adverse behaviour (n)
< 3 months
3 months to > 1 year
p-valuea
p-valueb
Odds Ratio (95% CI)b
Type of smoker (n = 2451) Daily Occasional Not at all
46.7 36.2 29.6
53.3 63.8 70.4
p <0.001
p <0.05
1.229 (1.002, 1.508)
Type of smoker while pregnant (n=1601) Daily Occasionally Not at all Number of cigarettes smoked daily while pregnant (daily smokers) (n = 224) 1 to 5 6 to 10 >10 Number of cigarettes smoked daily while pregnant (occasional smokers) (n = 212) 61 2 to 4 >4
52.7 44.9 30.7
47.3 55.1 69.3
p <0.001
p <0.01
1.638 (1.232, 2.178)
40.9 53.9 62.2
59.1 46.1 37.8
p = 0.245
p=0.558
52.1 39.4 50.9
47.9 60.6 49.1
p = 0.697
p = 0.558
0.909 (0.659, 1.252)
47.1 34.9 33.9
52.9 65.1 66.1
p <0.001
p <0.05
1.439 (1.075, 1.926)
Number of cigarettes smoked daily while breastfeeding of daily smokers (n=224) 2 to 5 6 to 10 >10 Number of cigarettes smoked daily while breastfeeding of occasional smokers (n = 187)
41.1 42.7 55.8
58.9 57.3 44.2
p = 0.341
p = 0.115
0.718 (0.475, 1.084)
61 2 to 4 >4
31.4 29.9 48.9
68.6 70.1 51.1
p = 0.156
p = 0.057
0.652 (0.420, 1.012)
Type of smoker while breastfeeding(n=1601) Daily Occasionally Not at all
a
0.568 (0.369, 0.874)4
p-value according to chi-square test to detect differences in duration of breastfeeding among different types of smokers and their frequency of smoking p-value and odds ratio according to binary logistic regression after adjusting for age, total household income, education, province of residency, marital status, and ethnicity
b
B. Bahadori et al. / Medical Hypotheses 81 (2013) 582–586
survey design when conducting statistical analysis.[55] Chi-square test was used to determine significance of test variables. P-values <0.05 were considered statistically significant. Binary logistic regression was used to generate odds ratios (OR) and 95% confidence intervals (CI). Binary logistic regression analyses were adjusted for age, total household income, educational level, geographic location, marital status and ethnic origin. A.4. Results Characteristics of study participants, including age, income, educational level, marital status and racial origin are given in Table 1. In detail, 3485 women reported a birth between 1998 and 2003 and were included in the presented study. Of these 3485 women, 33.5% reported breastfeeding up to 3 months and 66.5% reported to breastfed over 3 months. A.5. Associations between duration of breastfeeding and smoking Smoking behavior of study participants is given in Table 2. In detail, 20.4% of the women who gave birth reported themselves as daily smokers, while 6.2% were occasional smokers, and 73.4% reported not smoking at all. During pregnancy, 14.9% of women were self-reported daily smokers, 13.5% occasional smokers, and 71.6% reported not to smoke at all. Similarly, 14.1% of lactating mothers reported daily smoking, 11.8% were occasional smokers, and 74.1% non-smokers. Of those women who reported daily smoking during pregnancy, 27.8% claimed to smoke 1–5 cigarettes/day, 37.6% smoked 6–10 cigarettes/day, and 34.6% smoked more than 10 cigarettes/day. Of the women that were self-reported occasional smokers during pregnancy, 22.6% smoked one or less cigarettes/day, 51.4% smoked 2–4 cigarettes/day, and 25.9% smoked greater than four cigarettes/day. Of those women that reported daily smoking during breastfeeding, 25% smoked between 2–5 cigarettes/day, 36.6% smoked 6–10 cigarettes/day, and 38.4% smoked more than 10 cigarettes/day. Of the women that reported occasional smoking during breastfeeding, 18.7% reported having less than or equal to one cigarette/day, 57.2% had 2–4 cigarettes/ day, and 24.1% smoked more than 4 cigarettes/day. Analyses of smoking status and frequency of smoking during pregnancy and breastfeeding are outlined in Table 2. In detail, the type of smoker (p < 0.001), type of smoker while pregnant (p < 0.001) and type of smoker while breastfeeding (p < 0.001) were all significantly associated with duration of breastfeeding. Occasional and daily smokers were less likely to breastfeed greater than 3 months compared to women that never smoked. Associations remained significant in binary logistic regression analyses after adjustment for various socio-demographic factors listed above with odds ratios of 1.229 (95%CI: 1.002–1.508) for type of smoker, 1.638 (95%CI: 1.232, 2.178) for type of smoker while pregnant and 1.439 (95%CI 1.075, 1.926) for type of smoker while breastfeeding. The number of cigarettes smoked during pregnancy and breastfeeding did not show a significant association with duration of breastfeeding. References [1] Horta BL, Kramer MS, Platt RW. Maternal smoking and the risk of early weaning: a meta-analysis. Am J Public Health 2001;91(2):304–7. [2] Mansbach IK, Greenbaum CW, Sulkes J. Onset and duration of breast feeding among Israeli mothers: relationships with smoking and type of delivery. Soc Sci Med 1991;33(12):1391–7. [3] Ratner PA, Johnson JL, Bottorff JL. Smoking relapse and early weaning among postpartum women: is there an association ? Birth 1999;26(2):76–82. [4] Knudsen A, Pedersen H, Klebe JG. Impact of smoking on the duration of breastfeeding in mothers with insulin-dependent diabetes mellitus. Acta Paediatr 2001;90(8):926–30.
585
[5] Scott JA, Binns CW, Oddy WH, Graham KI. Predictors of breastfeeding duration: evidence from a cohort study. Pediatrics 2006;117(4):e646–55. [6] Liu J, Rosenberg KD, Sandoval AP. Breastfeeding duration and perinatal cigarette smoking in a population-based cohort. Am J Public Health 2006;96(2):309–14. [7] Giglia R, Binns CW, Alfonso H. Maternal cigarette smoking and breastfeeding duration. Acta Paediatr 2006;95(11):1370–4. [8] Baxter J, Cooklin AR, Smith J. Which mothers wean their babies prematurely from full breastfeeding? An Australian cohort study. Acta Paediatr 2009;98(8):1274–7. [9] Thulier D, Mercer J. Variables associated with breastfeeding duration. J Obstet Gynecol Neonatal Nurs 2009;38(3):259–68. [10] Weiser TM, Lin M, Garikapaty V, Feyerharm RW, Bensyl DM, Zhu BP. Association of maternal smoking status with breastfeeding practices: Missouri, 2005. Pediatrics 2009;124(6):1603–10. [11] Higgins TM, Higgins ST, Heil SH, et al. Effects of cigarette smoking cessation on breastfeeding duration. Nicotine Tob Res 2010;12(5):483–8. [12] Collins BN, DiSantis KI, Nair US. Longer previous smoking abstinence relates to successful breastfeeding initiation among underserved smokers. Breastfeed Med 2011;6(6):385–91. [13] Phillips RM, Merritt TA, Goldstein MR, Deming DD, Slater LE, Angeles DM. Prevention of postpartum smoking relapse in mothers of infants in the neonatal intensive care unit. J Perinatol 2012;32(5):374–80. [14] Dennis CL, Gagnon A, Van HA, Dougherty G, Wahoush O. Prediction of duration of breastfeeding among migrant and Canadian-born women: results from a multi-center study. J Pediatr 2013;162(1):72–9. [15] Xu F, Binns C, Zhang H, Yang G, Zhao Y. Paternal smoking and breastfeeding in Xinjiang, PR China. J Hum Lact 2010;26(3):242–7. [16] Ma H, Bernstein L, Pike MC, Ursin G. Reproductive factors and breast cancer risk according to joint estrogen and progesterone receptor status: a meta-analysis of epidemiological studies. Breast Cancer Res 2006;8(4):R43. [17] Jordan SJ, Cushing-Haugen KL, Wicklund KG, Doherty JA, Rossing MA. Breast-feeding and risk of epithelial ovarian cancer. Cancer Causes Control 2012 June;23(6):919–27. [18] Gouveri E, Papanas N, Hatzitolios AI, Maltezos E. Breastfeeding and diabetes. Curr Diabetes Rev 2011 March;7(2):135–42. [19] Duijts L, Ramadhani MK, Moll HA. Breastfeeding protects against infectious diseases during infancy in industrialized countries. A systematic review. Matern Child Nutr 2009;5(3):199–210. [20] Amir LH. Maternal smoking and reduced duration of breastfeeding: a review of possible mechanisms. Early Hum Dev 2001;64(1):45–67. [21] Amir LH, Donath SM. Does maternal smoking have a negative physiological effect on breastfeeding? The epidemiological evidence. Birth 2002;29(2):112–23. [22] Donath SM, Amir LH. The relationship between maternal smoking and breastfeeding duration after adjustment for maternal infant feeding intention. Acta Paediatr 2004;93(11):1514–8. [23] Amir LH, Donath SM. Does maternal smoking have a negative physiological effect on breastfeeding? The epidemiological evidence. Breastfeed Rev 2003;11(2):19–29. [24] Amir LH, Donath SM. Maternal diet and breastfeeding: a case for rethinking physiological explanations for breastfeeding determinants. Early Hum Dev 2012;88(7):467–71. [25] Vio F, Salazar G, Infante C. Smoking during pregnancy and lactation and its effects on breast-milk volume. Am J Clin Nutr 1991;54(6):1011–6. [26] Hopkinson JM, Schanler RJ, Fraley JK, Garza C. Milk production by mothers of premature infants: influence of cigarette smoking. Pediatrics 1992;90(6):934–8. [27] Andersen AN, Lund-Andersen C, Larsen JF, et al. Suppressed prolactin but normal neurophysin levels in cigarette smoking breast-feeding women. Clin Endocrinol (Oxf) 1982;17(4):363–8. [28] Andersen AN, Ronn B, Tjonneland A, Djursing H, Schioler V. Low maternal but normal fetal prolactin levels in cigarette smoking pregnant women. Acta Obstet Gynecol Scand 1984;63(3):237–9. [29] Bremme K, Lagerstrom M, Andersson O, Johansson S, Eneroth P. Influences of maternal smoking and fetal sex on maternal serum oestriol, prolactin, hCG, and hPI levels. Arch Gynecol Obstet 1990;247(2):95–103. [30] Andersen AN, Semczuk M, Tabor A. Prolactin and pituitary-gonadal function in cigarette smoking infertile patients. Andrologia 1984;16(5):391–6. [31] Baron JA, Bulbrook RD, Wang DY, Kwa HG. Cigarette smoking and prolactin in women. Br Med J (Clin Res Ed) 1986;293(6545):482–3. [32] Berta L, Frairia R, Fortunati N, Fazzari A, Gaidano G. Smoking effects on the hormonal balance of fertile women. Horm Res 1992;37(1–2):45–8. [33] Glintborg D, Mumm H, Hougaard DM, Ravn P, Andersen M. Smoking is associated with increased adrenal responsiveness, decreased prolactin levels and a more adverse lipid profile in 650 white patients with polycystic ovary syndrome. Gynecol Endocrinol 2012;28(3):170–4. [34] Weigert M, Hofstetter G, Kaipl D, et al. The effect of smoking on oocyte quality and hormonal parameters of patients undergoing in vitro fertilization-embryo transfer. J Assist Reprod Genet 1999;16(6):287–93. [35] Ben-Jonathan N, Hugo ER, Brandebourg TD, LaPensee CR. Focus on prolactin as a metabolic hormone. Trends Endocrinol Metab 2006;17(3):110–6. [36] Gabay MP. Galactogogues: medications that induce lactation. J Hum Lact 2002;18(3):274–9. [37] Jedrychowski W, Perera F, Mroz E, et al. Prenatal exposure to passive smoking
586
[38]
[39]
[40]
[41]
[42]
[43] [44]
[45]
B. Bahadori et al. / Medical Hypotheses 81 (2013) 582–586 and duration of breastfeeding in nonsmoking women: krakow inner city prospective cohort study. Arch Gynecol Obstet 2008;278(5):411–7. Sharp BM, Beyer HS. Rapid desensitization of the acute stimulatory effects of nicotine on rat plasma adrenocorticotropin and prolactin. J Pharmacol Exp Ther 1986;238(2):486–91. Sharp BM, Beyer HS, Levine AS, Morley JE, McAllen KM. Attenuation of the plasma prolactin response to restraint stress after acute and chronic administration of nicotine to rats. J Pharmacol Exp Ther 1987;241(2):438–42. Hulihan-Giblin BA, Lumpkin MD, Kellar KJ. Acute effects of nicotine on prolactin release in the rat: agonist and antagonist effects of a single injection of nicotine. J Pharmacol Exp Ther 1990;252(1):15–20. Hulihan-Giblin BA, Lumpkin MD, Kellar KJ. Effects of chronic administration of nicotine on prolactin release in the rat: inactivation of prolactin response by repeated injections of nicotine. J Pharmacol Exp Ther 1990;252(1):21–5. Matta SG, Sharp BM. The role of the fourth cerebroventricle in nicotinestimulated prolactin release in the rat: involvement of catecholamines. J Pharmacol Exp Ther 1992;260(3):1285–91. Terkel J, Blake CA, Hoover V, Sawyer CH. Pup survival and prolactin levels in nicotine-treated lactating rats. Proc Soc Exp Biol Med 1973;143(4):1131–5. Fuxe K, Janson AM, Jansson A, Andersson K, Eneroth P, Agnati LF. Chronic nicotine treatment increases dopamine levels and reduces dopamine utilization in substantia nigra and in surviving forebrain dopamine nerve terminal systems after a partial di-mesencephalic hemitransection. Naunyn Schmiedebergs Arch Pharmacol 1990;341(3):171–81. Rasmussen DD. Effects of chronic nicotine treatment and withdrawal on hypothalamic proopiomelanocortin gene expression and neuroendocrine regulation. Psychoneuroendocrinology 1998 April;23(3):245–59.
[46] Reymond MJ, Porter JC. Involvement of hypothalamic dopamine in the regulation of prolactin secretion. Horm Res 1985;22(3):142–52. [47] Shieh KR, Pan JT. Nicotinic control of tuberoinfundibular dopaminergic neuron activity and prolactin secretion: diurnal rhythm and involvement of endogenous opioidergic system. Brain Res 1997;756(1–2):266–72. [48] Andersson K, Eneroth P, Fuxe K, Mascagni F, Agnati LF. Effects of chronic exposure to cigarette smoke on amine levels and turnover in various hypothalamic catecholamine nerve terminal systems and on the secretion of pituitary hormones in the male rat. Neuroendocrinology 1985;41(6):462–6. [49] Fuxe K, Andersson K, Eneroth P, Harfstrand A, Agnati LF. Neuroendocrine actions of nicotine and of exposure to cigarette smoke: medical implications. Psychoneuroendocrinology 1989;14(1–2):19–41. [50] Rosecrans JA, Hendry JS, Hong JS. Biphasic effects of chronic nicotine treatment on hypothalamic immunoreactive beta-endorphin in the mouse. Pharmacol Biochem Behav 1985;23(1):141–3. [51] Deyo SN, Swift RM, Miller RJ. Morphine and endorphins modulate dopamine turnover in rat median eminence. Proc Natl Acad Sci USA 1979;76(6):3006–9. [52] Mineur YS, Abizaid A, Rao Y, et al. Nicotine decreases food intake through activation of POMC neurons. Science 2011;332(6035):1330–2. [53] Shaw D, Al’Absi M. Blunted opiate modulation of prolactin response in smoking men and women. Pharmacol Biochem Behav 2010;95(1):1–5. [54] Coleman DT, Bancroft C. Nicotine acts directly on pituitary GH3 cells to inhibit prolactin promoter activity. J Neuroendocrinol 1995;7(10):785–9. [55] Riediger ND, Shooshtari S, Moghadasian MH. The influence of sociodemographic factors on patterns of fruit and vegetable consumption in Canadian adolescents. J Am Diet Assoc 2007;107(9):1511–8.