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Original Research (Original Article) 


Hyder Osman Mirghani et al, 2020;4(3):700–705.

International Journal of Medicine in Developing Countries

Circadian misalignment effect on HbA1c among patients with diabetes

Hyder Osman Mirghani1, Sultan Saleh Albalawi2*, Hosam Hadi Awaji3, Abdulrahman Mohammed Naji Alharbi3, Ahmed Marwan Alamrani3, Saeed Ali Ibrahim Alzahrani3, Saud Abdulrahman Saad Alghamdi3, Nawaf Musallam Salem Albalawi3, Sultanah Faisal Alghabban3

Correspondence to: Sultan Saleh Albalawi

*Resident, Medical College, University of Tabuk, Tabuk, Saudi Arabia.

Email: s.s.s.alblawi [at] gmail.com

Full list of author information is available at the end of the article.

Received: 30 December 2019 | Accepted: 16 January 2020


ABSTRACT

Background:

Several research studies have been reporting an association between circadian rhythm and glucose levels. This study was aimed to calculate the prevalence of circadian misalignment in patients with diabetes, to identify the association between sleep parameters and glycemic control, and to investigate its effect on glycemic control, as assessed by hemoglobin a1c (HbA1c).


Methodology:

A cross-sectional study was carried out in the Diabetes Outpatient Clinic at the Diabetes Center, King Fahad Specialist Hospital, Tabuk city, Saudi Arabia. A convenient sample includes adult patients of 18 years or older with either type 1 or type 2 diabetes and residents of Tabuk city. Data collection was carried out through a face-to-face interview using a structured questionnaire.


Results:

This study included 187 diabetic patients. About one-fourth of them (27.3%) reported skipping breakfast three times or more. The bedtime lag between the weekdays and weekend was more than 2 hours in about half (51.3%) of them. Significantly, there was a higher median HbA1c in patients with a higher number (≥3) of skipped breakfast (8.0 vs. 7.0, respectively, p = 0.006). There was a significant negative association between the calculated bedtime lag between the weekdays and weekend and HbA1c (r = –0.16, p = 0.030).


Conclusion:

The findings of this study indicated an association between a circadian misalignment in the form of skipping breakfast ≥3 times/week, bedtime lag between the weekdays and weekends, and poor glycemic control in adult diabetic patients. These findings are expected to contribute to the prevention and risk reduction of complications in diabetic patients.


Keywords:

Circadian misalignment, HbA1c, diabetes.


Introduction

Diabetes mellitus (DM) is a chronic, life-threatening metabolic disorder with a huge disease burden that represents a great challenge to healthcare worldwide. It affects millions of people both globally and in the Middle East. In Saudi Arabia, several major socioeconomic and lifestyle changes predispose to the dramatically increased diabetic prevalence and it’s consistently rising-rate [1]. DM is associated with increased morbidity, and it has been reported to be a leading cause of chronic kidney disease and blindness [2]. Disease management involves lifestyle modifications through regular exercise, a healthy diet, and weight loss, in addition to compliance with suitable drug therapy [3]. The therapy of DM involves either insulin replacement (in type 1 DM) or the use of several classes of drugs such as biguanides, sulfonylureas, meglitinides, intestinal brush border glucosidase inhibitors, and thiazolidinediones (in type 2 DM). However, we have two major limitations to the use of such drugs: the cost (especially, in low-income countries) and the risk of adverse drug reactions such as weight gain, heart failure, and gastrointestinal disturbances [4]. Recent research work displays a growing body of evidence pointing to the role of the biological clock in metabolic homeostasis. Associations between circadian dysregulation and increased prevalence of major disorders such as cancers, obesity, and DM have been reported [5,6]. The circadian rhythms have been defined as endogenous rhythms (with behavioral and physiological components) that have a periodicity of about 24 hours and are synchronized through both photic and nonphotic stimuli. These rhythms are involved in the control of several vital biological processes, such as the sleep-wake cycle, feeding, energy homeostasis, hormone secretion, body temperature regulation, and cell cycle regulation [7]. The circadian system includes, besides several peripheral clocks, the master clock located in the suprachiasmatic nucleus of the hypothalamus, which is regarded as the endogenous biological pacemaker. Daily adjustments of the timing of the suprachiasmatic nucleus following exposure to stimuli, which signals the time of day, help to achieve synchrony with the earth’s rotation. A loss of the coordination of these rhythms could harmfully affect the body physiology and behaviors [8]. Evidence is accumulating about circadian misalignment as being a proposed risk factor for different metabolic diseases. Several research studies have been reporting an association between circadian rhythm disruption and obesity or increased plasma lipid and glucose levels [9]. There appear to be strong relationships between certain sleep parameters as being risk factors for the development of DM. Evolving evidence from several epidemiological and laboratory studies is supporting the fact that poor sleep is strongly associated with the development of glucose intolerance, insulin resistance, and ultimately DM [10]. Therefore, this study aimed to calculate the prevalence of circadian misalignment in patients with diabetes, to identify the association between sleep parameters and glycemic control, and to investigate the effect of circadian misalignment on glycemic control as assessed by hemoglobin a1c (HbA1c).


Subjects and Methods

This cross-sectional study was carried out at the Diabetes Outpatient Clinic, King Fahad Specialist Hospital, Tabuk city, Saudi Arabia. A convenient sample including adult patients of 18 years or older with either type 1 or type 2 diabetes and residents of Tabuk city, presenting for a routine follow-up, was recruited. Patients with gestational diabetes and those younger than 18 years old were excluded from the study. Furthermore, those with the episodes of acute diabetes complications (such as diabetic ketoacidosis or severe hypoglycemia) at the time of enrolment or within the past 3 months before the study and those who have a rapid journey between time zones within the 2 weeks before inclusion in the study were excluded. Data collection was carried out through a face-to-face interview using a structured questionnaire. The data included demographic information, such as age, gender, marital status, level of education, occupation, socioeconomic status; medical information, such as diabetes duration, treatment type, and doses, concomitant diseases, chronic complications, any medical therapy; blood pressure, height, weight, waist circumference, body mass index; HbA1c, fasting plasma glucose, total and high-density lipoprotein cholesterol, triglycerides, and information about bedtime, sleep onset latency, and wake-up time on weekdays and weekends during the previous month. Chronotype was estimated from the mid-sleep time, and circadian misalignment was reported from the working schedule. The Statistical Package for the Social Sciences (SPSS) version 22.0 (SPSS, Chicago, IL) was used for tabulation and all statistical analyses. Results were reported as the median and interquartile range (IQR) or as numbers and percentages. The differences in continuous variables were evaluated using the Mann–Whitney U test and Kruskal–Wallis test, and the differences in categorical variables were assessed using Pearson’s Chi-squared test. Bivariate Spearman’s correlation was used to assess sleep rhythms, circadian misalignment, and HbA1c changes. The multiple linear stepwise regression model includes statistically significant variables with HbA1c in correlation analysis and was adjusted for age, gender, body mass index (BMI), smoking, education, income, and duration of DM. The p < 0.05 was considered to indicate statistical significance.


Results

This study included 187 diabetic patients with a median age of 25 (IQR = 22.0–36.0), and most of them (73.3%) were females (Table 1).

Concerning the duration of DM, it ranged from 1.0– to 38.0 years with a median duration of 8.5 (IQR = 3.0–15.0). The median HbA1c level was 7.0 (IQR = 6.5–8.5), and 65.2% of patients were on insulin. Most of them (76.2%) were not developed complications, whereas the most frequently (14.6%) recorded complication was diabetic retinopathy and visual disturbances. The median usual time of sleep in the weekdays was 3:59 (IQR = 22:30–1:00 AM), whereas it was 3.0 (IQR = 1:30–6:00) in the weekend. The median calculated bedtime lag between the weekdays and weekend was 2.0 hours (IQR = 0.5–6.0), whereas the median calculated wake-up time lag between the weekdays and weekend was 3.54 hours (IQR = 1:08–5:59). In addition, the median hours of sleep in the weekdays were 7.0 (IQR = 6.0–8.0) which increased in the weekend to a median of 9.0 (IQR = 8.0–10.0). The median sleep-onset latency was 10.0 minutes (IQR = 5.0–20.0). Table 2 shows the prevalence of circadian misalignment of feeding and sleep among the studied patients. About one-fourth of them (27.3%) reported skipping breakfast three times or more, and most of them (76.5%) had daily meals three times or less.

A comparison of HbA1c among different categories of circadian misalignment revealed significantly higher median HbA1c in patients with a higher number (≥3) of skipped breakfast (8.0 vs. 7.0, respectively, p = 0.006). Other circadian misalignment showed nonsignificant differences in HbA1c levels as shown in Table 3.

Table 1. Baseline characteristics of the studied patients.

Age (years) Range 18.0–76.0
Median (IQR) 25.0 (22.0–36.0)
BMI Range 29.10–55.0
Mean ± SD 45.7 ± 6.0
N %
Gender Female 137 73.3
Male 50 26.7
Marital status Widow 2 1.1
Single 107 57.2
Married 72 38.5
Divorced 6 3.2
Education Primary 2 1.1
Read and write 5 2.7
Secondary 59 31.6
Diploma 111 59.4
Preparatory 10 5.3
Occupation Not employed 131 70.1
Employed 56 29.9
Monthly income 15,000–30,000 28 15.0
>30,000 6 3.2
<15,000 153 81.8
Do you work by shift? No 173 92.5
Yes 14 7.5
If yes, what is the duration? Variable 14 100.0
Smoking No 161 86.1
Yes 26 13.9
Number of rest hours <1 hour 12 6.4
>3 hours 131 70.1
2–3 hours 44 23.5

Table 2. Prevalence of circadian misalignment in the studied patients.

Numbers of breakfast skipping <3 136 72.7%
≥3 51 27.3%
Number of daily meals ≤3 143 76.5%
>3 44 23.5%
Calculated bedtime lag between the weekdays and weekend (hour) ≤2 91 48.7%
>2 96 51.3%
The calculated wake-up time lag between the weekdays and weekend (hour) ≤4 95 50.8%
>4 92 49.2%
Hours of sleep in the weekdays (hour) ≤8 145 77.5%
>8 42 22.5%
Hours of sleep in the weekend (hour) ≤8 79 42.2%
>8 108 57.8%
Time in bed before sleep (minutes)
“sleep-onset latency”
<30 146 78.1%
>60 14 7.5%
30–60 27 14.4%

Table 4 shows a correlation between sleep rhythms, circadian misalignment, and HbA1c among the studied patients. There was a significant negative association between the calculated bedtime lag between weekdays and weekend and HbA1c (r = –0.16, p = 0.030). In addition, the usual time of wake up during the weekdays showed a significant positive association with HbA1c (r = 0.208, p = 0.004).

A multiple linear stepwise regression model was performed to predict HbA1c from variables that showed significant association with it, and it was adjusted for age, gender, BMI, smoking, education, income, and duration of DM. The model was a good fit with a statistical significance (F = 7.206, p < 0.001). The proportion of variance in HbA1c that can be explained by the variables included in the model (adjusted R2) was 11.8%. It revealed that breakfast skipping, BMI, duration of DM, and monthly income added significantly to the prediction of HbA1c as shown in Table 5


Discussion

This study assessed the relationship between circadian feeding and sleep misalignment and poor glycemic control among Saudi adult diabetic patients. The term “circadian misalignment” describes a variety of circumstances, such as inappropriately timed sleep and wake and misalignment of sleep/wake with feeding rhythms [11]. The present study revealed a 25.9% frequency of skipping breakfast three times or more. Participants with a high frequency of skipped breakfast (≥3) showed significantly higher median HbA1c levels. Consistent with this finding, it has been reported that skipping breakfast was significantly associated with higher HbA1c values and poor glycemic control [12]. Another recent study among Japanese adults reported that subjects who skipped breakfast ≥3 times/week were at increased risk for poor glycemic control defined as HbA1c ≥6.5% [13]. Furthermore, a randomized clinical trial on diabetic patients found that skipping breakfast increased postprandial hyperglycemia after lunch and dinner [14]. The relationship between neglecting breakfast and poor glycemic control might be explained by reduced physical activity and exercise performance throughout the day [15]. Furthermore, a randomized controlled crossover trial concluded more 24- hours energy expenditure on days when breakfast was skipped (+41 kcal/day) compared with control days when three meals were consumed [16]. In our study, bedtime lag as one indicator of circadian misalignment (calculated as the absolute difference between usual bedtime in the weekdays and weekend) showed a significant negative association with HbA1c. The study of circadian misalignment in healthy volunteers has explored possible mechanisms linking circadian misalignment to abnormal glucose metabolism and increased glucose levels [17]. As well, circadian misalignment (caused by delaying bedtime) in healthy subjects was associated with insulin resistance independently of short sleep duration [18]. Furthermore, there was an association between circadian misalignment and poor glycemic control among type 1 diabetic patients. Moreover, there were increased insulin requirements among those with the higher levels of social jetlag [19]. In contrast, social jetlag (calculated based on the absolute difference between the mid-sleep time on the weekdays and weekends) was not significantly associated with higher HbA1c levels in the prediabetic population. They attributed this to the absence of social jetlag in the majority (68%) of their participants [20]. Compared to this, our study reported a bedtime lag in about half of the patients. In this study, patients who recorded a prolonged sleep duration of more than 8 hours on the weekend showed significantly higher HbA1c levels. Moreover, there was a significant positive association between the duration of sleep during the weekdays and weekends and HbA1c. This is in agreement with Ohkuma et al. [21] who demonstrated that both short and long sleep durations relative to the intermediate sleep duration were significantly associated with higher HbA1c levels in Japanese type 2 diabetic patients. In addition, a cross-sectional study among 161 African-American type 2 diabetic patients revealed that the higher HbA1c levels were correlated with shorter weekly sleep duration [22]. The relatively large sample in comparison to prior literature provided a statistical power to this work. However, we had to rely on single HbA1c measurement to assess glycemic control. While it would have been preferable to have multiple measurements, this still is the standard clinical control in patients with diabetes. Another limitation is that while the sleep parameters collected were based on the validated questionnaires, we did not incorporate the objective measures of sleep and circadian misalignment.

Table 3. Comparison of HbA1c among different categories of circadian misalignment.

HbA1c Mann–Whitney test and Kruskal–Wallis test
Median IQR Mean rank p-value
Numbers of breakfast skipping <3 7.0 6.5 8.0 87.35 0.006*
≥3 8.0 6.5 9.5 111.75
Number of daily meals ≤3 7.0 6.5 8.0 93.62 0.860
>3 7.3 6.3 9.3 95.25
Calculated bedtime lag between the weekdays and ­weekend (hour) ≤2 7.5 6.5 8.5 101.46 0.064
>2 7.0 6.5 8.0 86.93
The calculated wake-up time lag between the ­weekdays and weekend (hour) ≤4 7.5 6.5 8.5 98.36 0.259
>4 7.0 6.5 8.0 89.50
Hours of sleep in the weekdays (hour) <8 7.0 6.5 8.5 93.32 0.747
>8 7.5 6.5 8.5 96.35
Hours of sleep in the weekend (hour) <8 7.0 6.5 8.0 89.22 0.297
>8 7.0 6.5 8.5 97.50
Time in bed before sleep (minutes)
“sleep-onset latency”
<30 7.0 6.5 8.0 91.94 0.528
>60 8.0 6.5 9.0 107.64
30–60 7.0 6.5 8.5 98.72

*significant at p < 0.05

Table 4. Correlation between sleep rhythms, circadian misalignment, and HbA1c among the studied patients.

HbA1c
rs p-value
The usual time of sleep in the weekdays (hh: mm) 0.04 0.55
The usual time of sleep in the weekend (hh: mm) 0.41 0.57
Calculated bedtime lag between the weekdays and weekend (hh: mm) –0.16 0.030*
The usual time of wake up in the weekdays (hh: mm) 0.208 0.004*
The usual time of wake up in the weekend (hh: mm) 0.024 0.74
The calculated wake-up time lag between the weekdays and weekend (hh: mm) 0.136 0.063
Hours of sleep in the weekdays (hour) 0.061 0.407
Hours of sleep in the weekend (hour) 0.036 0.621
Number of minutes in bed before sleep (minutes) 0.116 0.115

*significant at p < 0.05

Table 5. A multiple linear stepwise regression model for HbA1c.

Model Unstandardized Standardized t p-value 95% Confidence Interval for B
B B Lower Bound Upper Bound
Constant 7.964 6.208 <0.001* 5.433 10.495
BMI –0.061 –0.192 –2.739 0.007* –0.105 –0.017
Breakfast skipping 0.739 0.172 2.450 0.015* 0.144 1.334
Duration of DM 0.044 0.171 2.475 0.014* 0.009 0.078
Income 0.391 0.147 2.111 0.036* 0.026 0.757

*significant at p < 0.05


Conclusion

The findings of this study indicated a positive association between a circadian misalignment in the form of skipping breakfast ≥3 times/week, prolonged sleep time, especially at the weekends, bedtime lag between the weekdays and weekends, and poor glycemic control in adult diabetic patients. These findings are expected to contribute to the prevention and risk reduction of complications in diabetic patients. Future studies are needed to determine whether behavioral interventions targeting breakfast eating or sleep timing could improve glycemic control in these patients.


List of Abbreviations

DM Diabetes Mellitus
HbA1c Hemoglobin A1c
SPSS Statistical Package for the Social Sciences

Conflict of interest

The authors declare that there is no conflict of interest regarding the publication of this article.


Funding

None.


Consent for publication

Informed consent was obtained from all the participants.


Ethical Approval

The study got ethical approval from the Research Ethics Committee of College of Medicine, Tabuk University, Saudi Arabia (provide the center for approval, date, and letter-number).


Author details

Hyder Osman Mirghani1, Sultan Saleh Albalawi2, Hosam Hadi Awaji3, Abdulrahman Mohammed Naji Alharbi3, Ahmed Marwan Alamrani3, Saeed Ali Ibrahim Alzahrani3, Saud Abdulrahman Saad Alghamdi3, Nawaf Musallam Salem Albalawi3, Sultanah Faisal Alghabban3

  1. Department of Internal Medicine and Endocrine, Medical College, University of Tabuk, Tabuk, Saudi Arabia
  2. Resident, Medical College, University of Tabuk, Tabuk, Saudi Arabia
  3. Intern, Medical College, University of Tabuk, Tabuk, Saudi Arabia

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How to Cite this Article
Pubmed Style

Mirghani HO, Albalawi SS, Awaji HH, Alharbi AMN, Alamrani AM, Alzahrani SAI, Alghamdi SAS, Albalawi NMS, Alghabban SF. Circadian misalignment effect on HbA1c among patients with diabetes. IJMDC. 2020; 4(3): 700-705. doi:10.24911/IJMDC.51-1577741348


Web Style

Mirghani HO, Albalawi SS, Awaji HH, Alharbi AMN, Alamrani AM, Alzahrani SAI, Alghamdi SAS, Albalawi NMS, Alghabban SF. Circadian misalignment effect on HbA1c among patients with diabetes. http://www.ijmdc.com/?mno=80020 [Access: March 29, 2020]. doi:10.24911/IJMDC.51-1577741348


AMA (American Medical Association) Style

Mirghani HO, Albalawi SS, Awaji HH, Alharbi AMN, Alamrani AM, Alzahrani SAI, Alghamdi SAS, Albalawi NMS, Alghabban SF. Circadian misalignment effect on HbA1c among patients with diabetes. IJMDC. 2020; 4(3): 700-705. doi:10.24911/IJMDC.51-1577741348



Vancouver/ICMJE Style

Mirghani HO, Albalawi SS, Awaji HH, Alharbi AMN, Alamrani AM, Alzahrani SAI, Alghamdi SAS, Albalawi NMS, Alghabban SF. Circadian misalignment effect on HbA1c among patients with diabetes. IJMDC. (2020), [cited March 29, 2020]; 4(3): 700-705. doi:10.24911/IJMDC.51-1577741348



Harvard Style

Mirghani, H. O., Albalawi, . S. S., Awaji, . H. H., Alharbi, . A. M. N., Alamrani, . A. M., Alzahrani, . S. A. I., Alghamdi, . S. A. S., Albalawi, . N. M. S. & Alghabban, . S. F. (2020) Circadian misalignment effect on HbA1c among patients with diabetes. IJMDC, 4 (3), 700-705. doi:10.24911/IJMDC.51-1577741348



Turabian Style

Mirghani, Hyder Osman, Sultan Saleh Albalawi, Hosam Hadi Awaji, Abdulrahman Mohammed Naji Alharbi, Ahmed Marwan Alamrani, Saeed Ali Ibrahim Alzahrani, Saud Abdulrahman Saad Alghamdi, Nawaf Musallam Salem Albalawi, and Sultanah Faisal Alghabban. 2020. Circadian misalignment effect on HbA1c among patients with diabetes. International Journal of Medicine in Developing Countries, 4 (3), 700-705. doi:10.24911/IJMDC.51-1577741348



Chicago Style

Mirghani, Hyder Osman, Sultan Saleh Albalawi, Hosam Hadi Awaji, Abdulrahman Mohammed Naji Alharbi, Ahmed Marwan Alamrani, Saeed Ali Ibrahim Alzahrani, Saud Abdulrahman Saad Alghamdi, Nawaf Musallam Salem Albalawi, and Sultanah Faisal Alghabban. "Circadian misalignment effect on HbA1c among patients with diabetes." International Journal of Medicine in Developing Countries 4 (2020), 700-705. doi:10.24911/IJMDC.51-1577741348



MLA (The Modern Language Association) Style

Mirghani, Hyder Osman, Sultan Saleh Albalawi, Hosam Hadi Awaji, Abdulrahman Mohammed Naji Alharbi, Ahmed Marwan Alamrani, Saeed Ali Ibrahim Alzahrani, Saud Abdulrahman Saad Alghamdi, Nawaf Musallam Salem Albalawi, and Sultanah Faisal Alghabban. "Circadian misalignment effect on HbA1c among patients with diabetes." International Journal of Medicine in Developing Countries 4.3 (2020), 700-705. Print. doi:10.24911/IJMDC.51-1577741348



APA (American Psychological Association) Style

Mirghani, H. O., Albalawi, . S. S., Awaji, . H. H., Alharbi, . A. M. N., Alamrani, . A. M., Alzahrani, . S. A. I., Alghamdi, . S. A. S., Albalawi, . N. M. S. & Alghabban, . S. F. (2020) Circadian misalignment effect on HbA1c among patients with diabetes. International Journal of Medicine in Developing Countries, 4 (3), 700-705. doi:10.24911/IJMDC.51-1577741348