Hypertension in Pregnancy, 2014; 33(3): 291–298 ! Informa Healthcare USA, Inc. ISSN: 1064-1955 print / 1525-6065 online DOI: 10.3109/10641955.2013.874441
ORIGINAL ARTICLE
The relationship between neck circumference and pregnancy-induced hypertension in the third trimester pregnant women Jun-Tao Shao,1 Jie Yu,1 Jun-Qiao Qi,2 and Xiao-Dong Liu1 1
Department of Ultrasound, Department of Gynaecology and Obstetrics, The First Hospital of Qinhuangdao, Qinhuangdao, Hebei Province, China
2
Objective: The purpose of this study was to evaluate the relationship between neck circumference (NC) and pregnancy-induced hypertension (PIH) in the third trimester pregnant women. Methods: The study included 126 women who were in the third trimester pregnancy. All subjects completed a standard sleep questionnaire, anthropometric measurements and ultrasonic testing. Results: Pregnant women with NC 34.7 cm had significantly higher frequency of PIH than pregnant women with NC 534.7 cm (35.6% versus 2.5%, 2 = 25.863, p = 0.000). Conclusions: The increase of NC was independent risk factor for PIH in the third trimester pregnant women. Keywords Neck circumference, Pregnancy, Pregnancy-induced hypertension.
INTRODUCTION China is one of the fastest developing countries in the world. Over the past two decades, China has encountered a great economic development. Rapid economic progress has resulted in changes to both diet and physical activity. As a result, the prevalence of overweight or obesity has significantly increased. The prevalence of overweight and obesity rose 49.5% between 1992 and 2002, from 20.0 to 29.9% (1,2). As we all know, obesity is an important risk factor for the development of atherosclerotic cardiovascular disease, type 2 diabetes, dyslipidemia, and hypertension. However, obesity is also associated with increased risks of adverse obstetric outcomes in women (3). Pregnancy-induced hypertension (PIH) is estimated to affect 5–10% of all pregnancies in the China. PIH is the major cause of maternal and perinatal morbidity. In China, PIH was the second cause of maternal deaths (10.3% of the total deaths) (4,5). Mother with PIH is accompanied by protein in the urine and swelling. The most serious consequences of PIH include brain damage in the mother due to brain swelling and oxygen deprivation during seizures. PIH could also increase the incidence of preterm delivery (with PIH 4.9%
Correspondence: Jun-tao Shao, Department of Ultrasound, The First Hospital of Qinhuangdao, No. 258 Wenhua Road, Qinhuangdao 066000, Hebei Province, China. Tel: +86 335 5908325. Fax: +86 335 3032042. E-mail: [email protected]
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versus without PIH 3.4%) and low birth weight (with PIH 3.6% versus without PIH 1.8%) (6). The known risk factors of PIH development are: multiple pregnancy, masculine sex of fetus, very young age of women (below 18 years), advanced age (above 40 years), and obesity of the pregnant woman (7). Maternal obesity increased risks of gestational hypertensive disorders. The risks of PIH among obese mothers was 4.67 times compared with the mothers with a normal weight (8). Neck circumference (NC) is another index for evaluating obesity. In 2008, Ursavas A et al. found that NC was an independent risk factor for PIH (9). There is a racial difference in the relationship between obesity and adverse obstetric outcomes. The impacts of obesity on pre-eclampsia, gestational diabetes and preterm delivery in Chinese women might be stronger than that in Caucasian (3). The aim of our study was to determine the relationship between NC and PIH in the third trimester pregnant women of Qinhuangdao.
METHODS Study Population In 2011, we conducted the study at the First Hospital of Qinhuangdao Hebei, China. A total of 126 pregnant women in the third trimester were recruited at an antenatal clinic. After completing an informed consent form, all subjects completed a standard sleep questionnaire, anthropometric measurements and ultrasonic testing. Socio-demographic variables were collected from women’s self-completed questionnaires and included: age, ethnicity, gestational weeks, body weight prior to pregnancy, smoking and drinking status. Women with a history of chronic hypertension, multiple births, and cardiac, pulmonary and neuromuscular disease were excluded from the study. Women with unknown body weight prior to pregnancy were also excluded. This study was approved by the ethics committee of the First Hospital of Qinhuangdao. Sleep Questionnaire The questionnaire was administered by research assistants. When completing the questionnaire, the women were accompanied by their partners. Women were asked about snoring, and these responses were graded on a Likert scale of 0–4 [0 = never, 1 = rarely (less than once a month), 2 = sometimes (less than once a week), 3 = often (at least once a week) and 4 = always (almost every night)]. Habitual snoring was snoring that occurred often or always. The questionnaire also included the Epworth Sleepiness Scale (ESS), a 24point scale that consists of eight situations requiring various degrees of vigilance, each with a score from 0 to 3 (10). This is a simple, self-administered questionnaire which is shown to provide a measurement of the subject’s general level of daytime sleepiness. Anthropometric Measurements Anthropometric measurements, including height, weight, NC and blood pressure, were obtained while the subjects were in light clothing and not wearing shoes. Body mass index (BMI) was calculated by dividing weight (kg) by height squared (m2).
Neck circumference and PIH
According to the NC, they were divided into two groups: normal group (pregnant women with NC534.7 cm, n = 81) and obese group (pregnant women with NC 34.7 cm, n = 45). Blood Pressure Measurements Blood pressure was measured twice with a mercury sphygmomanometer after 10 min of rest while the subjects were seated, and the average of the two measurements was used for analysis. Research assistants reviewed the medical records of the pregnant women. All pregnant women in the hypertensive range had repeated measurements on two subsequent occasions. PIH was defined as blood pressures of 140/90 mmHg or greater on all three occasions (9). Doppler Indices of Umbilical Artery Ultrasound machines utilized included standard Philips IU22 (Philips, Bothell, WA) with curved linear array transabdominal transducers (2–5 MHz). Color Doppler imaging was utilized in all cases. Doppler indices were obtained from the umbilical artery. In all patients, three separate images of Doppler waveforms were obtained to measure umbilical artery pulsatility index (PI) and systolic/diastolic ratio (S/D). Doppler indices were measured on each separate panel uniformly by ultrasound machine software. All ultrasound measurements were obtained by a single registered diagnostic medical sonographer. Statistical Analyses All analyses were performed using the SPSS 11.5 statistical software (SPSS 11.5 for Windows; SPSS, Inc., Chicago, IL). Values are expressed as mean with standard deviation. The two groups were compared using the Student t-test and 2 test. A Pearson correlation coefficient was used to measure the strength of association between variables. Multivariate logistic regression analysis was performed to examine the relationship between PIH and obesity. By using receiver operating characteristic (ROC) analysis, ROC curves of NC was drawn to show how well NC could separate subjects into groups with or without PIH. The area under the curve (AUC) ranges between 0 and 1; it can be interpreted according to the following principles: test equal to chance (AUC = 0.5), less accurate (0.55AUC 0.7), moderately accurate (0.75AUC 0.9), highly accurate (0.95AUC 1.0), and perfect performance (AUC = 1.0). p50.05 was considered statistically significant.
RESULTS Age, as well as clinical, and ultrasonographic data, are presented in Table 1. The frequency of habitual snoring was significantly higher in pregnant women with NC 34.7 cm than in pregnant women with NC 534.7 cm (p50.001). Pre-pregnancy weight, pre-pregnancy BMI, pregnancy weight, pregnancy BMI, weight increase during pregnancy, systolic blood pressure (SBP) and diastolic blood pressure (DBP) were all significantly higher in pregnant women with NC 34.7 cm than in pregnant women with NC 534.7 cm (p50.05). Table 1 also shows the data from the ultrasonic testing. The pregnant women
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J.-T. Shao et al. Table 1. Clinical and ultrasonic characteristics of the subjects with different neck circumference.
Variable Age (y) mean (SD) Gestational weeks (w) mean (SD) Smoking, n (%) Drinking, n (%) Habitual snoring, n (%) ESS mean (SD) Height(m) mean (SD) Pre-pregnancy weight (kg) mean (SD) Pre-pregnancy BMI (kg/m2) mean (SD) Pregnancy weight (kg) mean (SD) Pregnancy BMI (kg/m2) mean (SD) Weight increase during pregnancy (kg) mean (SD) Neck circumference (cm) mean (SD) SBP (mmHg) mean (SD) DBP (mmHg) mean (SD) PI mean (SD) S/D ratio mean (SD) Pregnancy-induced hypertension, n (%)
NC534.7 cm (n = 81)
NC 34.7 cm (n = 45)
t or 2
p
27.6 36.0 0 3 15 8.2 161.7 55.4 21.1 69.8 26.6 14.4
(4.2) (2.8) (0) (3.7) (18.5) (4.1) (4.8) (11.5) (4.6) (7.6) (2.3) (11.1)
28.0 36.2 1 3 26 10.4 163.5 65.4 24.4 84.9 31.7 19.4
(4.4) (2.5) (2.2) (6.7) (57.8) (4.9) (4.3) (14.7) (5.3) (11.9) (4.2) (13.7)
0.445 0.408 0.090 0.560 20.312 2.623 2.053 4.227 3.589 7.623 7.332 2.219
0.657 0.684 0.765 0.454 0.000 0.010 0.042 0.000 0.000 0.000 0.000 0.028
32.5 116.7 77.2 0.96 2.62 2
(1.0) (9.1) (7.8) (0.17) (0.43) (2.5)
36.0 126.9 85.0 1.17 3.10 16
(1.2) (12.7) (10.2) (0.46) (0.57) (35.6)
16.046 4.728 4.784 3.632 5.237 25.863
0.000 0.000 0.000 0.000 0.000 0.000
Values are expressed as mean (SD) and n(%). NC, neck circumference; SD, standard deviation; ESS, Epworth sleepiness scale; BMI, body mass index; SBP, systolic blood pressure; DBP, diastolic blood pressure; PI, pulsatility index; S/D, systolic/diastolic.
with NC 34.7 cm had a higher PI and S/D ratio of umbilical artery than the pregnant women with NC 534.7 cm (p50.001). The frequency of habitual snoring was significantly higher in pregnant women with PIH than in pregnant women without PIH (p50.01). Prepregnancy weight, pre-pregnancy BMI, pregnancy weight, pregnancy BMI, weight increase during pregnancy and NC were all significantly higher in pregnant women with PIH than in pregnant women without PIH (p50.05). The pregnant women with PIH had a higher PI and S/D ratio of umbilical artery than the pregnant women without PIH (p50.001) (Table 2). The correlation coefficients between NC and the other variables for all of the subjects are shown in Table 3. NC showed no correlation with age and gestational weeks (p40.05). NC was positively correlated with ESS (p50.05). NC was also positively correlated with pre-pregnancy weight, pre-pregnancy BMI, pregnancy weight, pregnancy BMI, weight increase during pregnancy, SBP and DBP (p50.05). NC was also positively correlated with PI and S/D ratio of umbilical artery (p50.05). Pregnant women with NC 34.7 cm had significantly higher frequency of PIH than pregnant women with NC 534.7 cm (35.6% versus 2.5%, 2 = 25.863, p = 0.000). After adjustment for age, gestational weeks, smoking, drinking, habitual snoring, pre-pregnancy BMI and pregnancy BMI, the frequency of PIH among pregnant women with NC 34.7 cm was 21.793 (95%CI: 4.717– 100.678, p = 0.000) times compared with pregnant women with NC 534.7 cm.
Neck circumference and PIH Table 2. Clinical and ultrasonic characteristics of the subjects with and without pregnancy-induced hypertension. Non-PIH group (n = 108)
Variable Age (y) mean (SD) Gestational weeks (w) mean (SD) Smoking n (%) Drinking n (%) Habitual snoring n (%) ESS mean (SD) Height(m) mean (SD) Pre-pregnancy weight(kg) mean (SD) Pre-pregnancy BMI (kg/m2) mean (SD) Pregnancy weight (kg) mean (SD) Pregnancy BMI (kg/m2) mean (SD) Weight increase during pregnancy (kg) mean (SD) Neck circumference (cm) mean (SD) SBP (mmHg) mean (SD) DBP (mmHg) mean (SD) PI mean (SD) S/D ratio mean (SD)
PIH group (n = 18)
t or 2
p
27.6 36.0 1 6 30 8.8 162.4 57.5 21.7 72.6 27.4 15.0
(4.5) (2.8) (0.9) (5.6) (27.8) (4.3) (4.7) (13.4) (5.1) (9.1) (2.8) (12.4)
28.2 36.2 0 0 11 10.0 162.1 68.0 25.8 91.1 34.5 23.1
(2.8) (2.2) (0.0) (0.0) (61.1) (5.3) (4.8) (10.8) (3.6) (13.7) (4.4) (8.9)
0.734 0.315 0.168 1.050 7.809 1.011 0.252 3.153 3.226 5.514 6.589 2.614
0.468 0.753 0.682 0.306 0.005 0.314 0.801 0.002 0.002 0.000 0.000 0.010
33.4 117.6 77.9 0.99 2.72
(1.7) (8.8) (7.4) (0.18) (0.53)
35.9 136.9 92.5 1.31 3.22
(2.0) (12.7) (11.0) (0.68) (0.40)
5.437 6.198 5.413 4.078 3.820
0.000 0.000 0.000 0.000 0.000
Values are expressed as mean (SD) and n(%). PIH, pregnancy-induced hypertension; SD, standard deviation; ESS, Epworth sleepiness scale; BMI, body mass index; SBP, systolic blood pressure; DBP, diastolic blood pressure; PI, pulsatility index; S/D, systolic/diastolic.
Table 3. Simple correlations between the neck circumference and other variables in the study subjects. Variable Age (y) Gestational weeks (w) ESS Height (m) Pre-pregnancy weight (kg) Pre-pregnancy BMI (kg/m2) Pregnancy weight (kg) Pregnancy BMI (kg/m2) Weight increase during pregnancy (kg) SBP (mmHg) DBP (mmHg) PI S/D ratio
r
p
0.059 0.080 0.227 0.225 0.361 0.302 0.734 0.737 0.307 0.431 0.344 0.381 0.490
0.510 0.373 0.011 0.011 0.000 0.001 0.000 0.000 0.000 0.000 0.000 0.000 0.000
ESS, Epworth sleepiness scale; BMI, body mass index; SBP, systolic blood pressure; DBP, diastolic blood pressure; PI, pulsatility index; S/D, systolic/diastolic.
The AUC values for the accuracy of NC and BMI in identifying PIH were 0.844 and 0.833, respectively, which indicates moderately accurate. The AUC value of NC was slightly higher than the AUC value of BMI.
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DISCUSSION The results of the present study show that the frequency of PIH was higher in pregnant women with larger NC. NC was positively correlated with SBP and DBP in the third trimester pregnant women. In our study, NC was an independent risk factor for PIH in to multivariate logistic regression. Traditionally, NC has been suggested to be more predictive of obstructive sleep apnea (11). By using a neck skinfold to assess upper body fat distribution as an index, Jean Vague was the first to suggest that morphology and type of fat distribution are associated with obesity (12). In 2001, Ben-Noun et al. found that NC measurement is a simple and time-saving screening measure for identifying overweight and obesity in adults (13). Increasing evidence has demonstrated that NC positively correlated with blood pressures. Changes in SBP and DBP correlated positively with changes in NC (14,15). The relationship between NC and PIH is likely related to the following mechanism. First, symptoms of sleep-disordered breathing are more common in pregnant women compared with non-pregnant women, especially in the third trimester of pregnancy. Snoring and daytime sleepiness were common symptoms of sleep-disordered breathing, and were associated with a higher likelihood of PIH (16,17). In our study, we found that symptoms of sleepdisordered breathing are more common in pregnant women with higher NC. Second, upper body sc fat, as estimated by NC, is a novel measure of cardiometabolic risk (18). Systemic free fatty acid concentrations are primarily determined by upper-body sc fat, suggesting that this fat depot may play an important role in risk factor pathogenesis. Elevated free fatty acid concentrations have been associated with insulin resistance and endothelial cell dysfunction (19). These are two key features in the pathophysiology of PIH (20,21). Measuring NC has several advantages in practice. First, NC measurement is convenient, especially in winter. It is unlike waist circumference measurement, NC measurement does not require the patient to remove her clothing. Second, data show that NC demonstrates good inter- and intra-rater reliability, and does not require multiple measurements for precision and reliability (22). Doppler examination of the umbilical artery flow velocity waveform is widely used in the evaluation of fetal well-being in the third trimester. The waveform is easily demonstrated using impedance indices such as the PI and systolic/diastolic (S/D) ratio permits the waveform to be described. Study using Doppler techniques demonstrates that a high impedance to flow in the uteroplacental circulation in the late second and third trimesters of pregnancy can predict the development of PIH (23). In our study, PI and S/D ratio increased with the NC. These results demonstrate the obesity has a close relationship with uteroplacental circulation. Two limitations of our study should be mentioned. First, reporting on snoring is subjective, although it was supported by their partners. There is no particular study which evaluated the reliability and validity of snoring self-report. Second, this study is a cross-sectional investigation. Prospective studies are warranted to elucidate the predictive value of pre-pregnancy NC for PIH in the third trimester pregnant women.
Neck circumference and PIH
In conclusion, maternal obesity increased risks of PIH. NC is an accurate and easier index for evaluating obesity in pregnancy. The increase of NC was independent risk factor for PIH in the third trimester pregnant women.
DECLARATION OF INTEREST The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the article.
REFERENCES 1. Wang Y, Mi J, Shan XY, et al. Is China facing an obesity epidemic and the consequences? The trends in obesity and chronic disease in China. Int J Obes (Lond) 2007;31:177–88. 2. Shen J, Goyal A, Sperling L. The emerging epidemic of obesity, diabetes, and the metabolic syndrome in china. Cardiol Res Pract 2012;2012:178675. 3. Leung TY, Leung TN, Sahota DS, et al. Trends in maternal obesity and associated risks of adverse pregnancy outcomes in a population of Chinese women. BJOG 2008;115:1529–37. 4. Liang J, Zhu J, Dai L, et al. Maternal mortality in China, 1996–2005. Int J Gynaecol Obstet 2010;110:93–6. 5. Qin M, Zhu LP, Zhang L, et al. Analysis of maternal deaths in Shanghai from 2000 to 2009. Zhonghua Fu Chan Ke Za Zhi 2011;46:24–49. 6. Ye RW, Li HT, Ma R, et al. Prospective cohort study of pregnancy-induced hypertension and risk of preterm delivery and low birth weight. Zhonghua Yu Fang Yi Xue Za Zhi 2010;44:70–4. 7. Heimrath J, Czekan´ski A, Krawczenko A, Dus´ D. The role of endothelium in the pathogenesis of pregnancy-induced hypertension. Postepy Hig Med Dosw (Online) 2007;61:48–57. 8. Gaillard R, Steegers EA, Hofman A, Jaddoe VW. Associations of maternal obesity with blood pressure and the risks of gestational hypertensive disorders. The Generation R Study. J Hypertens 2011;29:937–44. 9. Ursavas A, Karadag M, Nalci N, et al. Self-reported snoring, maternal obesity and neck circumference as risk factors for pregnancy-induced hypertension and preeclampsia. Respiration 2008;76:33–9. 10. Johns MW. A new method for measuring daytime sleepiness: the Epworth sleepiness scale. Sleep 1991;14:540–5. 11. Davies RJ, Ali NJ, Stradling JR. Neck circumference and other clinical features in the diagnosis of the obstructive sleep apnoea syndrome. Thorax 1992;47:101–5. 12. Vague J. The degree of masculine differentiation of obesities: a factor determining predisposition to diabetes, atherosclerosis, gout, and uric calculous disease. Am J Clin Nutr 1956;4:20–34. 13. Ben-Noun L, Sohar E, Laor A. Neck circumference as a simple screening measure for identifying overweight and obese patients. Obes Res 2001;9:470–7. 14. Ben-Noun LL, Laor A. Relationship between changes in neck circumference and changes in blood pressure. Am J Hypertens 2004;17:409–14. 15. Onat A, Hergenc¸ G, Yu¨ksel H, et al. Neck circumference as a measure of central obesity: associations with metabolic syndrome and obstructive sleep apnea syndrome beyond waist circumference. Clin Nutr 2009;28:46–51. 16. Bourjeily G, Raker CA, Chalhoub M, Miller MA. Pregnancy and fetal outcomes of symptoms of sleep-disordered breathing. Eur Respir J 2010;36:849–55. 17. Izci B, Martin SE, Dundas KC, et al. Sleep complaints: snoring and daytime sleepiness in pregnant and pre-eclamptic women. Sleep Med 2005;6:163–9. 18. Preis SR, Massaro JM, Hoffmann U, et al. Neck circumference as a novel measure of cardiometabolic risk: the Framingham Heart study. J Clin Endocrinol Metab 2010;95:3701–10.
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19. Santosa S, Jensen MD. Why are we shaped differently, and why does it matter? Am J Physiol Endocrinol Metab 2008;295:E531–5. 20. Sierra-Laguado J, Garcı´a RG, Celedo´n J, et al. Determination of insulin resistance using the homeostatic model assessment (HOMA) and its relation with the risk of developing pregnancy-induced hypertension. Am J Hypertens 2007;20:437–42. 21. Heimrath J, Krawczenko A, Kozlak J, Dus D. Trophoblasts and soluble adhesion molecules in peripheral blood of women with pregnancy-induced hypertension. Am J Reprod Immunol 2004;51:152–5. 22. LaBerge RC, Vaccani JP, Gow RM, et al. Inter- and intra-rater reliability of neck circumference measurements in children. Pediatr Pulmonol 2009;44:64–9. 23. Steel SA, Pearce JM, McParland P, Chamberlain GV. Early Doppler ultrasound screening in prediction of hypertensive disorders of pregnancy. Lancet 1990;335: 1548–51.
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ORIGINAL ARTICLE
The relationship between neck circumference and pregnancy-induced hypertension in the third trimester pregnant women Jun-Tao Shao,1 Jie Yu,1 Jun-Qiao Qi,2 and Xiao-Dong Liu1 1
Department of Ultrasound, Department of Gynaecology and Obstetrics, The First Hospital of Qinhuangdao, Qinhuangdao, Hebei Province, China
2
Objective: The purpose of this study was to evaluate the relationship between neck circumference (NC) and pregnancy-induced hypertension (PIH) in the third trimester pregnant women. Methods: The study included 126 women who were in the third trimester pregnancy. All subjects completed a standard sleep questionnaire, anthropometric measurements and ultrasonic testing. Results: Pregnant women with NC 34.7 cm had significantly higher frequency of PIH than pregnant women with NC 534.7 cm (35.6% versus 2.5%, 2 = 25.863, p = 0.000). Conclusions: The increase of NC was independent risk factor for PIH in the third trimester pregnant women. Keywords Neck circumference, Pregnancy, Pregnancy-induced hypertension.
INTRODUCTION China is one of the fastest developing countries in the world. Over the past two decades, China has encountered a great economic development. Rapid economic progress has resulted in changes to both diet and physical activity. As a result, the prevalence of overweight or obesity has significantly increased. The prevalence of overweight and obesity rose 49.5% between 1992 and 2002, from 20.0 to 29.9% (1,2). As we all know, obesity is an important risk factor for the development of atherosclerotic cardiovascular disease, type 2 diabetes, dyslipidemia, and hypertension. However, obesity is also associated with increased risks of adverse obstetric outcomes in women (3). Pregnancy-induced hypertension (PIH) is estimated to affect 5–10% of all pregnancies in the China. PIH is the major cause of maternal and perinatal morbidity. In China, PIH was the second cause of maternal deaths (10.3% of the total deaths) (4,5). Mother with PIH is accompanied by protein in the urine and swelling. The most serious consequences of PIH include brain damage in the mother due to brain swelling and oxygen deprivation during seizures. PIH could also increase the incidence of preterm delivery (with PIH 4.9%
Correspondence: Jun-tao Shao, Department of Ultrasound, The First Hospital of Qinhuangdao, No. 258 Wenhua Road, Qinhuangdao 066000, Hebei Province, China. Tel: +86 335 5908325. Fax: +86 335 3032042. E-mail: [email protected]
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versus without PIH 3.4%) and low birth weight (with PIH 3.6% versus without PIH 1.8%) (6). The known risk factors of PIH development are: multiple pregnancy, masculine sex of fetus, very young age of women (below 18 years), advanced age (above 40 years), and obesity of the pregnant woman (7). Maternal obesity increased risks of gestational hypertensive disorders. The risks of PIH among obese mothers was 4.67 times compared with the mothers with a normal weight (8). Neck circumference (NC) is another index for evaluating obesity. In 2008, Ursavas A et al. found that NC was an independent risk factor for PIH (9). There is a racial difference in the relationship between obesity and adverse obstetric outcomes. The impacts of obesity on pre-eclampsia, gestational diabetes and preterm delivery in Chinese women might be stronger than that in Caucasian (3). The aim of our study was to determine the relationship between NC and PIH in the third trimester pregnant women of Qinhuangdao.
METHODS Study Population In 2011, we conducted the study at the First Hospital of Qinhuangdao Hebei, China. A total of 126 pregnant women in the third trimester were recruited at an antenatal clinic. After completing an informed consent form, all subjects completed a standard sleep questionnaire, anthropometric measurements and ultrasonic testing. Socio-demographic variables were collected from women’s self-completed questionnaires and included: age, ethnicity, gestational weeks, body weight prior to pregnancy, smoking and drinking status. Women with a history of chronic hypertension, multiple births, and cardiac, pulmonary and neuromuscular disease were excluded from the study. Women with unknown body weight prior to pregnancy were also excluded. This study was approved by the ethics committee of the First Hospital of Qinhuangdao. Sleep Questionnaire The questionnaire was administered by research assistants. When completing the questionnaire, the women were accompanied by their partners. Women were asked about snoring, and these responses were graded on a Likert scale of 0–4 [0 = never, 1 = rarely (less than once a month), 2 = sometimes (less than once a week), 3 = often (at least once a week) and 4 = always (almost every night)]. Habitual snoring was snoring that occurred often or always. The questionnaire also included the Epworth Sleepiness Scale (ESS), a 24point scale that consists of eight situations requiring various degrees of vigilance, each with a score from 0 to 3 (10). This is a simple, self-administered questionnaire which is shown to provide a measurement of the subject’s general level of daytime sleepiness. Anthropometric Measurements Anthropometric measurements, including height, weight, NC and blood pressure, were obtained while the subjects were in light clothing and not wearing shoes. Body mass index (BMI) was calculated by dividing weight (kg) by height squared (m2).
Neck circumference and PIH
According to the NC, they were divided into two groups: normal group (pregnant women with NC534.7 cm, n = 81) and obese group (pregnant women with NC 34.7 cm, n = 45). Blood Pressure Measurements Blood pressure was measured twice with a mercury sphygmomanometer after 10 min of rest while the subjects were seated, and the average of the two measurements was used for analysis. Research assistants reviewed the medical records of the pregnant women. All pregnant women in the hypertensive range had repeated measurements on two subsequent occasions. PIH was defined as blood pressures of 140/90 mmHg or greater on all three occasions (9). Doppler Indices of Umbilical Artery Ultrasound machines utilized included standard Philips IU22 (Philips, Bothell, WA) with curved linear array transabdominal transducers (2–5 MHz). Color Doppler imaging was utilized in all cases. Doppler indices were obtained from the umbilical artery. In all patients, three separate images of Doppler waveforms were obtained to measure umbilical artery pulsatility index (PI) and systolic/diastolic ratio (S/D). Doppler indices were measured on each separate panel uniformly by ultrasound machine software. All ultrasound measurements were obtained by a single registered diagnostic medical sonographer. Statistical Analyses All analyses were performed using the SPSS 11.5 statistical software (SPSS 11.5 for Windows; SPSS, Inc., Chicago, IL). Values are expressed as mean with standard deviation. The two groups were compared using the Student t-test and 2 test. A Pearson correlation coefficient was used to measure the strength of association between variables. Multivariate logistic regression analysis was performed to examine the relationship between PIH and obesity. By using receiver operating characteristic (ROC) analysis, ROC curves of NC was drawn to show how well NC could separate subjects into groups with or without PIH. The area under the curve (AUC) ranges between 0 and 1; it can be interpreted according to the following principles: test equal to chance (AUC = 0.5), less accurate (0.55AUC 0.7), moderately accurate (0.75AUC 0.9), highly accurate (0.95AUC 1.0), and perfect performance (AUC = 1.0). p50.05 was considered statistically significant.
RESULTS Age, as well as clinical, and ultrasonographic data, are presented in Table 1. The frequency of habitual snoring was significantly higher in pregnant women with NC 34.7 cm than in pregnant women with NC 534.7 cm (p50.001). Pre-pregnancy weight, pre-pregnancy BMI, pregnancy weight, pregnancy BMI, weight increase during pregnancy, systolic blood pressure (SBP) and diastolic blood pressure (DBP) were all significantly higher in pregnant women with NC 34.7 cm than in pregnant women with NC 534.7 cm (p50.05). Table 1 also shows the data from the ultrasonic testing. The pregnant women
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J.-T. Shao et al. Table 1. Clinical and ultrasonic characteristics of the subjects with different neck circumference.
Variable Age (y) mean (SD) Gestational weeks (w) mean (SD) Smoking, n (%) Drinking, n (%) Habitual snoring, n (%) ESS mean (SD) Height(m) mean (SD) Pre-pregnancy weight (kg) mean (SD) Pre-pregnancy BMI (kg/m2) mean (SD) Pregnancy weight (kg) mean (SD) Pregnancy BMI (kg/m2) mean (SD) Weight increase during pregnancy (kg) mean (SD) Neck circumference (cm) mean (SD) SBP (mmHg) mean (SD) DBP (mmHg) mean (SD) PI mean (SD) S/D ratio mean (SD) Pregnancy-induced hypertension, n (%)
NC534.7 cm (n = 81)
NC 34.7 cm (n = 45)
t or 2
p
27.6 36.0 0 3 15 8.2 161.7 55.4 21.1 69.8 26.6 14.4
(4.2) (2.8) (0) (3.7) (18.5) (4.1) (4.8) (11.5) (4.6) (7.6) (2.3) (11.1)
28.0 36.2 1 3 26 10.4 163.5 65.4 24.4 84.9 31.7 19.4
(4.4) (2.5) (2.2) (6.7) (57.8) (4.9) (4.3) (14.7) (5.3) (11.9) (4.2) (13.7)
0.445 0.408 0.090 0.560 20.312 2.623 2.053 4.227 3.589 7.623 7.332 2.219
0.657 0.684 0.765 0.454 0.000 0.010 0.042 0.000 0.000 0.000 0.000 0.028
32.5 116.7 77.2 0.96 2.62 2
(1.0) (9.1) (7.8) (0.17) (0.43) (2.5)
36.0 126.9 85.0 1.17 3.10 16
(1.2) (12.7) (10.2) (0.46) (0.57) (35.6)
16.046 4.728 4.784 3.632 5.237 25.863
0.000 0.000 0.000 0.000 0.000 0.000
Values are expressed as mean (SD) and n(%). NC, neck circumference; SD, standard deviation; ESS, Epworth sleepiness scale; BMI, body mass index; SBP, systolic blood pressure; DBP, diastolic blood pressure; PI, pulsatility index; S/D, systolic/diastolic.
with NC 34.7 cm had a higher PI and S/D ratio of umbilical artery than the pregnant women with NC 534.7 cm (p50.001). The frequency of habitual snoring was significantly higher in pregnant women with PIH than in pregnant women without PIH (p50.01). Prepregnancy weight, pre-pregnancy BMI, pregnancy weight, pregnancy BMI, weight increase during pregnancy and NC were all significantly higher in pregnant women with PIH than in pregnant women without PIH (p50.05). The pregnant women with PIH had a higher PI and S/D ratio of umbilical artery than the pregnant women without PIH (p50.001) (Table 2). The correlation coefficients between NC and the other variables for all of the subjects are shown in Table 3. NC showed no correlation with age and gestational weeks (p40.05). NC was positively correlated with ESS (p50.05). NC was also positively correlated with pre-pregnancy weight, pre-pregnancy BMI, pregnancy weight, pregnancy BMI, weight increase during pregnancy, SBP and DBP (p50.05). NC was also positively correlated with PI and S/D ratio of umbilical artery (p50.05). Pregnant women with NC 34.7 cm had significantly higher frequency of PIH than pregnant women with NC 534.7 cm (35.6% versus 2.5%, 2 = 25.863, p = 0.000). After adjustment for age, gestational weeks, smoking, drinking, habitual snoring, pre-pregnancy BMI and pregnancy BMI, the frequency of PIH among pregnant women with NC 34.7 cm was 21.793 (95%CI: 4.717– 100.678, p = 0.000) times compared with pregnant women with NC 534.7 cm.
Neck circumference and PIH Table 2. Clinical and ultrasonic characteristics of the subjects with and without pregnancy-induced hypertension. Non-PIH group (n = 108)
Variable Age (y) mean (SD) Gestational weeks (w) mean (SD) Smoking n (%) Drinking n (%) Habitual snoring n (%) ESS mean (SD) Height(m) mean (SD) Pre-pregnancy weight(kg) mean (SD) Pre-pregnancy BMI (kg/m2) mean (SD) Pregnancy weight (kg) mean (SD) Pregnancy BMI (kg/m2) mean (SD) Weight increase during pregnancy (kg) mean (SD) Neck circumference (cm) mean (SD) SBP (mmHg) mean (SD) DBP (mmHg) mean (SD) PI mean (SD) S/D ratio mean (SD)
PIH group (n = 18)
t or 2
p
27.6 36.0 1 6 30 8.8 162.4 57.5 21.7 72.6 27.4 15.0
(4.5) (2.8) (0.9) (5.6) (27.8) (4.3) (4.7) (13.4) (5.1) (9.1) (2.8) (12.4)
28.2 36.2 0 0 11 10.0 162.1 68.0 25.8 91.1 34.5 23.1
(2.8) (2.2) (0.0) (0.0) (61.1) (5.3) (4.8) (10.8) (3.6) (13.7) (4.4) (8.9)
0.734 0.315 0.168 1.050 7.809 1.011 0.252 3.153 3.226 5.514 6.589 2.614
0.468 0.753 0.682 0.306 0.005 0.314 0.801 0.002 0.002 0.000 0.000 0.010
33.4 117.6 77.9 0.99 2.72
(1.7) (8.8) (7.4) (0.18) (0.53)
35.9 136.9 92.5 1.31 3.22
(2.0) (12.7) (11.0) (0.68) (0.40)
5.437 6.198 5.413 4.078 3.820
0.000 0.000 0.000 0.000 0.000
Values are expressed as mean (SD) and n(%). PIH, pregnancy-induced hypertension; SD, standard deviation; ESS, Epworth sleepiness scale; BMI, body mass index; SBP, systolic blood pressure; DBP, diastolic blood pressure; PI, pulsatility index; S/D, systolic/diastolic.
Table 3. Simple correlations between the neck circumference and other variables in the study subjects. Variable Age (y) Gestational weeks (w) ESS Height (m) Pre-pregnancy weight (kg) Pre-pregnancy BMI (kg/m2) Pregnancy weight (kg) Pregnancy BMI (kg/m2) Weight increase during pregnancy (kg) SBP (mmHg) DBP (mmHg) PI S/D ratio
r
p
0.059 0.080 0.227 0.225 0.361 0.302 0.734 0.737 0.307 0.431 0.344 0.381 0.490
0.510 0.373 0.011 0.011 0.000 0.001 0.000 0.000 0.000 0.000 0.000 0.000 0.000
ESS, Epworth sleepiness scale; BMI, body mass index; SBP, systolic blood pressure; DBP, diastolic blood pressure; PI, pulsatility index; S/D, systolic/diastolic.
The AUC values for the accuracy of NC and BMI in identifying PIH were 0.844 and 0.833, respectively, which indicates moderately accurate. The AUC value of NC was slightly higher than the AUC value of BMI.
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DISCUSSION The results of the present study show that the frequency of PIH was higher in pregnant women with larger NC. NC was positively correlated with SBP and DBP in the third trimester pregnant women. In our study, NC was an independent risk factor for PIH in to multivariate logistic regression. Traditionally, NC has been suggested to be more predictive of obstructive sleep apnea (11). By using a neck skinfold to assess upper body fat distribution as an index, Jean Vague was the first to suggest that morphology and type of fat distribution are associated with obesity (12). In 2001, Ben-Noun et al. found that NC measurement is a simple and time-saving screening measure for identifying overweight and obesity in adults (13). Increasing evidence has demonstrated that NC positively correlated with blood pressures. Changes in SBP and DBP correlated positively with changes in NC (14,15). The relationship between NC and PIH is likely related to the following mechanism. First, symptoms of sleep-disordered breathing are more common in pregnant women compared with non-pregnant women, especially in the third trimester of pregnancy. Snoring and daytime sleepiness were common symptoms of sleep-disordered breathing, and were associated with a higher likelihood of PIH (16,17). In our study, we found that symptoms of sleepdisordered breathing are more common in pregnant women with higher NC. Second, upper body sc fat, as estimated by NC, is a novel measure of cardiometabolic risk (18). Systemic free fatty acid concentrations are primarily determined by upper-body sc fat, suggesting that this fat depot may play an important role in risk factor pathogenesis. Elevated free fatty acid concentrations have been associated with insulin resistance and endothelial cell dysfunction (19). These are two key features in the pathophysiology of PIH (20,21). Measuring NC has several advantages in practice. First, NC measurement is convenient, especially in winter. It is unlike waist circumference measurement, NC measurement does not require the patient to remove her clothing. Second, data show that NC demonstrates good inter- and intra-rater reliability, and does not require multiple measurements for precision and reliability (22). Doppler examination of the umbilical artery flow velocity waveform is widely used in the evaluation of fetal well-being in the third trimester. The waveform is easily demonstrated using impedance indices such as the PI and systolic/diastolic (S/D) ratio permits the waveform to be described. Study using Doppler techniques demonstrates that a high impedance to flow in the uteroplacental circulation in the late second and third trimesters of pregnancy can predict the development of PIH (23). In our study, PI and S/D ratio increased with the NC. These results demonstrate the obesity has a close relationship with uteroplacental circulation. Two limitations of our study should be mentioned. First, reporting on snoring is subjective, although it was supported by their partners. There is no particular study which evaluated the reliability and validity of snoring self-report. Second, this study is a cross-sectional investigation. Prospective studies are warranted to elucidate the predictive value of pre-pregnancy NC for PIH in the third trimester pregnant women.
Neck circumference and PIH
In conclusion, maternal obesity increased risks of PIH. NC is an accurate and easier index for evaluating obesity in pregnancy. The increase of NC was independent risk factor for PIH in the third trimester pregnant women.
DECLARATION OF INTEREST The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the article.
REFERENCES 1. Wang Y, Mi J, Shan XY, et al. Is China facing an obesity epidemic and the consequences? The trends in obesity and chronic disease in China. Int J Obes (Lond) 2007;31:177–88. 2. Shen J, Goyal A, Sperling L. The emerging epidemic of obesity, diabetes, and the metabolic syndrome in china. Cardiol Res Pract 2012;2012:178675. 3. Leung TY, Leung TN, Sahota DS, et al. Trends in maternal obesity and associated risks of adverse pregnancy outcomes in a population of Chinese women. BJOG 2008;115:1529–37. 4. Liang J, Zhu J, Dai L, et al. Maternal mortality in China, 1996–2005. Int J Gynaecol Obstet 2010;110:93–6. 5. Qin M, Zhu LP, Zhang L, et al. Analysis of maternal deaths in Shanghai from 2000 to 2009. Zhonghua Fu Chan Ke Za Zhi 2011;46:24–49. 6. Ye RW, Li HT, Ma R, et al. Prospective cohort study of pregnancy-induced hypertension and risk of preterm delivery and low birth weight. Zhonghua Yu Fang Yi Xue Za Zhi 2010;44:70–4. 7. Heimrath J, Czekan´ski A, Krawczenko A, Dus´ D. The role of endothelium in the pathogenesis of pregnancy-induced hypertension. Postepy Hig Med Dosw (Online) 2007;61:48–57. 8. Gaillard R, Steegers EA, Hofman A, Jaddoe VW. Associations of maternal obesity with blood pressure and the risks of gestational hypertensive disorders. The Generation R Study. J Hypertens 2011;29:937–44. 9. Ursavas A, Karadag M, Nalci N, et al. Self-reported snoring, maternal obesity and neck circumference as risk factors for pregnancy-induced hypertension and preeclampsia. Respiration 2008;76:33–9. 10. Johns MW. A new method for measuring daytime sleepiness: the Epworth sleepiness scale. Sleep 1991;14:540–5. 11. Davies RJ, Ali NJ, Stradling JR. Neck circumference and other clinical features in the diagnosis of the obstructive sleep apnoea syndrome. Thorax 1992;47:101–5. 12. Vague J. The degree of masculine differentiation of obesities: a factor determining predisposition to diabetes, atherosclerosis, gout, and uric calculous disease. Am J Clin Nutr 1956;4:20–34. 13. Ben-Noun L, Sohar E, Laor A. Neck circumference as a simple screening measure for identifying overweight and obese patients. Obes Res 2001;9:470–7. 14. Ben-Noun LL, Laor A. Relationship between changes in neck circumference and changes in blood pressure. Am J Hypertens 2004;17:409–14. 15. Onat A, Hergenc¸ G, Yu¨ksel H, et al. Neck circumference as a measure of central obesity: associations with metabolic syndrome and obstructive sleep apnea syndrome beyond waist circumference. Clin Nutr 2009;28:46–51. 16. Bourjeily G, Raker CA, Chalhoub M, Miller MA. Pregnancy and fetal outcomes of symptoms of sleep-disordered breathing. Eur Respir J 2010;36:849–55. 17. Izci B, Martin SE, Dundas KC, et al. Sleep complaints: snoring and daytime sleepiness in pregnant and pre-eclamptic women. Sleep Med 2005;6:163–9. 18. Preis SR, Massaro JM, Hoffmann U, et al. Neck circumference as a novel measure of cardiometabolic risk: the Framingham Heart study. J Clin Endocrinol Metab 2010;95:3701–10.
297
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J.-T. Shao et al.
19. Santosa S, Jensen MD. Why are we shaped differently, and why does it matter? Am J Physiol Endocrinol Metab 2008;295:E531–5. 20. Sierra-Laguado J, Garcı´a RG, Celedo´n J, et al. Determination of insulin resistance using the homeostatic model assessment (HOMA) and its relation with the risk of developing pregnancy-induced hypertension. Am J Hypertens 2007;20:437–42. 21. Heimrath J, Krawczenko A, Kozlak J, Dus D. Trophoblasts and soluble adhesion molecules in peripheral blood of women with pregnancy-induced hypertension. Am J Reprod Immunol 2004;51:152–5. 22. LaBerge RC, Vaccani JP, Gow RM, et al. Inter- and intra-rater reliability of neck circumference measurements in children. Pediatr Pulmonol 2009;44:64–9. 23. Steel SA, Pearce JM, McParland P, Chamberlain GV. Early Doppler ultrasound screening in prediction of hypertensive disorders of pregnancy. Lancet 1990;335: 1548–51.
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