High Prevalence of Metabolic Syndrome in Middle-Aged Men Born in Spring

Abstract

Background:

Metabolic syndrome (MetS) is a major cause of increased cardiovascular disease mortality in middle-aged men. Previous studies examined the birth season and health status such as obesity and cardiovascular mortality in adulthood. However, the relationship between birth season and MetS has not yet been studied. In this study, we examined the prevalence of MetS in middle-aged men according to birth season.

Materials and Methods:

In this cross-sectional study, the data were collected from 4575 middle-aged men 30–50 years of age, who underwent a comprehensive health checkup examination. The subjects were separated into four seasons according to birth month.

Results:

There were no statistically significant differences in age according to birth season. However, there was a significant difference in the prevalence of MetS according to birth season: it was highest in spring (25.9%) and lowest in autumn (21.7%, odds ratio [OR] 0.787, 95% confidence interval [CI] 0.646–0.960, P = 0.001). Middle-aged men born in the spring had the highest body mass index (BMI) and prevalence of high waist circumference (WC), high fasting plasma glucose (FPG), and high blood pressure (BP), while those born in autumn had the lowest BMI (η ² = 0.007, P = 0.001) and prevalence of high WC (OR = 0.664, 95% CI 0.558–0.790, P = 0001), high FPG (OR = 0.761, 95% CI 0.624–0.928, P = 0.03), and high BP (OR = 0.633, 95% CI 0.531–0.755, P = 0.001). The prevalence of MetS according to birth months was highest in March (26.8%) and lowest in July (18.6%, OR 0.629, 95% CI 0.444–0.980, P = 0.001).

Conclusion:

Middle-aged men born in the spring had a higher prevalence of MetS than those born in the fall.

Background

Metabolic syndrome (MetS) is a major risk factor for cardiovascular disease (CVD) and all-cause mortality.^1,2 The prevalence of MetS is higher in middle-aged people, especially men.³ MetS is reportedly associated with factors such as physical activity,⁴ education and socioeconomic level,⁵ diet source,⁶ and even fetal characteristics.⁷ Many studies have shown that birth season or month affects adult health status.^8

–13 Interestingly, studies analyzing the correlation between obesity, CVD mortality, and birth season conducted in many countries within the Northern Hemisphere have shown that people born between winter and spring have high rates of obesity or high CVD mortality.^8

–13 It is also well known that the prevalence of MetS is very high among obese and overweight individuals.¹⁴ Mongraw-Chaffin et al.¹⁵ found that almost half of metabolically healthy obese people developed MetS during 12 years of follow-up. Therefore, MetS is also expected to be related to birth season; however, to the best of our knowledge, it has not been studied yet. In this study, we hypothesized that the prevalence of MetS would be higher during the spring season. This study aimed to examine the relationship between the prevalence of MetS and birth season in middle-aged men.

Materials and Methods

Study subjects

This cross-sectional study was conducted by a chart review of records in the Center for Health Promotion, a Pusan National University Yangsan Hospital, Yangsan, South Korea. Initially, the data were collected from 6078 subjects, who underwent a self-paid comprehensive health checkup examination, between January 2008 to December 2018, in Korean men (30–50 years old). Among them, we excluded the data for 1503 individuals for whom there was no information about birth month, metabolic profile, or anthropometric measurements. Finally, a total of 4575 middle-aged men were included in this analysis. As this study used pre-existing, de-identified data, it was exempt from institutional review board approval by the Institutional Review Board (IRB) of Pusan National University Hospital (IRB No. 05-2020-220).

Data collection

The health checkup date, gender, birth month, anthropometric measurements, and laboratory findings, including metabolic profile, were extracted from electronic medical records (EMR). Two experienced clinicians reviewed and abstracted the data. Data were entered into a computerized database and cross-checked. For the clinical data of the patient used in this study, EMR software (YES program 2.0) was used as a text EMR format, and the Yes program 2.0 was certified by Korean Health Information Service. In Korea, the EMR Certification System verifies the conformity of domestic EMR systems to national standards for the purpose of extending assistance for safety and continued treatment of patients. We have treated all data as protected health information and have securely stored it in a password-protected database.

Blood pressure, anthropometric, and laboratory measurements

Blood pressure (BP) was recorded using a sphygmomanometer (BP-203 RV II, Colin Corp., Aichi, Japan). Height and weight were measured with an electronic body meter HM-300 (Fanics Co., Ltd., Busan, South Korea) with a light-weight gown and a height of 0.1 cm and a body weight of 0.1 kg. Body mass index (BMI) (kg/m²) was calculated according to the measured height and weight. Waist circumference (WC) was measured at the narrowest point between the lower borders of the rib cage and the uppermost borders of the iliac crest, the patients were instructed to exhale normally to confirm to the guidelines of the World Health Organization, and the measurements were then recorded up to 0.1 cm. After 8 hr of overnight fasting, peripheral blood samples were collected in ethylenediaminetetraacetic acid tubes from all subjects in the morning. Total cholesterol was measured by the enzymatic colorimetric method, while low-density lipoprotein-cholesterol and high-density lipoprotein-cholesterol (HDL-C) were measured using the direct method (TBA-200FR; Toshiba Medical Systems, Tokyo, Japan). Triglyceride levels were measured using lipase, glycerol kinase, glycerol-3-phosphate oxidase, and peroxidase with glycerol blanking. Fasting glucose levels were determined using the glucose oxidase method (LX20; Beckman Coulter, Brea, CA, USA). All laboratory analyses were performed in a central laboratory.

Definition of MetS

MetS was defined using the National Cholesterol Education Program Adult Treatment Panel III criteria¹⁶ following Asian standards for abdominal obesity,¹⁷ that is, the presence of ≥3 of the following five components: (1) central obesity; WC of ≥90 cm for men and ≥85 cm for women in Koreans,^16,17 (2) hyperglycemia; fasting plasma glucose (FPG) ≥110 mg/dL, (3) high BP; systolic BP ≥130 mmHg or diastolic BP ≥85 mmHg, (4) hypertriglyceridemia; fasting plasma TG ≥150 mg/dL, and (5) reduced HDL-C; fasting level <40 mg/dL (men) and <50 mg/dL (women).

Statistical analyses

The subjects were divided into four groups according to four seasons (Spring, January to March; Summer, April to June; Autumn, July to September; and Winter, October to December) depending on the climate of Korea and the subjects' date of birth and were also divided into 12 groups according to birth months. Subject's age and BMI were reported average (standard deviation). The prevalence of MetS and each component of MetS were expressed as numbers (%). The subjects' age and BMI were compared using a one-way analysis of variance (ANOVA) with Tukey's posthoc test. The effect size of the categories was calculated by the partial eta-squared (η ²) using ANOVA in quantitative data and by the odds ratio (OR) in qualitative data to examine the effect of each birth season or birth month. η ² < 0.06 accounts for a small effect, 0.06 < η ² < 0.14 accounts for a medium effect, and η ² > 0.14 accounts for a big effect. Logistic regression analysis was used to determine the age-adjusted OR and 95% confidence interval (CI) for MetS and MetS components according to each birth season or birth month. P values less than 0.05 were considered significant. All analyses were performed using IBM SPSS statistics software program version 22.0 (IBM Corp., Armonk, NY, USA) and MedCalc for Windows version 9.6.4.0 (MedCalc Software, Mariakerke, Belgium).

Results

The mean male subject age was 41.8 years. Prevalence of MetS and each component of MetS according to the season of birth in middle-aged men is presented in Fig. 1A and Table 1. There were no statistically significant differences in age according to birth season. However, middle-aged men born in spring had the highest BMI and prevalence of high WC, high FPG, and high BP, while those born in autumn had the lowest BMI (η ² = 0.007, P = 0.001; Fig. 1B) and prevalence of high WC (OR 0.664, 95% CI 0.558–0.790, P = 0.001), high FPG (OR 0.761, 95% CI 0.624–0.928, P = 0.03), and high BP (OR 0.633, 95% CI 0.531–0.755, P = 0.001). There was a significant difference in the prevalence of MetS according to birth season: it was highest in spring (25.9%) and lowest in autumn (21.7%, OR 0.787, 95% CI 0.646–0.960, P = 0.001; Table 2).

FIG. 1.

(A) Prevalence of MetS by birth season. See the effect size (Table 3). (B) BMI by birth season. ^a P < 0.001 versus spring, P = 0.024 versus summer, and P = 0.009 versus winter by one-way ANOVA with Tukey's posthoc test. ANOVA, analysis of variance; BMI, body mass index; MetS, metabolic syndrome.

Table 1.

Prevalence of Metabolic Syndrome Components in Middle-Aged Men According to Birth Season

	Spring (n = 1010)	Summer (n = 1177)	Autumn (n = 1168)	Winter (n = 1220)	Total (N = 4575)
Age^a	41.7 (5.9)	41.7 (5.8)	41.8 (5.8)	41.9 (5.8)	41.8 (5.8)
High WC	445 (44.1)	375 (31.9)	401 (34.3)	490 (40.2)	1711 (37.4)
High TG	384 (38.0)	490 (41.6)	449 (38.4)	477 (39.1)	1800 (39.3)
Low HDL-C	156 (15.4)	192 (16.3)	187 (16.0)	171 (14.0)	706 (15.4)
High FPG	272 (26.9)	263 (22.3)	258 (22.1)	288 (23.6)	1081 (23.6)
High BP	421 (41.7)	487 (41.4)	365 (31.3)	509 (41.7)	1782 (38.0)

Data are presented as mean (SD) or number (%). High WC, >90 cm for men and >85 cm for women; High TG, ≥150 mg/dL; Low HDL-C, <40 mg/dL for men and <50 mg/dL for women; High FPG, ≥100 mg/dL; High BP, ≥120/85 mmHg.

P value >0.05 by one-way ANOVA with Tukey's posthoc test.

ANOVA, analysis of variance; BP, blood pressure; FPG, fasting plasma glucose; HDL-C, high-density lipoprotein-cholesterol; SD, standard deviation; TG, triglyceride; WC, waist circumference.

Table 2.

Odds Ratios of Metabolic Syndrome and Each Component of Metabolic Syndrome in Middle-Aged Men According to Birth Season

Birth season	MetS		High WC		High TG		Low HDL-C		High FPG		High BP
	P = 0.001		P = 0.001		P = 0.284		P = 0.405		P = 0.030		P = 0.001
	OR^a	95% CI	OR^a	95% CI	OR^a	95% CI	OR^a	95% CI	OR^a	95% CI	OR^a	95% CI
Spring	1		1		1		1		1		1
Summer	0.835	0.686–1.016	0.593	0.498–0.707	1.163	0.980–1.382	1.068	0.848–1.344	0.781	0.641–0.952	0.989	0.834–1.174
Autumn	0.787	0.646–0.960	0.664	0.558–0.790	1.017	0.856–1.210	1.043	0.827–1.315	0.761	0.624–0.928	0.633	0.531–0.755
Winter	0.870	0.717–1.056	0.853	0.720–1.010	1.045	0.881–1.241	0.891	0.705–1.127	0.826	0.681–1.003	0.997	0.841–1.181

High WC, >90 cm for men and >85 cm for women; High TG, ≥150 mg/dL; Low HDL-C, <40 mg/dL for men and <50 mg/dL for women; High FPG, ≥110 mg/dL; High BP, ≥130/85 mmHg.

Adjusted for age by logistic regression analysis.

CI, confidence interval; MetS, metabolic syndrome; OR, odds ratio.

According to birth month, middle-aged men born in March had the highest BMI and prevalence of high FPG, and high BP, while those born in July had the lowest BMI (η ² = 0.011, P < 0.001; Table 3) and prevalence of high WC (OR 0.596, 95% CI 0.439–0.811, P = 0.001). Middle-aged men born in October and August had the lowest prevalence of high FPG (OR 0.498, 95% CI 0.350–0.708, P = 0.001) and high BP (OR 0.689, 95% CI 0.550–0.949, P = 0.001), respectively. There was a significant difference in the prevalence of MetS according to birth months: it was highest in March (26.8%) and lowest in July (18.6%, OR 0.629, 95% CI 0.444–0.980, P = 0.001; Table 4).

Table 3.

Prevalence of Metabolic Syndrome and Each Component of Metabolic Syndrome in Middle-Aged Men According to Birth Month

Month (n)	BMI^a	MetS	High WC	High TG	Low HDL-C	High FPG	High BP
January (336)	25.2 (3.5)	84 (25.0)	144 (42.9)	126 (37.5)	45 (13.4)	78 (23.2)	142 (42.3)
February (357)	25.5 (3.6)	93 (26.1)	174 (48.7)	129 (36.1)	59 (16.5)	89 (24.9)	155 (43.4)
March (317)	25.6 (3.5)	85 (26.8)	127 (40.1)	129 (40.7)	52 (16.4)	105 (33.1)	124 (39.1)
April (362)	25.5 (3.7)	82 (22.7)	114 (31.5)	143 (39.5)	48 (13.0)	91 (25.1)	161 (44.5)
May (416)	25.0 (3.3)	87 (20.9)	135 (31.5)	168 (40.4)	75 (18.0)	79 (19.0)	151 (36.3)
June (399)	24.7 (3.0)	97 (24.3)	126 (31.6)	179 (44.9)	70 (17.5)	93 (23.3)	175 (43.9)
July (431)	24.3 (3.2)	80 (18.6)	123 (28.5)	154 (35.7)	67 (15.5)	90 (20.9)	139 (32.3)
August (356)	24.8 (3.0)	79 (22.2)	133 (37.4)	146 (41.0)	59 (16.6)	79 (22.2)	108 (30.3)
September (381)	24.9 (3.3)	94 (24.7)	145 (38.1)	149 (39.1)	61 (16.0)	89 (23.4)	118 (31.0)
October (371)	25.0 (3.5)	74 (19.9)	163 (43.9)	149 (40.2)	51 (13.7)	71 (19.1)	123 (33.2)
November (437)	25.1 (3.3)	114 (26.1)	163 (43.9)	179 (41.0)	61 (14.0)	106 (24.3)	198 (45.3)
December (412)	25.1 (3.2)	98 (23.8)	164 (39.8)	149 (36.2)	59 (14.3)	111 (26.9)	188 (45.6)
Total (4575)	25.0 (3.4)	1067 (23.3)	1171 (37.4)	1800 (39.3)	706 (15.4)	1081 (23.6)	1782 (39.0)

Data are presented as mean (SDs) or number (%). High WC, >90 cm for men and >85 cm for women; High TG, ≥150 mg/dL; Low HDL-C, <40 mg/dL for men and <50 mg/dL for women; High FPG, ≥110 mg/dL; High BP, ≥130/85 mmHg.

P value >0.05 by one-way ANOVA with Tukey's posthoc test.

BMI, body mass index.

Table 4.

Odds Ratio of Metabolic Syndrome and Each Component in Middle-Aged Men According to Birth Month

Birth month	MetS		High WC		High TG		Low HDL-C		High FPG		High BP
	P = 0.001		P = 0.001		P = 0.010		P = 0.001		P = 0.001		P = 0.001
	OR^a	95% CI	OR^a	95% CI	OR^a	95% CI	OR^a	95% CI	OR^a	95% CI	OR^a	95% CI
January	0.939	0.661–1.334	1.117	0.818–1.526	0.882	0.644–1.208	0.795	0.516–1.226	0.654	0.461–0.926	1.180	0.862–1.615
February	0.991	0.703–1.398	1.417	1.043–1.924	0.831	0.609–1.135	1.018	0.677–1.531	0.715	0.509–1.004	1.236	0.908–1.683
March	1		1		1		1		1		1
April	0.810	0.570–1.149	0.686	0.501–0.941	0.955	0.702–1.299	0.763	0.498–1.170	0.696	0.497–0.974	1.267	0.932–1.722
May	0.744	0.528–1.050	0.716	0.528–0.970	0.996	0.739–1.341	1.131	0.767–1.669	0.504	0.358–0.710	0.917	0.678–1.241
June	0.897	0.639–1.258	0.688	0.506–0.937	1.193	0.885–1.608	1.092	0.736–1.618	0.643	0.461–0.897	1.248	0.923–1.686
July	0.629	0.444–0.980	0.596	0.439–0.811	0.813	0.603–1.096	0.942	0.634–1.398	0.543	0.389–0.758	0.750	0.554–1.017
August	0.791	0.556–1.126	0.890	0.652–1.215	1.018	0.748–1.385	1.017	0.676–1.530	0.594	0.420–0.840	0.689	0.550–0.949
September	0.919	0.653–1.293	0.916	0.675–1.243	0.943	0.695–1.279	0.979	0.654–1.468	0.651	0.350–0.708	0.719	0.525–0.984
October	0.695	0.487–0.993	1.169	0.862–1.584	0.984	0.725–1.336	0.818	0.538–1.244	0.498	0.350–0.708	0.791	0.578–1.082
November	0.979	0.705–1.359	0.888	0.660–1.195	1.015	0.646–1.363	0.831	0.556–1.242	0.665	0.481–0.920	1.314	0.987–1.764
December	0.862	0.615–1.208	0.988	0.732–1.332	0.828	0.613–1.119	0.855	0.570–1.282	0.763	0.552–1.054	1.326	0.984–1.787

High WC, >90 cm for men and >85 cm for women; High TG, ≥150 mg/dL; Low HDL-C, <40 mg/dL for men and <50 mg/dL for women; High FPG, ≥110 mg/dL; High BP, ≥130/85 mmHg.

Adjusted for age by logistic regression analysis.

Discussion

In this study, the prevalence of MetS in middle-aged men was associated with birth season. The prevalence of MetS was significantly higher in subjects born in spring and lowest in those born in autumn. Most of the diagnostic components of MetS also showed the highest or a high tendency in middle-aged men born in the spring.

A meta-analysis study of three countries reported that birth month affects not only gestational diabetes but also the prevalence of diabetes in adulthood.¹⁸ Since diabetes is a major component of MetS, these studies report that the prevalence of diabetes varies according to birth season and can be a major explanation for the relationship between birth season and MetS. Previous studies reported that the prevalence of obesity was higher in subjects born in the winter or spring.^13,19 These results are similar to those of previous studies on birth season and CVD mortality conducted in several countries. The study results consistently demonstrated that people born in the winter and spring have a high risk of CVD mortality.^8

–12

The reason for the high prevalence of MetS in middle-aged adults born in spring has not been clearly defined; some interpretations that may be the reasons for the link between birth season and obesity prevalence or CVD mortality are detailed in previous studies.^18,20

–23 Many studies recently agreed that the intrauterine environment during the fetal period affects adults' health conditions after birth.⁷ Previous studies suggested that a cold temperature in utero at birth may affect adult BMI.²¹ The mechanism of the effect of fetal temperature exposure on adult BMI has not been fully known. However, in animal study, there have been studies showing that temperature affects the change of sex ratio in reptile.²⁴ It has been reported that temperature-dependent sperm selection or “genetically weak” embryos can abort due to temperature-dependent sex ratio.²⁵ It can be hypothesized that BMI and MetS in adulthood are affected by the drop-out of weak embryos and sperm selection at a low temperature at birth, such as the mechanism of the difference in sex ratio. Men who were born in a warmer month had a lower BMI than those born in a cold month.²⁰ A cross-sectional study of 4286 elderly women in the United Kingdom found that CVD prevalence was greater in women 60–79 years of age, who were born during the cold months.²² Other studies suggested that ultraviolet B and vitamin D can play important roles in adult body size.²¹ There is no experimental study of vitamin D and ultraviolet B effect on postnatal anthropometric levels in the human. However, through animal studies, maternal vitamin D levels, fetal vitamin D levels, and other anthropometric results showed correlation. In one experiment, vitamin D was injected into maternal rat, vitamin D increased even in fetal mice, and it was confirmed that this vitamin D was accumulated in the muscles of fetal rat.²⁶ Other animal studies have also found that vitamin D affects the differentiation on cultured myoblasts of chicks.²⁷ As for human studies, studies that maternal vitamin D affects intrauterine development have been reported only in observational studies after birth, but not in experimental study. However, animal studies suggest that high vitamin D affects fetal muscle growth and lowers the frequency of low BMI or MetS in fetuses into adulthood. Lv et al.²¹ reported that adult obesity status is linked to the amount of vitamin D exposure during the second or third trimester of pregnancy. Boland et al.¹⁸ found that the risk of type 2 diabetes mellitus later in life increased as vitamin D level decreased in the third trimester and perinatal period. An association between social status and birth season was reported by some studies.²³ Buckles and Hungerman²³ suggested that women with more favorable familial and socioeconomic factors chose to avoid colder months for the birth of their child.

This study has some limitations. First, it had a retrospective cross-sectional study design, making it difficult to determine causality. Second, we did not adjust for socioeconomic and lifestyle variables. Third, considering the weather today, it should be considered that the climate 50 years ago was colder than today during all four seasons.²⁸ Finally, because only the data of Korean men were enrolled, our findings cannot be generalized to other ethnicities or geographic regions. Despite the limitations of this study, to the best of our knowledge, it was the first study to analyze the association between birth season and the prevalence of MetS in middle-aged men. However, additional studies are required to confirm the results of this first-stage study, and in-depth follow-up studies are needed to explain the mechanisms by which these effects at birth may affect the development of MetS in middle-aged individuals.

Conclusions

In this study, we found that middle-aged men born in the spring had a higher prevalence of MetS than those born in the fall, especially July. This finding suggests that birth season may be an important factor in determining MetS. Therefore, the risk management of MetS by birth season is necessary. Further research is required to determine the relationship between birth season and MetS.

Footnotes

Authors' Contributions

S.R.L. and S.Y.L. conceived and designed the study, collected the data, and wrote the article. All authors analyzed the data, discussed the results, and contributed to the final article.

Statement of Ethics

As this study used pre-existing, de-identified data, it was exempt from institutional review board approval (IRB No. 05-2020-220). The procedures were in accordance with the Institutional Review Board at Pusan National University Yangsan Hospital and the Helsinki Declaration.

Author Disclosure Statement

No conflicting financial interests exist.

Funding Information

No funding was received for this article.

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