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WOMBI-340; No. of Pages 6 Women and Birth xxx (2014) xxx–xxx
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Sleep quality and stress in women with pregnancy-induced hypertension and gestational diabetes mellitus Mako Hayase a, Mieko Shimada a,*, Hiroyuki Seki b a b
Osaka University, Graduate School of Medicine, Division of Health Sciences, 1-7 Yamadaoka, Suita, Osaka, Japan Saitama Medical University, Saitama Medical Center, Center for Maternal, Fetal and Neonatal Medicine, 1981 Kamoda, Kawagoe, Saitama, Japan
A R T I C L E I N F O
Article history: Received 6 January 2014 Received in revised form 24 February 2014 Accepted 30 April 2014 Keywords: Pregnancy-induced hypertension Gestational diabetes mellitus Stress Secretory IgA Sleep quality
A B S T R A C T
Background: Pregnant women with complications including pregnancy-induced hypertension (PIH) and gestational diabetes mellitus (GDM) often experience disrupted sleep patterns because of activation of the sympathetic nervous system. These pathologies are aggravated by sympathetic nervous system activation and may be related to stress. The present study aimed to clarify the characteristics of and changes in sleep quality and stress in pregnant women with PIH and GDM during the second and third trimesters. Methods: We enrolled 56 women in their second or third trimesters who were diagnosed with PIH or GDM. Participants completed questionnaires, including the Pittsburgh Sleep Quality Index (PSQI) and the Perceived Stress Scale (PSS). Secretory immunoglobulin A (SlgA) concentrations were measured as a biological indicator of stress. Results: PSS scores and subjective stress parameters were significantly higher than those reported from previous studies of healthy pregnant women (15.2 points and 15.1 points for the second and third trimesters, respectively). Mean one-day values for SIgA were 168.3 and 205.7 mg/mL for the second and third trimesters, respectively. During the second and third trimesters, SIgA scores were higher than those reported for healthy pregnant women in previous studies. The PSQI component scores sleep disturbance (C5) and sleep duration (C3) in follow up case were significantly higher in the third trimester than in the second trimester. Discussion: This investigation suggests that pregnant women with PIH and GDM experience higher stress levels than do non-pregnant women and healthy pregnant women. Further, our results indicate that sleep quality worsens during the third trimester compared with the second trimester. ß 2014 Australian College of Midwives. Published by Elsevier Australia (a division of Reed International Books Australia Pty Ltd). All rights reserved.
1. Introduction According to the Japan Society of Obstetrics and Gynaecology database, the incidence of pregnancy-induced hypertension (PIH) from 2005 to 2009 was 4.6%,1 while that of gestational diabetes mellitus (GDM) was between 2.4% and 6%.2,3 Sympathetic nervous system activation, insulin resistance, and hyperlipidaemia are involved in PIH and GDM. These conditions, which are often
* Corresponding author at: Osaka University, Graduate School of Medicine, Division of Health Sciences, 1-7 Yamadaoka, Suita, Osaka 565-0871, Japan. Tel.: +81 6 6879 2532; fax: +81 6 6879 2532. E-mail addresses: [email protected], [email protected] (M. Shimada).
observed in lifestyle diseases such as hypertension, atherosclerosis (hyperlipidaemia), diabetes, and obesity may be related.4,5 Activation of the sympathetic nervous system6 in PIH disrupts circadian rhythms and increases wakefulness after sleep onset at night, impairing sleep patterns.7 In addition, insomnia often occurs in adult diabetic patients.8 Therefore, it appears that a lifestyle that includes a regular routine and good quality sleep during pregnancy is important in preventing perinatal abnormalities in women with lifestyle disease-like pathologies such as PIH and GDM. An experiment in pregnant rats determined that the sympathetic nervous system is activated by stress.9 Secretory immunoglobulin A (SIgA) is used as a biological marker of stress, because increased sympathetic nerve activity in response to acute stress enhances its secretion.10 Therefore, SIgA may increase in pregnant
http://dx.doi.org/10.1016/j.wombi.2014.04.002 1871-5192/ß 2014 Australian College of Midwives. Published by Elsevier Australia (a division of Reed International Books Australia Pty Ltd). All rights reserved.
Please cite this article in press as: Hayase M, et al. Sleep quality and stress in women with pregnancy-induced hypertension and gestational diabetes mellitus. Women Birth (2014), http://dx.doi.org/10.1016/j.wombi.2014.04.002
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women who have PIH and/or GDM, as these conditions involve increased sympathetic nerve activity. Furthermore, maternal stress has been demonstrated to be an important risk factor for adverse pregnancy and birth outcomes, and is associated with gestational hypertension and changes in various physiological systems, including the autonomic nervous and endocrine systems. In particular, increased stress reactivity during pregnancy is associated with increased risks of preterm birth and low birth weight.11,12 Thus far, no studies have investigated the correlation between pregnancy and sleep–wake rhythms, sleep quality, and stress. Therefore, the present study was conducted to clarify the characteristics of and changes in sleep quality and stress in pregnant women with PIH and GDM during the second and third trimesters. 2. Methods 2.1. Subjects We enrolled 56 pregnant women for this study from among subjects who were attending prenatal checkups at a University Hospital from February 2009 until April 2012. Women enrolled in the study were diagnosed with the pregnancy-related complications of PIH and/or GDM by an obstetrician at obstetric outpatient clinics during the second trimester (defined as 16 weeks, 0 days to 27 weeks 6 days) or the third trimester (defined as 28 weeks, 0 days to 40 weeks 6 days). In this study, 40 women were diagnosed with a complication in the second trimester of pregnancy, 27 of whom participated in a follow-up survey during their third trimester, and 16 women were diagnosed with a complication in the third trimester. The aim of the research was explained to the study participants who were diagnosed with a pregnancy-related complication at an obstetric outpatient clinic, and written informed consent was obtained from each participant before enrolment in the study. 2.2. Survey methods All study participants were asked to complete a questionnaire regarding their characteristics and lifestyles, as well as the Pittsburgh Sleep Quality Index (PSQI) and the Perceived Stress Scale (PSS), and saliva samples were obtained for SIgA measurements. Medical information regarding a subject’s diagnosis, treatment course, delivery style, number of gestational weeks, birth weight, delivery abnormalities, and postpartum course was obtained from medical records. The survey was initiated in the second trimester because pregnancy complications usually develop during the third trimester, and severe cases often experience the onset of complications during the second trimester that may lead to premature births. 2.3. Pittsburgh Sleep Quality Index The PSQI is a self-rated questionnaire, which evaluates sleep quality, and was developed by the Department of Psychiatry at the University of Pittsburgh, Pennsylvania, USA.13 The Japanese version created by Doi et al.,14 is a self-completed questionnaire comprising 18 items. Each item is scored on a scale from 0 to 3, using a 4-level Likert scale, for each of the following 7 elements: sleep quality (C1, subjective sleep quality in the past month), sleep latency (C2, time from going to bed until falling asleep; scoring of sleep latency), sleep duration (C3, scoring of sleeping duration), habitual sleep efficiency (C4, proportion of hours spent asleep in bed), sleep disturbance (C5, scoring of the frequency of items that relate to sleep difficulties: nocturnal or early morning waking,
waking to use the toilet, difficulty breathing, loud coughing or snoring, feeling cold, feeling hot, having bad dreams, and pain or other reasons, including foetal movement or breastfeeding), use of sleeping medication (C6, scoring the frequency of use), and daytime dysfunction (C7, scoring frequency of onset and enthusiasm get things done). The total scores were converted into an average PSQI global score (PSQIG), from 0 to 21 points. For each item, a higher score indicated greater sleep impairment and the total score cut-off value was 5.5 points.13,14 2.4. Perceived Stress Scale The PSS is a questionnaire designed to evaluate subjective stress. The PSS-10 is composed of 10 items that are assessed using a 5-level Likert scale (0 points: never; 4 points: always). Hence, PSS scores range from 0 to 40 points, with higher scores indicating higher stress levels. Its reliability and internal validity have been verified,15 and it is reliable in studies involving pregnant women. The questionnaire’s reliability was verified in the present study by using an alpha coefficient of 0.80 for pregnant women in the second trimester and an alpha coefficient of 0.84 for pregnant women in the third trimester.16 2.5. Secretory immunoglobulin A SIgA was measured as a biological indicator of stress. Saliva samples (1 mL) were taken by subjects at home 4-times a day for 3 days before breakfast, lunch, dinner, and before going to bed, because SIgA concentrations fluctuate throughout the day.17 Saliva samples were stored in 1.5-mL Safe Lock Tubes at 20 8C in the subjects’ freezers. Thawed saliva samples were centrifuged at 1500 rpm for 15 min at 4 8C. Quantitative measurements of SIgA concentrations were then conducted using an enzyme immunoassay kit (Salimetrics LLC, State College, PA, USA), and optical densities at 450 nm were determined using a spectrophotometer (Model 680, Bio-Rad Laboratories Japan, Inc., Tokyo, Japan). The intra- and inter-assay coefficient of variation were 2.13% and 2.90%, respectively. 2.6. Statistical analysis The unpaired t-test evaluated differences between mean values in the second and third trimesters. The paired t-test evaluated differences between mean values of parameters in the second and third trimesters obtained from participantsintheirsecondtrimesterswhoundertookfollow-upsurveysintheir thirdtrimesters.The x2 testwasusedtocomparetheexpectedfrequencieswith the observed frequencies for one or more categories, and a one-way analysis of variance (ANOVA) was used to compare diurnal variations in SIgA concentrations. The SPSS version 22.0 (SPSS, Inc., Chicago, IL, USA) was used for all statistical analyses. We analysed the participants and grouped them based on their diagnoses in subgroups as follows: women with diabetes and GDM were placed in the diabetes mellitus (DM) group and those with high blood pressure and PIH were placed in the hypertension (HT) group. 2.7. Ethical considerations The study was approved by the ethics committees of the Osaka University Graduate School of Medicine, Osaka, Japan and the Saitama Medical University, Saitama, Japan.
3. Results The participants’ backgrounds are summarised in Table 1.
Please cite this article in press as: Hayase M, et al. Sleep quality and stress in women with pregnancy-induced hypertension and gestational diabetes mellitus. Women Birth (2014), http://dx.doi.org/10.1016/j.wombi.2014.04.002
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WOMBI-340; No. of Pages 6 M. Hayase et al. / Women and Birth xxx (2014) xxx–xxx Table 1 Demographic characteristics of the 56 study participants with pregnancy-related complications. Characteristic
Mean
Age (years) 35.3 Height (cm) 157.5 Non-pregnant weight (kg) 66.8 Non-pregnant BMI (%) 26.8 Final weight (kg) 72.3 Weight increase (kg) 6.9 2891.7 Infant weight (g) Gestational age (weeks) 37.9 Employment Yes No Parity Primipara Multipara Complications PIH GDM Both Treatment during pregnancy Yes No Delivery manner Normal delivery Caesarean section Forceps delivery Postpartum treatment Yes No
SD
Range
4.2 6.3 17.5 6.2 15.0 5.1 444.5 1.3
27–45 142.7–170.4 40.0–106.6 18.4–41.7 40.8–116.0 6.8 to 18.0 1855–4168 34–40
n (%)
21 (37.5) 35 (62.5) 31 (55.4) 25 (44.6) 21 (37.5) 29 (51.8) 6 (10.7) 40 (71.4) 16 (28.6) 22 (39.3) 29 (51.8) 5 (8.9) 25 (44.6) 31 (55.4)
BMI, body mass index; GDM, gestational diabetes mellitus; PIH, pregnancy-induced hypertension; SD, standard deviation
3.1. Second and third trimester PSQIG scores Table 2 summarises the PSQIG scores and the component scores obtained during the second and third trimesters from women with pregnancy-related complications. No significant differences were observed between the PSQIG scores obtained during the second and third trimesters, which were 5.4 points (range: 1–13 points) and 6.2 points (range: 2–17 points), respectively. However, PSQIG scores obtained during both the second and third trimesters were higher than the cut-off value of 5.5 points. Subjects were divided into 2 groups according to the PSQIG cutoff value (5.5 points) and compared. In the second and third trimesters of pregnancy, 17 (42.5%) and 24 (55.8%) women, respectively, exceeded the 5.5 point cut-off value. In contrast, 23 (57.5%) and 19 (44.2%) women were below the 5.5 point cut-off value in the second and third trimesters, respectively. The proportion of subjects exceeding the cut-off value increased by approximately 13% in the third trimester. No statistically significant differences were observed between the groups separated on the basis of the PSQIG cut-off value. We investigated the changes in the PSQIG component scores C1–C7 during the second and third trimesters. Sleep disturbance (C5) was significantly higher during the third trimester (1.3 points) than during the second trimester (1.0 point) (unpaired-t test = 2.50, P < 0.05). Common reasons given for sleeping difficulties in the second trimester were ‘‘unable to sleep for 30 min or longer after going to bed’’ (54.1%), ‘‘waking up during the night or early morning’’ (74.4%), and ‘‘needing to use the toilet’’ (84.2%). Common reasons given for sleeping difficulties in the third trimester were ‘‘unable to sleep for 30 min or longer after going to bed’’ (62.8%), ‘‘waking up during the night or early morning’’ (83.7%), and ‘‘needing to use the toilet’’ (90.7%). For the cases followed from the second trimester to the third trimester (n = 27), sleep duration (C3) scores were significantly higher in the third
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Table 2 PSQIG scores and subscale items obtained during the second and third trimesters from women with pregnancy-related complications. PSQI component score
Second trimester (n = 40) score Mean (SD)
Third trimester (n = 43) score Mean (SD)
P value
C1 Sleep quality C2 Sleep latency C3 Sleep duration C4 Habitual sleep efficiency C5 Sleep disturbance C6 Use of sleeping medication C7 Daytime dysfunction PSQIG
1.3 1.3 0.9 0.4
1.4 1.4 1.0 0.2
(0.7) (1.1) (0.8) (0.6)
NS NS NS NS
1.0 (0.5) 0.1 (0.3)
1.3 (0.5) 0.1 (0.4)
* NS
0.5 (0.6) 5.4 (2.8)
0.6 (0.7) 6.2 (2.6)
NS NS
(0.7) (1.1) (0.9) (0.9)
Unpaired-t test: *P < 0.05. PSQIG, Pittsburgh Sleep Quality Index Global score; SD, standard deviation; NS, not significant.
trimester (1.0 point) than in the second trimester (0.6 point) (paired t-test = 2.46, P < 0.05). 3.2. Second and third trimester PSS values There was no significant difference in the mean PSS value between the participants in the second and third trimesters, which were 15.2 points (range: 3–26 points) and 15.1 points (range: 3–28 points), respectively, as shown in Table 3. Additionally, there were no significant differences between the participants in the second and third trimesters in relation to the diagnosis of complications, PSQIG cut-off value, parity (primipara or multipara), age (35 years vs. >35 years), or employment status. 3.3. Daily secretory IgA content in the saliva of participants during the second and third trimesters The mean SIgA levels from samples taken throughout the day, together with the mean times SIgA levels peaked, the daily fluctuations, and the daily mean concentration for participants during the second and third trimesters are summarised in Table 4. A significant diurnal fluctuation in SIgA content was observed during the second one-way ANOVA, P < 0.01, and third trimesters (P < 0.001); however, there was no significant difference in mean daily SIgA concentrations between participants in the second and third trimesters. Further, there were no significant differences between the second and third trimesters in those diagnosed with PIH or GDM in relation to the PSQIG cut-off value, the first or
Table 3 Perceived stress scale scores obtained from pregnant women with pregnancyinduced hypertension and gestational diabetes mellitus. PSS score
Second Trimester (n = 40) Mean (SE)
Hayase et al.
15.15 (5.88)
Third Trimester (n = 43) Mean (SE) 15.09 (4.59)
P value
NS
Previous studies
Gestational weeks
Participants (n)
PSS score Mean (SE)
Dalmida et al. (2010)18 Salacz et al. (2012)19
37–42
69
10.40 (6.90)***
36–38
79
12.27 (5.87)*
PSS, Perceived Stress Scale; SE, standard error. Unpaired-t test: ***P < 0.001; *P < 0.05; NS, not significant.
Please cite this article in press as: Hayase M, et al. Sleep quality and stress in women with pregnancy-induced hypertension and gestational diabetes mellitus. Women Birth (2014), http://dx.doi.org/10.1016/j.wombi.2014.04.002
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Table 4 Secretory immunoglobulin a in pregnant women with pregnancy-induced hypertension and gestational diabetes mellitus. SIgA measurement
Second trimester (n = 24)
SIgA peak value (mg/mL) Time of peak value (o’clock) SIgA variation (mg/mL) Morning SIgA (mg/mL) Midday SIgA (mg/mL) Evening SIgA (mg/mL) Night SIgA (mg/mL) SIgA daily mean value (mg/mL)
Winderstrom et al. (1984)21 Annie et al. (1991)22 Rockenbach et al. (2006)23
Third trimester (n = 23)
P value
Mean
SE
Mean
SE
264.32 11:46 166.47 239.08 147.97 125.80 160.34 168.30
22.10 1:19 17.61 21.54 19.18 17.16 19.93 15.07
298.90 9:52 192.24 285.27 211.52 139.19 166.16 205.73
34.15 0:44 27.98 33.98 29.20 21.03 20.82 27.07
NS § NS NS § NS NS NS
GS
n
Mean
SE
P value
34–42 30–34 19–35
15 30 22
101.10 154.00 118.90
51.40 105.00 47.00
*** *** ***
SIgA, secretory immunoglobulin A; GS, gestational weeks; SE, standard error. Unpaired t-test: ***P < 0.001; §P < 0.1; NS, not significant.
subsequent delivery, the age of the participant, or employment status. In the cases followed from their second trimesters to their third trimesters (n = 13), SIgA concentrations tended to increase in the third trimester, with morning SIgA concentrations at 218.2 mg/mL in the second trimester and at 274.0 mg/mL in the third trimester. The mean diurnal SIgA concentration was 145.4 mg/mL in the second trimester and 241.6 mg/mL in the third trimester, representing a significant increase in the third trimester (paired t-test = 2.59, P < 0.05). No significant differences were observed in the peak SIgA concentrations, SIgA amplitudes, the timing of the peak SIgA concentrations, or the daily average SIgA concentrations, between the second and third trimesters. 3.4. Correlations between sleep and stress parameters During the second trimester, a positive correlation was apparent between the PSS and PSQIG values (r = 0.414, P < 0.05), and a negative correlation was apparent between the PSS value and sleep duration (r = 0.420, P < 0.05). In addition, a negative correlation was observed between the PSQIG and sleep duration (r = 0.457, P < 0.05) during the second trimester. 3.5. Comparison of parameters between the treatment- and nontreatment groups In the group that received treatment, a positive correlation was observed between the second trimester PSS and PSQIG values (r = 0.393, P < 0.05). Women in the group that received treatment (n = 27) had a mean age of 36.6 (SD 4.9) years; mean body mass index, 27.5 (SD 6.2); weight increase, 7.7 (SD 4.1) kg; mean PSS score, 15.6 (SD 5.9) points; and mean PSQIG score, 5.1 (SD 3.1) points. Furthermore, 11 (37.9%) subjects exceeded the PSQIG cutoff value. The treatment group comprised 27.6% DM group, 51.7% HT group, and 20.7% groups with a combination of DM and HT. There was no significant correlation between the third trimester PSS and PSQIG values. Of the pregnant women who received treatment, oral medicine was administered to 20 participants; intravenous infusions, or injections that included antihypertensive medications and insulin, were administered to 32 women; dietary advice was given to 8 women; and 16 women were not treated. In the group that was treated during pregnancy, 55.0% of the women needed treatment during the postpartum period, while in the group that did not receive treatment during pregnancy, 18.8% of the women needed treatment during the postpartum period. Significantly more women required postpartum treatment in the group that received
treatment during pregnancy (16, 84.2%) than in the group that did not receive treatment during pregnancy (3, 15.8%) (x2 = 4.607, degrees of freedom = 1, P < 0.05).
4. Discussion We investigated stress and sleep quality in pregnant women with PIH and GDM in the second and third trimesters. Subjective stress was evaluated using the PSS, and the scores from participants in the second and third trimesters in this study were significantly higher when compared with published scores from the second and third trimesters of healthy pregnancies (unpaired ttest = 3.6, P < 0.00118; and unpaired t-test = 2.3, P < 0.05,19 respectively). This demonstrates that pregnant women with PIH and GDM may experience more subjective stress than those with uncomplicated pregnancies. SIgA concentrations were measured as a biological indicator of stress. A previous study reported that serum IgA levels in pregnant women are lower than those of non-pregnant women due to immunosuppressive activities.20 In another study, SIgA levels were reported to be higher in pregnant women than in non-pregnant women.21 In this study, daytime SIgA concentrations from pregnant women with pregnancy-related complications in the second and third trimesters were significantly higher than daytime SIgA concentrations published for uncomplicated pregnancies by Widerstro¨m and Bratthall21 (unpaired t test = 7.4, P < 0.001), for healthy primipara by Annie and Groe¨r22 (unpaired t test = 5.1, P < 0.001), and for healthy pregnant women by Rockenbach et al.23 (unpaired t test = 7.4, P < 0.001). Ahsan et al. reported that serum IgA concentrations were higher in woman with PIH compared with healthy pregnant women.24 The women who had pregnancyrelated complications in this study exhibited a state of high stress compared with the healthy pregnant women described previously, which is suggestive of higher SIgA concentrations and PSS scores. This study showed that greater subjective stress is associated with shorter sleep durations and progressively poorer sleep quality. Furthermore, the requirement for treatment by women in the second trimester who had pregnancy-related complications, suggests that these complications develop earlier than in healthy pregnancies, that the complications are usually more serious than in healthy pregnancies,25 and that stress increases, reducing the quality of sleep. In the present study, we found that PSQIG scores were often higher than the cut-off value of 5.5 points during third trimesters. PSQIG scores for women with pregnancy-related complications were approximately 1–2 points higher in both the second and third
Please cite this article in press as: Hayase M, et al. Sleep quality and stress in women with pregnancy-induced hypertension and gestational diabetes mellitus. Women Birth (2014), http://dx.doi.org/10.1016/j.wombi.2014.04.002
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trimesters than they were for healthy women of the same age range reported by Doi et al.,26 indicating that they experienced poor quality sleep. However, a comparison of healthy pregnant women by Ko et al. found no difference among the PSQIG scores and the subscale items.27 As noted above, the fact that no differences were apparent between women with pregnancyrelated complications and healthy pregnant women suggests that sleep quality for pregnant women deteriorates regardless of whether or not there are pregnancy-related complications. This study also found that the proportion of pregnant women with scores exceeding the PSQIG cut-off value increased from the second to the third trimester, indicating lower sleep quality during the third trimester. Subjects showed significantly higher scores in the third trimester than in the second trimester for the PSQIG subscale items relating to sleep disturbance (C5), which indicates that the closer the subjects came to the end of their pregnancies, the more difficulty they had sleeping. The reasons for these sleep disturbances included long sleep latency periods, nocturnal and early morning waking, and frequent waking to use the toilet, which were identical to the results of a previous study.26 Moreover, the cases who were followed up in this study from the second to the third trimester, indicated that sleep duration (C3) was significantly shorter during the third trimester than during the second trimester. These findings confirm that women who are further advanced in their pregnancies experience more sleep difficulties, shorter sleeping durations, and sleep of poorer quality. Previous publications have reported that the proportion of rapid eye movement sleep increases and that sleep becomes shallower during the third trimester,28 and that sleep quality deteriorates more in the third trimester.29 A previous study reported that reductions in sleep duration and in the quality of sleep activate the sympathetic nervous system,30 which would induce an increased risk for diabetes and elevated blood pressure.31 In addition, the sympathetic nervous system is activated by increases in stress,9,32 and in women with pregnancyrelated complications, situations may become more critical. Moreover, women receiving PIH treatment during pregnancy and women with a history of PIH have an increased risk of developing subsequent severe hypertension compared with healthy pregnant women (hazard ratio [HR]: 1.53; 95% confidence interval [CI]: 1.25–1.87 and HR: 2.53; 95% CI: 2.25–2.84, respectively).33,34 Pregnant women with GDM have an increased risk of developing DM compared with healthy pregnant women (risk ratio: 7.43; 95% CI: 4.79–11.51).35 Therefore, pregnant women who experience these complications must take care to reduce both mental and physical stress during gestation. In women with pregnancy complications who experience more stress than healthy pregnant women, particularly women requiring any type of treatment, self-care treatments, such as yoga, have been demonstrated to help sedate the sympathetic nervous system and reduce stress.36 Because mental stress reduces the quality and duration of sleep, which are known to have unfavourable effects on health, these women should moreover try to adjust their sleep and circadian rhythm in order to avoid aggravation of their condition. Midwives should advise on relaxation techniques such as yoga, and provide help to regulate the sleep patterns and rhythm of daily life, in order to further aid and support these pregnant women. A limitation of this study was that we did not investigate the potential confounding factors, except for age, employment status, and parity, because these factors were not related to stress by single analysis. Furthermore, logistic analyses were not carried out to clarify the confounding factors, and it will be necessary to study these other confounding factors further, before any firm conclusions can be drawn. Stress is associated with many different individual factors, such as age, employment status, and type of
5
work, personality, education level and socio-economic factors such as income, smoking status, and family relationships, as well as the health of the foetus and parity.11,37 Further, the current study comprised only a small sample size, because pregnant women with complications were excluded from the longitudinal study. Hence, future studies should involve greater numbers of participants. 5. Conclusion In conclusion, this study shows that pregnant women with complications of PIH and GDM experience more stress than do healthy pregnant women. The quality of sleep experienced by pregnant women who have these complications is worse than that of both healthy pregnant and non-pregnant women. Furthermore, sleep quality deteriorates from the second to the third trimester in pregnant women who have complications. Pregnant women who require treatment from the second trimester show more subjective stress, shorter sleep durations, and experience sleep of lesser quality than do those who do not require treatment during the second trimester. Acknowledgments This study was conducted with the aid of Grants-in-Aid for Scientific Research 2008–2012, Basic Research B (No. 20390562 for Mieko SHIMADA) from the Ministry of Education, Culture, Sports, Science and Technology, Japan. The authors thank Mizue Matsumoto, RM, head midwife, and her colleagues at the Center for Maternal, Fetal and Neonatal Medicine, Saitama Medical Center, Saitama Medical University, for assisting us with data collection. We also thank Motonao Nakamura PhD, Associate professor of Department of Biochemistry and Molecular Biology, graduate school of Medicine, The University of Tokyo, for advising us assay of Saliva IgA. References 1. Morikawa M, Cho K, Yamada T, Yamada T, Sato S, Minakami H. Risk factors for eclampsia in Japan between 2005 and 2009. Int J Gynaecol Obstet 2012;117(1):66–8. 2. Morikawa M, Yamada T, Yamada T, Akaishi R, Nishida R, Cho K, et al. Change in the number of patients after the adoption of IADPSG criteria for hyperglycemia during pregnancy in Japanese women. Diabetes Res Clin Pract 2010;90(3):339– 42. 3. Morikawa M, Yamada T, Yamada T, Sato S, Cho K, Minakami H. Prevalence of hyperglycemia during pregnancy according to maternal age and pre-pregnancy body mass index in Japan, 2007–2009. Int J Gynaecol Obstet 2012;118(3):198– 201. 4. Sebire NJ, Jolly M, Harris JP, Wadsworth J, Joffe M, Beard RW, et al. Maternal obesity and pregnancy outcome: a study of 287,213 pregnancies in London. Int J Obes 2001;25(8):1175–82. 5. McGrowder D, Grant K, Irving R, Gordon L, Crawford T, Alexander-Lindo R, et al. Lipid profile and clinical characteristics of women with gestational diabetes mellitus and preeclampsia. J Med Biochem 2009;28(2):72–81. 6. Airaksinen KE, Kirkinen P, Takkunen JT. Autonomic nervous dysfunction in severe pre-eclampsia. Eur J Obstet Gynecol Reprod Biol 1985;19(5):269–76. 7. Ekholm EM, Polo O, Rauhala ER, Ekblad UU. Sleep quality in preeclampsia. Am J Obstet Gynecol 1992;167(5):1262–6. 8. Sridhar GR, Madhu K. Prevalence of sleep disturbances in diabetes mellitus. Diabetes Res Clin Pract 1994;23(3):183–6. 9. Kanayama N, Tsujimura R, She L, Maehara K, Terao T. Cold-induced stress stimulates the sympathetic nervous system, causing hypertension and proteinuria in rats. J Hypertens 1997;15(4):383–9. 10. Tsujita S, Morimoto K. Secretory IgA in saliva can be a useful stress marker. Environ Health Prev Med 1999;4(1):1–8. 11. Christian LM. Physiological reactivity to psychological stress in human pregnancy: current knowledge and future directions. Prog Neurobiol 2012;99(2):106–16. 12. Fink NS, Urech C, Cavelti M, Alder J. Relaxation during pregnancy: what are the benefits for mother, fetus, and the newborn? A systematic review of the literature. J Perinat Neonat Nurs 2012;26(4):296–306. 13. Buysse DJ, Reynolds CF, Monk TH, Berman SR, Kupfer DJ. The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research. Psychiatry Res 1989;28(2):193–213.
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14. Doi Y, Minowa M, Uchiyama M, Okawa M, Kim K, Shibui K, et al. Psychometric assessment of subjective sleep quality using the Japanese version of the Pittsburgh Sleep Quality Index (PSQI-J) in psychiatric disordered and control subjects. Psychiatry Res 2000;97(2–3):165–72. 15. Cohen S, Williamson G. Perceived stress in a probability sample of the United States. In: Spacapan S, Oskamp S, editors. The social psychology of health. The Claremont symposium on applied social psychology. Thousand Oaks, CA, USA: Sage Publications Inc.; 1988. p. 31–67. 16. Hilmert CJ, Schetter CD, Dominguez TP. Stress and blood pressure during pregnancy: racial differences and associations with birthweight. Psychosom Med 2008;70(1):57–64. 17. Shirakawa T, Mitome M, Oguchi H. Circadian rhythms of S-IgA and cortisol in whole saliva—compensatory mechanism of oral immune system for nocturnal fall of saliva secretion. Pediatr Dent J 2004;14(1):115–20. 18. Dalmida SG, Robertson B, Carrion MM, Thompson W, Erskine N, Scruggs N, et al. Spirituality, religiousness, psychosocial factors, and maternal-infant outcomes in Latina mothers. Southern Online J Nurs Res 2010;10(3). 12p. 19. Salacz P, Csukly G, Haller J, Valent S. Association between subjective feelings of distress, plasma cortisol, anxiety, and depression in pregnant women. Eur J Obstet Gynecol Reprod Biol 2012;165(2):225–30. 20. Khirwadkar MA, Kher JR. Study of serum immunoglobulins in normal pregnancy. Indian J Physiol Pharmacol 1991;35(1):69–70. 21. Widerstro¨m L, Bratthall D. Increased IgA levels in saliva during pregnancy. Scand J Dent Res 1984;92(1):33–7. 22. Annie CL, Groe¨r M. Childbirth stress. An immunologic study. J Obstet Gynecol Neonatal Nurs 1991;20(5):391–7. 23. Rockenbach MI, Marinho SA, Veeck EB, Lindemann L, Shinkai RS. Salivary flow rate, pH, and concentrations of calcium, phosphate, and sIgA in Brazilian pregnant and non-pregnant women. Head Face Med 2006;2:44. 24. Ahsan T, Wahab F, Kamal MM, Islam SN. Serum immunoglobulins (IgG, IgA, IgM) levels in preeclampsia and eclampsia pregnancies. Intern J Third World Med 2009;8(1). http://archive.ispub.com/journal/the-internet-journal-of-thirdworld-medicine/volume-8-number-1/serum-immunoglobulins-igg-iga-igmlevels-in-preeclampsia-and-eclampsia-pregnancies.html#sthash.87xQ6ngy.dpuf [accessed 01.03.13].
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Sleep quality and stress in women with pregnancy-induced hypertension and gestational diabetes mellitus Mako Hayase a, Mieko Shimada a,*, Hiroyuki Seki b a b
Osaka University, Graduate School of Medicine, Division of Health Sciences, 1-7 Yamadaoka, Suita, Osaka, Japan Saitama Medical University, Saitama Medical Center, Center for Maternal, Fetal and Neonatal Medicine, 1981 Kamoda, Kawagoe, Saitama, Japan
A R T I C L E I N F O
Article history: Received 6 January 2014 Received in revised form 24 February 2014 Accepted 30 April 2014 Keywords: Pregnancy-induced hypertension Gestational diabetes mellitus Stress Secretory IgA Sleep quality
A B S T R A C T
Background: Pregnant women with complications including pregnancy-induced hypertension (PIH) and gestational diabetes mellitus (GDM) often experience disrupted sleep patterns because of activation of the sympathetic nervous system. These pathologies are aggravated by sympathetic nervous system activation and may be related to stress. The present study aimed to clarify the characteristics of and changes in sleep quality and stress in pregnant women with PIH and GDM during the second and third trimesters. Methods: We enrolled 56 women in their second or third trimesters who were diagnosed with PIH or GDM. Participants completed questionnaires, including the Pittsburgh Sleep Quality Index (PSQI) and the Perceived Stress Scale (PSS). Secretory immunoglobulin A (SlgA) concentrations were measured as a biological indicator of stress. Results: PSS scores and subjective stress parameters were significantly higher than those reported from previous studies of healthy pregnant women (15.2 points and 15.1 points for the second and third trimesters, respectively). Mean one-day values for SIgA were 168.3 and 205.7 mg/mL for the second and third trimesters, respectively. During the second and third trimesters, SIgA scores were higher than those reported for healthy pregnant women in previous studies. The PSQI component scores sleep disturbance (C5) and sleep duration (C3) in follow up case were significantly higher in the third trimester than in the second trimester. Discussion: This investigation suggests that pregnant women with PIH and GDM experience higher stress levels than do non-pregnant women and healthy pregnant women. Further, our results indicate that sleep quality worsens during the third trimester compared with the second trimester. ß 2014 Australian College of Midwives. Published by Elsevier Australia (a division of Reed International Books Australia Pty Ltd). All rights reserved.
1. Introduction According to the Japan Society of Obstetrics and Gynaecology database, the incidence of pregnancy-induced hypertension (PIH) from 2005 to 2009 was 4.6%,1 while that of gestational diabetes mellitus (GDM) was between 2.4% and 6%.2,3 Sympathetic nervous system activation, insulin resistance, and hyperlipidaemia are involved in PIH and GDM. These conditions, which are often
* Corresponding author at: Osaka University, Graduate School of Medicine, Division of Health Sciences, 1-7 Yamadaoka, Suita, Osaka 565-0871, Japan. Tel.: +81 6 6879 2532; fax: +81 6 6879 2532. E-mail addresses: [email protected], [email protected] (M. Shimada).
observed in lifestyle diseases such as hypertension, atherosclerosis (hyperlipidaemia), diabetes, and obesity may be related.4,5 Activation of the sympathetic nervous system6 in PIH disrupts circadian rhythms and increases wakefulness after sleep onset at night, impairing sleep patterns.7 In addition, insomnia often occurs in adult diabetic patients.8 Therefore, it appears that a lifestyle that includes a regular routine and good quality sleep during pregnancy is important in preventing perinatal abnormalities in women with lifestyle disease-like pathologies such as PIH and GDM. An experiment in pregnant rats determined that the sympathetic nervous system is activated by stress.9 Secretory immunoglobulin A (SIgA) is used as a biological marker of stress, because increased sympathetic nerve activity in response to acute stress enhances its secretion.10 Therefore, SIgA may increase in pregnant
http://dx.doi.org/10.1016/j.wombi.2014.04.002 1871-5192/ß 2014 Australian College of Midwives. Published by Elsevier Australia (a division of Reed International Books Australia Pty Ltd). All rights reserved.
Please cite this article in press as: Hayase M, et al. Sleep quality and stress in women with pregnancy-induced hypertension and gestational diabetes mellitus. Women Birth (2014), http://dx.doi.org/10.1016/j.wombi.2014.04.002
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women who have PIH and/or GDM, as these conditions involve increased sympathetic nerve activity. Furthermore, maternal stress has been demonstrated to be an important risk factor for adverse pregnancy and birth outcomes, and is associated with gestational hypertension and changes in various physiological systems, including the autonomic nervous and endocrine systems. In particular, increased stress reactivity during pregnancy is associated with increased risks of preterm birth and low birth weight.11,12 Thus far, no studies have investigated the correlation between pregnancy and sleep–wake rhythms, sleep quality, and stress. Therefore, the present study was conducted to clarify the characteristics of and changes in sleep quality and stress in pregnant women with PIH and GDM during the second and third trimesters. 2. Methods 2.1. Subjects We enrolled 56 pregnant women for this study from among subjects who were attending prenatal checkups at a University Hospital from February 2009 until April 2012. Women enrolled in the study were diagnosed with the pregnancy-related complications of PIH and/or GDM by an obstetrician at obstetric outpatient clinics during the second trimester (defined as 16 weeks, 0 days to 27 weeks 6 days) or the third trimester (defined as 28 weeks, 0 days to 40 weeks 6 days). In this study, 40 women were diagnosed with a complication in the second trimester of pregnancy, 27 of whom participated in a follow-up survey during their third trimester, and 16 women were diagnosed with a complication in the third trimester. The aim of the research was explained to the study participants who were diagnosed with a pregnancy-related complication at an obstetric outpatient clinic, and written informed consent was obtained from each participant before enrolment in the study. 2.2. Survey methods All study participants were asked to complete a questionnaire regarding their characteristics and lifestyles, as well as the Pittsburgh Sleep Quality Index (PSQI) and the Perceived Stress Scale (PSS), and saliva samples were obtained for SIgA measurements. Medical information regarding a subject’s diagnosis, treatment course, delivery style, number of gestational weeks, birth weight, delivery abnormalities, and postpartum course was obtained from medical records. The survey was initiated in the second trimester because pregnancy complications usually develop during the third trimester, and severe cases often experience the onset of complications during the second trimester that may lead to premature births. 2.3. Pittsburgh Sleep Quality Index The PSQI is a self-rated questionnaire, which evaluates sleep quality, and was developed by the Department of Psychiatry at the University of Pittsburgh, Pennsylvania, USA.13 The Japanese version created by Doi et al.,14 is a self-completed questionnaire comprising 18 items. Each item is scored on a scale from 0 to 3, using a 4-level Likert scale, for each of the following 7 elements: sleep quality (C1, subjective sleep quality in the past month), sleep latency (C2, time from going to bed until falling asleep; scoring of sleep latency), sleep duration (C3, scoring of sleeping duration), habitual sleep efficiency (C4, proportion of hours spent asleep in bed), sleep disturbance (C5, scoring of the frequency of items that relate to sleep difficulties: nocturnal or early morning waking,
waking to use the toilet, difficulty breathing, loud coughing or snoring, feeling cold, feeling hot, having bad dreams, and pain or other reasons, including foetal movement or breastfeeding), use of sleeping medication (C6, scoring the frequency of use), and daytime dysfunction (C7, scoring frequency of onset and enthusiasm get things done). The total scores were converted into an average PSQI global score (PSQIG), from 0 to 21 points. For each item, a higher score indicated greater sleep impairment and the total score cut-off value was 5.5 points.13,14 2.4. Perceived Stress Scale The PSS is a questionnaire designed to evaluate subjective stress. The PSS-10 is composed of 10 items that are assessed using a 5-level Likert scale (0 points: never; 4 points: always). Hence, PSS scores range from 0 to 40 points, with higher scores indicating higher stress levels. Its reliability and internal validity have been verified,15 and it is reliable in studies involving pregnant women. The questionnaire’s reliability was verified in the present study by using an alpha coefficient of 0.80 for pregnant women in the second trimester and an alpha coefficient of 0.84 for pregnant women in the third trimester.16 2.5. Secretory immunoglobulin A SIgA was measured as a biological indicator of stress. Saliva samples (1 mL) were taken by subjects at home 4-times a day for 3 days before breakfast, lunch, dinner, and before going to bed, because SIgA concentrations fluctuate throughout the day.17 Saliva samples were stored in 1.5-mL Safe Lock Tubes at 20 8C in the subjects’ freezers. Thawed saliva samples were centrifuged at 1500 rpm for 15 min at 4 8C. Quantitative measurements of SIgA concentrations were then conducted using an enzyme immunoassay kit (Salimetrics LLC, State College, PA, USA), and optical densities at 450 nm were determined using a spectrophotometer (Model 680, Bio-Rad Laboratories Japan, Inc., Tokyo, Japan). The intra- and inter-assay coefficient of variation were 2.13% and 2.90%, respectively. 2.6. Statistical analysis The unpaired t-test evaluated differences between mean values in the second and third trimesters. The paired t-test evaluated differences between mean values of parameters in the second and third trimesters obtained from participantsintheirsecondtrimesterswhoundertookfollow-upsurveysintheir thirdtrimesters.The x2 testwasusedtocomparetheexpectedfrequencieswith the observed frequencies for one or more categories, and a one-way analysis of variance (ANOVA) was used to compare diurnal variations in SIgA concentrations. The SPSS version 22.0 (SPSS, Inc., Chicago, IL, USA) was used for all statistical analyses. We analysed the participants and grouped them based on their diagnoses in subgroups as follows: women with diabetes and GDM were placed in the diabetes mellitus (DM) group and those with high blood pressure and PIH were placed in the hypertension (HT) group. 2.7. Ethical considerations The study was approved by the ethics committees of the Osaka University Graduate School of Medicine, Osaka, Japan and the Saitama Medical University, Saitama, Japan.
3. Results The participants’ backgrounds are summarised in Table 1.
Please cite this article in press as: Hayase M, et al. Sleep quality and stress in women with pregnancy-induced hypertension and gestational diabetes mellitus. Women Birth (2014), http://dx.doi.org/10.1016/j.wombi.2014.04.002
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WOMBI-340; No. of Pages 6 M. Hayase et al. / Women and Birth xxx (2014) xxx–xxx Table 1 Demographic characteristics of the 56 study participants with pregnancy-related complications. Characteristic
Mean
Age (years) 35.3 Height (cm) 157.5 Non-pregnant weight (kg) 66.8 Non-pregnant BMI (%) 26.8 Final weight (kg) 72.3 Weight increase (kg) 6.9 2891.7 Infant weight (g) Gestational age (weeks) 37.9 Employment Yes No Parity Primipara Multipara Complications PIH GDM Both Treatment during pregnancy Yes No Delivery manner Normal delivery Caesarean section Forceps delivery Postpartum treatment Yes No
SD
Range
4.2 6.3 17.5 6.2 15.0 5.1 444.5 1.3
27–45 142.7–170.4 40.0–106.6 18.4–41.7 40.8–116.0 6.8 to 18.0 1855–4168 34–40
n (%)
21 (37.5) 35 (62.5) 31 (55.4) 25 (44.6) 21 (37.5) 29 (51.8) 6 (10.7) 40 (71.4) 16 (28.6) 22 (39.3) 29 (51.8) 5 (8.9) 25 (44.6) 31 (55.4)
BMI, body mass index; GDM, gestational diabetes mellitus; PIH, pregnancy-induced hypertension; SD, standard deviation
3.1. Second and third trimester PSQIG scores Table 2 summarises the PSQIG scores and the component scores obtained during the second and third trimesters from women with pregnancy-related complications. No significant differences were observed between the PSQIG scores obtained during the second and third trimesters, which were 5.4 points (range: 1–13 points) and 6.2 points (range: 2–17 points), respectively. However, PSQIG scores obtained during both the second and third trimesters were higher than the cut-off value of 5.5 points. Subjects were divided into 2 groups according to the PSQIG cutoff value (5.5 points) and compared. In the second and third trimesters of pregnancy, 17 (42.5%) and 24 (55.8%) women, respectively, exceeded the 5.5 point cut-off value. In contrast, 23 (57.5%) and 19 (44.2%) women were below the 5.5 point cut-off value in the second and third trimesters, respectively. The proportion of subjects exceeding the cut-off value increased by approximately 13% in the third trimester. No statistically significant differences were observed between the groups separated on the basis of the PSQIG cut-off value. We investigated the changes in the PSQIG component scores C1–C7 during the second and third trimesters. Sleep disturbance (C5) was significantly higher during the third trimester (1.3 points) than during the second trimester (1.0 point) (unpaired-t test = 2.50, P < 0.05). Common reasons given for sleeping difficulties in the second trimester were ‘‘unable to sleep for 30 min or longer after going to bed’’ (54.1%), ‘‘waking up during the night or early morning’’ (74.4%), and ‘‘needing to use the toilet’’ (84.2%). Common reasons given for sleeping difficulties in the third trimester were ‘‘unable to sleep for 30 min or longer after going to bed’’ (62.8%), ‘‘waking up during the night or early morning’’ (83.7%), and ‘‘needing to use the toilet’’ (90.7%). For the cases followed from the second trimester to the third trimester (n = 27), sleep duration (C3) scores were significantly higher in the third
3
Table 2 PSQIG scores and subscale items obtained during the second and third trimesters from women with pregnancy-related complications. PSQI component score
Second trimester (n = 40) score Mean (SD)
Third trimester (n = 43) score Mean (SD)
P value
C1 Sleep quality C2 Sleep latency C3 Sleep duration C4 Habitual sleep efficiency C5 Sleep disturbance C6 Use of sleeping medication C7 Daytime dysfunction PSQIG
1.3 1.3 0.9 0.4
1.4 1.4 1.0 0.2
(0.7) (1.1) (0.8) (0.6)
NS NS NS NS
1.0 (0.5) 0.1 (0.3)
1.3 (0.5) 0.1 (0.4)
* NS
0.5 (0.6) 5.4 (2.8)
0.6 (0.7) 6.2 (2.6)
NS NS
(0.7) (1.1) (0.9) (0.9)
Unpaired-t test: *P < 0.05. PSQIG, Pittsburgh Sleep Quality Index Global score; SD, standard deviation; NS, not significant.
trimester (1.0 point) than in the second trimester (0.6 point) (paired t-test = 2.46, P < 0.05). 3.2. Second and third trimester PSS values There was no significant difference in the mean PSS value between the participants in the second and third trimesters, which were 15.2 points (range: 3–26 points) and 15.1 points (range: 3–28 points), respectively, as shown in Table 3. Additionally, there were no significant differences between the participants in the second and third trimesters in relation to the diagnosis of complications, PSQIG cut-off value, parity (primipara or multipara), age (35 years vs. >35 years), or employment status. 3.3. Daily secretory IgA content in the saliva of participants during the second and third trimesters The mean SIgA levels from samples taken throughout the day, together with the mean times SIgA levels peaked, the daily fluctuations, and the daily mean concentration for participants during the second and third trimesters are summarised in Table 4. A significant diurnal fluctuation in SIgA content was observed during the second one-way ANOVA, P < 0.01, and third trimesters (P < 0.001); however, there was no significant difference in mean daily SIgA concentrations between participants in the second and third trimesters. Further, there were no significant differences between the second and third trimesters in those diagnosed with PIH or GDM in relation to the PSQIG cut-off value, the first or
Table 3 Perceived stress scale scores obtained from pregnant women with pregnancyinduced hypertension and gestational diabetes mellitus. PSS score
Second Trimester (n = 40) Mean (SE)
Hayase et al.
15.15 (5.88)
Third Trimester (n = 43) Mean (SE) 15.09 (4.59)
P value
NS
Previous studies
Gestational weeks
Participants (n)
PSS score Mean (SE)
Dalmida et al. (2010)18 Salacz et al. (2012)19
37–42
69
10.40 (6.90)***
36–38
79
12.27 (5.87)*
PSS, Perceived Stress Scale; SE, standard error. Unpaired-t test: ***P < 0.001; *P < 0.05; NS, not significant.
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Table 4 Secretory immunoglobulin a in pregnant women with pregnancy-induced hypertension and gestational diabetes mellitus. SIgA measurement
Second trimester (n = 24)
SIgA peak value (mg/mL) Time of peak value (o’clock) SIgA variation (mg/mL) Morning SIgA (mg/mL) Midday SIgA (mg/mL) Evening SIgA (mg/mL) Night SIgA (mg/mL) SIgA daily mean value (mg/mL)
Winderstrom et al. (1984)21 Annie et al. (1991)22 Rockenbach et al. (2006)23
Third trimester (n = 23)
P value
Mean
SE
Mean
SE
264.32 11:46 166.47 239.08 147.97 125.80 160.34 168.30
22.10 1:19 17.61 21.54 19.18 17.16 19.93 15.07
298.90 9:52 192.24 285.27 211.52 139.19 166.16 205.73
34.15 0:44 27.98 33.98 29.20 21.03 20.82 27.07
NS § NS NS § NS NS NS
GS
n
Mean
SE
P value
34–42 30–34 19–35
15 30 22
101.10 154.00 118.90
51.40 105.00 47.00
*** *** ***
SIgA, secretory immunoglobulin A; GS, gestational weeks; SE, standard error. Unpaired t-test: ***P < 0.001; §P < 0.1; NS, not significant.
subsequent delivery, the age of the participant, or employment status. In the cases followed from their second trimesters to their third trimesters (n = 13), SIgA concentrations tended to increase in the third trimester, with morning SIgA concentrations at 218.2 mg/mL in the second trimester and at 274.0 mg/mL in the third trimester. The mean diurnal SIgA concentration was 145.4 mg/mL in the second trimester and 241.6 mg/mL in the third trimester, representing a significant increase in the third trimester (paired t-test = 2.59, P < 0.05). No significant differences were observed in the peak SIgA concentrations, SIgA amplitudes, the timing of the peak SIgA concentrations, or the daily average SIgA concentrations, between the second and third trimesters. 3.4. Correlations between sleep and stress parameters During the second trimester, a positive correlation was apparent between the PSS and PSQIG values (r = 0.414, P < 0.05), and a negative correlation was apparent between the PSS value and sleep duration (r = 0.420, P < 0.05). In addition, a negative correlation was observed between the PSQIG and sleep duration (r = 0.457, P < 0.05) during the second trimester. 3.5. Comparison of parameters between the treatment- and nontreatment groups In the group that received treatment, a positive correlation was observed between the second trimester PSS and PSQIG values (r = 0.393, P < 0.05). Women in the group that received treatment (n = 27) had a mean age of 36.6 (SD 4.9) years; mean body mass index, 27.5 (SD 6.2); weight increase, 7.7 (SD 4.1) kg; mean PSS score, 15.6 (SD 5.9) points; and mean PSQIG score, 5.1 (SD 3.1) points. Furthermore, 11 (37.9%) subjects exceeded the PSQIG cutoff value. The treatment group comprised 27.6% DM group, 51.7% HT group, and 20.7% groups with a combination of DM and HT. There was no significant correlation between the third trimester PSS and PSQIG values. Of the pregnant women who received treatment, oral medicine was administered to 20 participants; intravenous infusions, or injections that included antihypertensive medications and insulin, were administered to 32 women; dietary advice was given to 8 women; and 16 women were not treated. In the group that was treated during pregnancy, 55.0% of the women needed treatment during the postpartum period, while in the group that did not receive treatment during pregnancy, 18.8% of the women needed treatment during the postpartum period. Significantly more women required postpartum treatment in the group that received
treatment during pregnancy (16, 84.2%) than in the group that did not receive treatment during pregnancy (3, 15.8%) (x2 = 4.607, degrees of freedom = 1, P < 0.05).
4. Discussion We investigated stress and sleep quality in pregnant women with PIH and GDM in the second and third trimesters. Subjective stress was evaluated using the PSS, and the scores from participants in the second and third trimesters in this study were significantly higher when compared with published scores from the second and third trimesters of healthy pregnancies (unpaired ttest = 3.6, P < 0.00118; and unpaired t-test = 2.3, P < 0.05,19 respectively). This demonstrates that pregnant women with PIH and GDM may experience more subjective stress than those with uncomplicated pregnancies. SIgA concentrations were measured as a biological indicator of stress. A previous study reported that serum IgA levels in pregnant women are lower than those of non-pregnant women due to immunosuppressive activities.20 In another study, SIgA levels were reported to be higher in pregnant women than in non-pregnant women.21 In this study, daytime SIgA concentrations from pregnant women with pregnancy-related complications in the second and third trimesters were significantly higher than daytime SIgA concentrations published for uncomplicated pregnancies by Widerstro¨m and Bratthall21 (unpaired t test = 7.4, P < 0.001), for healthy primipara by Annie and Groe¨r22 (unpaired t test = 5.1, P < 0.001), and for healthy pregnant women by Rockenbach et al.23 (unpaired t test = 7.4, P < 0.001). Ahsan et al. reported that serum IgA concentrations were higher in woman with PIH compared with healthy pregnant women.24 The women who had pregnancyrelated complications in this study exhibited a state of high stress compared with the healthy pregnant women described previously, which is suggestive of higher SIgA concentrations and PSS scores. This study showed that greater subjective stress is associated with shorter sleep durations and progressively poorer sleep quality. Furthermore, the requirement for treatment by women in the second trimester who had pregnancy-related complications, suggests that these complications develop earlier than in healthy pregnancies, that the complications are usually more serious than in healthy pregnancies,25 and that stress increases, reducing the quality of sleep. In the present study, we found that PSQIG scores were often higher than the cut-off value of 5.5 points during third trimesters. PSQIG scores for women with pregnancy-related complications were approximately 1–2 points higher in both the second and third
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trimesters than they were for healthy women of the same age range reported by Doi et al.,26 indicating that they experienced poor quality sleep. However, a comparison of healthy pregnant women by Ko et al. found no difference among the PSQIG scores and the subscale items.27 As noted above, the fact that no differences were apparent between women with pregnancyrelated complications and healthy pregnant women suggests that sleep quality for pregnant women deteriorates regardless of whether or not there are pregnancy-related complications. This study also found that the proportion of pregnant women with scores exceeding the PSQIG cut-off value increased from the second to the third trimester, indicating lower sleep quality during the third trimester. Subjects showed significantly higher scores in the third trimester than in the second trimester for the PSQIG subscale items relating to sleep disturbance (C5), which indicates that the closer the subjects came to the end of their pregnancies, the more difficulty they had sleeping. The reasons for these sleep disturbances included long sleep latency periods, nocturnal and early morning waking, and frequent waking to use the toilet, which were identical to the results of a previous study.26 Moreover, the cases who were followed up in this study from the second to the third trimester, indicated that sleep duration (C3) was significantly shorter during the third trimester than during the second trimester. These findings confirm that women who are further advanced in their pregnancies experience more sleep difficulties, shorter sleeping durations, and sleep of poorer quality. Previous publications have reported that the proportion of rapid eye movement sleep increases and that sleep becomes shallower during the third trimester,28 and that sleep quality deteriorates more in the third trimester.29 A previous study reported that reductions in sleep duration and in the quality of sleep activate the sympathetic nervous system,30 which would induce an increased risk for diabetes and elevated blood pressure.31 In addition, the sympathetic nervous system is activated by increases in stress,9,32 and in women with pregnancyrelated complications, situations may become more critical. Moreover, women receiving PIH treatment during pregnancy and women with a history of PIH have an increased risk of developing subsequent severe hypertension compared with healthy pregnant women (hazard ratio [HR]: 1.53; 95% confidence interval [CI]: 1.25–1.87 and HR: 2.53; 95% CI: 2.25–2.84, respectively).33,34 Pregnant women with GDM have an increased risk of developing DM compared with healthy pregnant women (risk ratio: 7.43; 95% CI: 4.79–11.51).35 Therefore, pregnant women who experience these complications must take care to reduce both mental and physical stress during gestation. In women with pregnancy complications who experience more stress than healthy pregnant women, particularly women requiring any type of treatment, self-care treatments, such as yoga, have been demonstrated to help sedate the sympathetic nervous system and reduce stress.36 Because mental stress reduces the quality and duration of sleep, which are known to have unfavourable effects on health, these women should moreover try to adjust their sleep and circadian rhythm in order to avoid aggravation of their condition. Midwives should advise on relaxation techniques such as yoga, and provide help to regulate the sleep patterns and rhythm of daily life, in order to further aid and support these pregnant women. A limitation of this study was that we did not investigate the potential confounding factors, except for age, employment status, and parity, because these factors were not related to stress by single analysis. Furthermore, logistic analyses were not carried out to clarify the confounding factors, and it will be necessary to study these other confounding factors further, before any firm conclusions can be drawn. Stress is associated with many different individual factors, such as age, employment status, and type of
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work, personality, education level and socio-economic factors such as income, smoking status, and family relationships, as well as the health of the foetus and parity.11,37 Further, the current study comprised only a small sample size, because pregnant women with complications were excluded from the longitudinal study. Hence, future studies should involve greater numbers of participants. 5. Conclusion In conclusion, this study shows that pregnant women with complications of PIH and GDM experience more stress than do healthy pregnant women. The quality of sleep experienced by pregnant women who have these complications is worse than that of both healthy pregnant and non-pregnant women. Furthermore, sleep quality deteriorates from the second to the third trimester in pregnant women who have complications. Pregnant women who require treatment from the second trimester show more subjective stress, shorter sleep durations, and experience sleep of lesser quality than do those who do not require treatment during the second trimester. Acknowledgments This study was conducted with the aid of Grants-in-Aid for Scientific Research 2008–2012, Basic Research B (No. 20390562 for Mieko SHIMADA) from the Ministry of Education, Culture, Sports, Science and Technology, Japan. The authors thank Mizue Matsumoto, RM, head midwife, and her colleagues at the Center for Maternal, Fetal and Neonatal Medicine, Saitama Medical Center, Saitama Medical University, for assisting us with data collection. We also thank Motonao Nakamura PhD, Associate professor of Department of Biochemistry and Molecular Biology, graduate school of Medicine, The University of Tokyo, for advising us assay of Saliva IgA. References 1. Morikawa M, Cho K, Yamada T, Yamada T, Sato S, Minakami H. Risk factors for eclampsia in Japan between 2005 and 2009. Int J Gynaecol Obstet 2012;117(1):66–8. 2. Morikawa M, Yamada T, Yamada T, Akaishi R, Nishida R, Cho K, et al. Change in the number of patients after the adoption of IADPSG criteria for hyperglycemia during pregnancy in Japanese women. Diabetes Res Clin Pract 2010;90(3):339– 42. 3. Morikawa M, Yamada T, Yamada T, Sato S, Cho K, Minakami H. Prevalence of hyperglycemia during pregnancy according to maternal age and pre-pregnancy body mass index in Japan, 2007–2009. Int J Gynaecol Obstet 2012;118(3):198– 201. 4. Sebire NJ, Jolly M, Harris JP, Wadsworth J, Joffe M, Beard RW, et al. Maternal obesity and pregnancy outcome: a study of 287,213 pregnancies in London. Int J Obes 2001;25(8):1175–82. 5. McGrowder D, Grant K, Irving R, Gordon L, Crawford T, Alexander-Lindo R, et al. Lipid profile and clinical characteristics of women with gestational diabetes mellitus and preeclampsia. J Med Biochem 2009;28(2):72–81. 6. Airaksinen KE, Kirkinen P, Takkunen JT. Autonomic nervous dysfunction in severe pre-eclampsia. Eur J Obstet Gynecol Reprod Biol 1985;19(5):269–76. 7. Ekholm EM, Polo O, Rauhala ER, Ekblad UU. Sleep quality in preeclampsia. Am J Obstet Gynecol 1992;167(5):1262–6. 8. Sridhar GR, Madhu K. Prevalence of sleep disturbances in diabetes mellitus. Diabetes Res Clin Pract 1994;23(3):183–6. 9. Kanayama N, Tsujimura R, She L, Maehara K, Terao T. Cold-induced stress stimulates the sympathetic nervous system, causing hypertension and proteinuria in rats. J Hypertens 1997;15(4):383–9. 10. Tsujita S, Morimoto K. Secretory IgA in saliva can be a useful stress marker. Environ Health Prev Med 1999;4(1):1–8. 11. Christian LM. Physiological reactivity to psychological stress in human pregnancy: current knowledge and future directions. Prog Neurobiol 2012;99(2):106–16. 12. Fink NS, Urech C, Cavelti M, Alder J. Relaxation during pregnancy: what are the benefits for mother, fetus, and the newborn? A systematic review of the literature. J Perinat Neonat Nurs 2012;26(4):296–306. 13. Buysse DJ, Reynolds CF, Monk TH, Berman SR, Kupfer DJ. The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research. Psychiatry Res 1989;28(2):193–213.
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