Users Online: 267

Home Print this page Email this page Small font sizeDefault font sizeIncrease font size

Home | About us | Editorial board | Search | Ahead of print | Current issue | Archives | Submit article | Instructions | Subscribe | Contacts | Login 
     

   Table of Contents      
ORIGINAL ARTICLE
Year : 2021  |  Volume : 11  |  Issue : 1  |  Page : 64-70

Dietary Omega-6 to Omega-3 Fatty Acids Ratio is Correlated with High Molecular Weight Adiponectin Level in Indonesian Office Workers


1 Department of Nutrition, Faculty of Medicine, University of Indonesia, Jakarta,Department of Nutrition, Faculty of Medicine and Health Sciences, Krida Wacana Christian University, Jakarta, Indonesia
2 3Department of Biochemistry and Molecular Biology, Faculty of Medicine, University of Indonesia, Jakarta, Indonesia
3 Department of Nutrition, Faculty of Medicine, University of , Jakarta, Indonesia

Date of Submission09-Sep-2020
Date of Decision17-Oct-2020
Date of Acceptance08-Dec-2020
Date of Web Publication25-Jan-2021

Correspondence Address:
MS, PhD Ninik Mudjihartini
Department of Biochemistry and Molecular Biology, Faculty of Medicine, University of Indonesia, Jl. Salemba Raya No. 6, Jakarta 10430
Indonesia
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ijnpnd.ijnpnd_89_20

Rights and Permissions
   Abstract 


Context: Adiponectin is an adipokine that is secreted by adipocytes and acts to prevent obesity and obesity-related disorders. The high ratio of omega-6 to omega-3 fatty acids in modern dietary habits in working-age populations, urban areas in particular, is known to play a role in adiponectin secretion. However, previous studies showed inconclusive results. Aim: The study aims to determine the association of the dietary omega-6 to omega-3 fatty acids ratio with adiponectin levels in office workers in Jakarta, Indonesia. Settings and Design: This cross-sectional study included 55 office workers in East Jakarta, Indonesia. Methods: Data were collected via questionnaire, 3-day food record, anthropometric measurement, and serum collection. Statistical analysis used: Independent t test was applied to assess the relationship between subjects characteristics and dietary intake with high molecular weight adiponectin levels. Association of dietary omega-6/omega-3 fatty acids ratio and adiponectin were evaluated using Pearson correlation test (P < 0.05). Results: There is no statistically significant difference in adiponectin levels based on waist circumference category, as well as categories of physical activity, household income levels, total energy, and total fat intake. Conversely, in female subjects (P = 0.000), subjects with normal body mass index (P = 0.000), higher education levels (P = 0.031), and nonsmoking subjects (P = 0.019), significantly higher adiponectin levels are obtained. The ratio of dietary omega-6/omega-3 fatty acids is negatively correlated with adiponectin (P = 0.004, r = –0.383). Conclusions: The decrease in the ratio of omega-6/omega-3 fatty acids is inversely related to higher level of adiponectin, indicating that dietary changes may potentially play a role in prevention strategies for obesity and obesity-related diseases.

Keywords: HMW adiponectin, obesity, omega-3 fatty acid, omega-6 fatty acid, workers


How to cite this article:
Fabiani H, Mudjihartini N, Lestari W. Dietary Omega-6 to Omega-3 Fatty Acids Ratio is Correlated with High Molecular Weight Adiponectin Level in Indonesian Office Workers. Int J Nutr Pharmacol Neurol Dis 2021;11:64-70

How to cite this URL:
Fabiani H, Mudjihartini N, Lestari W. Dietary Omega-6 to Omega-3 Fatty Acids Ratio is Correlated with High Molecular Weight Adiponectin Level in Indonesian Office Workers. Int J Nutr Pharmacol Neurol Dis [serial online] 2021 [cited 2021 Mar 7];11:64-70. Available from: https://www.ijnpnd.com/text.asp?2021/11/1/64/308618



Key message: A balanced ratio of omega-6 to omega-3 fatty acids in a healthy diet is essential for obesity and its related disease prevention strategies through adiponectin hormone regulation.


   Introduction Top


Obesity and diseases related to obesity are the major causes of mortality and morbidity worldwide.[1] Prevalence of obesity in urban areas with the largest population in Indonesia, such as Jakarta, almost reached 30%, which is the most vulnerable group of the working population with a high socio-economic status.[2] Modern life habits are thought to be a highly influential aspect of urban obesity.[3],[4] Compared to manufacturing workers, office professionals are at greater risk of an energy imbalance due to unhealthy diets, such as high fat and sedentary lifestyle in the workplace and at home.[5]

In obese states, adipocyte dysfunction develops well before obesity emerges and induces dysregulation in certain adipokines secreted by adipose tissue, such as adiponectin.[6],[7] Adiponectin is a protein hormone that has the effect of increased insulin sensitivity and oxidation of fatty acids, anti-atherogenic, and anti-inflammatory agent.[8] Unhealthy dietary habits can contribute to reduced adiponectin secretion, causing dietary modification more relevant to obesity prevention strategies.[6],[9]

Omega-3 fatty acid or alpha-linolenic acid and omega-6 fatty acid or linoleic acid are essential nutrients believed to influence adiponectin concentrations. Eicosapentaenoic acid and docosahexaenoic acid are anti-inflammatory agents that are derived from alpha-linolenic acid and are known to increase adiponectin mRNA expression in adipose tissue. However, this function of omega-3 fatty acids is affected by the pro-inflammatory derivatives of omega-6 fatty acids, arachidonic acid.[10],[11] This is due to the presence of competition between the two fatty acids in the metabolic process, so that the intake of the two fatty acids should be at an acceptable ratio of 1 to 4:1. Modern dietary habits in urban environments, with constantly increasing consumption of omega-6 fatty acids and reduced intake of omega-3 fatty acids, induce a ratio of changes from 1:1 to 20:1 or higher.[3]

Studies on the relationship between omega-6/omega-3 fatty acids intake ratio with adiponectin levels have not been reviewed thoroughly and showed inconclusive results. Thus, differences in dietary intake and genetic variation in each population can be affected.[12],[13] A study found an association between erythocyte omega-3 and omega-3 fatty acid levels with adiponectin.[14] In contrast, other studies have shown that adiponectin levels are declining as the omega-6 fatty acid intake ratio to omega-3 increases, although not statistically significant.[15]

This study aims to assess the ratio of omega-6 fatty acid intake to omega-3 and its association with adiponectin in office workers in one of the regions with the largest working population in Indonesia, East Jakarta.


   Subjects and Methods Top


Study participants

A cross-sectional study with nonprobability consecutive sampling method was conducted from January to July 2020 at Kalbe Farma Company Group in East Jakarta, Indonesia. Office workers, aged 19 to 49 years, that have body mass index (BMI) between 18.5 and 24.9 kg/m2 were screened. Subjects with a history of chronic or metabolic disease based on physical examination and latest medical check-up results; taking antidiabetic, antihyperlipidemic, anti-obesity, glucocorticoids drugs; have a history of alcohol dependency over the past 3 months; are pregnant or breastfeeding; or have been subjected to menopause were excluded. Prior to participation, written informed consent was taken from subjects. Subjects were also asked to complete a socio-demographic questionnaire. A validated Global Physical Activity Questionnaire (GPAQ) Indonesian version was used to generate data on physical activity.[16] The study protocol was approved by the Ethical Committee Faculty of Medicine, University of Indonesia, Jakarta.

Dietary intake

Dietary data were collected from each participant using a validated semi-quantitative food frequency questionnaire (FFQ) for the intake of omega-3 and omega-6 fatty acids over the past 1 month.[17] For total energy and fat intake, 3-day food record was used. Dietary intake was calculated based on local and Asian countries’ food composition data.

Anthropometric measurement

The height and weight measurement were performed according to the standard procedure by using a height measuring board (ShorrBoard, Olney, USA, nearest 0.1 cm) and a weighing scale (Seca GmbH & Co. KG., Hamburg, Germany, nearest 0.1 kg), as well as a measuring tape (Seca GmbH & Co. KG., Hamburg, Germany, nearest 0.1 cm) for waist circumference.

Blood collection and laboratory analysis

An 8-hour fasting blood samples were drawn and centrifuged for 10 minutes at 3000 rpm; the serum was aliquoted into sterile tubes and stored frozen at −20°C until analyzed in the laboratory of the Department of Biochemistry and Molecular Biology, Faculty of Medicine, University of Indonesia, Jakarta. Human high molecular weight (HMW) adiponectin ELISA Kit (Elabscience Biotechnology Co., Ltd, Houston, USA) was used to determine serum adiponectin concentrations. The sensitivity was 3.75 ng/ml, whereas inter-assay and intra-assay coefficients were 3.1% to 6.2% and 3.6% to 5.3%, respectively.

Statistical analysis

The Statistical Package for the Social Sciences (SPSS Ins., Chicago, IL, USA) version 20.1 was used for data analysis. NutriSurvey 2007 (Germany) was used to evaluate dietary intake data. Means and standard deviations (SD) were used to express numerical data. Frequencies and percentages were used to describe categorical data. The relationship between subjects’ characteristics and dietary intake with adiponectin levels was assessed using independent t test. Pearson’s correlation test was applied to evaluate the association of omega-6 fatty acid dietary intake to omega-3 with adiponectin. The association is considered to be significant if P < 0.05.


   Results Top


Fifty-five office workers were recruited, with an average age of 29.9 ± 0.9 years and a female-sex majority. On BMIs that have been restricted, most workers had normal BMI. The mean waist circumference of the subjects was 76.1 ± 9.5 cm. The median physical activity score was 320 (0–3240) metabolic equivalents (METs)/week, with the majority of subjects having low activity levels. Most subjects were nonsmoking, highly educated workers, and only few subjects had a low-income level. Adiponectin levels were obtained the lowest and highest levels, successively being at 4.3 and 7.4 μg/ml [Table 1].
Table 1 Subjects characteristics.

Click here to view


[Table 2] indicates that most subjects did not meet the Institute of Medicine Dietary Reference Intake (DRI) for total energy. Conversely, most subjects had a high total fat intake.[18] The median intake of omega-3 fatty acids in males and females were 1.3 (0.3–5.9) g/day and 1.1 (0.3–4.5) g/day, respectively, while omega-6 fatty acid intake was 11 (1.8–35.9) g/day in males and 9.4 ± 4.9 g/day in females. The maximum ratio of omega-6 fatty acid to omega-3 was 18:1.
Table 2 Distribution of total energy, total fat, omega-6 to omega-3 fatty acid intake ratio.

Click here to view


Adiponectin levels in male workers were significantly lower than in females. Most subjects had sufficient energy intake and the mean difference of adiponectin between these two groups was insignificant. Adiponectin levels were also higher in low total fat intake groups than high total fat intake groups, but not statistically significant. Normoweight subjects had higher adiponectin levels than overweight (P = 0.000), whereas adiponectin levels based on waist circumference did not significantly differ between the two groups [Table 3].
Table 3 The association of HMW adiponectin with subjects characteristic.

Click here to view


[Table 3] also indicates that the mean of adiponectin levels in high-activity level groups was higher than the group whose physical activity is low, although not statistically significant. The mean of adiponectin concentrations in smoking-related groups was lower than in nonsmoking groups (P = 0.019). Subjects with lower education had lower adiponectin levels than higher education groups (P = 0.031). The mean difference of adiponectin levels based on household income level was insignificant.

A weak correlation between dietary omega-6 fatty acid ratio to omega-3 and adiponectin was found in this study (P = 0.004). This shows that the reduction in the omega-6/omega-3 fatty acids ratio will be followed by an increase in the adiponectin and vice versa [Figure 1].
Figure 1 Scatter plot of correlation between omega-6/omega-3 fatty acids ratio and adiponectin.

Click here to view



   Discussion Top


Overall, the adiponectin levels in this study were within the acceptable range.[11] Adiponectin levels in male subjects were substantially lower than in females. Previous studies had also consistently demonstrated adherent findings, where it is understood that high levels of androgen hormones in males are negatively correlated with a decrease in the concentration of adiponectin.[15],[19],[20],[21],[22],[23]

Subjects with normal BMI had significantly higher levels of adiponectin compared to overweight subjects. This finding was consistent with previous studies that have measured adiponectin in conjunction with C-reactive protein, an inflammatory marker. It was found that the increase in BMI will cause elevated C-reactive protein levels.[6],[24] The effects of this inflammatory state contribute to the incidence of adipocyte dysfunction and impaired function of adiponectin mRNA in adipocytes, which decreases the concentration of adiponectin.8

Subjects with normal waist circumference showing higher levels of adiponectin in abdominally obese subjects, although these differences were not statistically significant. A similar finding was also found in research on the African population.25 The body fat distribution can be influenced by ethnic factors, even though it is in the same population.[22],[24],[25] Specific measurement of body fat distribution is needed, whereas in the present study, only a waist circumference examination was conducted to measure the subjects’ visceral fat.

Adiponectin levels in subjects with high levels of activity were slightly higher than those with low levels of activity, but these differences were not statistically significant. Physical activity is associated with body fat reduction, resulting in increased concentrations of adiponectin and its receptors.[6],[22],[24] The effects of this physical activity are thought to be more complex, where the intensity and duration of physical activity are known to have varying effects on adiponectin.[11],[26] However, this study did not specifically measure the duration and intensity of physical activity in the subject.

The low percentage of smoking in this study may have been affected by the high education level in most subjects, where higher education is associated with better health awareness.[21] Adiponectin levels in smoking workers were also slightly lower than those who do not smoke. This finding was consistent with a study in Japan. Nicotine in cigarettes increases tumor necrosis factor-α and free fatty acids that may inhibit the expression of adiponectin genes in adipose tissue. Adiponectin also accumulates and is absorbed by walls of blood vessels that have suffered damage due to smoking.[27]

A positive association between the educational status and adiponectin level in the present study was confirmed by an earlier finding, which resulted in higher adiponectin levels in subjects with higher education levels. Higher education was related to a better knowledge of health, including dietary habits.[21] Lora et al. observed a strong association between the level of education with omega-3 fatty acid intake, where it was understood that omega-3 fatty acids could improve adiponectin secretion.[28],[29] Analysis of dietary intake data on the subject of this study revealed that, in addition to fish products, other omega-3 fatty acids food sources such as chia seeds and fortified chicken eggs, or fish oil supplementation were regularly consumed by highly educated subjects.

Adiponectin levels were significantly higher in subjects with lower income levels compared to high income in this study. This finding was followed by studies of the African-American population, which yielded finding close to the present study.[21] The accessibility to numerous food choices in urban areas has contributed to dietary habits transition in developing countries, where high-economic status populations often appear to consume processed foods rich in saturated fatty acids that may influence adiponectin.[11],[21],[28] Dietary intake data of subjects in this study, an urban population in a developing country, also indicated that high fat intake and processed food are more commonly found in subjects with high income levels.

Compared to previous research, adiponectin levels were lower, although not statistically significant, in subjects with low energy intake than adequate energy intake in the present study. Silva et al. observed that low energy consumption resulted in a rise in the concentration of adiponectin.[10] The discrepancies in this study with previous research may be attributable to the fat intake as a confounding factor. Although energy intake was lower, the percentage of total fat intake was high in this group. The use of palm oil in food production is thought to lead to a high proportion of saturated fatty acids intake, which had been reported in the subject of this study.[30] However, it is identified that saturated fat intake is negatively correlated to adiponectin.[11],[19],[20]

Higher concentrations of adiponectin were found in subjects with low fat intake level, although not statistically significant. Chin et al. also found no such association in their study.[22] In contrast, earlier studies found that high-fat food consumption was strongly inversely associated with adiponectin levels.[19],[20] In addition to fat intake, the intake of carbohydrates also potentially affects adiponectin. High-carbohydrate diet causes fat transfer from peripheral to central and decreases adiponectin activity in peripheral adipose tissue.[6],[19] This is compatible with the dietary intake analysis for this study, which showed that subjects whose low fat intake level tends to have higher intakes of carbohydrates compared to subjects with excess fat intake.

In most subjects in this study, both the adequacy of omega-3 fatty acid intake and its percentage of total energy did not meet DRI. Although most subjects had a low intake of omega-6 fatty acids, compared to total energy, the percentage of omega-6 fatty acid intake in the subjects still exceeded the recommended limit of 2% to 3% of total energy.[18] This finding showed that the contribution of omega-6 fatty acid intake to energy is relatively high. A lower average omega-6 fatty acid intake ratio to omega-3 was observed in this study than in previous studies.[15],[31] Nevertheless, only 7.3% had a ratio of 1 to 4:1 on its own.

The high ratio indicates that the intake of omega-3 fatty acids in most subjects was still relatively low compared to omega-6. The presence of this disparity ratio is considered to raise the incidence of obesity and obesity-related diseases.[3] The development of food technology and accessibility in metropolitan areas and accommodated by high-income office employees may impact that ratio.[3],[4],[5] Low consumption of fish or other fish products and high consumption of saturated fatty acids, as well as the use of palm oil in food processing found in the dietary intake data of most subjects, led to the high intake ratio of omega-6 fatty acids to omega-3.[30]

In the present study, the ratio of omega-6 fatty acid intake to omega-3 was weakly negatively correlated to adiponectin concentrations (r = –0.383; P < 0.05). A stronger correlation was obtained in the study by An et al.,[14] which investigated the association between adiponectin and omega-3 and omega-6 fatty acid levels in erythrocyte membranes, respectively, r = 0.58 and r = –0.64 (P < 0.05). A research analyzing diet focused on the omega-6 fatty acid to omega-3 intake ratio showed that the lowest ratio group of subjects had the highest levels of adiponectin than others.[32]

Omega-6 fatty acid derivatives have potent pro-inflammatory properties. Conversely, omega-3 fatty acid derivatives, are less pro-inflammatory.[33] These inflammatory eicosanoids of omega-6 fatty acids activate pathways leading to adipogenesis. In contrast, omega-3 fatty acids inhibit the activation of this pathway. Although omega-6 fatty acids increase the triglyceride content in adipocytes, omega-3 fatty acids increase fat oxidation.[3],[6],[33] This balanced ratio allows the production of eicosanoids in these two fatty acids to be regulated; thus, the inflammation can be reduced and enhances adiponectin production [3],[6],[24],[32],[33]

Omega-6 fatty acid-derived endocannabinoids can enhance appetite by stimulating their receptors in many tissues. In comparison, omega-3 fatty acids reduce appetite by inhibiting the adaptation of certain endocannabinoid receptors and by inducing anorexigenic neuropeptide proopiomelanocortins in the hypothalamus. The reduction of appetite contributes to a decrease in energy consumption and body fat, which increases adiponectin.[3],[10],[33] Directly, omega-3 fatty acids are the natural ligands of peroxisome proliferator-activated receptor-γ, that is, the key regulator of adiponectin gene transcription.[3],[29],[33]

Although some of the earlier studies confirmed the findings of this study, other studies reported conflicting results. Torres-Castillo et al. found insignificant differences in adiponectin between the three classes of participants depending on the omega-6 fatty acid intake ratio to omega-3. However, adiponectin levels showed an increasing trend as the ratio of these two fatty acids decreases.[15] Murakami et al. studies on the Japanese population also found a corresponding result.[34] Studies on workers in Nigeria also discovered no correlation between omega-3 fatty acid levels and plasma omega-6 with adiponectin.[20]

Murakami et al. did not exclude the history of using drugs as done in this study.[34] While some drugs are known to affect adiponectin.[23] Previous studies used the 3-day food record and the FFQ self-report form to determine the intake of these two fatty acids.[15],[34] Although the semi-quantitative FFQ used in the present study is considered most valid for the assessment of omega-3 and omega-6 fatty acids intake.[17] In previous studies, the form of adiponectin used was total adiponectin.[20] Although the reported adiponectin HMW was the most biologically active form of adiponectin in this research, more precise data could be seen.[11]

The weak correlation found in the present study could be impacted by the research method used. A previous study that used omega-3 and omega-6 fatty acids levels in the erythrocyte membranes found a stronger association, which is known to define intake over a long period of time, making it more precisely relative to dietary intake assessment alone.[14] Fatty acid desaturase gene polymorphism allows the metabolism of these two fatty acids to vary to influence the levels of omega-3 and omega-6 fatty acids in the plasma and erythrocyte membranes.[12] The presence of differences in the ADIPOQ gene controlling adiponectin can also influence the adiponectin gene’s response to these two fatty acids.[13] Polymorphism of these two genes has also probably played a part in the various findings of these studies.The semi-quantitative FFQ of omega-3 and omega-6 fatty acid intake used in this research has a limitation, because it depends on memory that can contribute to bias recall. Lack of omega-3 and omega-6 fatty acids in the Indonesian food database will prompt underestimation or overestimation of the dietary intake analysis. A selection bias induced by sampling methods is another limitation of the present study. The challenge to obtain subjects with complete medical check-up records and meet research criteria into consideration when choosing the sampling method in this study.

Finally, the use of food record methods was a strength of this study. Thus, memory biases can be avoided, particularly in the estimation of total energy and fat intake. In addition, the study findings can also be improved by using HMW adiponectin, which is considered to be the most physiologically active form of adiponectin and could improve the precision of the study findings.[11]


   Conclusion Top


The ratio of dietary omega-6 fatty acid intake to omega-3 in office workers in East Jakarta is weakly negatively associated with adiponectin levels. The proportion of omega-6 to omega-3 fatty acids ratio in the working population should be acknowledged by promoting health education to increase employee’s understanding of the importance of balanced omega-6 to omega-3 fatty acids ratio in the prevention of obesity and obesity-related diseases. Further study is needed on the food composition of omega-3 and omega-6 fatty acids in Indonesia and the use of biomarkers, such as omega-3 and omega-6 fatty acid levels in erythrocytes membrane.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
   References Top

1.
WHO. Noncommunicable Diseases Country Profiles 2018 [Internet]. Geneva: World Health Organization; 2018. p. 11-2. Available from: https://www.who.int/nmh/publications/ncd-profiles-2018/en/. Accessed November 12, 2019.  Back to cited text no. 1
    
2.
Harbuwono DS, Pramono LA, Yunir E, Subekti I. Obesity and central obesity in Indonesia: evidence from a national health survey. Med J Indones 2018;27:53-59.  Back to cited text no. 2
    
3.
Simopoulos AP. An increase in the omega-6/omega-3 fatty acid ratio increases the risk for obesity. Nutrients 2016;8:1-17.  Back to cited text no. 3
    
4.
Mayén AL, Marques-Vidal P, Paccaud F, Bovet P, Stringhini S. Socioeconomic determinants of dietary patterns in low- and middle-income countries: a systematic review. Am J Clin Nutr 2014;100:1520-31.  Back to cited text no. 4
    
5.
Kim JY, Park YH, An EN. The relationship between lifestyles and obesity of office workers in Korea. Int J Control Autom 2015;8:349-60.  Back to cited text no. 5
    
6.
Paniagua JA. Nutrition, insulin resistance and dysfunctional adipose tissue determine the different components of metabolic syndrome. World J Diabetes 2016;7:483.  Back to cited text no. 6
    
7.
Meiliana A, Dewi NM, Wijaya A. Adipose tissue, inflammation (meta-inflammation) and obesity management. Indones Biomed J 2015;7:129.  Back to cited text no. 7
    
8.
Torre-Villalvazo I, Bunt AE, Aleman G, Marques-Mota CC, Diaz-Villasenor A, Noriega LG. Adiponectin synthesis and secretion by subcutaneous adipose tissue is impaired during obesity by endoplasmic reticulum stress. J Cell Biochem 2018;119:5970-84.  Back to cited text no. 8
    
9.
Gariballa S, Alkaabi J, Yasin J, Al Essa A. Total adiponectin in overweight and obese subjects and its response to visceral fat loss. BMC Endocr Disord 2019;19:1-6.  Back to cited text no. 9
    
10.
Silva FM, De Almeida JC, Feoli AM. Effect of diet on adiponectin levels in blood. Nutr Rev 2011;69:599-612.  Back to cited text no. 10
    
11.
Tishinsky JM, Dyck DJ, Robinson LE. Lifestyle factors increasing adiponectin synthesis and secretion. In: Litwack G, editor. Adiponectin (Vitamins and Hormones). 1st ed. San Diego: Elsevier 2012. p. 1-30.  Back to cited text no. 11
    
12.
Brayner B, Kaur G, Keske MA, Livingstone KM. FADS polymorphism, omega-3 fatty acids and diabetes risk: a systematic review. Nutrients 2018;10:1-11.  Back to cited text no. 12
    
13.
Alsaleh A, Sanders TAB, O’Dell SD. Effect of interaction between PPARG, PPARA and ADIPOQ gene variants and dietary fatty acids on plasma lipid profile and adiponectin concentration in a large intervention study. Proc Nutr Soc. 2012;71:141-53.  Back to cited text no. 13
    
14.
An W, Son Y, Kim S et al. Association of adiponectin and leptin with serum lipids and erythrocyte omega-3 and omega-6 fatty acids in dialysis patients. Clin Nephrol 2011;75:195-203.  Back to cited text no. 14
    
15.
Torres-Castillo N, Silva-Gómez JA, Campos-Perez W et al. High dietary ω-6:ω-3 PUFA ratio is positively associated with excessive adiposity and waist circumference. Obes Facts 2018;11:344-53.  Back to cited text no. 15
    
16.
WHO. Global Physical Activity Questionnaire (GPAQ) Analysis Guide [Internet]. Geneva: World Health Organization. 2012. p. 1-22. Available from: http://scholar.google.com/scholar?hl=en&btnG=Search&q=intitle:Global+Physical+Activity+Questionnaire+(GPAQ)+Analysis+Guide#1. Accessed November 15, 2019.  Back to cited text no. 16
    
17.
Ansari MR, Agustina R, Khusun H, Prafiantini E, Cahyaningrum F, Permadhi I. Development and evaluation of a semiquantitative food frequency questionnaire for estimating omega-3 and omega-6 fatty acid intakes in Indonesian children. Asia Pac J Clin Nutr 2016;25:S20-9.  Back to cited text no. 17
    
18.
Institute of Medicine. Dietary Reference Intakes for Energy, Carbohydrates, Fiber, Fat, Fatty adds, Cholesterol, Proteins, and Amino Acids [Internet]. Vol. 7, National Academy of Sciences. Washington: National Academy of Sciences; 2005. Available from: https://www.nal.usda.gov/sites/default/files/fnic_uploads/energy_full_report.pdf.  Back to cited text no. 18
    
19.
Ostrowska L, Fiedorczuk J, Adamska E. Effect of diet and other factors on serum adiponectin concentrations in patients with type 2 diabetes. Rocz Państwowego Zakładu Hig 2013;64:61-66.  Back to cited text no. 19
    
20.
Godwill OC, E K. Relationship between serum adiponectin and plasma fatty acids composition in off-shore (Rig) workers in Bayelsa State, Nigeria. IOSR J Pharm 2013;03:39-46.  Back to cited text no. 20
    
21.
Davis SK, Xu R, Riestra P et al. Association of adiponectin and socioeconomic status in African American men and women: the Jackson heart study. BMC Public Health 2016;16:1-11.  Back to cited text no. 21
    
22.
Chin KH, Sathyasurya DR, Saad HA, Mohamed HJBJ. Effect of ethnicity, dietary intake and physical activity on plasma adiponectin concentrations among Malaysian patients with type 2 diabetes mellitus. Int J Endocrinol Metab 2013;11:167-74.  Back to cited text no. 22
    
23.
Ohman-Hanson RA, Cree-Green M, Kelsey MM et al. Ethnic and sex differences in adiponectin: From childhood to adulthood. J Clin Endocrinol Metab 2016;101:4808-15.  Back to cited text no. 23
    
24.
Conroy SM, Chai W, Lim U, Franke AA, Cooney RV, Maskarinec G. Leptin, adiponectin, and obesity among Caucasian and Asian women. Mediators Inflamm 2011;2011:1-7.  Back to cited text no. 24
    
25.
Awede B, Adovoekpe D, Adehan G et al. Adiponectin, in contrast to leptin, is not associated with body mass index, waist circumference and HOMA-IR in subjects of a west-African population. Physiol Rep 2018;6:1-6.  Back to cited text no. 25
    
26.
Falconer CL, Cooper AR, Walhin JP et al. Sedentary time and markers of inflammation in people with newly diagnosed type 2 diabetes. Nutr Metab Cardiovasc Dis 2014;24:956-62.  Back to cited text no. 26
    
27.
Kotani K, Hazama A, Hagimoto A et al. Adiponectin and smoking status: a systematic review. J Atheroscler Thromb 2012;19:787-94.  Back to cited text no. 27
    
28.
Lora KR, Lewis NM, Eskridge KM, Stanek-Krogstrand K, Travnicek DA. Correlation of omega-3 fatty acids intakes with acculturation and socioeconomic status in Midwestern Latinas. J Immigr Minor Heal 2011;13:111-8.  Back to cited text no. 28
    
29.
Song J, Li C, Lv Y, Zhang Y, Amakye WK, Mao L. DHA increases adiponectin expression more effectively than EPA at relative low concentrations by regulating PPARγ and its phosphorylation at Ser273 in 3T3-L1 adipocytes. Nutr Metab. 2017;14:1-11.  Back to cited text no. 29
    
30.
Harika RK, Eilander A, Alssema M, Osendarp SJM, Zock PL. Intake of fatty acids in general populations worldwide does not meet dietary recommendations to prevent coronary heart disease: a systematic review of data from 40 countries. Ann Nutr Metab 2013;63:229-38.  Back to cited text no. 30
    
31.
Angelia SR, Manikam NRM, Lubis AMT, Siagian C, Mudjihartini N. Association between the ratio of omega-6/omega-3 fatty acids intake to plasma malondialdehyde level in patients with knee osteoarthritis. IOP Conf Ser Earth Environ Sci 2019;217:1-6.  Back to cited text no. 31
    
32.
Fragopoulou E, Panagiotakos DB, Pitsavos C et al. The association between adherence to the Mediterranean diet and adiponectin levels among healthy adults: the ATTICA study. J Nutr Biochem 2010;21:285-9.  Back to cited text no. 32
    
33.
Wang L. Omega-3 and omega-6 fatty acids: role in body fat gain and development of obesity. North Am J Med Sci 2015;8:163-71.  Back to cited text no. 33
    
34.
Murakami K, Sasaki S, Uenishi K. Serum adiponectin concentration in relation to macronutrient and food intake in young Japanese women. Nutrition 2013;29:1315-20.  Back to cited text no. 34
    


    Figures

  [Figure 1]
 
 
    Tables

  [Table 1], [Table 2], [Table 3]



 

Top
 
 
  Search
 
    Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
    Access Statistics
    Email Alert *
    Add to My List *
* Registration required (free)  

 
  In this article
    Abstract
     Introduction
     Subjects and Methods
     Results
     Discussion
     Conclusion
    References
    Article Figures
    Article Tables

 Article Access Statistics
    Viewed289    
    Printed4    
    Emailed0    
    PDF Downloaded12    
    Comments [Add]    

Recommend this journal