Acessibilidade / Reportar erro

Morningness/eveningness in gestational diabetes mellitus: clinical characteristics and maternal-neonatal outcomes

ABSTRACT

Objective:

This study aims to evaluate the impact of morning-evening preference in pregnancy outcomes in gestational diabetes mellitus (GDM).

Materials and methods:

This is a prospective cohort study of 2nd-3rd trimester GDM outpatient care in Fortaleza, Brazil (2018-2020). Eveningness was defined by the Horne-Östberg Morningness-Eveningness-Questionnaire (MEQ ≤ 41). Furthermore, we obtained a 7-day actigraphic register. Subjective sleep quality, daytime somnolence, insomnia, fatigue and depressive symptoms were also evaluated. Associations with pregnancy outcomes were investigated.

Results:

Among 305 patients with GDM, evening preference was found in 21 (6.9%). Patients with evening preference had worse sleep quality (p < 0.01), greater severity of insomnia (p < 0.005), fatigue (p < 0.005) and depressive symptoms (<0.009). Evening chronotype was associated with preeclampsia [p = 0.01; OR = 0.27; CI 0.09-0.79] and a greater need for admission to a neonatal intensive care unit (NICU) [p = 0.02; OR = 0.23; CI .0.06-0.80]. A lower MEQ score confirmed an association with preeclampsia [p = 0.002; OR = 0.94; CI 0.90-0.97] and this was maintained after controlling for age, arterial hypertension, sleep quality, fatigue and depressive symptoms [p < 005; OR = 0.91; CI 0.87-0.95].

Conclusion:

In GDM, patients with evening preference had worse sleep quality, more insomnia, fatigue, and depressive symptoms. Furthermore, eveningness was independently associated with preeclampsia. These results indicate the important role of eveningness in adverse pregnancy outcomes.

Keywords:
Circadian rhythm; pregnancy outcome; diabetes, gestational; sleep wake disorders; actigraphy

INTRODUCTION

The circadian rhythms of body functions are controlled by a central clock in the suprachiasmatic nucleus (SCN) of the hypothalamus and peripheral clocks located throughout body tissues. Light and food cues entrain these clocks to the time of day, and this synchronicity regulates a variety of physiological processes such as body temperature, sleep-wake cycles, blood pressure (BP) and glucose metabolism. Pregnancy has its cyclical characteristics and relates to a variable expression of the circadian timekeeping system (11 Olcese J. Circadian Clocks and Pregnancy. Front Endocrinol (Lausanne). 2014;5:123.,22 Wharfe MD, Wyrwoll CS, Waddell BJ, Mark PJ. Pregnancy-induced changes in the circadian expression of hepatic clock genes: implications for maternal glucose homeostasis. Am J Physiol Endocrinol Metab. 2016;311:E575-86.). Hence, a functional circadian system is necessary during gestation (33 Miller BH, Takahashi JS. Central Circadian Control of Female Reproductive Function. Front Endocrinol (Lausanne). 2014;4:195.). In mice, disruption of endogenous circadian timekeeping dramatically reduces pregnancy success (44 Summa KC, Vitaterna MH, Turek FW. Environmental perturbation of the circadian clock disrupts pregnancy in the mouse. PLoS One. 2012;7:e37668.). Circadian system alterations may also be associated with increasing risk of adverse pregnancy outcomes in humans (55 Reschke L, McCarthy R, Herzog ED, Fay JC, Jungheim ES, England SK. Chronodisruption: An untimely cause of preterm birth? Best Pract Res Clin Obstet Gynaecol. 2018;52:60-7.,66 McCarthy R, Jungheim ES, Fay JC, Bates K, Herzog ED, England SK. Riding the Rhythm of Melatonin Through Pregnancy to Deliver on Time. Front Endocrinol (Lausanne). 2019;10:616.). The sleep-wake cycle is a circadian behavioral expression that may be importantly associated with pregnancy outcomes (11 Olcese J. Circadian Clocks and Pregnancy. Front Endocrinol (Lausanne). 2014;5:123.). Nevertheless, few studies have explored its role in pregnancy.

Important adaptations in the metabolic system are necessary to balance fetal and placental demands with the maintenance of maternal homeostasis (22 Wharfe MD, Wyrwoll CS, Waddell BJ, Mark PJ. Pregnancy-induced changes in the circadian expression of hepatic clock genes: implications for maternal glucose homeostasis. Am J Physiol Endocrinol Metab. 2016;311:E575-86.). Glucose metabolism, the main energetic substrate used by the fetus, obeys circadian oscillation, and regulates according to a large number of genes encoding glucoregulatory enzymes of rhythmic expression (77 Jones CT, Rolph TP. Metabolism during fetal life: a functional assessment of metabolic development. Physiol Rev. 1985;65:357-430.). Consequently, circadian rhythm disruption is associated with metabolic imbalance (11 Olcese J. Circadian Clocks and Pregnancy. Front Endocrinol (Lausanne). 2014;5:123.). Disorder of glucose metabolism is a common complication affecting 7.5% to 27.0% of pregnancies worldwide. Hyperglycemia first detected during pregnancy leads to a greater risk for adverse outcomes, notably, infants large for gestational age or macrosomia and maternal pre-eclampsia/hypertensive disorders. Disturbance in glucose metabolism is also related to preterm delivery (88 Diagnostic criteria and classification of hyperglycaemia first detected in pregnancy: A World Health Organization Guideline. Diabetes Res Clin Pract. 2014;103(3):341-63.). Importantly, low and middle-income patients are more affected, and this can be related to unhealthy diet and lifestyle factors (99 Baz B, Riveline JP, Gautier JF. Endocrinology of pregnancy: Gestational diabetes mellitus: definition, aetiological and clinical aspects. Eur J Endocrinol. 2016;174:R43-51.). Therefore, events associated with maternal/neonatal risk in Gestational Diabetes Mellitus (GDM) must be identified and addressed.

Sleep-wake alterations, common during gestation (1010 Warland J, Dorrian J, Morrison JL, O’Brien LM. Maternal sleep during pregnancy and poor fetal outcomes: A scoping review of the literature with meta-analysis. Sleep Med Rev. 2018;41:197-219.), are related to poor pregnancy outcomes. An extensive review and meta-analysis examining sleep duration in pregnancy, involving 18,203 subjects at baseline and 1294 GDM cases with follow-up, showed that poor sleep quality and extremes of sleep duration during pregnancy are associated with the development of gestational diabetes (1111 Xu YH, Shi L, Bao YP, Chen SJ, Shi J, Zhang RL, et al. Association between sleep duration during pregnancy and gestational diabetes mellitus: a meta-analysis. Sleep Med. 2018;52:67-74.).

Other sleep related variables, e.g., chronotype, may be associated with maternal and fetal outcomes in GDM patients. Chronotype is a variation in the behavior of the individual circadian rhythm that expresses different forms of synchronization of the so-called biological clock. They determine the individual’s predisposition to feel peak energy or tiredness, according to the time of day, influencing well-being and health. Morning-evening preference influences mood, eating habits, body temperature and other biological functions. For instance, evening preference has been associated with night eating and obesity (1212 Melo MCA, de Oliveira Ribeiro M, de Araújo CFC, de Mesquita LMF, de Bruin PFC, de Bruin VMS. Night eating in bipolar disorder. Sleep Med. 2018;48:49-52.). Evening preference is also connected with anxiety-depression and symptom severity in bipolar patients (1313 Melo MC, Garcia RF, Araújo CF de, Luz JH, Bruin PF de, Bruin VM de. Chronotype in bipolar disorder: an 18-month prospective study. Braz J Psychiatry. 2020;42:68-71.). In fact, the role of sleep/wake rhythm in GDM is yet to be better clarified.

The objective of this study is to evaluate morning-evening preference in patients with GDM, the association with clinical variables and maternal/neonatal outcomes.

MATERIALS AND METHODS

Study population and design

This was a longitudinal and prospective cohort study of GDM patients at the Center for Diabetes and Hypertension (CIDH-CE) in Fortaleza, Brazil. This is an institutional referral center unit serving approximately 600 outpatient pregnant women with diabetes per year. The study population was derived as a non-probability sampling, consecutively recruited over a 23-month period, from March 2018 to February 2020. Women with singleton pregnancy, during the second or third trimester, 20 years of age or older, diagnosed with GDM per IADPSG criteria (1414 International Association of Diabetes and Pregnancy Study Groups Consensus Panel, Metzger BE, Gabbe SG, Persson B, Buchanan TA, Catalano PA, et al. International Association of Diabetes and Pregnancy Study Groups Recommendations on the Diagnosis and Classification of Hyperglycemia in Pregnancy. Diabetes Care. 2010;33:676–82.) were invited to participate. The study was performed in accordance with the ethical guidelines of the 1975 Declaration of Helsinki and approved by the Ethics Committee of the Federal University of Ceará – COMEPE-UFC ethics board (2.521.562). A written informed consent was obtained from all patients after full explanation of the purpose of the study.

Data collection

Three trained paramedical professionals obtained data using face-to-face interviews. Socio-demographics, clinical and obstetric information were collected using a structured questionnaire. Information about maternal and gestational age, parity and previous history of sleep or mood disturbances were derived from patient interviews and further confirmed through chart review. BMI and blood pressure information were verified. Objective sleep parameters such as sleep duration, efficiency and sleep mid-point were obtained through 7 days of actigraphy recording in 53 patients (Motionlogger, Ambulatory Monitoring Inc., Ardsley, NY, USA). Data regarding pregnancy and neonatal outcomes were collected in the first post-partum visit and confirmed through chart review.

Assessments of sleep, mood and chronotype

In this work, the Horne-Östberg Morning-Evening Questionnaire (MEQ), Portuguese version (1515 Benedito-Silva AA, Menna-Barreto L, Marques N, Tenreiro S. A self-assessment questionnaire for the determination of morningness-eveningness types in Brazil. Prog Clin Biol Res. 1990;341B:89-98.), was used to establish the chronotype. This is a self-assessment questionnaire developed to evaluate circadian rhythm and sleep rhythm patterns. The sum of all scores in MEQ gives a result ranging from 16 to 86; scores of 41 and below indicate “evening types”, scores of 59 and above indicate “morning types”, and scores between 42-58 indicate “intermediate types”, Essentially, low scores reflect more of an evening orientation, whereas high scores reflect a morning orientation. In this study, we used a cut off of ≤ 41 to define eveningness (1616 Horne JA, Ostberg O. A self-assessment questionnaire to determine morningness-eveningness in human circadian rhythms. Int J Chronobiol. 1976;4:97-110.). Demographic and clinical information included gestation data, comorbidities, previous history of depressive symptoms and insomnia.

Additionally, GDM patients completed a sleep log and wore an activity monitor (Motionlogger, Ambulatory Monitoring Inc., Ardsley, NY, USA) on their non-dominant wrist for five to seven consecutive 24-hour periods, including a weekend, to record activity levels at 1-minute intervals (zero crossing mode). Activity data were used to calculate (Action W-2 software; Ambulatory Monitoring) the following parameters: sleep onset time (the first of at least three consecutive minutes with an activity frequency count of 0); sleep offset time (the final activity frequency count of 0 before waking in the morning); total sleep time (TST; sleep duration minus the sum of the durations of all awakenings); sleep midpoint (the midpoint between sleep onset and sleep offset), and sleep efficiency (TST/sleep duration×100). The bedtime and waking time from each subject’s daily sleep log were used to guide the analysis of the actigraphy data recording. Additional behavioral questionnaires evaluated sleep quality (Pittsburgh Sleep Questionnaire Index – PSQI) (1717 Buysse DJ, Reynolds CF 3rd, Monk TH, Berman SR, Kupfer DJ. Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research. Psychiatry Res. 1989;28(2):193-213.), daytime sleepiness (Epworth Sleepiness Scale – ESS) (1818 Johns MW. A new method for measuring daytime sleepiness: the Epworth sleepiness scale. Sleep. 1991;14:540-5.), insomnia (Insomnia Severity Index – ISI) (1919 Morin CM, Belleville G, Bélanger L, Ivers H. The Insomnia Severity Index: psychometric indicators to detect insomnia cases and evaluate treatment response. Sleep. 2011;34:601-8.), fatigue (Fatigue Severity Scale) (2020 Krupp LB, LaRocca NG, Muir-Nash J, Steinberg AD. The fatigue severity scale. Application to patients with multiple sclerosis and systemic lupus erythematosus. Arch Neurol. 1989;46:1121-3.) and depressive symptoms (Edinburgh Postnatal Depression Scale) (2121 Cox JL, Holden JM, Sagovsky R. Detection of Postnatal Depression. Br J Psychiatry. 1987;150:782-6.). All instruments were validated in the Brazilian Portuguese language and were previously used in pregnancy. Low educational level was defined if there was < 8 years of schooling. Low family income if < U$ 420.00/month and sedentary lifestyle if < 150 minutes activity per week was registered (2222 Meander L, Lindqvist M, Mogren I, Sandlund J, West CE, Domellöf M. Physical activity and sedentary time during pregnancy and associations with maternal and fetal health outcomes: an epidemiological study. BMC Pregnancy and Childbirth. 2021;21:166.).

Assessments of pregnancy outcomes

Maternal adverse outcomes included gestational weight gain, gestational age at delivery determined by the last menstrual period or ultrasound dating, Caesarian delivery, gestational hypertension and preeclampsia (2323 Burton GJ, Redman CW, Roberts JM, Moffett A. Pre-eclampsia: pathophysiology and clinical implications. BMJ. 2019;366:l2381.), pharmacological treatment for DM, and postpartum glucose tolerance status. Neonatal outcomes included head circumference, birth weight, Apgar score (5 and 10 minutes), being small for gestational age (SGA) defined as a birth weight < 10th percentile for gestational age by gender, or large for gestational age (LGA) defined as birth weight larger than the 90th percentile for gestational age by gender (2424 Villar J, Cheikh Ismail L, Victora CG, Ohuma EO, Bertino E, Altman DG, et al. International standards for newborn weight, length, and head circumference by gestational age and sex: the Newborn Cross-Sectional Study of the INTERGROWTH-21st Project. Lancet. 2014;384:857-68.), macrosomia defined as birth weight greater than more than 4,000 grams (8 pounds, 13 ounces) (2525 Macrosomia. Obstet Gynecol. 2020;135:e18-35.), need for a neonatal intensive care unit (ICU) and prematurity defined as babies born alive before 37 weeks of pregnancy.

Statistical methods

Data are presented as mean/standard deviation or frequency when appropriate. Fisher’s exact test examined the associations between categorical variables. A t test compared variables with normality and equality of variance. The Mann-Whitney U test was used for between groups comparison of behavioral scores. Factors associated with eveningness were examined using regression analyses. All variables were initially examined in univariate models. To control for confounding factors, we then performed multivariate regression analysis (Enter method) including variables that showed association in the univariate models (p < 0.2). We used a Poisson regression with robust model to calculate relative risk (RR). SPSS version 17.5.1 J software for Windows (SPSS Inc., Tokyo) was used for the above statistical analyses. A P value of less than 0.05 was considered a statistically significant difference.

RESULTS

Clinical and demographic characteristics are specified in Table 1. The study involved 305 patients with GDM. Evening preference (MEQ ≤ 41) was found in 21 patients (6.9%). In detail, MEQ scores revealed that patient’s preference or chronotype were classified as morning type (N = 151; 49.5%), intermediate type (N = 133; 43.6%), and evening type (N = 21; 6.9%). In this study, evening types were compared to morning and intermediate types. As expected, actigraphic study showed a sleep delayed mid-point (p = 0.04) for the evening preference patients (Table 2). Patients with evening preference were younger, had more unstable marital status and insomnia before pregnancy. Abortion was more frequent in the older morning and intermediate types (Table 1). In addition, GDM patients with evening preference had worse sleep quality (PSQI), greater insomnia severity (ISI), more fatigue, and depressive symptoms (EDPS) (Table 2). Maternal and neonatal outcomes are described in Table 3. The presence of an evening chronotype was associated with preeclampsia [p = 0.01; OR = 0.27; CI 0.09-0.79] and a higher need for neonatal intensive care unit (NICU) treatment after birth [p = 0.02; OR = 0.23; CI .0.06-0.80]. A trend for preterm delivery was observed in GDM patients with evening chronotypes [p = 0.07; OR = 0.36; CI 0.12-1.10]. Of note, the BMI was similar among evening and non-evening preference women (Table 1), and there was no difference in the prevalence of obesity (adjusted for gestational age) among women regarding the presence or absence of pre-eclampsia (57.1% versus 44,6%; p = 0.14).

Table 1
Characteristics of patients with Gestational Diabetes Mellitus according to chronotype (Morning/Indifferent Intermediate Horne-Östberg MEQ ≥ 41 and Eveningness Horne-Östberg MEQ < 41)
Table 2
Behavioral Scales and Actigraphy Data in Pregnancy with Gestational Diabetes (mean ± SD; range)
Table 3
Pregnancy outcomes in Gestational Diabetes Mellitus according to chronotype (Morning & Intermediate – Horne-Östberg MEQ > 41 vs. Eveningness – Horne-Östberg MEQ ≤ 41)

A multivariate logistic regression analysis (Poisson robust model) showed that patients with eveningness and arterial hypertension had a higher relative risk for pre-eclampsia, and these results were maintained after controlling for age, poor sleep quality, fatigue and depressive symptoms: eveningness [p < 0.005; RR = 0.94; CI: 0.91-0.98] and hypertension [p < 0.005; RR = 4.6; CI: 2.48-8.54] (Table 4). A linear regression analysis confirmed that lower MEQ scores were associated with preeclampsia [p = 0.002; 0.94; CI 0.90-0.97] (Figure 1). The accuracy, specificity and sensitivity of this model are presented in Figure 2.

Table 4
Logistic regression multivariate analysis (using Poisson robust model) of factors influencing pre-eclampsia before and after controlling for variables (p < 0.2)
Figure 1
Eveningness (lower MEQ score) is associated with preeclampsia in gestational diabetes mellitus.
Figure 2
Accuracy, specificity and sensitivity of this model.

DISCUSSION

This study is the first to evaluate sleep alterations and the chronotype in a significant group of women with GDM. The present data confirm that sleep alterations are common in GDM. Moreover, patients with evening preference had worse sleep quality, increased severity of insomnia, depressive symptoms, and fatigue. Importantly, eveningness was associated with the development of preeclampsia and a greater need for NICU. These findings indicate that the evening chronotype has an unfavorable association with maternal and neonatal outcomes.

In this work, the evening chronotype was found in 6.9% of patients, a small percentage of the study population. Eveningness is generally observed in approximately one fifth to one third of the population in Brazil and is naturally more expressed in young individuals (2626 von Schantz M, Taporoski TP, Horimoto ARVR, Duarte NE, Vallada H, Krieger JE, et al. Distribution and heritability of diurnal preference (chronotype) in a rural Brazilian family-based cohort, the Baependi study. Sci Rep. 2015;5:9214.). Lower levels of evening chronotype have also been reported in other adult population studies (Korea: 5.9%; New Zealand: 5.6%) (2727 Paine SJ, Gander PH, Travier N. The epidemiology of morningness/eveningness: Influence of age, gender, ethnicity, and socioeconomic factors in adults (30-49 years). J Biol Rhythms. 2006;21:68-76.,2828 Yu JH, Yun CH, Ahn JH, Suh S, Cho HJ, Lee SK, et al. Evening chronotype is associated with metabolic disorders and body composition in middle-aged adults. J Clin Endocrinol Metab. 2015;100:1494-502.). Research indicates that pregnancy induces an earlier chronotype in both mice and women (2929 Martin-Fairey CA, Zhao P, Wan L, Roenneberg T, Fay J, Ma X, et al. Pregnancy Induces an Earlier Chronotype in Both Mice and Women. J Biol Rhythms. 2019;34:323-31.) and this might contribute to the low prevalence of eveningness presently found. In partial agreement with our findings, a report from Finland evaluating the chronotype of 1,653 normal pregnant women using a shortened version of the morningness-eveningness questionnaire, described eveningness in about 13% of patients (3030 Merikanto I, Paavonen EJ, Saarenpää-Heikkilä O, Paunio T, Partonen T. Eveningness associates with smoking and sleep problems among pregnant women. Chronobiol Int. 2017;34:650-8.).

The present study was conducted in Northeastern Brazil, which has a latitudinal cline favoring generous and stable sunlight exposure throughout the year. Sunlight exposure is considered a strong zeitgeber that entrains circadian rhythms. However, it must be kept in mind that multiple zeitgebers interact to synchronize the circadian rhythms. Despite the influence of daylight exposure, artificial light, social interaction, physical exercise, and feeding patterns are also implicated as important time cues (3131 Leocadio-Miguel MA, Louzada FM, Duarte LL, Areas RP, Alam M, Freire MV, et al. Latitudinal cline of chronotype. Sci Rep. 2017;7:5437.). Ontogenetic characteristics of chronotype have formerly been recognized. For instance, younger individuals have a clear tendency toward eveningness, whereas older age is strongly associated with morningness (3131 Leocadio-Miguel MA, Louzada FM, Duarte LL, Areas RP, Alam M, Freire MV, et al. Latitudinal cline of chronotype. Sci Rep. 2017;7:5437.). In fact, chronotype has been accepted to be maintained until the age of 35: from this age and, thereafter, morningness increases. Evidence indicates that females reach the maximum of their eveningness sooner than males and this gender effect disappears around the age of 50, the average age of menopause (3232 Randler C, Engelke J. Gender differences in chronotype diminish with age: a meta-analysis based on morningness/chronotype questionnaires. Chronobiol Int. 2019;36:888-905.). In accordance with this concept, a younger age was also found among pregnant women with evening preference in this group. Studies involving larger samples may further clarify differences in circadian behavior regarding pregnancy.

Previously, we compared the circadian behavior of GDM patients with 93 non-GDM pregnant women with similar gestational age (control group). The GDM group was older and more obese. Overall, a higher prevalence of morning preference in both groups was observed (52%), with a non-significant difference in evening preference rates: (GDM 6.1% vs. non-GDM 3.3%, P = 0.2). Interestingly, a linear analysis of MEQ showed a higher score in non-GDM patients, suggesting a trend toward a morning preference in the control group (P = 0.05).

Evening chronotype, independent of the presence of diabetes or other comorbidities, has been associated with a greater risk of sleep alterations and mood symptoms [13]. In a previous report on non-diabetic pregnancy, evening chronotype was not related to adverse outcomes nor gestational diabetes (3333 Punjala-Patel A, Rowe D, Singleton M, Street L. Early Bird or Night Owl? Investigating the Relationship Between Chronotype and Pregnancy Complications [11L]. Obstet Gynecol. 2020;135:127S.). Conversely, another study retrospectively evaluating 313 pregnant women showed that lower MEQ was associated with preterm delivery and preeclampsia (3434 Takmaz T, Unal B, Ozcan P, Arici Halici BN, Gorchiyeva I, Gokmen Karasu AF, et al. Are chronotype and subjective sleep quality associated with preeclampsia and preterm birth? Biol Rhythm Res. 2020;00:1-13.). Furthermore, evening chronotype has also been related to sleep problems and unhealthy life habits during pregnancy (3030 Merikanto I, Paavonen EJ, Saarenpää-Heikkilä O, Paunio T, Partonen T. Eveningness associates with smoking and sleep problems among pregnant women. Chronobiol Int. 2017;34:650-8.). Importantly, in our analysis, GDM patients with evening chronotype had a history of insomnia before pregnancy and more unstable marital status. It could be hypothesized that eveningness was present before pregnancy.

In partial agreement with our findings, a previous study observed an association between circadian rhythm disorders and pre-eclampsia in shift workers (3535 Ditisheim AJ, Dibner C, Philippe J, Pechère-Bertschi A. Biological Rhythms and Preeclampsia. Front Endocrinol (Lausanne). 2013;4:47.). A key strength of our study is that it is the first to report an association of preeclampsia and evening chronotype in GDM pregnancy. A connection exists between sleep disorders, circadian rhythm dysfunction, insulin resistance and arterial hypertension. The interrelationships between hypertensive syndromes during pregnancy and rhythm disorders have aroused much interest from the scientific community. An extensive study showed that arterial hypertension was related to long and short sleep duration (3636 Merikanto I, Lahti T, Puolijoki H, Vanhala M, Peltonen M, Laatikainen T, et al. Associations of chronotype and sleep with cardiovascular diseases and type 2 diabetes. Chronobiol Int. 2013;30:470-7.). Interestingly, in the present work, arterial hypertension and MEQ scores were the only independent measures associated with preeclampsia.

Blood pressure varies over a 24-hour period following a circadian rhythm profile. Healthy individuals experience a 10%-20% decrease in BP at night (3737 Douma LG, Gumz ML. Circadian clock-mediated regulation of blood pressure. Free Radic Biol Med. 2018;119:108-14.). The loss of this rhythm has been shown to be an initial event responsible for cardiovascular complications both inside and outside pregnancy, and the suppression of a nighttime pressure drop is a hallmark of eclamptic syndromes in pregnancy (3838 Soydinc HE, Davutoglu V, Sak ME, Ercan S, Evsen MS, Kaya H, et al. Circadian Variation of Blood Pressure Is Impaired in Normotensive Pregnant Women with Gestational Diabetes Mellitus. Clin Exp Hypertens. 2013;35:128-33.,3939 Hayase M, Shimada M, Seki H. Sleep quality and stress in women with pregnancy-induced hypertension and gestational diabetes mellitus. Women Birth. 2014;27:190-5.). Therefore, the hypothesis that the misalignment of circadian rhythm would be a potential risk factor for pre-eclampsia is intriguing and could offer a new field of investigation and approach to this disease related to adverse pregnancy outcomes.

Depressive symptoms are common and a genuine concern in GDM (4040 Damé P, Cherubini K, Goveia P, Pena G, Galliano L, Façanha C, et al. Depressive Symptoms in Women with Gestational Diabetes Mellitus: The LINDA-Brazil Study. J Diabetes Res. 2017;2017:1-6.). Sleep disorders are also widely recognized as having an adverse effect on glucose metabolism and as a risk factor for the development of complications in pregnancy, including GDM (4141 Gooley JJ, Mohapatra L, Twan DCK. The role of sleep duration and sleep disordered breathing in gestational diabetes mellitus. Neurobiol Sleep Circadian Rhythms. 2018;4:34-43.). Our study confirms a relationship of evening chronotype with sleep and mood disorders similar to previous reports on other clinical conditions (4242 Au J, Reece J. The relationship between chronotype and depressive symptoms: A meta-analysis. J Affect Disord. 2017;218:93-104.). Importantly, chronotype influences neuroendocrine secretion, alertness, cognition, feeding, renal, ovary and pulmonary function, and many of these functions are connected to glucose control and other metabolic dysfunction (4343 Aguilar-Galarza A, García-Gasca T, Mejía C, Díaz-Muñoz M, Pérez-Mendoza M, Anaya-Loyola MA, et al. “Evening chronotype associates with increased triglyceride levels in young adults in two independent populations”. Clin Nutr. 2021;40(4):2373-80.). In this study, depressive symptoms were not associated with hypertensive syndromes in pregnancy or a greater need for NICU admission. A suggestion on how chronotype, gestational diabetes, other key variables and outcomes might be related is illustrated in a theoretical model (Figure 3).

Figure 3
A theoretical model: The relationship among evening chronotype, gestational diabetes, other key variables and outcomes.

Limitations to this study must be acknowledged. A reduced number of GDM patients with evening preference undermined the power of the analysis. Possibly, an explanation for these findings is the trend for morning preference in pregnancy. Actigraphy data confirmed a delayed sleep mid-term point in GDM patients with evening preference. Furthermore, MEQ scores were independently associated with pre-eclampsia.

All these findings indicate a negative influence of evening chronotype in maternal-neonatal outcomes e.g., preeclampsia and a greater need for NICU admission in GDM. Eveningness was related to poor sleep quality, higher severity of insomnia, depressive symptoms and fatigue. Importantly, chronotype can be established with simple and affordable tasks during routine prenatal care and could provide a feasible way in the prediction of adverse pregnancy outcomes. Attention to healthy habits including morning exposure to bright light, exercise and a reduction of screen blue light at night may improve the care of GDM patients with evening preference.

  • Declarations: professor P. F. C. de Bruin and Prof. V. M. S. de Bruin receive support from CNPq. All other authors have nothing to declare.
  • Funding: no funding was received

Acknowledgments and funding: no funding was received.

REFERENCES

  • 1
    Olcese J. Circadian Clocks and Pregnancy. Front Endocrinol (Lausanne). 2014;5:123.
  • 2
    Wharfe MD, Wyrwoll CS, Waddell BJ, Mark PJ. Pregnancy-induced changes in the circadian expression of hepatic clock genes: implications for maternal glucose homeostasis. Am J Physiol Endocrinol Metab. 2016;311:E575-86.
  • 3
    Miller BH, Takahashi JS. Central Circadian Control of Female Reproductive Function. Front Endocrinol (Lausanne). 2014;4:195.
  • 4
    Summa KC, Vitaterna MH, Turek FW. Environmental perturbation of the circadian clock disrupts pregnancy in the mouse. PLoS One. 2012;7:e37668.
  • 5
    Reschke L, McCarthy R, Herzog ED, Fay JC, Jungheim ES, England SK. Chronodisruption: An untimely cause of preterm birth? Best Pract Res Clin Obstet Gynaecol. 2018;52:60-7.
  • 6
    McCarthy R, Jungheim ES, Fay JC, Bates K, Herzog ED, England SK. Riding the Rhythm of Melatonin Through Pregnancy to Deliver on Time. Front Endocrinol (Lausanne). 2019;10:616.
  • 7
    Jones CT, Rolph TP. Metabolism during fetal life: a functional assessment of metabolic development. Physiol Rev. 1985;65:357-430.
  • 8
    Diagnostic criteria and classification of hyperglycaemia first detected in pregnancy: A World Health Organization Guideline. Diabetes Res Clin Pract. 2014;103(3):341-63.
  • 9
    Baz B, Riveline JP, Gautier JF. Endocrinology of pregnancy: Gestational diabetes mellitus: definition, aetiological and clinical aspects. Eur J Endocrinol. 2016;174:R43-51.
  • 10
    Warland J, Dorrian J, Morrison JL, O’Brien LM. Maternal sleep during pregnancy and poor fetal outcomes: A scoping review of the literature with meta-analysis. Sleep Med Rev. 2018;41:197-219.
  • 11
    Xu YH, Shi L, Bao YP, Chen SJ, Shi J, Zhang RL, et al. Association between sleep duration during pregnancy and gestational diabetes mellitus: a meta-analysis. Sleep Med. 2018;52:67-74.
  • 12
    Melo MCA, de Oliveira Ribeiro M, de Araújo CFC, de Mesquita LMF, de Bruin PFC, de Bruin VMS. Night eating in bipolar disorder. Sleep Med. 2018;48:49-52.
  • 13
    Melo MC, Garcia RF, Araújo CF de, Luz JH, Bruin PF de, Bruin VM de. Chronotype in bipolar disorder: an 18-month prospective study. Braz J Psychiatry. 2020;42:68-71.
  • 14
    International Association of Diabetes and Pregnancy Study Groups Consensus Panel, Metzger BE, Gabbe SG, Persson B, Buchanan TA, Catalano PA, et al. International Association of Diabetes and Pregnancy Study Groups Recommendations on the Diagnosis and Classification of Hyperglycemia in Pregnancy. Diabetes Care. 2010;33:676–82.
  • 15
    Benedito-Silva AA, Menna-Barreto L, Marques N, Tenreiro S. A self-assessment questionnaire for the determination of morningness-eveningness types in Brazil. Prog Clin Biol Res. 1990;341B:89-98.
  • 16
    Horne JA, Ostberg O. A self-assessment questionnaire to determine morningness-eveningness in human circadian rhythms. Int J Chronobiol. 1976;4:97-110.
  • 17
    Buysse DJ, Reynolds CF 3rd, Monk TH, Berman SR, Kupfer DJ. Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research. Psychiatry Res. 1989;28(2):193-213.
  • 18
    Johns MW. A new method for measuring daytime sleepiness: the Epworth sleepiness scale. Sleep. 1991;14:540-5.
  • 19
    Morin CM, Belleville G, Bélanger L, Ivers H. The Insomnia Severity Index: psychometric indicators to detect insomnia cases and evaluate treatment response. Sleep. 2011;34:601-8.
  • 20
    Krupp LB, LaRocca NG, Muir-Nash J, Steinberg AD. The fatigue severity scale. Application to patients with multiple sclerosis and systemic lupus erythematosus. Arch Neurol. 1989;46:1121-3.
  • 21
    Cox JL, Holden JM, Sagovsky R. Detection of Postnatal Depression. Br J Psychiatry. 1987;150:782-6.
  • 22
    Meander L, Lindqvist M, Mogren I, Sandlund J, West CE, Domellöf M. Physical activity and sedentary time during pregnancy and associations with maternal and fetal health outcomes: an epidemiological study. BMC Pregnancy and Childbirth. 2021;21:166.
  • 23
    Burton GJ, Redman CW, Roberts JM, Moffett A. Pre-eclampsia: pathophysiology and clinical implications. BMJ. 2019;366:l2381.
  • 24
    Villar J, Cheikh Ismail L, Victora CG, Ohuma EO, Bertino E, Altman DG, et al. International standards for newborn weight, length, and head circumference by gestational age and sex: the Newborn Cross-Sectional Study of the INTERGROWTH-21st Project. Lancet. 2014;384:857-68.
  • 25
    Macrosomia. Obstet Gynecol. 2020;135:e18-35.
  • 26
    von Schantz M, Taporoski TP, Horimoto ARVR, Duarte NE, Vallada H, Krieger JE, et al. Distribution and heritability of diurnal preference (chronotype) in a rural Brazilian family-based cohort, the Baependi study. Sci Rep. 2015;5:9214.
  • 27
    Paine SJ, Gander PH, Travier N. The epidemiology of morningness/eveningness: Influence of age, gender, ethnicity, and socioeconomic factors in adults (30-49 years). J Biol Rhythms. 2006;21:68-76.
  • 28
    Yu JH, Yun CH, Ahn JH, Suh S, Cho HJ, Lee SK, et al. Evening chronotype is associated with metabolic disorders and body composition in middle-aged adults. J Clin Endocrinol Metab. 2015;100:1494-502.
  • 29
    Martin-Fairey CA, Zhao P, Wan L, Roenneberg T, Fay J, Ma X, et al. Pregnancy Induces an Earlier Chronotype in Both Mice and Women. J Biol Rhythms. 2019;34:323-31.
  • 30
    Merikanto I, Paavonen EJ, Saarenpää-Heikkilä O, Paunio T, Partonen T. Eveningness associates with smoking and sleep problems among pregnant women. Chronobiol Int. 2017;34:650-8.
  • 31
    Leocadio-Miguel MA, Louzada FM, Duarte LL, Areas RP, Alam M, Freire MV, et al. Latitudinal cline of chronotype. Sci Rep. 2017;7:5437.
  • 32
    Randler C, Engelke J. Gender differences in chronotype diminish with age: a meta-analysis based on morningness/chronotype questionnaires. Chronobiol Int. 2019;36:888-905.
  • 33
    Punjala-Patel A, Rowe D, Singleton M, Street L. Early Bird or Night Owl? Investigating the Relationship Between Chronotype and Pregnancy Complications [11L]. Obstet Gynecol. 2020;135:127S.
  • 34
    Takmaz T, Unal B, Ozcan P, Arici Halici BN, Gorchiyeva I, Gokmen Karasu AF, et al. Are chronotype and subjective sleep quality associated with preeclampsia and preterm birth? Biol Rhythm Res. 2020;00:1-13.
  • 35
    Ditisheim AJ, Dibner C, Philippe J, Pechère-Bertschi A. Biological Rhythms and Preeclampsia. Front Endocrinol (Lausanne). 2013;4:47.
  • 36
    Merikanto I, Lahti T, Puolijoki H, Vanhala M, Peltonen M, Laatikainen T, et al. Associations of chronotype and sleep with cardiovascular diseases and type 2 diabetes. Chronobiol Int. 2013;30:470-7.
  • 37
    Douma LG, Gumz ML. Circadian clock-mediated regulation of blood pressure. Free Radic Biol Med. 2018;119:108-14.
  • 38
    Soydinc HE, Davutoglu V, Sak ME, Ercan S, Evsen MS, Kaya H, et al. Circadian Variation of Blood Pressure Is Impaired in Normotensive Pregnant Women with Gestational Diabetes Mellitus. Clin Exp Hypertens. 2013;35:128-33.
  • 39
    Hayase M, Shimada M, Seki H. Sleep quality and stress in women with pregnancy-induced hypertension and gestational diabetes mellitus. Women Birth. 2014;27:190-5.
  • 40
    Damé P, Cherubini K, Goveia P, Pena G, Galliano L, Façanha C, et al. Depressive Symptoms in Women with Gestational Diabetes Mellitus: The LINDA-Brazil Study. J Diabetes Res. 2017;2017:1-6.
  • 41
    Gooley JJ, Mohapatra L, Twan DCK. The role of sleep duration and sleep disordered breathing in gestational diabetes mellitus. Neurobiol Sleep Circadian Rhythms. 2018;4:34-43.
  • 42
    Au J, Reece J. The relationship between chronotype and depressive symptoms: A meta-analysis. J Affect Disord. 2017;218:93-104.
  • 43
    Aguilar-Galarza A, García-Gasca T, Mejía C, Díaz-Muñoz M, Pérez-Mendoza M, Anaya-Loyola MA, et al. “Evening chronotype associates with increased triglyceride levels in young adults in two independent populations”. Clin Nutr. 2021;40(4):2373-80.

Publication Dates

  • Publication in this collection
    03 Oct 2022
  • Date of issue
    Feb 2023

History

  • Received
    11 Nov 2021
  • Accepted
    30 May 2022
Sociedade Brasileira de Endocrinologia e Metabologia Rua Botucatu, 572 - Conjuntos 81/83, 04023-061 São Paulo SP Brasil, Tel: (55 11) 5575-0311 - São Paulo - SP - Brazil
E-mail: aem.editorial.office@endocrino.org.br