Abstract
The aim of this study is to determine the association between environmental organic pollutants with type 2 diabetes. This prospective study was conducted in Federal Urdu University of Arts, Science and Technology (FUUAST) Gulshan-e-Iqbal Campus Karachi in duration from January 2016 to June 2017. This study was ethically approved from the Institutional Review Board of FUUAST. The study included 50 male and female convenient subjects with type 2 diabetes. Subject with other type of diabetes was excluded. Consent was obtained by each individual. Self-structured questionnaire was used for data collection. The comparative results suggest that the maximum level of summation polychlorinated biphenyls (PCBs) mean value was found in age group 27-33 as 0.695 mg/kg in 73% having total individual eleven. Median (interquartile range) of pesticides levels among subjects with normal weight, over weight and obesity were 0.49 (0.26-2.13), 1.53 (0.60-2.65), and 1.60 (1.23-2.05) respectively. It was observed that Organochlorine pesticides (OCS) levels of subjects with overweight and obesity were almost similar (P-value > 0.05) but significantly higher as compared to subjects with normal weight (P-value < 0.05). No significant differences were observed between PCB levels of subjects in terms of body mass index (BMI). In present study we trace the important elements involve in the deposition of persistent organic pollutants and established an association between pollutants with etiology of diabetes and associated disorders such as obesity.
Keywords:
persistent organic pollutants; association; type II diabetes
Resumo
O objetivo deste estudo é determinar a associação entre poluentes orgânicos ambientais com diabetes tipo 2. Este estudo prospectivo foi conduzido na Universidade Federal Urdu de Artes, Ciência e Tecnologia (FUUAST), Gulshan-e-Iqbal, Campus Karachi, com duração de janeiro de 2016 a junho de 2017. Este estudo foi eticamente aprovado pelo Comitê de Revisão Institucional da FUUAST. O estudo incluiu 50 indivíduos convenientes do sexo masculino e feminino com diabetes tipo 2. Indivíduos com outro tipo de diabetes foram excluídos. O consentimento foi obtido por cada indivíduo. Um questionário autoestruturado foi utilizado para a coleta de dados. Os resultados comparativos sugerem que o nível máximo de soma de bifenilas policloradas (PCBs) valor médio foi encontrado na faixa etária 27-33 como 0,695 mg / kg em 73%, tendo total de 11 indivíduos. A mediana (intervalo interquartil) dos níveis de pesticidas entre indivíduos com peso normal, sobrepeso e obesidade foi de 0.49 (0.26-2.13), 1.53 (0.60-2.65) e 1.60 (1.23-2.05), respectivamente. Observou-se que os níveis de pesticidas organoclorados (OCS) de indivíduos com sobrepeso e obesidade eram quase semelhantes (valor P > 0.05), mas significativamente maiores em comparação com indivíduos com peso normal (valor P < 0.05). Não foram observadas diferenças significativas entre os níveis de PCB dos indivíduos em termos de índice de massa corporal (IMC). No presente estudo, rastreamos os elementos importantes envolvidos na deposição de poluentes orgânicos persistentes e estabelecemos uma associação entre os poluentes com a etiologia do diabetes e doenças associadas, como a obesidade.
Palavras-chave:
poluentes orgânicos persistentes; associação; diabetes tipo II
1. Introduction
Type 2 diabetes has become as a major health problem of public and its pandemic cause burden for health care professionals throughout the world (Onyango and Onyango, 2018ONYANGO, E.M. and ONYANGO, B.M., 2018. The rise of noncommunicable diseases in Kenya: an examination of the time trends and contribution of the changes in diet and physical inactivity. Journal of Epidemiology and Global Health, vol. 8, no. 1-2, pp. 1-7. http://dx.doi.org/10.2991/j.jegh.2017.11.004. PMid:30859780.
http://dx.doi.org/10.2991/j.jegh.2017.11...
). This disease has impact on quality of life and activities of an individual that leads towards an increased morbidity and mortality of individuals (Ramtahal et al., 2015RAMTAHAL, R., KHAN, C., MAHARAJ-KHAN, K., NALLAMOTHU, S., HINDS, A., DHANOO, A., YEH, H.-C., HILL-BRIGGS, F. and LAZO, M., 2015. Prevalence of self-reported sleep duration and sleep habits in type 2 diabetes patients in south Trinidad. Journal of Epidemiology and Global Health, vol. 5, no. 4, suppl. 1, pp. S35-S43. http://dx.doi.org/10.1016/j.jegh.2015.05.003. PMid:26073574.
http://dx.doi.org/10.1016/j.jegh.2015.05...
). Currently, focus has increased on diabetes related deaths in people less than age of 60 years (Alotaibi et al., 2017ALOTAIBI, A., PERRY, L., GHOLIZADEH, L. and AL-GANMI, A., 2017. Incidence and prevalence rates of diabetes mellitus in Saudi Arabia: an overview. Journal of Epidemiology and Global Health, vol. 7, no. 4, pp. 211-218. http://dx.doi.org/10.1016/j.jegh.2017.10.001. PMid:29110860.
http://dx.doi.org/10.1016/j.jegh.2017.10...
). Elements including unhealthy diets and sedentary lifestyles, resulting in elevated Body Mass Index (BMI) and fasting plasma glucose are considered for these circumstances (Lone et al., 2017LONE, S., LONE, K., KHAN, S. and PAMPORI, R.A., 2017. Assessment of metabolic syndrome in Kashmiri population with type 2 diabetes employing the standard criteria’s given by WHO, NCEPATP III and IDF. Journal of Epidemiology and Global Health, vol. 7, no. 4, pp. 235-239. http://dx.doi.org/10.1016/j.jegh.2017.07.004. PMid:29110863.
http://dx.doi.org/10.1016/j.jegh.2017.07...
). Particularly, individuals with elevated Body mass index are prone to have type 2 diabetes (Mahanta et al., 2013MAHANTA, T.G., JOSHI, R., MAHANTA, B.N. and XAVIER, D., 2013. Prevalence of modifiable cardiovascular risk factors among tea garden and general population in Dibrugarh, Assam, India. Journal of Epidemiology and Global Health, vol. 3, no. 3, pp. 147-156. http://dx.doi.org/10.1016/j.jegh.2013.04.001. PMid:23932057.
http://dx.doi.org/10.1016/j.jegh.2013.04...
). Unless these traditional risk factors evidence on the contribution of environmental contaminants to the prompt rise in the incidence of type 2 diabetes (Wolf et al., 2019WOLF, K., BONGAERTS, B.W.C., SCHNEIDER, A., HUTH, C., MEISINGER, C., PETERS, A., SCHNEIDER, A., WITTSIEPE, J., SCHRAMM, K.-W., GREISER, K.H., HARTWIG, S., KLUTTIG, A. and RATHMANN, W., 2019. Persistent organic pollutants and the incidence of type 2 diabetes in the CARLA and KORA cohort studies. Environment International, vol. 129, pp. 221-228. http://dx.doi.org/10.1016/j.envint.2019.05.030. PMid:31132656.
http://dx.doi.org/10.1016/j.envint.2019....
).
Persistent organic pollutants (POPs), are group of environmental pollutants, that involved to enhance quality of some products commonly used in our daily living, but their properties of being bio-accumulated in environment induce unexpectedly harmful effects to human health (Yang et al., 2017YANG, C., KONG, A.P.S., CAI, Z. and CHUNG, A.C., 2017. Persistent organic pollutants as risk factors for obesity and diabetes. Current Diabetes Reports, vol. 17, no. 12, p. 132. http://dx.doi.org/10.1007/s11892-017-0966-0. PMid:29098478.
http://dx.doi.org/10.1007/s11892-017-096...
). To overcome the strategy the National Toxicology Program (NTP) at the National Institute of Environmental Health Sciences (NIEHS) conducted a workshop in the month of January year 2011(Taylor et al., 2013TAYLOR, K.W., NOVAK, R.F., ANDERSON, H.A., BIRNBAUM, L.S., BLYSTONE, C., DEVITO, M., JACOBS, D., KÖHRLE, J., LEE, D.H., RYLANDER, L., RIGNELL-HYDBOM, A., TORNERO-VELEZ, R., TURYK, M.E., BOYLES, A.L., THAYER, K.A. and LIND, L., 2013. Evaluation of the association between Persistent Organic Pollutants (POPs) and diabetes in epidemiological studies: a national toxicology program workshop review. Environmental Health Perspectives, vol. 121, no. 7, pp. 774-783. http://dx.doi.org/10.1289/ehp.1205502. PMid:23651634.
http://dx.doi.org/10.1289/ehp.1205502...
). They examine the associations between certain chemicals and obesity along with diabetes. A wide variety of chemicals were included in the POPs category. The relation between persistent organic pollutants (POPs) and the development of type 2 diabetes had shown for over ten years, additionally many reviews and one meta-analysis of epidemiological studies combined the findings validating the initial statements (Wolf et al., 2019WOLF, K., BONGAERTS, B.W.C., SCHNEIDER, A., HUTH, C., MEISINGER, C., PETERS, A., SCHNEIDER, A., WITTSIEPE, J., SCHRAMM, K.-W., GREISER, K.H., HARTWIG, S., KLUTTIG, A. and RATHMANN, W., 2019. Persistent organic pollutants and the incidence of type 2 diabetes in the CARLA and KORA cohort studies. Environment International, vol. 129, pp. 221-228. http://dx.doi.org/10.1016/j.envint.2019.05.030. PMid:31132656.
http://dx.doi.org/10.1016/j.envint.2019....
).
Few from previous studies reported environmental pollutants are responsible for dysfunction of energy metabolism in adipose tissue (Grün and Blumberg, 2006GRÜN, F. and BLUMBERG, B., 2006. Environmental obesogens: organotins and endocrine disruption via nuclear receptor signaling. Endocrinology, vol. 147, no. 6, suppl., pp. S50-S55. http://dx.doi.org/10.1210/en.2005-1129. PMid:16690801.
http://dx.doi.org/10.1210/en.2005-1129...
). Moreover, there are substantial differences in phenotypic characteristics and profiles of diabetes related complications in patients with diabetes worldwide, suggesting the possible contributions of environmental factors, including pollutants, on top of genetic factors, which add to the complexity of the understanding of diabetes (Kong et al., 2013KONG, A.P., XU, G., BROWN, N., SO, W.Y., MA, R.C. and CHAN, J.C., 2013. Diabetes and its comorbidities—where East meets West. Nature Reviews. Endocrinology, vol. 9, no. 9, pp. 537-547. http://dx.doi.org/10.1038/nrendo.2013.102. PMid:23712250.
http://dx.doi.org/10.1038/nrendo.2013.10...
). The aim of this study is to determine the association between environmental organic pollutants with type 2 diabetes.
2. Materials and Methods
This prospective study was conducted in Federal Urdu University of Arts, Science and Technology (FUUAST) Gulshan-e-Iqbal Campus Karachi in duration from January 2016 to June 2017. This study was ethically approved from the Institutional Review Board of FUUAST. The study included 50 male and female convenient subjects with type 2 diabetes. Subject with other type of diabetes was excluded. These individuals were selected conveniently from the general residents of Karachi city of Pakistan. Consent was obtained by each individual. Self-structured questionnaire was used for data collection (Ahn et al., 2007AHN, Y., KWON, E., SHIM, J.E., PARK, M.K., JOO, Y., KIMM, K., PARK, C. and KIM, D.H., 2007. Validation and reproducibility of food frequency questionnaire for Korean genome epidemiologic study. European Journal of Clinical Nutrition, vol. 61, no. 12, pp. 1435-1441. http://dx.doi.org/10.1038/sj.ejcn.1602657. PMid:17299477.
http://dx.doi.org/10.1038/sj.ejcn.160265...
). Obesity was defined as BMI (kg/m2) which were categorized as follows: normal weight (18-22.9 kg/m2), overweight (23.0-24.9 kg/m2) and and obese (≥25.0 kg/m2).
2.1. Sample site areas
We select the samples from industrial areas where use excessive harmful substances and due to less sufficient facilities found a lot of environmental contamination. The use of unusual resources, and continuously destruction of environmental resources causes harmful effect to unban productivity.
Collection of blood samples: Blood collection was very simply, as blood drawn from inside the elbow vein. The phlebotomists insert the syringe slightly in this vein and draw small amount of blood (up to 10ml) collected in to airtight tube attached to the syringe needle and then remove the elastic band from the arm and then syringe from the vein. The blood samples were kept carefully in the ice flask and stored at minus 20ᵒC in the deep freezer for further analysis.
2.2. Serum sepration
The blood samples kept in room temperature for few minutes until the sample become defrost then centrifuged the samples for 5 minutes at 3000 rpm. The separated serum collected from the blood by centrifugation then transfer into another vials and the rest of the blood is discarded carefully by covering in the polythene bags.
2.3. Extraction of pesticides from serum
The 5ml of serum from each sample were equilibrating at room temperature by adding 2ml of methanol and shake for 1 minute. After this 5ml n-hexane and diethyl ether (1׃1 v/v) added and left the samples for 2 minutes and again centrifuge these samples for 5 minutes at 3000 rpm.
Following the centrifugation, the organic phase collects and aqueous phase remove twice with n-hexane, diethyl ether (1׃1 v/v). After this the organic phase allows to evaporate until 1ml organic phase remain in a vacuum concentrator. Then 1ml concentrated H2SO4 added in organic phase, and shake well for 1 minute and centrifuged for 5 minutes at 2500 rpm.
Once again organic phase collected and aqueous phase was extracted twice with 1ml of n-hexane. Obtain organic phase was evaporated and allow to dried completely in a vacuum concentrator. The dry residues were dissolved for cleanup purpose in 1ml of n-hexane (Frías et al., 2004FRÍAS, M.M., TORRES, M.J., FRENICH, A.G., VIDAL, J.L.M., OLEA-SERRANO, F. and OLEA, N., 2004. Determination of organochlorine compounds in human biological samples by GC-MS/MS. Biomedical Chromatography, vol. 18, no. 2, pp. 102-111. http://dx.doi.org/10.1002/bmc.300. PMid:15039962.
http://dx.doi.org/10.1002/bmc.300...
).
Column chromatography (clean-up) of extracted samples: For recovery of pesticides the extracted samples were passed 2 to 3 times through the column during the column chromatography (Lopez-Avila et al., 1989LOPEZ-AVILA, V., MILANES, J., DODHIWALA, N.S. and BECKERT, W.F., 1989. Clean up of environmental sample extracts using Florisil solid-phase extraction cartridges. Journal of Chromatographic Science, vol. 27, no. 5, pp. 209-215. http://dx.doi.org/10.1093/chromsci/27.5.209. PMid:2745661.
http://dx.doi.org/10.1093/chromsci/27.5....
).
2.4. Statistical analysis
Statistical analyses were conducted by using SPSS version 20. Demographic data was presented in percentage (%). Association between POPs and pattern of obesity presented in median (interquartile range). Mann Whitney U test was applied. Statistical significance was set at P-value < 0.05.
3. Results
Total 50 subjects were included in this study, out of which 46(92%) were males and 4(8%) females. Age was categorized into three groups 27-33 years (n=11, 22%), 34-40 years (n=20, 40%) and 41-47 years (n=19,38%). Majority of subjects have primary level of education, consumed both vegetable and meat also they were addicted of tea/ice-cream. Half of the study subjects shown family history of diabetes (Table 1).
The comparative results suggest that the maximum level of summation PCBs mean value was found in age group 27-33 as 0.695 mg/kg in 73% having total individual eleven. While the age group 34-40 having summation, PCBs mean value as 0.548 mg/kg in 95% present in volunteers slightly lower than previous age group and having maximum individuals of about twenty. However, the lowest mean value of summation. The trends of mean value of pesticides gradually decrease according to age as age increases. The greatest number of pesticides found in younger persons than older ones (Figure 1).
Median (interquartile range) of pesticides levels among subjects with normal weight, over weight and obesity were 0.49 (0.26-2.13), 1.53 (0.60-2.65), and 1.60 (1.23-2.05) respectively. Level of pesticides were significantly lower among subjects with normal weight as compared to subjects with overweight and obesity. While no significant difference was found between pesticides level of subjects with overweight and obesity (Figure 2).
Median (IQR) of OCS levels in subjects with normal weight, over weight and obesity were 0.38 (0.08-0.92), 1.12 (0.29-1.65) and 1.20 (0.73-1.60) respectively. It was observed that OC levels in subjects with overweight and obesity were almost similar (P-value > 0.05) but significantly higher as compared to subjects with normal weight (P-value<0.05) (Figure 3).
Median (IQR) of PCB levels in subjects with normal weight, over weight and obesity were 0.23 (0.08-0.92), 0.41 (0.22-1.05) and 0.40 (0.33-0.63) respectively. No significant differences were observed between PCB levels of subjects in terms of BMI (Figure 4).
4. Discussion
In present study we have observed the association between POPs in subject with type 2 diabetes with respect to age groups. Organochlorine pesticides (OCs) and polychlorinated biphenyls (PCBs) are present consistently in humans. It was found that higher exposure of all ∑PCBs, ∑OCs and ∑ Pesticides in younger age group as compared with others. Although inconsistent findings on the trend of POPs have been observed that increased with age increases in both sexes (Moon et al., 2014MOON, H.J., LIM, J.E. and JEE, S.H., 2014. Association of Persistent Organic Pollutants (POPs) with age and body mass index in Korean adults. Journal of Environment and Health Sciences, vol. 40, no. 6, pp. 442-453. http://dx.doi.org/10.5668/JEHS.2014.40.6.442.
http://dx.doi.org/10.5668/JEHS.2014.40.6...
).
In this study majority of the subjects with type 2 diabetes were found with overweight that indicated the cause for the development of future metabolic disorders. This finding suggested the excess weight along with POPs in subjects contributed in the etiology of diabetes and other disorders. Lee et al study describes that obesity in the result of deformity in the production of pancreatic hormone, insulin resistance, and over production of insulin leads to diabetes (Lee et al., 2011LEE, D.-H., STEFFES, M.W., SJÖDIN, A., JONES, R.S., NEEDHAM, L.L. and JACOBS JUNIOR, D.R., 2011. Low dose organochlorine pesticides and polychlorinated biphenyls predict obesity, dyslipidemia, and insulin resistance among people free of diabetes. PLoS One, vol. 6, no. 1, p. e15977. http://dx.doi.org/10.1371/journal.pone.0015977. PMid:21298090.
http://dx.doi.org/10.1371/journal.pone.0...
). Even though the exposure of OC pesticides and PCBs were associated with insulin resistance and dyslipidemia in healthy individuals.
There were numerous components that contributing high accumulation of POPs which ultimately cause of different metabolic disorders. In current study we observed life style factors such as oil proportion in meal, sea food, vegetable, and meal consumption in their diet. The relationship between dietary habits and serum OCP and PCB levels were distinguishable that suggesting metabolic syndrome may alter the influence of food intake on POPs (Kim et al., 2018KIM, J.T., KANG, J.H., CHANG, Y.S., LEE, D.H. and CHOI, S.D., 2018. Determinants of serum organochlorine pesticide and polychlorinated biphenyl levels in middle-aged Korean adults. Environmental Science and Pollution Research International, vol. 25, no. 1, pp. 249-259. http://dx.doi.org/10.1007/s11356-017-0382-7. PMid:29032525.
http://dx.doi.org/10.1007/s11356-017-038...
). In other studies analyses revealed that factor like age and meat intake had positive impact on serum total level OCPs that is consistent with our study results, while green leafy vegetables and beans intake had negative impact on OCPs level (Lee et al., 2007LEE, S.-A., DAI, Q., ZHENG, W., GAO, Y.-T., BLAIR, A., TESSARI, J.D., JI, B.J. and SHU, X.-O., 2007. Association of serum concentration of organochlorine pesticides with dietary intake and other lifestyle factors among urban Chinese women. Environment International, vol. 33, no. 2, pp. 157-163. http://dx.doi.org/10.1016/j.envint.2006.08.010. PMid:17055057.
http://dx.doi.org/10.1016/j.envint.2006....
). Hence present study results describe that dietary intake found as an important factor for deposition of environmental pollutants.
The ability of pollutants to accumulate in human fat tissue cause a disruption in the endocrine system, which in turn increases body weight and waist circumference. Pesticides and OCS levels were found in association with BMI, but PCB levels found no significant differences in current study. In earlier studies the inverse association between BMI and PCB, whereas positive association with organochlorine pesticides were established (Ibarluzea et al., 2011IBARLUZEA, J., ALVAREZ-PEDREROL, M., GUXENS, M., MARINA, L.S., BASTERRECHEA, M., LERTXUNDI, A., ETXEANDIA, A., GOÑI, F., VIOQUE, J., BALLESTER, F. and SUNYER, J., 2011. Sociodemographic, reproductive and dietary predictors of organochlorine compounds levels in pregnant women in Spain. Chemosphere, vol. 82, no. 1, pp. 114-120. http://dx.doi.org/10.1016/j.chemosphere.2010.09.051. PMid:20965545.
http://dx.doi.org/10.1016/j.chemosphere....
). This may be due to high intake of fish meat. Weight gain was associated with Organochlorine whereas DDE neglected cause of lower concentration in the environment in previous study (Roos et al., 2012ROOS, A.J., ULRICH, C.M., SJODIN, A. and MCTIERNAN, A., 2012. Adiposity, body composition, and weight change in relation to organochlorine pollutant plasma concentrations. Journal of Exposure Science & Environmental Epidemiology, vol. 22, no. 6, pp. 617-624. http://dx.doi.org/10.1038/jes.2012.43. PMid:22588213.
http://dx.doi.org/10.1038/jes.2012.43...
) .
5. Conclusion
Nevertheless, present study highlighted the important elements that are responsible for the deposition of POPs in the human body. Furthermore, association between pollutants with etiology of diabetes and associated disorders is established. Consequently, epidemiological studies on large scale required for validation of our findings and planning of preventive measures to minimize the harmful exposure towards populations.
References
- AHN, Y., KWON, E., SHIM, J.E., PARK, M.K., JOO, Y., KIMM, K., PARK, C. and KIM, D.H., 2007. Validation and reproducibility of food frequency questionnaire for Korean genome epidemiologic study. European Journal of Clinical Nutrition, vol. 61, no. 12, pp. 1435-1441. http://dx.doi.org/10.1038/sj.ejcn.1602657 PMid:17299477.
» http://dx.doi.org/10.1038/sj.ejcn.1602657 - ALOTAIBI, A., PERRY, L., GHOLIZADEH, L. and AL-GANMI, A., 2017. Incidence and prevalence rates of diabetes mellitus in Saudi Arabia: an overview. Journal of Epidemiology and Global Health, vol. 7, no. 4, pp. 211-218. http://dx.doi.org/10.1016/j.jegh.2017.10.001 PMid:29110860.
» http://dx.doi.org/10.1016/j.jegh.2017.10.001 - FRÍAS, M.M., TORRES, M.J., FRENICH, A.G., VIDAL, J.L.M., OLEA-SERRANO, F. and OLEA, N., 2004. Determination of organochlorine compounds in human biological samples by GC-MS/MS. Biomedical Chromatography, vol. 18, no. 2, pp. 102-111. http://dx.doi.org/10.1002/bmc.300 PMid:15039962.
» http://dx.doi.org/10.1002/bmc.300 - GRÜN, F. and BLUMBERG, B., 2006. Environmental obesogens: organotins and endocrine disruption via nuclear receptor signaling. Endocrinology, vol. 147, no. 6, suppl., pp. S50-S55. http://dx.doi.org/10.1210/en.2005-1129 PMid:16690801.
» http://dx.doi.org/10.1210/en.2005-1129 - IBARLUZEA, J., ALVAREZ-PEDREROL, M., GUXENS, M., MARINA, L.S., BASTERRECHEA, M., LERTXUNDI, A., ETXEANDIA, A., GOÑI, F., VIOQUE, J., BALLESTER, F. and SUNYER, J., 2011. Sociodemographic, reproductive and dietary predictors of organochlorine compounds levels in pregnant women in Spain. Chemosphere, vol. 82, no. 1, pp. 114-120. http://dx.doi.org/10.1016/j.chemosphere.2010.09.051 PMid:20965545.
» http://dx.doi.org/10.1016/j.chemosphere.2010.09.051 - KIM, J.T., KANG, J.H., CHANG, Y.S., LEE, D.H. and CHOI, S.D., 2018. Determinants of serum organochlorine pesticide and polychlorinated biphenyl levels in middle-aged Korean adults. Environmental Science and Pollution Research International, vol. 25, no. 1, pp. 249-259. http://dx.doi.org/10.1007/s11356-017-0382-7 PMid:29032525.
» http://dx.doi.org/10.1007/s11356-017-0382-7 - KONG, A.P., XU, G., BROWN, N., SO, W.Y., MA, R.C. and CHAN, J.C., 2013. Diabetes and its comorbidities—where East meets West. Nature Reviews. Endocrinology, vol. 9, no. 9, pp. 537-547. http://dx.doi.org/10.1038/nrendo.2013.102 PMid:23712250.
» http://dx.doi.org/10.1038/nrendo.2013.102 - LEE, D.-H., STEFFES, M.W., SJÖDIN, A., JONES, R.S., NEEDHAM, L.L. and JACOBS JUNIOR, D.R., 2011. Low dose organochlorine pesticides and polychlorinated biphenyls predict obesity, dyslipidemia, and insulin resistance among people free of diabetes. PLoS One, vol. 6, no. 1, p. e15977. http://dx.doi.org/10.1371/journal.pone.0015977 PMid:21298090.
» http://dx.doi.org/10.1371/journal.pone.0015977 - LEE, S.-A., DAI, Q., ZHENG, W., GAO, Y.-T., BLAIR, A., TESSARI, J.D., JI, B.J. and SHU, X.-O., 2007. Association of serum concentration of organochlorine pesticides with dietary intake and other lifestyle factors among urban Chinese women. Environment International, vol. 33, no. 2, pp. 157-163. http://dx.doi.org/10.1016/j.envint.2006.08.010 PMid:17055057.
» http://dx.doi.org/10.1016/j.envint.2006.08.010 - LONE, S., LONE, K., KHAN, S. and PAMPORI, R.A., 2017. Assessment of metabolic syndrome in Kashmiri population with type 2 diabetes employing the standard criteria’s given by WHO, NCEPATP III and IDF. Journal of Epidemiology and Global Health, vol. 7, no. 4, pp. 235-239. http://dx.doi.org/10.1016/j.jegh.2017.07.004 PMid:29110863.
» http://dx.doi.org/10.1016/j.jegh.2017.07.004 - LOPEZ-AVILA, V., MILANES, J., DODHIWALA, N.S. and BECKERT, W.F., 1989. Clean up of environmental sample extracts using Florisil solid-phase extraction cartridges. Journal of Chromatographic Science, vol. 27, no. 5, pp. 209-215. http://dx.doi.org/10.1093/chromsci/27.5.209 PMid:2745661.
» http://dx.doi.org/10.1093/chromsci/27.5.209 - MAHANTA, T.G., JOSHI, R., MAHANTA, B.N. and XAVIER, D., 2013. Prevalence of modifiable cardiovascular risk factors among tea garden and general population in Dibrugarh, Assam, India. Journal of Epidemiology and Global Health, vol. 3, no. 3, pp. 147-156. http://dx.doi.org/10.1016/j.jegh.2013.04.001 PMid:23932057.
» http://dx.doi.org/10.1016/j.jegh.2013.04.001 - MOON, H.J., LIM, J.E. and JEE, S.H., 2014. Association of Persistent Organic Pollutants (POPs) with age and body mass index in Korean adults. Journal of Environment and Health Sciences, vol. 40, no. 6, pp. 442-453. http://dx.doi.org/10.5668/JEHS.2014.40.6.442
» http://dx.doi.org/10.5668/JEHS.2014.40.6.442 - ONYANGO, E.M. and ONYANGO, B.M., 2018. The rise of noncommunicable diseases in Kenya: an examination of the time trends and contribution of the changes in diet and physical inactivity. Journal of Epidemiology and Global Health, vol. 8, no. 1-2, pp. 1-7. http://dx.doi.org/10.2991/j.jegh.2017.11.004 PMid:30859780.
» http://dx.doi.org/10.2991/j.jegh.2017.11.004 - RAMTAHAL, R., KHAN, C., MAHARAJ-KHAN, K., NALLAMOTHU, S., HINDS, A., DHANOO, A., YEH, H.-C., HILL-BRIGGS, F. and LAZO, M., 2015. Prevalence of self-reported sleep duration and sleep habits in type 2 diabetes patients in south Trinidad. Journal of Epidemiology and Global Health, vol. 5, no. 4, suppl. 1, pp. S35-S43. http://dx.doi.org/10.1016/j.jegh.2015.05.003 PMid:26073574.
» http://dx.doi.org/10.1016/j.jegh.2015.05.003 - ROOS, A.J., ULRICH, C.M., SJODIN, A. and MCTIERNAN, A., 2012. Adiposity, body composition, and weight change in relation to organochlorine pollutant plasma concentrations. Journal of Exposure Science & Environmental Epidemiology, vol. 22, no. 6, pp. 617-624. http://dx.doi.org/10.1038/jes.2012.43 PMid:22588213.
» http://dx.doi.org/10.1038/jes.2012.43 - TAYLOR, K.W., NOVAK, R.F., ANDERSON, H.A., BIRNBAUM, L.S., BLYSTONE, C., DEVITO, M., JACOBS, D., KÖHRLE, J., LEE, D.H., RYLANDER, L., RIGNELL-HYDBOM, A., TORNERO-VELEZ, R., TURYK, M.E., BOYLES, A.L., THAYER, K.A. and LIND, L., 2013. Evaluation of the association between Persistent Organic Pollutants (POPs) and diabetes in epidemiological studies: a national toxicology program workshop review. Environmental Health Perspectives, vol. 121, no. 7, pp. 774-783. http://dx.doi.org/10.1289/ehp.1205502 PMid:23651634.
» http://dx.doi.org/10.1289/ehp.1205502 - WOLF, K., BONGAERTS, B.W.C., SCHNEIDER, A., HUTH, C., MEISINGER, C., PETERS, A., SCHNEIDER, A., WITTSIEPE, J., SCHRAMM, K.-W., GREISER, K.H., HARTWIG, S., KLUTTIG, A. and RATHMANN, W., 2019. Persistent organic pollutants and the incidence of type 2 diabetes in the CARLA and KORA cohort studies. Environment International, vol. 129, pp. 221-228. http://dx.doi.org/10.1016/j.envint.2019.05.030 PMid:31132656.
» http://dx.doi.org/10.1016/j.envint.2019.05.030 - YANG, C., KONG, A.P.S., CAI, Z. and CHUNG, A.C., 2017. Persistent organic pollutants as risk factors for obesity and diabetes. Current Diabetes Reports, vol. 17, no. 12, p. 132. http://dx.doi.org/10.1007/s11892-017-0966-0 PMid:29098478.
» http://dx.doi.org/10.1007/s11892-017-0966-0
Publication Dates
-
Publication in this collection
09 May 2022 -
Date of issue
2024
History
-
Received
07 Sept 2021 -
Accepted
18 Dec 2021