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Groundwater for Sustainable Development 7 (2018) 20–29

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Groundwater for Sustainable Development


journal homepage: www.elsevier.com/locate/gsd

Review article

Impact of pesticides in karst groundwater. Review of recent trends in T


Yucatan, Mexico

Angel Gabriel Polanco Rodrígueza, , María Inmaculada Riba Lópezb, Ángel DelValls Casillasb,
Jesús Alfredo Araujo Leónc, Sudip Datta Banikd
a
Centro de Investigaciones Regionales, Universidad Autonoma de Yucatan, Laboratorio de Medicina Social y Salud Pública, Av. Itzaez x 59 # 490, Centro, C.P. 97000
Mérida, Yucatán, Mexico
b
UNESCO/UNITWIN Wicop, Departamento de Química Física, Facultad de Ciencias del Mar y Ambientales, Universidad de Cádiz, Puerto Real, Cádiz, Spain
c
Laboratorio de Cromatografía, Facultad de Química, Universidad Autónoma de Yucatán, C. 43 No. 613 × C. 90 Col. Inalámbrica, C.P. 97069 Mérida, Yucatán, Mexico
d
Centro de Investigaciones y de Estudios Avanzados del Instituto Politecnico Nacional-CINVESTAV-Mérida, México, Departamento de Ecologia Humana, Km 6 carretera a
Progreso, Cordemex C.P. 97310, Mexico

A R T I C L E I N F O A B S T R A C T

Keywords: The anthropogenic activities in karst aquifer increase the vulnerability for groundwater pollution by organo-
Pesticides chlorine pesticides (OCP). Recent research have been published about high level of OCP in water, as well as the
Karst bioaccumulation of OCP in blood of women with cancer and in breast milk. The use of banned OCP such as DDT,
Water pollution heptachlore, lindane, endosulfan, aldrin, are the main sources of pollution of groundwater in Yucatan, Mexico.
Bioaccumulation
In Yucatan, the water pollution is increased by 30% of deforestation, large zones of geological fracturing with
Health
high permeability, and high density of sinkholes (cenotes) in the karst soils. Diverse studies indicate Yucatan as a
zone with high impact of water pollution (3.2 ppm of endrin, 10.86 ppm of δ-lindane, 5.23 ppm of γ-lindane,
6.53 ppm of α-lindane, 13.61 and 12.54 ppm of heptachlore). 30% of the population drink water from polluted
wells and sinkholes. A study showed high levels of OCP in the blood of women with cervical uterine cancer:
7.352 ppm of endosulfan I, 3.695 ppm of aldrin, 2.336 ppm of 4,4′ DDD, 1.434 ppm of heptachlore. Furthermore,
recent research show high levels of pesticides in breast milk, indicating 18.436 ppm of heptachlore epoxide and
1.024 and 2.10 ppm of dieldrin. Social conditions such as poverty, low education level, lack of regulation and
capacitation in the agricultural sector, as well as environmental vulnerabilities have a high impact on the karst
groundwater and the public health. This review showed the evidence of the need of regulation of OCP, the
promotion of public health and implementation of agroecological programs.

1. Introduction Tabrez et al., 2014). The problem is that banned OCP (Stockholm,
2009; Zhang et al., 2011) are being used in the developing countries for
The chronic exposure of toxic pollutants present in groundwater has agricultural and livestock activities and for vector control in public
adverse effects on the public health and causes severe diseases like health for the prevention of vector born diseases, such as dengue and
cancer, neurological affections, damage to the reproductive system, malaria. The research evidence suggests that their use has affected the
congenital malformation, and in recent years, diabetes mellitus environment and the public health (Power, 2010; Valavanidis and
(Alavanja et al., 2004; Damalas and Eleftherohorinos, 2011). Organo- Vlachogianni, 2010; Atreya et al., 2011).
chlorine pesticides (OCP) are toxic chemicals of high impact because of The use of OCP causes more than 3 millions of severe intoxications
their persistence in the environment and bioaccumulation in humans and more than 220,000 deaths per year in the world. Cancer, allergies,
(Sachin et al., 2013; Velasco et al., 2014). Gene-Environment-Interac- neurologic and reproductive disorders has been related with OCP ex-
tion (GEI) refers the combined influences of genetic and environmental posure (WHO, 1992; Ledirac et al., 2005; Alavanja, 2008; Faniband
factors on the health disease process (Tabrez et al., 2014). The tox- et al., 2014). Due to the persistence of OCP in the environment and the
icological effects of environmental pollutants can play an important ability to be transported by natural means like water, soil or air, OCP
role on the etiology of diseases in humans, such as mutagenicity and can be found in almost any region, and when they are transported, also
carcinogenicity (Tabrez and Ahmad, 2009; Waliszewski et al., 2013; affect neighboring countries (Reigarts and Roberts, 1999; Schinas et al.,


Corresponding author.
E-mail addresses: polanco07@gmail.com, angel.polanco@correo.uady.mx (A.G.P. Rodríguez).

https://doi.org/10.1016/j.gsd.2018.02.003
Received 4 January 2018; Accepted 15 February 2018
Available online 17 February 2018
2352-801X/ © 2018 Published by Elsevier B.V.
A.G.P. Rodríguez et al. Groundwater for Sustainable Development 7 (2018) 20–29

2000; Waliszewski et al., 2003; Li and Macdonald, 2006; Chandra et al., Permissible limits of quality and treatments to which the water must
2015). undergo for its purification (SSA, 2000), that regulate the maximum
The Organization for Economic Co-operation and Development permitted limits of pesticides and their residues in drinking water
(OECD) issued a warrant over the impact of pesticides in surface waters, (Table 3).
underground and seawater, caused by agricultural activities (World Unfortunately, although there are laws and regulations for the use
Bank, 1994; Parris, 2011). This relates to the development of new and importation of organochlorine pesticides in Mexico, they are not
diseases by pesticides and represents a hazard for the health of human applied. Although Mexico is part of the Rotterdam Agreement (2010)
being (Ferrer, 2003; Bergel, 2007; UNESCO, 2008). The main cause of and Stockholm Convention (2009), it does not comply with this inter-
water pollution is agriculture and livestock sector (Shortle and Abler, national regulation and recommendations for organochlorine pesti-
2001; FAO, 2006; Pérez and Aguilar, 2012). Approximately 884 million cides.
of people lack access to safe drinking water and more than 2600 mil- In Mexico there is a list of pesticides registered for their use in the
lions lack access to basic sanitary facilities (WHO, 2011). the Federal Commission for the Protection Against Sanitary Risk
The OCP are endocrine disrupters, with high impact on the public (COFEPRIS) that includes organochlorines pesticides. This Commission
health (EEA, 2012). The reports describe an increased of prevalence in is an organ of the Health Secretary of Mexico with the objective of
the last 20 years in several countries for congenital malformations, protection of the health risks (Cofepris, 2010). However, this goal is not
neurotoxic damage, diverse cancer, sperm low count, as well as asthma, fulfilled due to the use of organochlorine pesticides in practice and
fetal and child death (Van Maele Fabry et al., 2006; Cohn et al., 2007; based on the evidence of their occurrence/concentrations in water and
Famiglini et al., 2008; Mnif et al., 2011; Brophy et al., 2012; Cherin their bioaccumulation in Yucatan, Mexico.
et al., 2012).
On the other hand, 25% of the world population of Europe, Asia and 1.2. Use of agrochemicals in Yucatan
America are supplied mostly by karstic aquifers that are highly vul-
nerable to contamination (Ford and Williams, 2007). Karst landscapes Pesticides frequently used by farmers in the municipalities of the
are recognized by the presence of bedrock in the surface, cenotes Ring of Sinkholes are shown in Table 4.
(sinkholes) or caves. The rainwater generally percolates through the The objective of this article is to review and show the impacts of
bedrock contact to the karst aquifer. Water in the karst aquifer moves banned OCP in human health under conditions of high fragility such as
through sinkholes, failures and fractures on the terrain, subterranean karst groundwater in Yucatan, Mexico.
caves and conduits that act as main flow paths of water (Steinich and
Marín, 1996a; Steinich et al., 1996b; Steinich et al., 1997; Gunn, 2004). 2. Method
The karstic soils can act as a point of introduction of pollutants to the
groundwater system (Wang et al., 2013). The management of karst This work is a revision of studies on OCP polluted karst aquifer in
aquifer should focus on protecting the integrity of the groundwater Yucatan, Mexico. Analysis of these studies was performed based on
from anthropogenic activities on the surface, due to the very high fil- vulnerability and risks of OCP to the public health, human bioccumu-
tration and vulnerability of the terrain (Pulido-Bosch, 1999; Stokes lation, management and regulation.
et al., 2007). In Mexico, soil samples from the south, central and north
regions have shown that OCP are used and can act as a potential source 3. Places of study
of contamination on site or be transported when volatilized (Wong
et al., 2009, 2010). These studies were developed in 32 municipalities of Yucatan, state
The use of soil for productive systems is mainly restricted to the of high poverty in Mexico (CONAPO, 2010). The water study was in an
agriculture in the south, and livestock on the northeast of Yucatan; important fractured karstic area called the Ring of Sinkholes in 11
however, livestock breeding over the decades have led to the high levels municipalities (Fig. 2), which is a regional structure for groundwater
of deforestation and generalized land degradation in the state (Fig. 1). recharge and water conduction, composed by 99 sinkholes. The Ring of
Sinkholes surrounds the east, west and south of Merida, the capital city
1.1. Regulation of Yucatan (Perry et al., 1995; Rohrer Patrick, 2012). In Yucatan, the
only source of fresh water is the karstic aquifer through wells and the
The OCP included in the Rotterdam Convention (2010), were clas- sinkholes (Schmitter-Soto et al., 2002), and the Ring of Sinkholes is an
sified as highly dangerous to human health and the environment. The important area for geographical distribution of groundwater. According
main objective of this convention was to generate an international to Rohrer Patrick (2012), there are over 4000 sinkholes in Yucatan. The
council worldwide on the commercialization and manipulation of these karstic characteristics in Yucatan favor pollutant entry to the aquifer
pesticides. In the convention, specifically in Article 5, there is reference (Marin and Perry, 1994; Smart et al., 2006; Metcalfe et al., 2011), and
to the “Procedures for banned or severely restricted chemicals”, in studies on processes of contaminant transport are necessary in this re-
order to adopt a final regulatory action in terms of notifying the Se- gion.
cretariat in writing of such action (FAO and PNUMA) to prohibit and/or The study of OCP in blood of Maya women with cervico uterine
severely restrict chemicals that affect the environment and human cancer was realized in the 18 municipalities of highest mortality for
health. Annex III is included in the Rotterdam Convention, are the cervix uterine cancer, this area include the agriculture, livestock and
chemicals subject to the procedure of prior informed consent metropolitan area of Yucatan (Polanco Rodríguez Ángel et al., 2017a)
(Rotterdam Convention, 2015) (Table 1). (Fig. 3).
Stockholm Convention on Persistent Organic Pollutants is an in- The study of levels of pesticides in breast milk was realized in three
ternational environmental treaty that aims to eliminate or restrict to municipalities in the agriculture, metropolitan and coastal area
eliminate or restrict the production and use of persistent organic pol- (Polanco Rodríguez Ángel et al., 2017b) (Fig. 4).
lutants (POPs). The chemicals targeted by the Stockholm Convention
are listed in the Table 2. Parties must take measures to restrict the 4. Results and discussion
production and use of the chemicals listed. Although Mexico is part of
the Rotterdam Agreement (2010) and Stockholm Convention (2009), 4.1. Levels of OCP in water
does not comply with these international regulations.
In Mexico there are Official Norms e.g. NOM 127-SSA1–1994: In the water area of the Ring of Sinkholes was detected highest le-
Environmental health. Water for human use and consumption. vels of OCP, 3.2 ppm of endrin, 10.86 ppm of δ-lindane, 5.23 ppm of γ-

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A.G.P. Rodríguez et al. Groundwater for Sustainable Development 7 (2018) 20–29

Fig. 1. Generalized productive systems and deforestation in Yucatan, Mexico.

Table 1 Table 3
Organochlorine pesticides included in Rotterdam Convention. Maximum limits for main organochloride pesticides and its residues for drinking water in
Mexico and the United States of America (US).
Pesticide CAS Category
Pollutant Mexico (ppm) US-EPA (ppm)
Aldrina 309-00-2 Pesticide
Dieldrina 60-57-1 Pesticide Endosulfan – 0.0003
DDT 50-29-3 Pesticide Gamma Lindane 2.0 0.0002
Endosulfan 115-29-7 Pesticide Heptachlore 0.03 0.0004
Heptacloro 76-44-8 Pesticide Aldrin 0.03 0.002
Lindano 58-89-9 Pesticide Dieldrin 0.03 0.002
Endrin 0.03 0.002
*
Rotterdam Convention (2010). DDT (total) 1

NOM-127-SSA1–1994, EPA 2009.


Table 2
US-EPA: Environment Protection Agency of USA.
Organochlorine pesticides of Stockholm Convention (Annex A
- No information.
and B, Stockholm, 2008).
* Forbidden.
Pesticide Condition
2015b).
Aldrin Elimination The level of pesticide contamination in the karst aquifer and their
Dieldrin Elimination
bioaccumulation in the humans, a relationship between the natural and
Endrin Elimination
Heptacloro Elimination social vulnerabilities in the pollution process and their high impact on
Lindano Elimination the public health should be considered a multifactorial complex pro-
Endosulfan Elimination blem. A similar karst area in southern Italy shown that agricultural
Hexaclorobenzene Elimination
activities permitted in the area could increase the high risk to the
DDT Restringed
aquifer pollution (Ducci et al., 2008).
The high density of sinkholes, which are open-air water bodies that
lindane, 6.53 ppm of α-lindane, 13.61 and 12.54 ppm of heptachlore are highly susceptible to pollution because they act as traps for rains
(Polanco Rodríguez et al., 2015a). At same time, to know the point of and surface runoffs rich in pesticides due the productive activities.
view of the population about the use and management of agrochemicals There is a close relationship between the pollution of sinkholes and the
and their impact in the environment and public health, a qualitative groundwater pollution (Wang et al., 2013). Karstic aquifers are highly
study about the risk perception of the population on agrochemicals heterogenic systems due to the local development of their conduction
management was carried out in the area (Polanco Rodríguez et al., systems, which require research efforts to describe their routes of flow

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Table 4
Main organochlorine pesticides use in agriculture and livestock activities.

Municipality Insecticide Commercial Names Regulation Classification

Abala, Buctzotz, Chocholá, Endosulfan: Thiofor, Thiodan, Thionex, Thiosulfan, Included in Rotterdam Agreement Prohibited in the Carcinogenicity:
Dzilam,Izamal, Kinchil, Thiotox, Thiofor, Ensure, Endosol, Hildan, European Union. Reserved (USEPA 2012a).
Kopoma, Tecoh,Tekit, Insectophene, Crisulfan, Cyclodan Mexico: Conditional importation since 2012. Possible teratogen
Sacalum (Cofepris, 2010). (Cofepris, 2010)
Buctzotz, Dzilam, Kopoma, Tecoh Lindane: Gammex, Novigam, Gamma Mean 400, Included in Rotterdam Agreement and Stockholm Possible carcinogen.
Kinchil,Tekit Lindane, Lindano Técnico, Gamaphex, Gamahexane, Convention (USEPA 2012b)
HCCH, HCH,Hexachloran, HGI Prohibited in at least 11countries, Rotterdam
Agreement. Mexico: Conditional import and use
(Cicoplafest, 1991).
Abala, Buctzotz, Dzilam Aldrin/Dieldrin: HHDN, Octaleno, Aldrite,Octalox, Included in Rotterdam Agreement and Stockholm Possible carcinogen
Quintox, Dieldrite Convention (USEPA 2012c).
Banned in at least 23 countries of Rotterdam
Agreement. Mexico: Forbidden use and import since
1991 (Castro y Díaz, 2007; Cofepris, 2010).
Buctzotz, Celestun, Dzilam DDT: Aavero-extra, Agritan, Anofex, Arkotine, Azotox, Included in Rotterdam Agreement and Stockholm Possible carcinogen
Kinchil,Sacalum Bosan Supra, Bovidermol, Chlofenotan, Convention (USEPA 2012d)
Chlorophenothane, Citox, 4,4’-DDT, p,p’-DDT, Deoval, Prohibited in at least 26 countries since 1970. Cancer IARC 2B (possible
Detox, Detoxan, Dibovin, Dicophane, Dodat, Dykol, Mexico: Conditional import for vector control since carcinogen).
Estonate, Gesafid, Gesarol, Ivoran, Mutoxan, Neocid, 1993.
Neocidol, Paraclorocidum, Pentachlorin, Santobane, Restricted use (Cofepris, 2010)
Tafidex, Zerdane
Buctzotz, Dzilam, Tecoh Heptachlor: Heptagran, Heptamul, Heptagranox, Included in Rotterdam Agreement and Stockholm Possible carcinogen
Heptachloran, Heptamak, Basaklor, Drinox, Soleptax, Convention (USEPA 2012e).
Gold Crest H-60, Termide,Velsicol Prohibited in 21 countries. Mexico: Forbidden import
104,Heptox,Goldcrest since 1994, however the Clordane (Octachlor) are in
the Catalogue of Registred Pesticides for their use,
importation and commercialization (Cofepris, 2010).

Polanco Rodríguez et al., 2015b.

Fig. 2. Area of the Ring of Sinkholes.

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A.G.P. Rodríguez et al. Groundwater for Sustainable Development 7 (2018) 20–29

Fig. 3. Place of study of levels of OCP in blood of women with cancer in 18 municipalities of Yucatan.

and discharge points (Steinich and Marín, 1996a, 1997; Oehlmann The evidence show a high degradation of the water quality, mainly
et al., 2013). in the livestock area, with high levels of 13.61 and 12.54 ppm of hep-
The Ring of Sinkholes of Yucatan is a complex geohydrological net tachlor in the municipality of Dzilam Gonzalez at North-East of Yucatan
that acts as a dumper and conduction of water, enabling the transpor- (discharge zone of the Ring of Sinkholes to the Gulf of Mexico); in
tation of pesticides (Perry et al., 1995). In this sense, an unappropriate Celestun in the North-West of Yucatan (discharge zone to Gulf of
use and management of agrochemical in agricultural area can severely Mexico) with levels of 3.2 ppm of endrin, 4.1 ppm of ɗ-lindane, and in
affect the aquifer and the human health (Miller, 1996; Miller and Tecoh (recharge zone at centre of the Ring of Sinkholes) of 5.23 ppm of
Sharpe, 1998). γ-lindane, 6.53 ppm of α-lindane (Polanco Rodríguez et al., 2015a).

Fig. 4. Study area selected for levels of pesticides on


breast milk: (1) metropolitan area (Kanasin), (2)
coastal area (Maxcanu), and (3) agricultural area
(Peto) (Polanco Rodríguez Ángel et al., 2017b).

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This is a problem for the water conservation in the Ring of Sinkholes sinkholes (Polanco Rodríguez et al., 2015b).
because it is a declared Natural Area for Protection (DOF, 2013). The water pollution is a potential risk for public health in Maya
In the municipality of Tecoh, in the centre of the recharge zone of communities since the 30% of inhabitants still drink polluted water
the Ring of Sinkholes, there are 128 cenotes and 724 agricultural pro- from the wells and sinkholes. The communities have a very low risk
duction units, distributed over the area of about 4000 ha. In the other perception about the impact of pesticides on the human health and the
hand, this recharge zone of the Ring of Sinkholes can receive pollutants environment, and therefore health promotion programs and official
from the main agriculture area in the southern area of Yucatan, and can support are needed (Torresan, 2011; Polanco Rodríguez et al., 2015b).
affect the underground water flow from the South-West to North-East This scenery in Mexico is similar to the Indian pollution by pesticides
during the dry season. In the study, the highest levels of pesticides in and their impact on the public health (Mathur, 2008; Thakur, 2008;
water were in dry period, by concentration of pollutants in a scarce Abhilash and Singh, 2009), as well as in Tunisia when users, manage-
water flow (Polanco Rodríguez et al., 2015a). ment, and regulatory bodies are dispersed (Mekki et al., 2017).
The municipality of Dzilam Gonzalez, one of the discharge zone is
located in the main livestock breeding region of the Yucatan peninsula, 4.2. Bioaccumulation of OCP
covering 440,000 ha of grasslands, large areas of pasture for livestock
that have replaced indigenous tropical forest since the 1940s (INEGI, Diverse studies of epidemiology occupational have shown associa-
2013). One of the vulnerabilities of the groundwater comes from the tions between agriculture and pesticides management with endometrial
intensified deforestation in Yucatan in the last 24 years (30% loss of cancer in Jaipur, India (Mathur et al., 2008), breast and uterus cancers
vegetation), with highest impact at northeast of Yucatan (Durán, 2010). mortality in Punjab, India (Thakur et al., 2008). There are very few
Deforestation by land use has promoted soil erosion and facilitated investigations of pesticide levels in blood and maternal milk in Mexico.
infiltration of OCP to the groundwater (Rashid, 2011). Agricultural A study in Veracruz, Mexico, showed that concentrations of DDT and its
activities have potential impacts on soil and water in karst regions, metabolites were larger in women with breast cancer than in a control
including deforestation, changes in grazing intensity and application of group (Waliszewski et al., 2003). Another study detected high levels of
fertilizers, pesticides and storage of farm wastes, with a particular focus OCP in breast milk in Chelem, Yucatan, Mexico, in the cost area (Rodas-
on water quality including suspended sediment, nitrate, pesticides, and Ortiz et al., 2008). The role of pesticides as endochrine disruptors (ECD)
microbial pathogens (Coxon, 2011). The environmental responses to have related with cancers in the reproductive system with impacts on
reforestation increases a range of environmental benefits. Areas with the public health. ECD include a group of molecules of organochlorine
shallow aquifers can be reforested to reduce water pollution. Refor- pesticides. Epidemiologic studies in a country or region are crucial to
estation should be used to build forest networks surrounded by low- alert the health systems and researchers about the geographical trends
intensity land use and that provide links within regions and between and prevalent spatial distribution of disease-carrying agents (Diamanti-
biomes (Cunningham et al., 2015). Kandarakis et al., 2009).
Other vulnerability in this livestock area comes from the highest The International Agency for Research on Cancer (IARC) are
density of sinkholes, worsening the vulnerability of the aquifer to working on diverse environmental factors that can increase the risk of
contamination from the intensive farming and agricultural activities in human cancer. These include chemicals, complex mixtures, occupa-
the area (Perry et al., 2002). Celestun, the other geographical discharge tional exposures, physical agents, biological agents, and lifestyle fac-
zone of the Ring to the Gulf of Mexico in the North-West, with high tors. Interdisciplinary working groups of expert scientists review the
levels of heptachlore and lindane, receives pollutants in situ and from published studies and evaluate the weight of the evidence that an agent
the municipalities that are close to the southern part of the Ring of can increase the risk of cancer (IARC, 2017).
Sinkholes, the main agricultural area. There are three areas with The high level of pesticides in water at livestock area are similar for
highest pollution with organochlorine pesticides: in the discharge zone, the results of high level of pesticides in blood of women with cervical
Dzilam Gonzalez and Celestun at coast of Gulf of Mexico and in the uterine cancer from the same area (livestock area) of Yucatan, that
recharge zone, at centre of the Ring of Sinkholes, mainly the munici- showed concentrations of 7.352 ppm of endosulfan I, 3.695 ppm of al-
pality of Tecoh (Fig. 5). drin, 2.336 ppm of 4,4′dichlorodiphenyldichloroethane, 1.434 ppm of
Furthermore, to the North East of the Ring of Sinkholes in the li- heptachlore in blood (Polanco Rodríguez Angel et al., 2017a, 2017b).
vestock area, there is a large geographical zone of highest permeability Maya women with cancer showed a 72.2% of detection for OCP in
that is vulnerable to pollution due to geological failures and strata blood, the highest frequency of detection of pesticides were dieldrin at
fracturing, as shown in the Geologic Map of Failures and Fractures 66.6% and endosulfan I at 44.4% in agricultural and metropolitan area;
(INEGI, 2010) (Fig. 6). heptachlore at 38.8%, ɗ-HCH, 4,4 DDD, 4,4 DDE at 33.3% in the li-
These geological failures and fractures are formed by the dissolving vestock area. In the metropolitan area, Kanasin and Progreso had high
action of the carbonic gas within the rocks of karstic hydric systems frequency of detection for dieldrin and endrin, HCH, heptachlore, en-
(SARH, 1988), and they facilitate the transport of pollutants into the dosulfan I, II, endosulfan sulphate, DDT and their metabolites (Polanco
underground aquifer (Bauer et al., 2011). Moreover, in this livestock Rodríguez Angel et al., 2017a). The chronic exposure of Maya women
activity area, there is the highest concentration of sinkholes in Yucatan by long periods to OCP can be related to these high levels of detection
(Fig. 7). of pesticides in blood. The epidemiologic scientific literature actually
Another factor of pesticide groundwater pollution is the possibility are related with diverse cancer in the reproduction system of human
of non-point source pollution coming from the south of Yucatan (main being because OCP are endocrine disruptors, interfering with the
agricultural area) dragging the water pollutants, traversing the Ring of synthesis, transport, storage, binding, and activity of natural hormones,
Sinkholes, spreading them to the north, east and west, and eventually this factors can be associated with the cancer risk (Falconer et al., 2006;
reaching to the Gulf of Mexico (Perry et al., 1993, 1995; Leonard, 1990; Mustafa, 2010; Mnif et al., 2011; EEA, 2010).
Albanis et al., 1998). This pattern of the flow dynamic in the study area On the other hand, the high concentrations of pesticides in water at
may explain the presence of particular spots of pollution in the recharge recharge area of the Ring of Sinkholes can be related with highest levels
and discharge areas of the Ring of the Sinkholes. It is relevant that the detected of 18.436 ppm of heptachlore epoxide in breast milk in
regional and local flow of the groundwater can be leakage to sinkholes Yucatan, in the municipality of Kanasin, near to the recharge zone of
(Wang et al., 2001). Groundwater are interconnected and can transport Ring of Sinkholes. These results indicate that children are being feed of
pollutants from diverse source of contamination that can be of high breast milk with high levels of OCP, which may have an impact on
impact to the human health, in this regard it has been stated that 30% central nervous system and cognitive development of child. This pro-
of the population from Yucatan drink water from polluted wells and blem also need a monitoring system in the official Health System.

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Fig. 5. Zones of recharge and discharge of highest pollution in the Ring of Sinkholes.

OCP studies on pollution that was conducted in Yucatan, Mexico, vulnerabilities in the karstic ecosystem of high fragility to the pollution.
reported high levels of concentration of these pesticides in the karstic The use of OCP in Yucatan, together with the natural factor, and
aquifer, high bioaccumulation in the blood of women with cervix their social condition, have contributed to to the chronic exposure of
uterine cancer, and high levels of OCP in breast milk samples from these pesticides in the population, with high impacts on the natural
healthy women, which shows that there is a generalization of bioac- ecosystem and public health problems.
cumulation of OCP in the human, due to the social scenario and natural The social factors and the natural vulnerability of the karst aquifer

Fig. 6. Geologic map of failures and fractures, INEGI (2010).

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Fig. 7. High density of sinkholes (cenotes) in Yucatan (Naturalist Newsletter, 2005).

could explain why in the last 20 years the state of Yucatan has high vulnerabilities and take mitigation measures for a better adaptability
rates to diverse cancer in women and men, as well as increases in birth and sustainable development.
defects, fetal and infant mortality (INEGI, 2006, 2009).
The qualitative study of farmers and family mothers showed that the Acknowledgements
people in rural communities of Yucatan have a very low risk perception
about handling of OCP due to the low educative level, which is of high Part of this work was supported by the research lines from
impact for the public health (Polanco Rodríguez et al., 2015b), and a UNESCO/UNITWIN_WiCop and Erasmus Mundus Joint Ph.D. in
transition to sustainable agricultural and food systems is necessary Marine and Coastal Management from University of Cadiz, Spain.
(FAO, 2012). To the National Council for Science and Technology (CONACYT) for
This scenery in Mexico indicate that programs for sustainable funding this project: Background: M0023-Fomix Yucatan, México.
agriculture, a program to the karst groundwater conservation, health Application 132076 "Evaluation of pesticide levels in the Ring of
regulation in the use of OCP, and promotion health programs are ne- Cenotes: its impact on the ecosystem and public health in the geohy-
cessary to decrease the chronic pesticide exposure of farmers and drologic reserve supply drinking water to the city of Mérida and me-
women, as is the case of Culturama, Brazil and developing countries tropolitan area".
(Celina et al., 2006). In Yucatan, Mexico, official regulations are ne- To the National Council for Science and Technology (CONACYT) for
cessary to protect the karstic aquifer, the environment and the human funding this project 88055 “Salud y Medio Ambiente: cáncer cervi-
health. couterino y mamario, factores de riesgo por agroquímicos y alimentos
contaminados en el Estado de Yucatán.
Acknowledge specially to the women who collaborated to make this
5. Conclusions
project possible, to the municipality authorities, and the head of the
Rural Clinics of Health.
These results of high levels of OCP in water, blood, and breast milk,
showed that the groundwater karst system fragility, the social condi-
Conflict of interest
tions of poverty, the lack of official programs for the monitoring of
pollutants, and lack of application of the environmental laws, are im-
The authors declare that they have no conflict of interest.
portant factors that contribute to these complex problem for the human
health and the environment conservation.
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