Int Arch Occup Environ Health

DOI 10.1007/s00420-009-0482-x

ORIGINAL ARTICLE

Exposure of children to polycyclic aromatic hydrocarbons in Mexico: assessment of multiple sources

Rebeca I. Martínez-Salinas · M. Elena Leal · Lilia E. Batres-Esquivel · Gabriela Domínguez-Cortinas · Jacqueline Calderón · Fernando Díaz-Barriga · Iván N. Pérez-Maldonado

Received: 12 June 2009 / Accepted: 19 October 2009© Springer-Verlag 2009

AbstractPurpose Biological monitoring of polycyclic aromatichydrocarbons (PAHs) has expanded rapidly since urinary1-hydroxypyrene (1-OHP) was suggested as a biologicalindex for pyrene. Taking into account that pyrene is oftenpresent in PAHs mixtures, 1-OHP has also been consideredan indirect indicator of exposure to these mixtures. Sourcesof PAHs in developing countries are numerous; however,exposure of children to PAHs has not been studied in detail.Therefore, the aim of this study was to assess exposure ofchildren to PAHs in diVerent scenarios: (a) children livingnext to highways with heavy traYc; (b) sanitary landWll; (c)brick kiln communities and (d) children exposed to biomasscombustion.Methods A total of 258 children (aged 3–13) participatedin the study. The analyses were performed by HPLC withXuorescence detector. Urinary 1-OHP concentrations werethen adjusted by urinary creatinine.

Results The highest levels of 1-OHP in this study werefound in children exposed to biomass combustion (meanvalue 3.25 �mol/mol creatinine), but exposure was alsodetected in children living in communities with brick kilnindustry (mean 0.35 �mol/mol creatinine), or in a commu-nity next to a sanitary landWll (with waste combustion)(0.30 �mol/mol creatinine) and in children exposed totraYc (mean value 0.2 �mol/mol creatinine and 0.08 �mol/mol creatinine).Conclusions Considering our results and taking intoaccount that millions of children in Mexico are living inscenarios similar to those studied in this work, the assess-ment of health eVects in children exposed to PAHs isurgently needed; furthermore, PAHs have to be declaredcontaminants of concern at a national level.

Keywords Polycyclic aromatic hydrocarbons · Children · Indoor air pollution · 1-Hydroxypyrene · Mexico

Introduction

Polycyclic aromatic hydrocarbons (PAHs) are a group ofover 100 diVerent chemicals that are formed during theincomplete burning of coal, oil and gas, garbage or otherorganic substances like tobacco or charbroiled meat.(ATSDR 2006). Because they have both natural and anthro-pogenic sources, they can be easily found in the environ-ment; moreover, they are ubiquitous because of theirenvironmental persistence (ATSDR 2006). Relevantsources of PAHs are smoking, fossil fuel combustion, woodand organic materials’ combustion, vehicle exhaust, amongothers (Franco et al. 2008). PAHs are used as intermediatesubstances in the production of plasticizers, pigments, dry-ing agents and pesticides, but the environment probably

The work described in the manuscript was conducted in accordance with national and institutional guidelines for the protection of human subjects.

R. I. Martínez-Salinas · M. Elena Leal · L. E. Batres-Esquivel · G. Domínguez-Cortinas · J. Calderón · F. Díaz-Barriga · I. N. Pérez-Maldonado (&)Departamento de Toxicología Ambiental, Facultad de Medicina, Universidad Autónoma de San Luis Potosí, Avenida Venustiano Carranza 2405, 78210 San Luis Potosí, S.L.P., Mexicoe-mail: ivan.perez@uaslp.mx

I. N. Pérez-MaldonadoUnidad Académica Multidisciplinaria Zona Media, Universidad Autónoma de San Luis Potosí, San Luis Potosí, S.L.P., Mexico

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receives only small amounts as a direct result of these activ-ities; the most signiWcant emissions are from incompletecombustion of organic materials (Franco et al. 2008). Inthis context, in recent years, indoor combustion of woodhas also been considered an important source of PAHsexposure.

The widespread distribution of PAHs in the environmenthas raised public health concerns. Some PAHs are now rec-ognized as carcinogens or probable carcinogens for humanand other mammals (Franco et al. 2008). Recent studiesdemonstrate that PAHs with more than three aromatic ringsaccount for 70–90% of the total carcinogenic eVect relatedto sources mentioned previously (smoking, fossil fuel com-bustion, wood and organic materials combustion, vehicleexhaust), thus posing a serious health threat (Franco et al.2008). Moreover, eVects such as genotoxicity (Gamboaet al. 2008), oxidative stress (Svecova et al. 2009), asthma(Perera et al. 2009) and in neurodevelopment (Perera et al.2008) have been reported in children exposed to PAHs.

Considering this background information, we need toasses exposure and eVects in areas impacted by PAHs.Regarding exposure, 1-hydroxypyrene (1-OHP) has beentaken as a representative biomarker of exposure in popula-tions exposed to PAHs’ mixtures (Jongeneelen 2001; Jacoband Seidel 2002), taking into account that this compound isa pyrene metabolite, and in its turn, pyrene is often presentin PAHs mixtures. Moreover, Jongeneelen (2001) proposeda benchmark guideline for occupational exposure to PAHs,based on urinary levels of 1-OHP (Wrst level: 0.24 �mol/mol creatinine and 0.76 �mol/mol creatinine for non-smok-ers and smokers, respectively; second level: 1.4 �mol/molcreatinine and third level: 2.3 �mol/mol creatinine and4.9 �mol/mol creatinine for two types of industry, cokeovens and primary aluminum production, respectively).

Sources of PAHs in developing countries are numerous;however, exposure of children to PAHs has not been stud-ied in detail. Therefore, the aim of this study was to assessexposure of children to PAHs in diVerent residential cate-gories (sites included in the study are recognized for theirindustrial activity, indoor wood combustion, waste disposaland brick manufacturing using diVerent materials as fuelsources).

Methods

Materials

Chemicals used in this study were all HPLC grade. 1-OHPnon-aqueous sodium acetate, L-ascorbic acid (99%) and�-glucuronidase/arylsulfatase enzyme from Helix PomatiaH-2 98000 U were obtained from Aldrich (Milwaukee, WI,USA). Reference standard for 1-OHP was from IRIS Clin

Cal-Recipe number 50013 and 50014 (Munich/Germany).HPLC-grade methanol and acetonitrile were obtained fromBurdick & Jackson (Muskegon, MI, USA), glacial aceticacid was obtained from E. MERCK (Darmstadt, Germany)and ultra-pure water (Millipore Q quality; Bedford, MA,USA) was used in all the analyses.

Population

Sampling sites were selected considering previous knowl-edge of the activity in each place. Sites included in thestudy are recognized for their industrial activity, indoorwood combustion, waste disposal and brick manufacturingusing diVerent materials as fuel sources. We performed arandom sampling in nine communities in Mexico (Fig. 1;Table 1). Children who had lived in the selected area sincebirth and children attending 1st to 6th grade in schoolslocated in these communities were screened for study eligi-bility through in-person interviews. The parents of the chil-dren were informed previously about the study and all gavetheir informed consent prior to their inclusion in the study.Urine samples were taken in 258 children (aged 3–13) andstored at ¡20°C prior to being analyzed. The participantgroup consisted of 65 children living in communities withbrick furnaces (communities of San Vicente and Tercera);105 children who live in houses where Wrewood is thedomestic fuel (communities of Ramonal, Ventanilla, Victo-ria and Tancuime); 32 children living next to a municipallandWll in San Luis Potosi city with waste combustion(community of Milpillas) and 56 children living in areasnext to highways with moderate and high vehicular traYc(communities of El Centro and Domingo, respectively).Characteristics such as age, weight, height, smoke tobaccoexposure, sociodemographic characteristics, occupation offamily members and food habits were obtained through aquestionnaire. As an inclusion criteria, children in the studywere not exposed to passive smoking. The study wasapproved by the ethics committee of the School of Medi-cine, Universidad Autonoma de San Luis Potosi.

Urine collection

Urine samples were taken in the morning (Wrst morningurine), collected in sealable plastic bottles and stored in adeep freezer until analysis (¡20°C). Before analysis, sam-ples were thawed at room temperature, homogenized, and10 mL of urine was transferred to test tube.

Determination of urinary 1-OHP

1-OHP was quantiWed following the method described byJongeneelen et al. (1987) and Kuusimaki et al. (2004). Eachsample (10 mL) was mixed with sodium acetate buVer

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(10 mL, 0.2 mol/L, pH 5.0), then 30 �L of �-glucuronidase/arylsulfatase enzyme was added and the sample was incu-bated at 37°C for 12 h. The analyte was extracted by solidphase with C-18 cartridges eluted with methanol (1%) inacetic acid. The material was then concentrated with nitro-gen at 1 mL. The concentrated material was Wltered througha polyvinylidene Xuoride (PDFV) Wlter (13 mm, 0.45 �m,Millex Durapore, Millipore, Bedford, Mass., USA), and aaliquot was transferred to silanized vials. Then, the analyseswere performed by HPLC (HP1100, Agilent Technologies)using a Xuorescence detector (G1321A). The pre-columnwas Zorbax SB-C18, and the column was a Zorbax EclipseXDB-C18. The column temperature was set to 40°C, Xowwas adjusted to 1 mL/min and the injection volume was20 �L. The eluent was 88:12 methanol:water and 1% ascorbicacid. Data were collected and processed with HP ChemStationsoftware. Urinary 1-OHP concentrations were adjusted to

urinary creatinine. Urinary creatinine was determined bythe JaVe colorimetric method, (Taussky 1954). Under ourconditions, the method detection and quantiWcation limitswere 1.0 and 3.6 nmol/L, respectively. Control quality wascertiWed using standards: IRIS Clin Cal Recipe (Munich,Germany) 50013, 8867 and 50014 (9.1, 15.6 and32.5 nmol/L 1-OHP), the recovery was 99%.

Statistics

To satisfy normality criteria, levels of 1-OHP were log-transformed. Therefore, all the results are shown as geo-metric means. Mean levels of 1-OHP were comparedbetween communities, using one way analysis of variance(ANOVA), followed by Tukey’s test. For all statisticalanalyses, we used Jmpin Start Statistics Software 5.0 (SASInstitute).

Fig. 1 Location of studied communities in Mexico

MILPILLAS••TERCERA

• CENTRO• SAN VICENTE• DOMINGO• TANCUIME

RAMONAL

VICTORIAVENTANILLA

Table 1 Characteristics of the studied sites

S.L.P., San Luis Potosí; n, number of children that participated in study

Community n Characteristics

Victoria, Chiapas 25 Rural community with biomass combustion

Ventanilla, Oaxaca 21 Rural community with biomass combustion

Ramonal, Quintana Roo 40 Rural community with biomass combustion

Tancuime, S.L.P. 19 Rural community with biomass combustion

San Vicente, S.L.P. 35 Community with 50 brick kilns using diVerent materials as fuel source

Milpillas, S.L.P. 32 Small community living next to municipal landWll, in the city of San Luis Potosí (municipal and industrial waste)

Tercera S.L.P. 30 Community with 75 brick kilns using diVerent materials as fuel source

Domingo, S.L.P. 17 Small community in San Luis Potosi state exposed to heavy vehicular traYc

Centro, S.L.P. 39 Urban community in the city of San Luis Potosi with moderate vehicular traYc

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Results

In order to facilitate comparisons with urinary 1-OHP pub-lished earlier, we presented our data in both unadjusted andadjusted with urinary creatinine concentrations. The meanlevels and distributions for 1-OHP are depicted in Tables 2and 3. The total 1-OHP mean levels in all children studiedranged from 0.08 to 4.4 �mol/mol creatinine (0.6–5.9 �g/L). The highest levels of 1-OHP in this study were found inVictoria, Chiapas (mean, 4.4 § 3.7 �mol/mol creatinine;5.9 § 5.1 �g/L), in this community, children are exposed tobiomass combustion. Interestingly, the communities thatalso are using biomass combustion as Victoria (i.e.,Ramonal, Ventanilla and Tancuime) had children with uri-nary 1-OHP mean levels, similar to those found in Victoria(Tables 2, 3) On the other hand, four communities (SanVicente, Milpillas, Tercera and Domingo) had childrenwith mean levels of 1-OHP in urine lower than those ofcommunities exposed to biomass combustion, but higherthan the urinary concentration in the community of Centro,which is an urban area with moderate vehicular traYc(Tables 2, 3). Similar results were found when we use dataunadjusted and adjusted with urinary creatinine concentra-tions. (Tables 2, 3).

When grouped by exposure scenario, (a) moderatevehicular traYc; (b) heavy vehicular traYc; (c) fumes froma municipal landWll; (d) fumes from brick kilns and (e)indoor air pollution by biomass combustion, the highestlevels of urinary 1-OHP were found in children exposed toindoor air pollution (approximately one order of magnitudehigher than the other scenarios; Fig. 2). Children living incommunities with brick kiln industry, children living inMilpillas (landWll) and children living in Domingo (heavy

vehicular traYc) were the next communities in order(Fig. 2), leaving the community of El Centro (moderatevehicular traYc) at the end. Interestingly, a similar distribu-tion of communities was found when they were ordered interms of the percentage of children in each of the bench-mark guideline levels (Table 4; Jongeneelen 2001).

Discussion

The 1-OHP levels found in this study (in all diVerent expo-sure scenarios; Tables 2, 3 and Fig. 2) are higher than levelsdetected in children in other studies (Mucha et al. 2006;Freire et al. 2009; Lee et al. 2007; NHANES III 2005;Schulz et al. 2009; Tuntawiroon et al. 2007; Ruchirawatet al. 2007). For example, the geometric mean in childrenaged 6–11 in NHANES III in the United States is»0.05 �mol/mol creatinine (0.091 �g/L; NHANES III). InGermany, a reference value of 0.5 �g/L was derived basedon the representative data collection of the German Envi-ronmental Survey on children 2003–2006 (Schulz et al.2009) and in our study, any community (Pc 95; Tables 2, 3)were below this German reference value. German referencevalues are statistically derived values that indicate theupper margin (Pc95) of background exposure to a givenpollutant in a given population at a given time.

Moreover, Jongeneelen (2001) proposed a benchmarkguideline for occupational exposure to PAHs, taking intoaccount urinary 1-hydroxypyrene levels. Following thisguideline, the reference value as a 95th percentile in non-occupational exposed controls is 0.24 �mol/mol creatinineand 0.76 �mol/mol creatinine for non-smokers and smok-ers, respectively (Wrst level). A no-biological-eVect-level of1-hydroxypyrene in urine for exposed workers was Wxed at

Table 2 Urinary 1-OHP concentration in exposed children (�mol/molcreatinine)

Urinary 1-OHP concentrations are shown in �mol/mol creatinine

Values are geometric means

SD, standard deviation

* p < 0.05 when compared to all communities; ** p < 0.05 when com-pared to San Vicente, Milpillas, Tercera and Domingo; <LOD belowdetection limit

Community Mean SD Pc25 Pc50 Pc75 Pc95 n

Victoria 4.4** 3.7 2.1 4.4 5.4 12.3 25

Ventanilla 3.8** 2.7 2.5 3.8 5.7 8.5 21

Ramonal 2.6** 4.6 1.2 2.7 5.1 14.5 40

Tancuime 2.2** 0.2 1.3 2.0 2.9 4.2 19

San Vicente 0.5 0.4 0.2 0.3 0.5 1.3 35

Milpillas 0.3 0.4 0.2 0.3 0.4 1.1 32

Tercera 0.2 0.2 0.09 0.2 0.4 0.7 30

Domingo 0.2 0.2 <LOD 0.1 0.2 0.5 17

Centro 0.08* 0.2 0.04 0.08 0.1 0.7 39

Table 3 Urinary 1-OHP concentration in exposed children (�g/L)

Urinary 1-OHP concentrations are shown in �g/L

Values are geometric means

SD standard deviation

* p < 0.05 when compared to all communities; ** p < 0.05 when com-pared to San Vicente, Milpillas, Tercera and Domingo; <LOD belowdetection limit

Community Mean SD Pc25 Pc50 Pc75 Pc95 n

Victoria 5.9** 5.1 1.7 5.7 7.4 15.9 25

Ventanilla 5.4** 2.8 1.9 4.9 8.2 10.6 21

Ramonal 4.3** 4.7 0.7 4.6 7.5 12.9 40

Tancuime 3.1** 1.4 1.1 2.9 5.4 7.8 19

San Vicente 1.9 1.7 0.6 2.1 3.5 5.2 35

Milpillas 1.5 1.1 0.5 1.6 1.9 4.9 32

Tercera 1.3 0.9 0.2 1.4 1.8 3.7 30

Domingo 1.2 0.5 <LOD 1.1 2.0 4.6 17

Centro 0.4* 0.8 0.2 0.5 1.6 3.5 39

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1.4 �mol/mol creatinine. It is the lowest reported level atwhich no genotoxic eVects were found and therefore theestimate for the second level of the benchmark guideline.Finally, two reference values for the third level were pro-posed 2.3 �mol/mol creatinine and 4.9 �mol/mol creati-nine, in two types of industry, coke ovens and primaryaluminum production, respectively, and it was designatedoccupational exposure limit (OEL). When our results inchildren were compared with this guideline for adult work-ers, again, only in El Centro did we Wnd a low risk condi-tion; in the rest of the communities, an importantpercentage of children were found at risk (Table 4). It isimportant to note that the guideline values proposed byJongeneelen (2001) are derived for workers and for adultpopulations. Thus, our results are more important in terms

of public health as we studied children in non-occupationalscenarios.

Our results demonstrated that the children most exposedto PAHs were those living in rural communities exposed toindoor air pollution, due to the use of biomass as a principalenergy source. A second group was that of children livingin communities with brick kilns or living next to a munici-pal landWll; and Wnally, less exposed children were thoseexposed to vehicular traYc (Tables 2, 3).

It has been reported that exposure to PAHs due todomestic heating and cooking using biomass as a fuel,resulted in signiWcantly increased levels of 1-OHP(Siwinska et al. 1999). For example, exposed individualsliving in rural districts of Burundi had urinary concentra-tions of 1-OHP in the range of 0.26–15.6 �mol/mol creati-nine (mean: 1.50 �mol/mol creatinine) (Viau et al. 2000),these concentrations were similar to those found in ruralareas in the present study (Table 2). It is important to pointout that in this scenario, 1-OHP can also be used to followthe reduction in risk after a remediation plan. For example,by improving housing conditions (introduction of woodburning stoves, removal of indoor soot adhering to roofsand internal walls and paving of dirt Xoors), we obtained areduction of exposure to PAHs (reduction of a 29% in uri-nary 1-OHP, when compared to levels before the interven-tion program) (Torres-Dosal et al. 2008). Interestingly, inthose individuals, we also found a reduction in the geno-toxic eVect (measured by the comet assay).

PAHs have been analyzed in environmental samples inlandWlls. For example, in a study in Greece, high concentra-tions of total PAHs were found in soil inside a municipallandWll (1,475 �g/Kg soil), whereas concentrations in thesurroundings soils ranged between 11.2–28.1 �g/Kg(Chrysikou et al. 2008). In another study, this performed inthe municipal landWll of Algiers, Algeria, PAHs were foundin ambient air during or after waste combustion (Yassaaet al. 2001). Taking into account, this information and ourdata in Milpillas, but also considering the number of com-munities next to municipal landWlls (hundreds) in Mexico,

Fig. 2 Urine concentrations of 1-OHP in children by exposure sce-nario. Urine concentrations are shown in �mol/mol creatinine. Valuesare geometric means. a, Urban community with moderate vehiculartraYc (SLP); b, community with high vehicle traYc (Domingo); c,largest sanitary landWll in San Luis Potosí city (Milpillas); d, commu-nities with brick kilns industry (Tercera and San Vivente); e, commu-nities that use biomass as principal energy source (Tancuime, Victoria,Ramonal and Ventanilla); f, NHANES III (children aged 6–11)

e)4

ol c

reat

inin

eP

(µm

ol/m

o

13

1- O

HP

0

Residential groupa b c d e f

Table 4 Percentage of children in each range of 1-OHP urinary levels

Community <0.24 �mol/mol creatinine (%)

0.24–1.39 �mol/mol creatinine

1.4–2.3 �mol/mol creatinine

>2.3 �mol/mol creatinine (%)

Victoria 8.0 4.0 20.0 68.0

Ventanilla 0.0 5.0 16.0 79.0

Ramonal 20.0 12.5 15.0 52.5

Tancuime 0.0 35.0 50.0 15.0

San Vicente 26.0 71.0 3.0 0.0

Milpillas 66.0 32.0 2.0 0.0

Tercera 76.5 23.5 0.0 0.0

Domingo 53.0 47.0 0.0 0.0

Centro 95.0 5.0 0.0 0.0

Distribution of communities was found when they were ordered in terms of the percentage of chil-dren in each of the benchmark

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where child labor is a common social issue, it is then obvi-ous that in order to design intervention programs, the deW-nition of pathways of exposure for children (particlesinhalation, soil/dust ingestion, occupational exposure, etc.)becomes a matter of public health concern.

Some of the areas of concern studied in this work werecommunities with small-scale traditional brick kilns. Aver-aging 10 square meters, these primitive open-topped adobekilns are principally Wred with scrap wood and sawdust thatis often impregnated with laminates and varnishes. Usedtires, plastic containers and other types of refuse are oftenburned. Brick kilns are primarily associated with carbonmonoxide and particulate emissions, but they may also emitvolatile organic compounds, nitrogen oxide, sulfur dioxideand heavy metals depending on the type of fuel burned(Blackman and Bannister 1998). Considering our informa-tion from brick-kiln communities (San Vicente and Ter-cera), it is relevant that an important percentage of childrenwith higher than normal levels of urinary 1-OHP werefound. The public health issue is that there are thousands ofbrick kilns in Mexico; thus, thousands of children areexposed to PAHs through this source; moreover, around30% of the children living in these communities work inmaking bricks.

Finally, the levels of urinary 1-OHP found in childrenliving in Domingo (rural area exposed to high traYc) aresimilar to those of children living in cities with high vehicu-lar traYc, such as Bangkok Thailand. For example, themean level of 1-OHP reported by Ruchirawat et al. (2007)in Thai children was 0.18 § 0.01 �mol/mol creatinine,while for Domingo, the mean level was 0.2 § 0.2 �mol/mol creatinine. In its turn, children living in El Centro, anurban area with moderate vehicular traYc had similar lev-els of 1-OHP (0.08 § 0.2 �mol/mol creatinine) to childrenliving in other urban areas studied around the world (Freireet al. 2009; Hansen et al. 2006; Mucha et al. 2006; Leeet al. 2007).

Our study has some limitations such as the lack of infor-mation regarding environmental media and dietary sources.However, our data indicate high exposure levels in childrenliving in all the communities studied in this work. There-fore, more studies are needed in order to elucidate the expo-sure pathways to PAHs.

Most studies have focused primarily on children exposedto PAHs from traYc and/or dietary sources (Fiala et al.2001; Kanoh et al. 1993; Vyskocil et al. 2000; Zhao et al.1990; Tuntawiroon et al. 2007; Ruchirawat et al. 2007).However, our study indicates that in developing countries,other sources can be as or more important than traYc ordiet. Considering these further sources (indoor air pollu-tion, municipal landWlls and small-scale enterprises such asbrick kilns), we can estimate that thousands and probablymillions of children are exposed, some heavily exposed, to

PAHs, all over the world. Therefore, other studies areneeded in order to know more about the health eVects ofPAHs in this vulnerable sector of our population. PAHs arecontaminants of grave concern for children.

Acknowledgments This work was supported by grants from thePROMEP/103.5/07/2574 and PROMEP/103.5/09/603.

ConXict of interest statement The authors declare that they have noconXict of interest.

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