Introduction

The number of pesticides currently used is high and of varied composition. The panorama of pesticide use at the national level in México is far from complete. _I The patterns of pesticide use in agricultural practices in México have been poorly documented. The publications are often qualitative reports obtained through interviews or through the count of empty containers. No national statistics exist on the use of these compounds (^{García-Hernández et al., 2018}; ^{Herrera-Moreno et al., 2018}; ^{Silveira-Gramont et al., 2018}). The health damages caused by exposure to organophosphates, carbamates, pyrethroids and organochlorines pesticides have been studied in agricultural workers in the Mexican population. There are reports of the different damages due to exposure to Parathion, Methamidophos, Endosulfan, Dimethoate, Diazinon, Chlorpyrifos, Malathion, Dicofol, Permethrin, Carbaryl, Azinphos methyl, Metasystox, Acephate, Trifluralin, Dichlorvos, Paraquat, Aldicarb, Cypermethrin, Dicamba, Monocrotophos and Carbosulfan, among others (^{Recio et al., 2005}; ^{Pérez-Herrera et al., 2008}; ^{Martínez-Valenzuela et al., 2009}; ^{Zúñiga-Violante et al., 2012}; ^{Carbajal-López, Gómez-Arroyo, Villalobos-Pietrini, Calderón-Segura & Martínez-Arroyo, 2016}).

The agricultural sector is considered the population group with the highest risk of exposure to pesticides. Floriculturists stand out, since flower harvesting is performed every day and pesticides are applied two or three times a week. In addition to this, they are used in mixtures and the compounds used differ between floriculturists (^{Castillo, 2011}).

In México, regulations exist establishing measures to protect floriculturists, the general population and the environment from the harmful effects of agricultural activities. The two main ones are NOM-003-STPS-1999, which establishes the conditions of safety and hygiene for handling, storing and transferring pesticides and raw materials for plant nutrition or fertilizers, as well as emergency actions in cases of acute exposure or poisoning. The second one is NOM-017-STPS-2008, which dictates the safety conditions for floriculturists and the protective equipment to be used in the workplace.

Any reports have been made on the practices for the use and application of pesticides reflecting the occupational risk to which farmers are exposed to the formulation of pesticide mixtures, incorrect use or absence of protective equipment (^{García, Ramírez & Lacasaña 2002}) and manual application on crops (^{Blanco-Muñoz & Lacasaña, 2011}). Effects on the health of farmers have also been reported, since the presence of carbamates, pyrethroids, organochlorines and organophosphates has been detected in samples of breast milk, urine and serum (^{Castillo-Cadena et al., 2006}; ^{López-Gálvez, Wagoner, Beamer, de Zapien & Rosales, 2018}). The manifestation of symptoms due to exposure such as headache, dizziness and skin burning sensation (^{Cortés-Genchi et al., 2008}).

In floriculture, a high number of workers are employed in relation to land area, approximately 16 people per hectare, so it is considered a labor intensive activity (^{Ascoflores, 2002}), using insecticides, fungicides, acaricides and herbicides ( ^{Ortiz, Avila-Chávez & Torres, 2017}).

The use of pesticides and agrochemicals requires specific measures. However, in countries such as Greece, Spain, India, Australia, Colombia and México, pesticide application is carried out with poor or no personal protective equipment (^{García et al., 2002}; ^{Macfarlane et al., 2008}; ^{Singh & Gupta 2009}; ^{Damalas-Christos & Hashemi-Seyyed, 2010}; ^{Blanco-Muñoz & Lacasaña, 2011}; ^{Feola, Gallati & Binder, 2012}). This affects the health of farmers, since it is estimated that every year 300,000 cases of pesticide poisoning occur around the world, making it a public health problem (^{Sabarwal, Kumar & Singh, 2018}). The after-work hygiene practices of workers contribute to the levels of pesticides in their homes. Preventive measure training is needed to decrease the risk of home contamination, such as removing work shoes before entering the home, changing clothes before going home or after arrival, showering promptly after work, and so, fore (^{McCauley et. al., 2003}).

Prolonged exposure and retention of pesticides within the body can cause damage to human health, such as dermatological, gastrointestinal, neurological, carcinogenic, respiratory, reproductive or endocrine damage (^{Mostafalou & Abdollahi, 2013}; ^{Nicolopoulou-Stamati, Maipas, Kotampasi, Stamatis & Hens, 2016}) and congenital malformations (^{Castillo-Cadena, Mejia-Sanchez & López-Arriaga 2017}).

The floricultural zone of Estado de México covers 6,740 hectares. Floriculture is the main economic activity in the municipalities of Tenancingo de Degollado, Zumpahuacan, Coatepec Harinas, Villa Guerrero, and Ixtapan de la Sal. It is estimated that it contributes up to 80% to flower exports from Mexico (^{Castillo-Cadena et al., 2017}). In these municipalities, the cultivation and harvest of flowers is carried out all year round. Furthermore, pesticides and mixtures of them are applied massively throughout the year and these vary despite being the same crop (^{Ortiz et al., 2017}; ^{Castillo-Cadena et al., 2006}; ^{Castillo-Cadena et al., 2017}). In addition to this, there is an underreporting of pesticides use, the form of application and precautionary measures if any, which makes it difficult to assess the risk of damage to health and make decisions to avoid them. In order to contribute to the registration of pesticides in flower crops and occupational risk, the objective of this work was to describe the hygienic habits, type of pesticides and personal protective equipment used by floriculturists in Santa Ana Ixtlahuatzingo, Tenancingo, Estado de México.

Methodology

Location of study

Santa Ana Ixtlahuatzingo is a community in the municipality of Tenancingo de Degollado and geolocated in the coordinates 18°57'38"N 99°34'32"O (Figure 1). Its main economic activity and trade is the production of flowers and ornamental plants. Men, women, children and the elderly carry out this activity (^{Mejia-Sanchez, Montenegro-Morales & Castillo-Cadena, 2017}).

Figure 1 Location of Santa Ana Ixtlahuatzingo, community of the municipality of Tenancingo de Degollado (^{Saldívar-Iglesias, Laguna-Cerda, Esquivel-Álvarez & González-Esquivel, 2012}). 

Results

Discussion

The Environmental Guide for Floriculture from Colombia (^{Ascoflores, 2002}), recommends that the use of pesticides requires safe handling to protect workers and the environment where the activity takes place. This to avoid negative impacts on the environment and human health due to the handling of pesticides, considering it necessary to take preventive and control measures in some cases.

To this context, the work of floriculturists in Mexico has a higher risk to human health, compared to other types of agriculture. One of the main differences is the frequent application of pesticides, an activity that is carried out three times a week and throughout the year, increasing the exposure to these substances. (^{Mejia-Sanchez et al., 2017}). Despite the existence of specific official regulations on the use of personal protective equipment for handling and application of pesticides (^{NOM, 1999}), the actual practice in the horticultural and floricultural community of Santa Ana Ixtlahuatzingo is far from what is established in said regulations.

Bad practices in the cultivation of flowers are common in the floricultural zone of the Estado de México and have been reported in previous investigations in which the lack of exclusive areas for cultivation, and the presence of crops and greenhouses in the central parts of towns and populated areas are mentioned (^{Ortiz et al., 2017}; ^{Mejia-Sanchez et al., 2017}). This makes floriculturists and the open population susceptible to developing harmful effects on health, as a consequence of exposure to these toxic substances and the contamination of water, soil and air (^{Bolognesi, 2003}; ^{Hernández-Antonio & Hansen, 2011}).

Our results on the use of protective equipment during the application of pesticides showed that floriculturists use it partially, without observing the provisions ofthe aforementioned standard, which specifies the use of waterproof boots, hat and gloves, long-sleeved clothing, googles and mask. The absence of protective equipment in this area has been previously documented by ^{Castillo-Cadena et al., 2006}, who studied 52 floriculturists from the town of Santa María Aransazú, and reported that only 3.8% of workers wear waterproof gloves and overalls during the application of pesticides. However, the floricultural zone of the State of México is not the only region in this country where studies of this nature have been carried out. Similar results have been reported in other regions, one of these was carried out by ^{Blanco-Muñoz & Lacasaña 2011}, where they studied 99 agricultural workers in central México and found that around 50% do not use protective equipment. While ^{López-Martínez et al., 2018}, studied 126 agricultural workers from occident Mexico, of which 50% do not use protective equipment. In this same region, ^{Herrera-Moreno et al., 2018}, studied 209 fumigators, and identified that 73.6% reported that they do not use protective equipment. In addition to the above, there are also reports in other countries such as Ghana, Greece, Australia and the USA, where studied groups of farmers have shown deficiencies in the correct use of protective equipment during the application of pesticides (^{Macfarlane et al., 2008}; ^{Damalas-Christos & Hashemi-Seyyed, 2010}; ^{Arcury, Quandt, Rao & Russell, 2001}; ^{Okoffo, Mensah, Fosu-Mensah, 2016}). The use of personal protective equipment is the most elementary action to reduce the risk to health before compounds that replace those currently used are available and subsequently eliminated. To this end, the authorities in charge of the proper use of pesticides must intervene.

With respect to hygiene habits, the Official Mexican Standard NOM-003-STPS-1999 establishes that workers must shower or wash exposed body areas at the end of each working day and wash or change their protective clothing or equipment daily. However, most of the floriculturists surveyed do not follow these recommendations. This increases the risk of exposure and consequently damage to health. Such as study conducted by ^{McCauley et al., 2003}, where found high levels of pesticides in the homes of workers who waited more than 2 hours before changing out of their work clothes, providing evidence that they were increasing the risk of pesticide exposure for themselves and other family members within the home. Behavior from bad hygiene habits, also was reported by ^{López-Martínez et al., 2018}, who studied 20 Mexican farmers, of which only 20% change their clothes daily. In contrast, ^{García et al., 2002}, studied 89 Spanish farmers and found that 71% shower at the end of the day. ^{Mohanty et al., 2013}, studied 100 farmers in India and mentioned that 63% take a shower and wash the clothes used after the application of pesticides. It appears that agricultural workers in other countries show better hygienic practices, possibly because the work areas provide adequate facilities for cleaning workers; such conditions that do not regularly exist in the Mexican countryside.

With reference to the pesticides used in the study locality, compounds prohibited by the PAN were identified as highly toxic and with carcinogenic potential, these were Dichlorvos, Carbofuran, Iprodione, Chlorothalonil, Aldicarb and Aldrin. While COFEPRIS has no registration for Carbofuran, Aldicarb and Aldrin. However, these pesticides are still available in this region.

These findings are not exclusive to Santa Ana Ixtlahuatzingo, since in other investigations carried out in the neighboring municipality of Villa Guerrero, which is eminently floricultural, ^{Martínez-Luna et al., 2014}, identified that the most widely used pesticides were Methomyl, Mancozeb, Carbofuran and Methamidophos. While ^{Mejia-Sanchez et al., 2017}, reported Methomyl, Carbofuran, Captan, Methamidophos and Imidan as the most used. It is important to highlight that the compounds used in both locations are different despite being the same crop. The presence of Methamidophos stands out, which is a compound of restricted use. This shows that in Villa Guerrero pesticides prohibited by the PAN are also used.

About the application of pesticide mixtures, our results show that Dichlorvos and Captan make up the most frequent mixture. ^{Oliva, Rodríguez & Silva, 2005}, reported in their study in Bella Vista, a community in the same floricultural area, that the formulation of mixtures and their application is carried out with total ignorance of the impact that they could cause on human health. Our experience in this research leads us to consider with high probability that the same happens in this community.

The information obtained on the protection measures adopted during the application of pesticides in the town of Santa Ana Ixtlahuatzingo reflects that the training and education on the use, application and protection measures during the application was not carried out by qualified personnel, but inherited by the ancestors of floriculturists.

These results invite us to consider the need for continuous training of floriculturists. Such training should address the essential elements of protective equipment, its proper use, as well as the correct selection and application of pesticides in order to reduce risks to the health of workers and damage to the environment.

Conclusions

The conditions under which flower cultivation is carried out in Santa Ana Ixtlahuatzingo, municipality of Tenancingo, Estado de México in relation to the personal protective equipment and the pesticides used, are outside the established Mexican regulations. The results of this research contribute to generate a registry of pesticides applied in floriculture, particularly in the Estado de México, which will facilitate the regulation of their use.

It is recommended that the competent authority promote and supervise the use of pesticides and working conditions in accordance with current regulations.

Conflicts of interest

All authors have no conflicts of interest to declare.