Association between Dietary Zinc and Self-Reported Eye Affliction/Retinopathy in Individuals with Diabetes: National Health and Nutrition Examination Survey, 2007–2018

doi:10.21203/rs.3.rs-1615559/v1

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Research Article

Association between Dietary Zinc and Self-Reported Eye Affliction/Retinopathy in Individuals with Diabetes: National Health and Nutrition Examination Survey, 2007–2018

https://doi.org/10.21203/rs.3.rs-1615559/v1

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Background

Emerging evidence supported that dietary zinc is beneficial for diabetes. However, few studies were available concerning the association between dietary zinc and diabetic retinopathy (DR). The present study aimed to describe the association between dietary zinc intake and the risk of DR in US adults.

Methods

A total of 3749 diabetic patients with self-reported eye affliction/retinopathy from the National Health and Nutrition Examination Survey (NHANES) 2007–2018 were involved. Stratified analysis by gender was performed, and logistic regression and restricted cubic spline (RCS) models were applied to assess the association between dietary zinc and DR. Receiver operating characteristic (ROC) curve was used to determine the optimal cut-off value of zinc intake for predicting DR.

Results

Dietary zinc was inversely associated with diabetic retinoapthy in men (OR: 0.981, 95%CI:0.965–0.997), while this trend was not significant in women. Higher quartile of dietary zinc was associated with lower occurrence of diabetic retinopathy (OR: 0.531, 95%CI: 0.334–0.846). Furthermore, increased amounts of dietary zinc was significantly associated with reduced occurrence of diabetic retinopathy (OR: 0.622, 95%CI: 0.411–0.941). ROC analysis identified a daily dietary zinc intake of 7.53 mg as the optimal cut-off value for predicting DR.

Conclusion

Higher levels of dietary zinc are suggested to reduce the risk of diabetic retinopathy and have been observed to have a dose-response effect in men. Assessment of dietary zinc levels may be part of the treatment of patients with diabetic complications.

antioxidant

dietary zinc

diabetic retinopathy

Diabetic retinopathy (DR), remains the most common and serious microvascular complications of diabetes mellitus [1]. The prevalence of DR increases with the number of diabetics, and nearly all persons with type 1 diabetes and more than 60% of those with type 2 have some retinopathy after 20 years [2, 3]. It is also considered to be the leading cause of sight-threatening disease in working-aged people [4]. Factors that are known to influence the development of diabetic retinopathy include modifiable factors, such as blood glucose and blood pressure, smoking, and some non-modifiable factors, such as age, race, and duration of diabetes [5–7].

Zinc is an essential trace element that is obtained from food. It plays an important role in growth and development, immune function, and material metabolism [8–10]. Moreover, zinc has an antioxidant effect, mainly through the following two mechanisms protect tissues from oxidative stress, protect sulfhydryl groups from oxidation, and inhibit the production of reactive oxygen by transition metals [11, 12]. In addition, studies have shown that it can also reduce oxidative stress by inhibiting anti-inflammatory response [13]. Some studies support that zinc can affect glucose homeostasis and improve glycemic control in diabetic patients [14]. Zinc can protect diabetic retinopathy by inhibiting pericytes apoptosis, capillary leakage, and neovascularization, it may be beneficial to prevent diabetic retinopathy [15].

At present, the research on the beneficial effects of antioxidant nutrients on various disorders caused by oxidative stress and diseases has also received widespread attention. However, there are few studies on the potential effects of dietary antioxidant nutrients on diabetes retinopathy. So this paper focuses on the relationship between dietary zinc intake and diabetic retinopathy in US adults through the National Health and Nutrition Examination Survey database.

Methods

1.1 Study Population

The data used in this study were obtained from the NHANES database. NHANES is a cross-sectional survey launched by the National Center for Health Statistics (NCHS) to assess the health and nutritional status of adults and children in the United States. It is released to the public in a two-year cycle. For data users and researchers throughout the world, survey data are available on the internet [16]. The NHANES protocol was approved by the National Center for Health Statistics Ethics Review Board of the US CDC, and all subjects participating in the survey have signed informed consent.

In this study, a total of 59842 individuals participated in the NHANES during 2007 to 2018, of which, 23226 adults aged 40 years and over were identified. In addition, we excluded those who were pregnant (n = 18) and lactating (n = 16). Those who did not complete the dietary review survey (n = 2690) and with an incomplete disease definition questionnaire (n = 16676) were also excluded. Moreover, the individuals with extreme dietary total energy intake (women: <500 or > 5000 kcal/day, men: <500 or > 8000 kcal/day) were further excluded from our study population (n = 32). Finally, 3794 participants (2001 men and 1793 women) were included in the analysis. The detailed process is shown in Fig. 1.

1.2 The Definition of Diabetic Retinopathy

In the main analysis, “diabetes” was defined as the response of "yes" for any of the following questions: “Other than during pregnancy, have you ever been told by a doctor or health professional that you have diabetes or sugar diabetes” or “Are you now taking insulin?” or “Are you now taking diabetic pills to lower blood sugar?” Similarly, we classified respondents as having DR if they answered “yes” to the NHANES question, “Has a doctor ever told you that diabetes has affected your eyes or that you had retinopathy?” [17] .

1.3 Dietary Zinc Intake Assessment

Dietary intake data were assessed by using two 24-hour recall interviews. The first dietary recall interview was collected face-to-face interview between the food interviewer and the participants in the Mobile Examination Center (MEC), and the second dietary recall was collected by telephone and was scheduled 3 to 10 days later. The total dietary intake of zinc was the average intake of two 24-hour dietary review survey data. If participants had not participated in the second survey, the single dietary recall data were used. In addition, the supplements intake of zinc during the past 30 days was also collected, and the average value was taken to represent the daily supplementary intake. Finally, the total zinc intake was calculated by summing the daily dietary and supplementary intake.

1.4 Covariates

The following covariates were included in this study: gender, age, race, educational level, marital status, BMI, annual family income, hypertension, smoking, and total energy intake were obtained from 24-hour dietary recall. We stratified blood glucose control according to HbA1c levels into well-controlled (HbA1c < 7%) and poorly controlled (HbA1c ≥ 7%). Duration of diabetes (< 5 years, 5–10 years, at least 10 years) was calculated from the reported age at screening minus the age of the subject when first told he/she had diabetes.

1.5 Statistical Analysis

All analyses were conducted using SPSS 24.0 and R 3.5.2. According to NHANES analytical guidelines, new special 12-year dietary weights were created by taking one-sixth of the 2-year dietary weights. Kolmogorov-Smirnov normality test was used to verify the normality of continuous variables. Characteristics were described as mean ± standard deviation for normal variables, median (interquartile range) for non-normal variables, and number (percentage) for categorical variables. The differences between continuous and categorical variables were investigated using the independent t-test and the Chi-squared test, respectively.Binary logistic regression analyses were used to explore whether there were associations between dietary zinc intake and DR. We conducted a gender stratified analysis. Model 1: unadjusted. Model 2: adjusted for age. Model 3: adjusted by model 2, race, education, marital status, family income, duration of diabetes, glycemic control, hypertension, smoking, and total energy. In addition, we used a restricted cubic spline (RCS) to further explore the dose-response relationships between dietary zinc intake and DR. To assess the optimal cut-off points of dietary zinc intake, a receiver operating characteristic (ROC) curve analysis was conducted. A two-sided P-value < 0.05 was considered statistically significant.

2.1 Study Population Characteristics

Table 1 showed the demographic characteristics and dietary zinc intake of participants based on gender stratification. We compared the baseline characteristics of individuals with and without DR. In the male, we found that the DR group have lower intake levels of dietary zinc intake (P = 0.005), about half were non-Hispanic white race (P = 0.045), and more likely to be long diabetes duration (P < 0.001) and glycemic poorly controlled (P = 0.005), to have lower education (P = 0.012) and income (P = 0.015). Meanwhile, in female, we found that the DR group have lower education (P = 0.006), income (P = 0.03), and total energy (P = 0.003), to have the characteristics of hypertension (P = 0.003) and smoking (P = 0.019), similarly, and more likely to be long diabetes duration (P < 0.001) and glycemic poorly controlled (P < 0.001). However, there was no significant difference between the two groups identified in terms of age and BMI both in men and women.

Table 1

Characteristics of the population by DR status
Characteristics	Male			Female
Characteristics	DR (+)	DR (-)	P-value	DR (+)	DR (-)	P-value
Age (%)			0.801			0.454
< 65	224 (57.3)	782 (54.6)		174 (52.6)	778 (56.1)
65–79	188 (36.0)	632 (38.0)		146 (34.2)	504 (33.7)
≥ 80	33 (6.7)	162 (7.3)		46 (13.2)	145 (10.2)
Race (%)			0.045			0.681
Mexican American	73 (10.2)	262 (8.4)		64 (11.0)	251 (8.6)
Other Hispanic	49 (5.3)	146 (4.6)		55 (7.0)	166 (6.1)
Non-Hispanic white	129 (58.1)	624 (66.1)		113 (55.6)	459 (58.3)
Non-Hispanic black	115 (15.9)	382 (11.7)		101 (18.3)	425 (17.6)
Other Race	59 (10.4)	162 (9.2)		33 (8.1)	126 (9.3)
Education (%)			0.012			0.006
Less than high school	150 (26.2)	517 (21.0)		156 (37.1)	495 (24.5)
High school	98 (26.8)	339 (21.6)		83 (27.9)	345 (28.4)
More than high school	177 (47.0)	716 (57.4)		126 (34.9)	584 (47.1)
Marital status (%)			0.993			0.008
Married/Living with partner	305 (71.9)	1113 (72.1)		145 (45.5)	679 (55.0)
Widowed/Divorced/Separated	93 (20.7)	342 (20.4)		192 (48.7)	628 (37.3)
Never married	27 (7.4)	119 (7.5)		29 (5.7)	118 (7.8)
Family income (%)			0.015			0.030
< 20000	107 (21.2)	348 (15.6)		128 (33.4)	433 (25.2)
≥ 20000	297 (78.8)	1148 (84.4)		205 (66.6)	928 (74.8)
BMI(‾x ± s)	32.11 ± 0.49	31.98 ± 0.29	0.810	34.67 ± 0.58	33.74 ± 0.29	0.151
Duration of Diabetes (%)			< 0.001			< 0.001
< 5 years	65 (14.1)	467 (33.8)		48 (16.5)	421 (32.0)
5–10 years	60 (14.5)	381 (22.9)		46 (12.3)	331 (23.9)
> 10 years	300 (71.4)	718 (43.3)		266 (71.1)	655 (44.2)
Glycemic control (%)			0.005			< 0.001
well-controlled (HbA1c < 7%)	161 (37.9)	778 (51.5)		138 (41.8)	748 (58.6%)
poorly controlled (HbA1c ≥ 7%)	241 (62.1)	753 (48.5)		215 (58.2)	609 (41.4)
Hypertension (%)			0.459			0.003
Yes	336 (79.8)	1184 (77.7)		316 (86.8)	1127 (77.3)
No	89 (20.2)	392 (22.3)		50 (13.2)	300 (22.7)
Smoking (%)			0.287			0.019
Yes	265 (63.3)	953 (58.8)		133 (36.4)	576 (45.3)
No	160 (36.7)	622 (41.2)		233 (63.6)	851 (54.7)
Total energy (‾x ± s)	2062.13 ± 58.41	2091.88 ± 27.16	0.653	1479.09 ± 45.23	1606.30 ± 24.62	0.022
Zinc (‾x ± s)	15.11 ± 0.61	17.34 ± 0.50	0.005	12.18 ± 0.77	13.81 ± 0.46	0.145

2.2 Association between Dietary Zinc and Diabetic Retinopathy

Table 2 showed that dietary zinc intake was associated with a decreased likelihood of DR with an OR of 0.983 (95% CI: 0.968–0.999) in the total population. In the men group, dietary zinc intake had a substantial correlation with a decreased likelihood of DR with an OR of 0.981 (95% CI: 0.965–0.997) in the fully adjusted model. However, there was no significant difference between dietary zinc intake and DR in the women group (P = 0.215).

Table 2

Weighted odds ratios and 95% confidence intervals of DR according to the daily dietary zinc intake
Model	Total		Male		Female
Model	OR (95%CI)	P-value	OR (95%CI)	P-value	OR (95%CI)	P-value
Model 1^a
Zinc	0.983 (0.970–0.996)	0.011	0.981 (0.968–0.994)	0.005	0.985 (0.965–1.005)	0.145
Model 2^a
Zinc	0.983 (0.970–0.996)	0.011	0.981 (0.968–0.994)	0.006	0.984 (0.965–1.005)	0.128
Model 3^a
Zinc	0.983 (0.968–0.999)	0.042	0.981 (0.965–0.997)	0.024	0.984 (0.959–1.010)	0.215
a: Adjusted covariates:

Model 1: unadjusted

Model 2: adjusted by age

Model 3: adjusted by model 2 + race, education, marital status, family income, duration of diabetes, glycemic control, hypertension, smoking, and total energy

2.3 Association between Quartile of Dietary Zinc and Diabetic Retinopathy

Table 3 estimated associations between the quartiles of dietary zinc intake and risk of DR stratified by gender. In the multivariate-adjusted model, the inverse association of DR for dietary zinc intake was statistically significant in the men group. The multivariate-adjusted OR (95% CI) of DR for the highest versus lowest category of zinc intake were 0.548 (0.369–0.812), 0.548 (0.368–0.816) and 0.531 (0.334–0.846) in model 1, model 2, and model 3, respectively. There was still no significant difference between the women groups (P = 0.340).

Table 3

Weighted odds ratios and 95% confidence intervals of DR across quartiles of dietary zinc intake
Dietary zinc intake(mg/d)	Intake cutoff	Model 1	Model 2	Model 3
		OR (95%CI)	OR (95%CI)	OR (95%CI)
Male
Quartile 1 (low)	≤ 7.14	1.00 (reference)	1.00 (reference)	1.00 (reference)
Quartile 2	7.15–10.71	0.774 (0.447–1.340)	0.781 (0.450–1.355)	0.798 (0.441–1.446)
Quartile 3	10.72–17.74	0.568 (0.380–0.851)*	0.568 (0.378–0.852)*	0.511 (0.317–0.823)*
Quartile 4 (high)	≥ 17.95	0.548 (0.369–0.812)*	0.548 (0.368–0.816)*	0.531 (0.334–0.846)*
p-value		0.016	0.017	0.030
Female
Quartile 1 (low)	≤ 7.14	1.00 (reference)	1.00 (reference)	1.00 (reference)
Quartile 2	7.15–10.71	0.862 (0.510–1.458)	0.862 (0.509–1.460)	1.023 (0.570–1.835)
Quartile 3	10.72–17.74	0.952 (0.587–1.544)	0.950 (0.582–1.551)	1.093 (0.630–1.897)
Quartile 4 (high)	≥ 17.95	0.531 (0.334–0.844)*	0.531 (0.334–0.843)*	0.607 (0.321–1.149)
p-value		0.058	0.057	0.350
Model 1: unadjusted
Model 2:adjusted by age
Model 3:adjusted by model 2 + race, education, marital status, family income, duration of diabetes, glycemic control, hypertension, smoking, and total energy.
*P < 0.05

2.4 Association between Dietary Zinc and the Risk of Diabetic Retinopathy

Furthermore, Fig. 2 showed the RCS on the association between daily dietary zinc intake levels and DR, indicating that the risk of DR generally decreased with increasing daily dietary zinc intake (Figure. 2a, P = 0.002), however, this relationship trend was not obvious in women groups (Figure. 2b, P = 0.107). Additionally, the ROC analysis further showed that a daily dietary zinc intake of 7.53 mg was the optimal cut-off value for predicting DR, with 79.98% specificity and 29.4% sensitivity (Figure. 3). Moreover, by further dividing the individuals into two groups based on daily dietary zinc intake (below or equal to and above the optimal cut-off value), the logistic regression analysis revealed that participants with a daily dietary zinc intake of ≥ 7.53 mg had a 0.526-fold increased odds of DR after adjustment for covariates of age, and 0.622-fold increased odds of DR after the adjustment for all covariates (Table 4).

Table 4

Weighted odds ratios and 95% confidence intervals of DR according to the optimal cut-off value of daily dietary zinc intake
Dietary zinc intake (mg/d)	DR/n	Model 1	Model 2	Model 3
Optimal cut-off
< 7.53	125/409	1 (reference)	1 (reference)	1 (reference)
≥ 7.53	300/1592	0.526 (0.369–0.749)*	0.526 (0.368–0.752)*	0.622 (0.411–0.941)*
p-trend		0.001	0.001	0.025
Model 1: unadjusted
Model 2:adjusted by age
Model 3:adjusted by model 2 + race, education, marital status, family income, duration of diabetes, glycemic control, hypertension, smoking, and total energy
*P < 0.05

In this cross-sectional study based on NHANES (2007–2018), after multivariate logistic regression analysis, we found that dietary zinc was negatively associated with DR in men, while there is no similar significant association was observed in women. This hypothesis was also further tested when we performed a logistic regression analysis of the quartiles of dietary zinc with DR again. To our knowledge, this is the first study to explore the dose-response relationship between dietary zinc intake and DR risk in US adults.

It is well recognized that increased oxidative stress may play a major role in the development of DR, and therefore the use of appropriate antioxidants may have a potential role in the metabolic and functional abnormalities of DR [18, 19]. Antioxidants can increase the ability of antioxidant defense enzymes, inhibit the production of reactive oxygen species (ROS), neutralize free radicals to inhibit abnormal metabolismand slow the progression of DR [20, 21]. Some animal experiments have demonstrated the positive effect of dietary antioxidants on the development of DR. The experimental results suggest that zinc may prevent elevated retinal lipid peroxidation in diabetic rats by binding and stabilizing cell membranes [22, 23]. It has also been shown that long-term intake of nutrients containing antioxidants such as vitamin C and E, carotene, and selenium in diabetic rats can inhibit the development of early diabetic retinopathy [24, 25].

However, clinical trials are few and the results are ambiguous. A cross-sectional study from the US indicated that higher levels of dietary calcium and potassium may reduce the risk of DR [26]. Several studies have also shown that dietary flavonoids, vitamins C and E, carotenoids, and selenium also have some antioxidant properties that reduce the risk of DR with increased intake [27, 28]. However, it has also been suggested that dietary antioxidant vitamins C, E, and β-carotene do not appear to be associated with DR [29, 30]. The reason for such inconsistent results may be that there is such a lack of research on the association between micronutrients and diabetic retinopathy, so it is difficult to find a true link between them.

We have known that zinc is a trace element with antioxidant properties, which can prevent diabetes-induced retinal glutathione loss [13, 22]. It is well known that an important risk factor for DR is blood sugar level, studies have found that zinc is involved in insulin synthesis and transport, reducing blood sugar and insulin resistance, while improving pancreatic β-cell function and reducing disease progression to diabetes [31, 32]. Studies have reported that moderately high dietary zinc intake reduces the risk of T2DM by 13% [33]. In our study, the protective effect of dietary zinc intake on DR was seen in men, although a statistically significant association between DR and gender was not found in this study. A cross-sectional study of diabetic patients over 40 years of age in the US, showed no statistically significant difference in the prevalence of DR between genders, but stepwise logistic regression analyses revealed that compared with women, men had a 50% higher risk of having any DR (OR = 1.50; P = 0.006) [34]. Several studies have also suggested that men may be an independent risk factor for DR, and gender appears to be an important factor influencing diabetic retinopathy [35, 36]. However, the reasons for the difference between men and women are unclear, and more evidence may be needed for the underlying biological plausibility of the association between dietary zinc intake and DR. In addition, in our study, the daily dietary zinc intake of 7.53 mg was determined by the ROC analysis was the best cut-off value for predicting DR, which means that dietary zinc intake should not be less than 7.53 mg per day to obtain a potentially lower risk of DR for adult men over 40 years old in the US. Moreover, an appropriate dietary zinc intake can meet the needs of the organism and maintain proper nutrient reserves in the organization and body health. Too much or too little dietary zinc intake can have certain side effects on the body [37]. Therefore, monitoring and regulating daily dietary zinc intake regularly is of great significance.

Some limitations of this study should be noted. First, the causal relationship could not be determined because of the cross-sectional design in the study. Second, it may be subject to response bias because the definition of DR is based on self-reported data.Third, dietary data were obtained through two 24-hour dietary recall interviews, which may lead to recall bias. Fourth, although we have adjusted for some confounding factors, there may still be some unknown confounding factors left.

dietary zinc was negatively associated with DR in men adjusted by multivariate, and there was a dose-response relationship between dietary zinc intake and DR. Future studies should delve into the relationships between them and the mechanisms of dietary zinc impact on DR, respectively.

Funding

The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.

Competing Interests

The authors have no relevant financial or non-financial interests to disclose.

Author Contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Han Xu, Xinxin Dong and Jin Wang. The first draft of the manuscript was written by Han Xu and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Data Availability

All data generated or analysed during this study are included in this published article [and its supplementary information files].

Ethics approval

Ethics approval was accepted by the institutional review board of the NCHS and study design was confirmed in accordance with the Helsinki Declaration.

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Reviewers agreed at journal
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You are reading this latest preprint version

Association between Dietary Zinc and Self-Reported Eye Affliction/Retinopathy in Individuals with Diabetes: National Health and Nutrition Examination Survey, 2007–2018

Status:

Version 1

Abstract

Background

Methods

Results

Conclusion

Figures

1 Introduction

1.1 Study Population

1.2 The Definition of Diabetic Retinopathy

1.3 Dietary Zinc Intake Assessment

1.4 Covariates

1.5 Statistical Analysis

2 Results

2.1 Study Population Characteristics

2.2 Association between Dietary Zinc and Diabetic Retinopathy

2.3 Association between Quartile of Dietary Zinc and Diabetic Retinopathy

2.4 Association between Dietary Zinc and the Risk of Diabetic Retinopathy

3 Discussion

4 Limitations

5 Conclusion

Declarations

References

Competing Interests

Status:

Version 1