Indoor air pollution in a Mexican indigenous community: Evaluation ...

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ava i l a b l e a t w w w. s c i e n c e d i r e c t . c o m
w w w. e l s ev i e r. c o m / l o c a t e / s c i t o t e n v
Indoor air pollution in a Mexican indigenous community:
Evaluation of risk reduction program using biomarkers of
exposure and effect
Arturo Torres-Dosal, Iván N. Pérez-Maldonado⁎, Yolanda Jasso-Pineda,
Rebeca I. Martínez Salinas, Jorge A. Alegría-Torres, Fernando Díaz-Barriga
Laboratorio de Toxicología Ambiental, Facultad de Medicina, Avenida Venustiano Carranza 2405, 78210, San Luis Potosí, S.L.P., Mexico
A R T I C L E I N F O
Article history:
Received 8 September 2006
Received in revised form
15 October 2007
Accepted 16 October 2007
Available online 26 November 2007
Keywords:
Wood smoke
Comet assay
Carboxyhemoglobin
Indoor pollution
1-OHP
A B S T R A C T
Indoor air pollution can be an important risk factor for human health, considering that people
spend more than 60% of their time indoors. Fifty percent of the world population and
approximately 90% of the rural population in developing countries are using biomass as energy
source. Latin America represents 12% of the global consumption of biomass; in Mexico, 27
million people use wood as an energy source. Therefore, in this study we evaluated a 3-stage
risk reduction program. The stages were: 1) removal of indoor soot adhered to roofs and
internal walls; 2) paving the dirt floors; and 3) introduction of a new wood stove with a metal
chimney that expels smoke outdoors. The complete intervention program was applied. In 20
healthy subject residents from an indigenous community in San Luis Potosí, Mexico, we
measured blood carboxyhemoglobin (% COHb), DNA damage (comet assay) in nucleated blood
cells, and urinary 1-OHP levels before and after the program. Before intervention individuals
had a geometric mean COHb level of 4.93% and 53% of the population presented levels above
2.5% considered a safe level. However, in all the studied individuals the levels of COHb were
reduced to below 2.5% (mean level 1.0%) one month after the intervention. Moreover, when
compared, DNA damage in people exposed before the intervention was higher (5.8±1.3 of Tail
Moment) than when the program was introduced (2.8±0.9 of Tail Moment) (PN0.05) and a same
trend was observed with urinary 1-OHP levels; 6.71±3.58 μmol/mol creatinine was the
concentration before intervention; whereas, 4.80±3.29 μmol/mol creatinine was the one after
the program. The results suggest that the intervention program offers an acceptable risk
reduction to those families that use biomass for food cooking.
© 2007 Elsevier B.V. All rights reserved.
1. Introduction
Indoor air pollution can be an important risk factor for human
health, considering that people spend more than 60% of their
time in their houses. Fifty percent of the world population and
approximately 90% of the rural population in developing
countries use biomass as energy source (WHO, 2000a). Some
studies consider that Latin America represents 12% of the global
consumption of biomass (FAO, 1999). In Mexico, 27 million
people use wood with an estimated daily consumption of 2.1 kg/
individual (Masera et al., 2005).
Biomass fuels used for domestic cooking include: wood, crop
residues, agricultural wastes, and animal dung, with wood being
the most commonly used (WHO, 2000a). Biomass combustion
emits a complex mixture of organic compounds and gases,
which include carbon monoxide (CO), nitrogen and sulphur
oxides (NO x and SO x ), aldehydes, polycyclic aromatic hydrocarbons
(PAHs), volatile organic compounds (VOCs), chlorinated
⁎ Corresponding author. Tel./fax: +52 48 262 354.
E-mail address: ivannelinho@hotmail.com (I.N. Pérez-Maldonado).
0048-9697/$ – see front matter © 2007 Elsevier B.V. All rights reserved.
doi:10.1016/j.scitotenv.2007.10.039

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363
Fig. 1 – Location of Tancuime in San Luis Potosi, Mexico.
dioxins, breathable particulate matter (PM) with diameters b10
microns (PM10), and free radicals (Albalak, 2001; Mishra, 2003).
Moreover, wood users rely on simple and rustic stoves such as
open “three-stone” fires and mud, clay, or metal stoves that
result in incomplete and inefficient combustion (Reddy et al.,
1997; WHO, 1997).
Health problems associated with indoor air pollution
include acute lower respiratory infection among children,
chronic respiratory pulmonary disease (COPD) (WHO, 2002),
asthma (Mishra, 2003; Wallace et al., 2003) low birth weight
(Boy et al., 2002), and an increased risk of tuberculosis (Mishra
et al., 1999). Other reports have described that wood smoke is a
risk factor for several types of cancer, including: nasopharyngeal
carcinoma, laryngeal, oral (Clifford, 1972; Franco et al.,
1989; Pintos et al., 1998) and lung (WHO, 2000b).
Since carbon monoxide (CO) is probably the most important
single contaminant emitted during combustion of wood (Viau
et al., 2000), determination of its concentration is also important.
In industrialized countries, concentration limits have
been set at 10 mg/m 3 for outdoor ambient air, while occupational
exposure limits lie around 29–55 mg/m 3 (Viau et al.,
2000). Monitoring of pollution and personal exposures in
biomass-burning households has shown concentration many
times higher than those industrialized countries (Smith, 1987;
Ezzati et al., 2000; Smith et al., 2000; Smith, 1993; Kammen,
1995; Smith, 1988; Terblanche et al., 1994). For example, CO was
monitored in traditional houses in Burundi, India, that use
wood combustion as a major energy source, the study revealed
mean concentration of CO reaching 115 mg/m 3 , a value greatly
above the limit in industrialized countries.
A marker use to indirectly assess CO exposure is carboxyhemoglobin
(COHb) that reflects binding of CO to the hem
portion of hemoglobin. A concentration of COHb b2.5% is currently
considered safe (Kleinman, 2000). The lowest level of
COHb, at which adverse effects are observed, ranges from 2.9 to
3% (Estrella et al., 2005). Moreover, COHb concentrations N5%
are associated with effects, such as neurobehavioral function,
impaired visual function, task performance, and maintaining
alertness (WHO, 1999; EPA, 2000; Raub and Benignus, 2002).
Polycyclic aromatic hydrocarbons (PAHs) are a group of
three- and four-ring compounds that are formed as a result of
incomplete combustion. Thus, the exposure to PAHs has also
been used in indoor air pollution studies (Naumova et al., 2002;
Ohura et al., 2005). Because PAH exposure occurs as a mixture of
compounds, and because pyrene is almost always found in this
mixture, pyrene and its metabolite 1-hydroxypyrene (1-OHP) are
considered appropriate surrogate markers of total PAH exposure
(Jacob and Seidel, 2002).
Wood combustion products such as sulfur dioxide, nitrogen
dioxide, total suspended particulate (TSP), PM2.5, PM10, CO,
VOCs, dioxins and total hydrocarbons have also been shown to
be mutagenic (Tokiwa et al., 1985; Gao et al., 1994; Yin et al., 1998)
and genotoxic in “in vitro” studies (Brits et al., 2004), in exposed
animals (Yin et al., 1994) and in human populations (Yin et al.,
1998; Maffei et al., 2005; Ozturk et al., 2002; Pandey et al., 2005).
On the other hand, diverse in vitro, animal and human studies
indicate that exposure to PAH (emitted during combustion)
causes genotoxicity (Cebulska-Wasilewska et al., 2005; Xue and
Warshawsky, 2005; Zhao et al., 2004; Lemiere et al., 2004).
Taking all this information into account, it is evident that
wood smoke is a serious problem and that intervention
programs are needed to reduce indoor exposure in people that
use biomass as energy source. Therefore, the aim of this study
was to evaluate a risk reduction program using biomarkers of
exposure (COHb and 1-OHP) and a biomarker of effect (DNA
damage).

364 S C I E N C E O F T H E T O T A L E N V I R O N M E N T 3 9 0 ( 2 0 0 8 ) 3 6 2 – 3 6 8
2. Methods
2.1. Population
We studied 20 healthy subjects (ten houses; 10 children aged
5–17 years and 10 adults aged 20–35 years) residents from the
indigenous community of Tancuime, Aquismón in San Luis
Potosi (Fig. 1). This community has 300 families living in
similar conditions. The studied individuals had a similar
ethnic and socioeconomic background and had lived in their
community since they were born. After informed consent was
obtained, a questionnaire was applied and blood and urine
samples were taken. Samples of peripheral blood were
collected into heparinized bottles. The questionnaire registered
characteristics such as age, weight, height, smoke
tobacco exposure, principally. Also with this instrument, we
registered household and sociodemographic characteristics,
occupation of family members, and food habits. All the
families in the study had a low income; they were using
wood as the only fuel source for food cooking, they live in
traditional dwellings (wood-made walls and roof), and usually
spend 60% of their time indoors, the average number of
members in each family was 5. Anthropometrics assessment
was used for evaluation of the nutritional status.
2.2. Intervention program
An initial census survey of the study area was used to identify
homes with open fires stoves, indoor soot adhered to roofs and
internal walls and dirt floors. Thus, for the intervention we
offered 1) removal of indoor soot adhered to roofs and internal
walls, 2) paving dirt floors, and 3) an improved stove (the Patzari
stove), which is constructed using sand, clay and cement; it also
has a metal chimney that expels the smoke outdoors (Masera
et al., 2007). The complete 3-stage risk reduction program was
applied in all houses studied. We applied a questionnaire to
confirm that the improved stove was well accepted by people in
the community. The program was introduced in ten indigenous
houses during August 2005; we assessed exposure to carbon
monoxide, PAHs (1-OHP) and DNA damage previously and one
month after the intervention program.
Table 2 – Levels of urinary 1-OHP before and after risk
reduction program
Stage N Mean±SD (μmol/mol Cr) a Range (μmol/mol Cr)
Before 20 6.72 ±3.58⁎ 1.1–17.8
After 20 4.80±3.29 0.35–18.20
Urinary 1-OHP was measured as stated in Methods.
a Values are geometric data.
⁎pb0.05 when compared after intervention.
and West, (1984). Briefly, 25 μl of whole blood were added to
3 ml of an hemolyzing solution (KH 2 PO 4 /K 2 HPO 4 , 0.01 mol/L,
pH 6.85) in a small test tube and mixed. After 5 min, 0.1 ml of
this mixture was introduced into a test tube, which already
contained 1.15 ml of a diluting solution (25 mg of sodium
hydrosulfite in 20 ml of buffer just before use). After 10 min the
absorbance was read at 420 and 432 nm against a matched test
tube containing only COHb diluting solution.
2.4. Determination of urinary 1-OHP
We quantified 1-OHP following the method described by
Jongeneelen et al. (1987) and Kuusimaki et al. (2004). Under our
conditions, the method detection limits were 0.24 μg/L. Intralaboratory
reproducibility was 16%. The repeatability precision
was 6.0% and recoveries averaged 99%. The urinary 1-OHP concentrations
were adjusted by urinary creatinine. Urinary creatinine
was determined by the Jaffe colorimetric method, (1982).
2.5. DNA damage
In this work DNA damage was evaluated using the comet
assay. Single cell gel electrophoresis was performed as
previously described (Yañez et al., 2003)
2.6. Statistics
To satisfy normality criteria the levels of COHb, urinary 1-OHP
and Tail Moment were logarithm-transformed. Therefore, all
2.3. Carboxyhemoglobin determination
COHb was measured by a spectrometry assay and expressed
as a percentage of plasma hemoglobin as described by Beutler
Table 1 – Levels of carboxyhemoglobin before and after
the risk reduction program
Mean S.D. %b2.5 b %N2.5 c Range
(% COHb) a (% COHb) a (% COHb)
Before 4.9⁎ 4.3 45 55 1.05–13.88
After 1.0 0.14 100 0.0 0.65–1.30
The % of carboxyhemoglobin was measured as stated in Methods.
a Values are geometric data.
b Percentage of people with levels of carboxyhemoglobin below 2.5%.
c Percentage of people with levels of carboxyhemoglobin above 2.5%.
⁎pb0.05 when compared after intervention.
Fig. 2 – DNA damage in people before and after the risk
reduction program. DNA damage was measured using the
comet assay (Tail Moment), as stated in Methods. Values
are geometric data. ( * ) p b0.05 when compared to before
intervention. (A) Tail Moment before intervention. (B) Tail
Moment after intervention.

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365
differences were observed in COHb levels when the studied
population was divided by gender or age groups.
Urinary 1-OHP was used to assess the exposure to PAHs
(Table 2). Results show that the geometric mean level of 1-OHP
before intervention was significantly higher in studied people
(6.71±3.58 μmol/mol Cr) than after the program (4.80±3.29 μmol/
mol Cr).
The amount of DNA damage in the studied people is depicted
in Fig. 2. When compared, DNA damage in people
exposed before the intervention was higher (5.8±1.3 of Tail
Moment) than when the program was introduced (2.8±0.9 of
Tail Moment) (Pb0.05). When the studied population was
divided by gender or age groups, we did not observe differences
in Tail Moment.
Moreover, significant positive correlation was obtained
between urinary 1-OHP and DNA damage in blood cells
(Fig. 3a). This correlation was lost when the intervention program
was implemented (Fig. 3b).
4. Discussion
Fig. 3 – Relation between 1-OHP urinary and DNA damage.
(a) Correlation before intervention program. (b) Correlation
after intervention program.
results are presented as geometric means. For COHb analyses
subjects were divided according to COHb levels, using as a
cutoff point the concentration of COHb level considered to be
safe (2.5%) (Kleinman, 2000). Mean COHb levels, urinary 1-OHP
and Tail Moment before and after intervention were compared
using paired-t test. For all statistical analyses we used Jmpin
Start Statistics Software 5.0 (SAS Institute).
3. Results
Among the studied volunteers, 65% were females, and 100% of
the participants were not smokers, cotinine negative (data not
shown). All families were using wood as the only combustible
available for food cooking.
Table 1 shows the geometric mean COHb level in all
subjects studied before and after intervention. Before intervention
all individuals had a geometric mean COHb level of
4.93% and 55% of those people presented COHb levels above
2.5% considered a safe level. Moreover, this 55% of people had
geometric mean COHb levels of 8.39%. However, in all the
studied individuals the levels of COHb were reduced to below
2.5% (mean level 1.0%) one month after intervention. No
Indoor air pollution has been considered a serious public health
issue in Mexico (SSA, 2002). In this regard, Riojas-Rodriguez et al.
(2001), and Zuk et al., (2007), studied the impact of improved
wood burning stoves on indoor air pollution in rural communities
in Chiapas and Michoacán, Mexico; in both studies the use
of stoves reduced the mean levels of PM10 and PM2.5. Moreover,
Riojas-Rodriguez et al. (2001), observed improvements in respiratory
symptoms.
We designed a risk reduction program for rural communities
similar to Riojas-Rodriguez et al. (2001) and Zuk et al.
(2007). This program included three components: 1) removal of
indoor soot adhered to roofs and internal walls; 2) paving dirt
floors; and 3) introduction of a new wood stove with a metal
chimney that expels smoke outdoors. In this work we are
presenting the results of the health impact of such a program,
as we studied biomarkers of exposure (percentage of COHb,
and urinary 1-OHP) and a biomarker of effect (DNA damage in
blood cells), before and after the program.
It has been shown that the main indoor sources of environmental
CO are smoking and domestic fuel combustion
(Collings et al., 1990; Kleinman, 2000; Puente-Maestu et al.,
1998). Even a relatively low CO exposure may increase COHb
levels in human peripheral blood (Raub and Benignus, 2002).
Higher levels of COHb have been observed in smokers compared
with no smokers. In addition, children living in
houses with smokers, wood, coal or gas heating system
exhibit an increment in COHb levels (Vazquez et al., 1997).
The observed COHb levels in our study before intervention
were very high, almost half of the individuals (55%) had a
COHb level consistent with levels associated with effects
(N2.5% of COHb; Raub and Benignus, 2002; WHO, 1999; EPA,
2000). Moreover, in comparison with others scenarios, the
mean COHb levels reported in our study (4.9%) are high. For
example, a gradient of COHb levels was observed in children
with different type of heating system; COHb concentration
were 0.88 ± 1.34% for wood and coal heating, 0.58 ± 0.97%
for gas heating, and 0.28 ± 0.4% for electric system (Vazquez
et al., 1997).

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In the present study, the geometric mean urinary 1-OHP
concentration was 6.72 μmol/mol creatinine (range: 1.1–17.8)
before intervention and it decreased to 4.80 μmol/mol
creatinine (range: 0.35–18.20) after the program. Both values
are higher than the mean urinary 1-OHP concentrations from
people throughout the world (range: 0.03–0.76 μmol/mol
creatinine) (Levine, 1995; Zhao et al., 1992). These values are
also higher than levels observed in people living in traditional
houses from rural districts in Burundi (1.50 μmol/mol creatinine,
range: 0.26–15.62), that use wood as the principal fuel
(Viau et al., 2000). We don't know the type of wood burned in
Burundi, but it is possible that the difference in exposure
between Mexico (our study) and Burundi is the type of wood
used. It has been shown that different emission rates of PAHs
and other compounds are dependent on fuel and burning
conditions (Jenkins et al., 1996; Zhang and Smith, 1999;
Mcdonald et al., 2000).
Our data suggest that DNA damage in lymphocytes is at
least partially related to exposure to wood smoke, as a relationship
was found between DNA damage in lymphocytes and
levels of 1-OHP in urine of people studied before the program
(Fig. 3). Furthermore, DNA damage decreased after the program
was implemented (Fig. 2.). In addition, evidence of
genotoxic effects in human exposed to biomass fuel smoke
has been shown (Pandey et al., 2005; Musthapa et al., 2004).
DNA damage assessed with the comet assay in lymphocytes
was reported in rural Indian women exposed to biomass fuel
smoke (Pandey et al., 2005). In that study, Olive Tail Moment
was 3.83±0.15 (Pandey et al., 2005). In another study, an
increase frequency of micronucleus and chromosomal aberrations
were found in exposed women (Musthapa et al., 2004).
Moreover, relationships between 1-OHP urinary and early
genotoxic effects: siter chromatid exchanges (SCE), micronuclei
(MC), and DNA damage (assessed with comet assay) has
been shown (Buchet et al., 1995; Vanhummelen et al., 1993;
Siwinska et al., 2004).
Usually, risk reduction programs for indoor air pollution
caused by biomass combustion only include the installation of
a stove with a chimney (Chapman et al., 2005; Smith-Sivertsen
et al., 2004; Khushk et al., 2005; Naeher et al., 2000). Those
programs were evaluated either through a decrease of indoor
air pollution (Riojas-Rodriguez et al., 2001; Naeher et al., 2000;
Khushk et al., 2005; Zuk et al., 2007) and/or by a reduction in the
incidence of diseases related with this kind of contamination
(Riojas-Rodriguez, et al., 2001; Chapman et al., 2005; Boy et al.,
2000; Smith-Sivertsen et al., 2004). We believe that our study
represents an improvement in this area, as we installed a stove
with a metal chimney that expels smoke outdoors, but also
indoor soot adhering to roofs and internal walls was removed,
and dirt floors were paved (it has been shown that biomass
burning might be the major origin of PAHs in rural soil; Zhang
et al., 2006). It is important to mention that soot is a sink of
several chemicals generated during combustion (Jonker and
Koelmans, 2002a, 2002b) and moreover, an extremely slow
desorption of PAHs from soot has been demonstrated (Jonker
et al., 2005). Therefore, although we do not have information
regarding the importance of each stage in risk reduction, the
elimination of soot sources (in roofs, walls and dirt floor) is a
relevant action considering that this material is a sink of
hydrophobic compounds such as PAHs and Dioxins. Children
and adults can be exposed to this material, by inhalation
(indoor air particles), ingestion (dust particles) or direct dermal
exposure.
This work was a pilot study and although with the limitation
in sample size, the improvement in exposure (1-0HP, and COHb)
and effect (comet assay) was so homogeneous that the State
Government of San Luis Potosi, using the precautionary principle
has expanded the program to different communities. We
are following our studies in these sites.
Acknowledgments
This work was supported by grants from the Consejo Nacional
de Ciencia y Tecnología, Mexico, FOMIX SLP (FMSLP-2005-CO1-
26), Instituto Potosino de la Juventud and Club Rotario San Luis
Potosí, UNION 2000.
“The work described in the manuscript was conducted in
accordance with national and institutional guidelines for the
protection of human subjects.”
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