Zarin Subah*
Jae Hyeon Ryu- College of Natural Resources and College of Agricultural and Life Sciences, University of Idaho Boise, Boise, ID, United States
Introduction
Among the array of organochlorine pesticides utilized for pest control, DDT stands as a prominent example due to its exceptional persistence and resistance to biodegradation (1–5). Comprising various derivatives such as p,p'-DDT (constituting 77 percent of DDT) and o,p'-DDT (constituting 15%), DDT finds widespread use in agricultural domains, fisheries, and vector control, notably targeting mosquitoes and other insects (6). Following the Stockholm Convention, annual averge of DDT usage was roughly 5388 metric tons from 2001 to 2007, reducing to around 3772 metric tons annually from 2008 to 2014. According to WHO, India remained the primary consumer of DDT, using it mostly to combat malaria and leishmaniasis (7). As its exposure is continuous in the environment, it is transferred to the higher consumer level of the food chain through accumulation and persistence in fatty tissues (8). DDT exhibits multifaceted effects on avian, aquatic, and, arthropod populations, precipitating species extinction, as evidenced by studies illustrating its adverse impact on birds like brown pelicans and eagles through eggshell thinning, consequently threatening habitat integrity (9, 10). Recent studies have been able to detect the impact of DDT on human beings. Recognized as a xenoestrogen, DDT disrupts the endocrine system, manifesting reproductive toxicity (11). Its proclivity for stability and bioaccumulation facilitates its entry into human adipose tissues and subsequently into breast milk. Through these lipid reservoirs, DDT infiltrates the circulatory system, affecting various physiological functions (2). Consequently, the augmented risk of cancer poses critical health threats, especially to infants consuming DDT through maternal breast milk, potentially leading to fatal consequences (10). The cumulative toxicity of DDT over prolonged exposure periods can significantly alter morphogenesis, induce carcinogenic diseases, and precipitate failures within the reproductive system (12–14).
The underlying chemical mechanism of DDT's toxicity involves its interference with the function of ATP in the shell gland membrane, notably inhibiting calcium adenosine triphosphatase (9, 15–18). DDT exerts an impact on mitochondrial metabolism in humans, potentially disrupting hepatocyte maintenance and integrity (19, 20). Mitochondrial dysfunction serves as a key contributor to chemically induced hepatic toxicity and the onset of carcinogenic disturbances (9). The metabolite p,p'-DDE [1,1'-dichloro-2,2'-bis(p-chlorophenyl)ethylene] is the primary stage of the harmful and persistent p,p'-DDT. Studies have indicated a correlation between elevated serum levels of p,p'-DDT and o,p'-DDT and an increased incidence of breast cancer in young females, particularly when DDT usage is extensive (21). This persistent toxicity poses a concerning threat to the health and wellbeing of Bangladeshi women, particularly in their role as primary caregivers and the transference of contaminants to the next generation through breastfeeding (22).
DDT usage in Bangladesh
The historical use of DDT in Bangladesh has been mainly linked to its application in pest control, agricultural improvement, and disease control programs—most notably, the 1960s and 1970s malaria eradication efforts. The aquatic resources in Bangladesh serve as a vital component of the country's sustenance, with marine organisms and fishes being preserved and dried to meet substantial consumer demand. In the preservation process, insecticides, notably DDT, have historically been employed to deter insect-related spoilage of dried fish products (23). However, increasing concerns regarding its persistent nature in the environment, bioaccumulation in organisms, and potential adverse impacts on human health prompted regulatory interventions. Despite the official ban on DDT following the Stockholm Convention Treaty of 2007, its continued usage persists within the country (24). Research investigations have revealed varying concentrations of DDT in fishes, ranging from 3.04 to 875.0 parts per billion (ppb), with notably elevated levels observed in specific species such as ribbon fish (131.6 to 149.4 ppb), shrimp (3.04 to 318.2 ppb), and Bombay duck (61.9 to 875.0 ppb) (23, 25, 26). These findings were derived from samples collected across food markets in Dhaka and Chittagong. The absence of stringent regulatory measures in Bangladesh has resulted in the unrestricted use of several organochlorine insecticides, including DDT, without prescribed limits or guidelines (27, 28). Consequently, the lack of regulatory oversight coupled with the affordability of these insecticides has led to the potential presence of high concentrations of DDT in dried fish products, accentuating the need for comprehensive regulatory frameworks and guidance in pesticide usage (8, 29).
Discussion: environmental and health consequences of DDT exposure
When DDT is introduced in the food chain of the environment as a pesticide, the bioaccumulation process happens where the derivatives of DDT magnify in each trophic level. DDT with its isomers enters into the human body upon inhalation or ingestion through the food web (30). These metabolites bind with the estrogenic receptors and disrupt the function and lead to carcinogenic cell development in women's bodies. The negative effect of the serum level DDT and its isomers impacting the menopausal estrogens cause an increase of breast cancer (6, 14, 31). Besides breast cancer, DDT also has an impact in disrupting menstruation cycle and creating further reproductive system failure. Polymenorrhea (occurring before the 21 days cycle) and oligomenorrhea (occurring 40 or more days apart) in ovarian function due to the impact of DDT enhances failure in pregnancy and development of cancer in the reproductive system (32, 33).
DDT in enhancing the risks of breast cancer
In Breastfeeding, the isomer of DDT which is p,p'-DDT is transferred into breast milk from its usage for the interruption of malaria spreading (34). Studies show that malaria affected areas where DDT is used to prevent mosquito growth and it has been found that a high amount of DDT exists in breast milk (35–38). Based on the assessment of the literature, it is possible that Bangladeshi women's breast milk contains significant concentrations of DDT, particularly in the regions of the country where malaria is endemic and DDT is used to control mosquitoes (39). However, there are no specific research in Bangladesh that investigate this correlation directly. Furthermore, DDT is found to be conveyed to infants as their blood serum is found contaminated with DDT (1, 33).
The in utero exposure of DDT enhances the risk of breast cancer through several deleterious impacts in breast and genital tract which leads to the development of carcinogenic cells (14, 40). The malformation in this process leads to cancer and it has probability to affect not only the mother but also the off-springs of the mother. The high level of o,p'-DDT in the serum of mother can result in future risk of breast cancer in her daughter. The process happens in a way where the receptor of estrogen and progesterone becomes positive and the protein kinase erbB-2, a receptor tyrosine (also called HER2) becomes negative. This process can result in vital effects in the women who are below 14 years old. The risk increases 5-fold for breast cancer for them and also further transferred in daughters breastfed by those mothers. Thus, the researchers assure that the risk is increased in women who are exposed to DDT during mammogenesis, which means the period between fetal and pubertal development. The remodeling of carcinogenic tissues happens in adulthood. DDT acts like an environmental endocrine disruptor altering the endogenous hormones and breast morphogenesis (4).
Relationship of DDT and menstruation cycle disruption
Exposure of p,p'-DDT through several pesticides ingested by women from several food items create disruption in hormone signaling (41). The polychlorinated biphenyls (PCBs), from p,p'-DDTs affect the function of the hypothalamus-pituitary-ovarian axis besides hormone signaling. The chemical reaction among these shortens the menstruation cycle and affects the reproductive system of the creation of ovum (42, 43). o,p'-DDT which is the isomer of DDT and its metabolic products such as DDE and DDD with their isomers o,p'-DDD, o,p' DDE have binding assay with women's estrogen receptor. Besides, the other two isomers of DDT, such as p,p'-DDT and also p,p'-DDE have high affinity to bind with progesterone receptors which play a role in maintaining menstruation cycle and pregnancy (44). These binding affinities of DDT severely affect the endocrine function and lead to reproductive system failure in women. A study has found that the luteal phase in the menstrual cycle decreases with 0.6 days with the doubling rate (2 × ) of DDT isomer p,p'-DDE and for quartile increase (4 × ) of it decreases the metabolic activities of progesterone (2).
Effect of DDT exposure detected in Bangladesh women health
Bangladesh, being predominantly agrarian, has witnessed a surge in the usage of persistent organochlorine insecticides like DDT, HCH, PCB, and HCB in recent years. These compounds, characterized by their enduring nature and limited biodegradability, persist within the environment over extended periods (45). Despite the prohibition of DDT in Bangladesh, its continued use in agriculture, fisheries, and vector control has resulted in elevated concentrations detected notably in food sources such as fish (25, 46). Consequently, high levels of DDT have been identified in the plasma cells of Bangladeshi individuals due to the ingestion of DDT-contaminated foods (47).
The impact of DDT on Bangladeshi women, particularly those of reproductive age, demonstrated complex relationships between dietary patterns and increased exposure to this substance, most notably through food consumption and a variety of exposure routes (23). Studies have indicated a substantial disparity in the concentration of organochlorine insecticides, such as DDT, in Bangladeshi mothers' breast milk compared to levels observed in Europe and the United States (48). This significant variance suggests an augmented risk for mothers incurring breast cancer and raises concerns regarding potential implications for daughters who are breastfed or exposed to organochlorines like DDT transmitted through maternal sources. Breast cancer affects ~13,000 women in Bangladesh each year, and over 7,000 of them die as a result of the disease. The incidence of breast cancer in the country is expected to be 22.5 per 100,000 females of any age and it is the most common among women aged 15 to 44 years old (49, 50). Also, a significant correlation is found between BMI, education level, and serum p,p'-DDE concentration, suggesting that high socio-economic profile women tended to consume expensive, higher-fat foods like meat and fatty fish, influencing increased DDT exposure (22–24). Moreover, a weak positive link between p,p'-DDE levels and beef consumption among Nullipara women hinted at beef and fish being significant contributors to DDT intake in Bangladesh (24). Beef emerged as a key route of DDT intake for reproductive-age women in Bangladesh. DDT concentrations were notably high in meat, house dust, and breast milk, indicating varied exposure sources. While daily DDT intake levels didn't surpass WHO guidelines, p,p'-DDT levels exceeded the US EPA's oral reference dose. Another study in the Dhaka city, Bangladesh, detected substantial p,p'-DDT levels in cord blood of pregnant mother-newborn in Bangladesh, signifying recent DDT exposure (22, 51). Nevertheless, the future risk of the mother suffering from breast cancer and also the daughter who is breastfed or consuming organochlorine i.e., DDT by those mothers can also be affected by reproductive system failure or breast cancer (52–56).
Conclusion
The reason behind the continued usage of DDT in Bangladesh is the lack of consciousness among people about its adverse effect and there is strict regulation in prohibiting its usage. The fatal effect of DDT needs to be researched more in Bangladeshi mothers and their daughters inheriting DDT based carcinoma living in different cities of Bangladesh. Besides this, the harmful impacts DDT in human health needs to be conveyed in farmers and fishermen who continuously use DDT so that consciousness can be built to stop the usage of DDT. Also, the alternative bio-pesticides which are easily biodegradable need to be introduced to Bangladeshi people in order to reduce the use of DDT and encourage the use of eco-friendly components that benefit both the environment and human health.
Author contributions
ZS investigated the proposed research and wrote the manuscript. JR provided supervised directions as an academic advisor at the University of Idaho.
Funding
The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. This publication activity is supported partially by the National Institute of Food and Agriculture, U.S. Department of Agriculture (USDA), under JR's Hatch project 1023305. Any opinions, findings, or recommendations expressed in this publication are those of the authors and do not necessarily reflect the view of USDA.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
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References
1. Bouwman H, Becker P, Cooppan R, Reinecke A. Transfer of DDT used in malaria control to infants via breast milk. Bull World Health Organ. (1992) 70:241.
2. Perry MJ, Ouyang F, Korrick SA, Venners SA, Chen C, Xu X, et al. A prospective study of serum DDT and progesterone and estrogen levels across the menstrual cycle in nulliparous women of reproductive age. Am J Epidemiol. (2006) 164:1056–64. doi: 10.1093/aje/kwj329
3. Mishra K, Sharma RC. Contamination of aquatic system by chlorinated pesticides and their spatial distribution over North-East India. Toxicol Environ Health Sci. (2011) 3:144–55. doi: 10.1007/s13530-011-0092-3
4. Soto AM, Sonnenschein C. DDT, endocrine disruption and breast cancer. Nat Rev Endocrinol. (2015) 11:507–8. doi: 10.1038/nrendo.2015.125
5. Mansouri A, Cregut M, Abbes C, Durand MJ, Landoulsi A, Thouand G, et al. The environmental issues of DDT pollution and bioremediation: a multidisciplinary review. Appl Biochem Biotechnol. (2017) 181:309–39. doi: 10.1007/s12010-016-2214-5
6. Sturgeon SR, Potischman N, Rothman N, Brinton LA, Hoover RN, Brock JW, et al. Serum concentrations of organochlorine compounds and endometrial cancer risk (United States). Cancer Causes Control. (1998) 9:417–24. doi: 10.1023/A:1008823802393
8. Bhuiyan MNH, Bhuiyan HR, Rahim M, Ahmed K, Haque KF, Hassan MT, et al. Screening of organochlorine insecticides (DDT and heptachlor) in dry fish available in Bangladesh. Bangladesh J Pharmacol. (2008) 3:114–20. doi: 10.3329/bjp.v3i2.997
9. Harada T, Takeda M, Kojima S, Tomiyama N. Toxicity and carcinogenicity of dichlorodiphenyltrichloroethane (DDT). Toxicol Res. (2016) 32:21–33. doi: 10.5487/TR.2016.32.1.021
10. Petrakis D, Vassilopoulou L, Mamoulakis C, Psycharakis C, Anifantaki A, Sifakis S, et al. Endocrine disruptors leading to obesity and related diseases. Int J Environ Res Pub Health. (2017) 14:1282. doi: 10.3390/ijerph14101282
11. Cha M, Lee HJ, Kim JS, Kim E. Environmental assessment of estrogenic pollutants in Nam River of Korea using indirect competitive ELISA and E-screen assay. Toxicol Environ Health Sci. (2012) 4:262–8. doi: 10.1007/s13530-012-0145-2
12. Schecter A, Toniolo P, Dai L, Thuy L, Wolff M. Blood levels of DDT and breast cancer risk among women living in the north of Vietnam. Arch Environ Contam Toxicol. (1997) 33:453–6. doi: 10.1007/s002449900276
13. Hatzidaki E, Pagkalou M, Katsikantami I, Vakonaki E, Kavvalakis M, Tsatsakis AM, et al. Endocrine-disrupting chemicals and persistent organic pollutants in infant formulas and baby food: legislation and risk assessments. Foods. (2023) 12:1697. doi: 10.3390/foods12081697
14. Syed S, Qasim S, Ejaz M, Sammar KN, Ali H, Zaker H, et al. Effects of dichlorodiphenyltrichloroethane on the female reproductive tract leading to infertility and cancer: systematic search and review. Toxics. (2023) 11:725. doi: 10.3390/toxics11090725
15. Faroon O, Harris MO. Toxicological profile for DDT, DDE, and DDD. Atlanta, GA: US Department of Health and Human Services (2002).
16. Turusov V, Rakitsky V, Tomatis L. Dichlorodiphenyltrichloroethane (DDT): ubiquity, persistence, and risks. Environ Health Perspect. (2002) 110:125–8. doi: 10.1289/ehp.02110125
17. Wilson TG. Drosophila: sentinels of environmental toxicants. Integr Comp Biol. (2005) 45:127–36. doi: 10.1093/icb/45.1.127
18. Joußen N, Heckel DG, Haas M, Schuphan I, Schmidt B. Metabolism of imidacloprid and DDT by P450 CYP6G1 expressed in cell cultures of Nicotiana tabacum suggests detoxification of these insecticides in Cyp6g1-overexpressing strains of Drosophila melanogaster, leading to resistance. Pest Manage Sci Form Pesticide Sci. (2008) 64:65–73. doi: 10.1002/ps.1472
19. Pessayre D, Mansouri A, Haouzi D, Fromenty B. Hepatotoxicity due to mitochondrial dysfunction. Cell Biol Toxicol. (1999) 15:367–73. doi: 10.1023/A:1007649815992
20. Jaeschke H, Gores GJ, Cederbaum AI, Hinson JA, Pessayre D, Lemasters JJ, et al. Mechanisms of hepatotoxicity. Toxicol Sci. (2002) 65:166–76. doi: 10.1093/toxsci/65.2.166
21. Cohn BA, Wolff MS, Cirillo PM, Sholtz RI. DDT and breast cancer in young women: new data on the significance of age at exposure. Environ Health Perspect. (2007) 115:1406–14. doi: 10.1289/ehp.10260
22. Leung M, Nøst TH, Wania F, Papp E, Herzke D, Mahmud AA, et al. Maternal-child exposures to persistent organic pollutants in Dhaka, Bangladesh. Expos Health. (2020) 12:79–87. doi: 10.1007/s12403-018-0286-x
23. Haque R, Inaoka T, Fujimura M, Ahmad AS, Ueno D. Intake of DDT and its metabolites through food items among reproductive age women in Bangladesh. Chemosphere. (2017) 189:744–51. doi: 10.1016/j.chemosphere.2017.09.041
24. Haque R, Inaoka T, Fujimura M, Watanabe C, Ahmad AS, Kakimoto R, et al. Dietary patterns and serum of DDT concentrations among reproductive-aged group of women in Bangladesh. Environ Sci Pollut Res. (2018) 25:17665–73. doi: 10.1007/s11356-018-1958-6
25. Hossain MA, Shoeb M, Nahar N. DDT and its metabolites in fresh water fish samples. J Food Sci Engin. (2016) 6:344–50. doi: 10.17265/2159-5828/2016.06.006
26. Shoeb M, Mahim A, Mamun M, Nahar N. Organochlorine pesticide residues in poultry meats of Bangladesh. Croatian J Food Sci Technol. (2016) 8:30–3. doi: 10.17508/CJFST.2016.8.1.04
27. Al Mahmud M, Khalil F, Rahman MM, Mamun M, Shoeb M, Abd El-Aty A, et al. Analysis Of DDT and its metabolites in soil and water samples obtained in the vicinity of a closed-down factory in Bangladesh using various extraction methods. Environ Monitor Assessm. (2015) 187:1–12. doi: 10.1007/s10661-015-4965-9
28. Hasanuzzaman M, Rahman M, Salam M. Identification and quantification of pesticide residues in water samples of Dhamrai Upazila, Bangladesh. Appl Water Sci. (2017) 7:2681–8. doi: 10.1007/s13201-016-0485-1
29. Mustafa T, Naser MN, Latifa GA, Shoeb M, Nahar N. Organochlorine pesticide residues in different fishes and shell fishes collected from the flood plains of Sonargaon upazila, Bangladesh. Bangladesh J Zool. (2019) 47:137–48. doi: 10.3329/bjz.v47i1.42029
30. Renieri EA, Goumenou M, Kardonsky DA, Veselov VV, Alegakis AK, Buha A, et al. Indicator PCBs in farmed and wild fish in Greece-Risk assessment for the Greek population. Food Chem Toxicol. (2019) 127: 260–9. doi: 10.1016/j.fct.2019.03.027
31. Mrema EJ, Rubino FM, Brambilla G, Moretto A, Tsatsakis AM, Colosio C, et al. Persistent organochlorinated pesticides and mechanisms of their toxicity. Toxicology. (2013) 307:74–88. doi: 10.1016/j.tox.2012.11.015
32. Windham GC, Lee D, Mitchell P, Anderson M, Petreas M, Lasley B, et al. Exposure to organochlorine compounds and effects on ovarian function. Epidemiology. (2005) 12:182–90. doi: 10.1097/01.ede.0000152527.24339.17
33. Amir S, Shah STA, Mamoulakis C, Docea AO, Kalantzi OI, Zachariou A, et al. Endocrine disruptors acting on estrogen and androgen pathways cause reproductive disorders through multiple mechanisms: a review. Int J Environ Res Pub Health. (2021) 18:1464. doi: 10.3390/ijerph18041464
34. Snedeker SM. Pesticides and breast cancer risk: a review of DDT, DDE, and dieldrin. Environ Health Perspect. (2001) 109:35–47. doi: 10.1289/ehp.01109s135
35. White AJ, Teitelbaum SL, Wolff MS, Stellman SD, Neugut AI, Gammon MD, et al. Exposure to fogger trucks and breast cancer incidence in the long island breast cancer study project: a case–control study. Environ Health. (2013) 12:1–12. doi: 10.1186/1476-069X-12-24
36. Tsakiris IN, Goumenou M, Tzatzarakis MN, Alegakis AK, Tsitsimpikou C, Ozcagli E, et al. Risk assessment for children exposed to DDT residues in various milk types from the Greek market. Food Chem Toxicol. (2015) 75:156–65. doi: 10.1016/j.fct.2014.11.012
37. Parada Jr H, Wolff MS, Engel LS, White AJ, Eng SM, Cleveland RJ, et al. Organochlorine insecticides DDT and chlordane in relation to survival following breast cancer. Int J Cancer. (2016) 138:565–75. doi: 10.1002/ijc.29806
38. Niehoff NM, Nichols HB, White AJ, Parks CG. Childhood and adolescent pesticide exposure and breast cancer risk. Epidemiology. (2016) 27:326. doi: 10.1097/EDE.0000000000000451
39. Sinha I, Sayeed AA, Uddin D, Wesolowski A, Zaman SI, Faiz MA, et al. Mapping the travel patterns of people with malaria in Bangladesh. BMC Med. (2020) 18:45. doi: 10.1186/s12916-020-1512-5
40. McDonald JA, Cirillo PM, Tehranifar P, Krigbaum NY, Engmann NJ, Cohn BA, et al. In utero DDT exposure and breast density in early menopause by maternal history of breast cancer. Reprod Toxicol. (2020) 92:78–84. doi: 10.1016/j.reprotox.2019.08.009
41. Chen A, Zhang J, Zhou L, Gao ES, Chen L, Rogan WJ, et al. DDT serum concentration and menstruation among young Chinese women. Environ Res. (2005) 99:397–402. doi: 10.1016/j.envres.2004.12.015
42. Ouyang F, Perry M, Venners S, Chen C, Wang B, Yang F, et al. Serum DDT, age at menarche, and abnormal menstrual cycle length. Occup Environ Med. (2005) 62:878–84. doi: 10.1136/oem.2005.020248
43. Bretveld RW, Thomas CM, Scheepers PT, Zielhuis GA, Roeleveld N. Pesticide exposure: the hormonal function of the female reproductive system disrupted? Reprod. Biol Endocrinol. (2006) 4:1–14. doi: 10.1186/1477-7827-4-30
44. Barmpas M, Vakonaki E, Tzatzarakis M, Sifakis S, Alegakis A, Grigoriadis T, et al. Organochlorine pollutants' levels in hair, amniotic fluid and serum samples of pregnant women in Greece. A cohort study Environ Toxicol Pharmacol. (2020) 73:103279. doi: 10.1016/j.etap.2019.103279
45. Oehme M. Dispersion and transport paths of toxic persistent organochlorines to the Arctic—levels and consequences. Sci Total Environ. (1991) 106:43–53. doi: 10.1016/0048-9697(91)90019-B
46. Chowdhury M, Amin-Ud-Din M, Malek M, Zaman M. DDT residue and its metabolites in dried fishes of Dhaka city markets. Soil Environ. (2010) 29:117–21.
47. Zamir R, Hossain M, Shoeb M, Mosihuzzaman M, Nahar N. Organochlorine pesticides in three fish samples. Dhaka Univ J Sci. (2013) 61:215–6. doi: 10.3329/dujs.v61i2.17075
48. Bergkvist C, Aune M, Nilsson I, Sandanger TM, Hamadani JD, Tofail F, et al. Occurrence and levels of organochlorine compounds in human breast milk in Bangladesh. Chemosphere. (2012) 88:784–90. doi: 10.1016/j.chemosphere.2012.03.083
49. Ahmed S, Azad K, Chakraborty RR, Sultana N, Ahmed FU. Prevalence of breast cancer at divisional level in Bangladesh. J Chittagong Med College Teachers' Assoc. (2018) 29:4–8. doi: 10.3329/jcmcta.v29i2.62509
50. Nessa A, Hussain T, Alam SM, Faruk I, Jahan I. Age distribution pattern of female breast cancer patients in Bangladesh-developing early and presenting late. Int Surg J. (2018) 5:379–82. doi: 10.18203/2349-2902.isj20180112
51. Luo D, Pu Y, Tian H, Cheng J, Zhou T, Tao Y, et al. Concentrations of organochlorine pesticides in umbilical cord blood and related lifestyle and dietary intake factors among pregnant women of the Huaihe River Basin in China. Environ Int. (2016) 92:276–83. doi: 10.1016/j.envint.2016.04.017
52. Cohn BA, Cirillo PM, Wolff MS, Schwingl PJ, Cohen RD, Sholtz RI, et al. DDT and DDE exposure in mothers and time to pregnancy in daughters. Lancet. (2003) 361:2205–6. doi: 10.1016/S0140-6736(03)13776-2
53. Michalakis M, Tzatzarakis MN, Kovatsi L, Alegakis AK, Tsakalof AK, Heretis I, et al. Hypospadias in offspring is associated with chronic exposure of parents to organophosphate and organochlorine pesticides. Toxicol Lett. (2014) 230:139–45. doi: 10.1016/j.toxlet.2013.10.015
54. Vafeiadi M, Georgiou V, Chalkiadaki G, Rantakokko P, Kiviranta H, Karachaliou M, et al. Association of prenatal exposure to persistent organic pollutants with obesity and cardiometabolic traits in early childhood: the Rhea mother–child cohort (Crete, Greece). Environ Health Perspect. (2015) 123:1015–21. doi: 10.1289/ehp.1409062
55. Yamazaki K, Itoh S, Araki A, Miyashita C, Minatoya M, Ikeno T, et al. Associations between prenatal exposure to organochlorine pesticides and thyroid hormone levels in mothers and infants: The Hokkaido study on environment and children's health. Environ Res. (2020) 189:109840. doi: 10.1016/j.envres.2020.109840
56. Helou K, Matta J, Harmouche-Karaki M, Sayegh N, Younes H, Mahfouz Y, et al. Maternal and cord serum levels of polychlorinated biphenyls (PCBs) and organochlorine pesticides (OCPs) among Lebanese pregnant women and predictors of exposure. Chemosphere. (2021) 266:129211. doi: 10.1016/j.chemosphere.2020.129211
Keywords: DDT, toxicity, breast cancer, menstruation, women's health
Citation: Subah Z and Ryu JH (2024) Impact of DDT on women's health in Bangladesh: escalating breast cancer risk and disturbing menstrual cycle. Front. Public Health 12:1309499. doi: 10.3389/fpubh.2024.1309499
Received: 01 November 2023; Accepted: 19 January 2024;
Published: 12 February 2024.
Edited by:
Ciro Fernando Bustillo LeCompte, Toronto Metropolitan University, CanadaReviewed by:
Aristidis M. Tsatsakis, University of Crete, GreeceCopyright © 2024 Subah and Ryu. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Zarin Subah, c3ViYTI0NTUmI3gwMDA0MDt2YW5kYWxzLnVpZGFoby5lZHU=