RESEARCH ARTICLE Open Access
Adherence to reduced-polluting biomass fuel
stoves improves respiratory and sleep symptoms
Roberto A Accinelli1,2,3*, Oscar Llanos1, Lidia M López1, María I Pino1, Yeny A Bravo1,2,3, Verónica Salinas1,
María Lazo1, Julio R Noda1, Marita Sánchez-Sierra1, Lacey Zárate1, Joao da Silva1, Fabiola Gianella1,
Leila Kheirandish-Gozal4,5and David Gozal4,5*
Background: Symptoms of sleep apnea are markedly increased in children exposed to smoke from biomass fuels
and are reduced by kitchen stoves that improve indoor biomass pollution. However, the impact of adherence to
the use of improved stoves has not been critically examined.
Methods: Sleep-related symptom questionnaires were obtained from children <15 years of age in 56 families
residing in the communities of Lliupapuquio, Andahuaylas province in Peru before and 2 years after installation of
less-polluting Inkawasi cooking stoves.
Results: 82 children with lifetime exposures to indoor fuel pollution were included. When compared to those
alternating between both types of stoves or those using traditional stoves only, those children who exclusively
used Inkawasi cooking stoves showed significant improvements in sleep and respiratory related symptoms, but
some minor albeit significant improvements occurred when both stoves were concomitantly used.
Conclusions: Improvements in respiratory and sleep-related symptoms associated with elevated indoor biomass
pollution occur only following implementation and exclusive utilization of improved kitchen stoves.
Keywords: Biomass fuel pollution, Sleep, Respiration, Kitchen stoves
Indoor biomass pollution is one of the most important
sources of pollution particularly in the developing world.
 Indoor fuel sources can be either solid, liquid, or gas
combustibles, with biomass fuel and coal constituting by
far the most frequently used solid fuels. Biomass fuel re-
fers to plant or animal-derived material products (wood,
agriculture waste, and dung) burned for cooking or heat-
ing purposes. [2,3] In 2007, solid fuel was used in 42% of
all households worldwide, and in 76% of rural households.
 In developing countries, women and young children
are the most exposed to this form of air pollution because
they spend the greatest proportion of time near the do-
mestic hearth, while this is further exacerbated in highland
areas, since people spend more time indoors because of
the cold climate [5-8].
In-house exposures to biomass pollution have been asso-
ciated with an increased prevalence of lung diseases, in-
cluding COPD [9-17], recurrent acute respiratory tract
infections in children [18-20], lung cancer , asthma
[22,23], tuberculosis [24-26], interstitial lung disease [27,28]
and non pulmonary disease, such as cataracts, nasopharyn-
geal cancer, ischemic heart disease and cor pulmonale .
However, the potential associations between biomass in-
door pollution and sleep-disordered-breathing (SDB) have
not been as extensively explored. Indeed, in a recent study
from our group, we showed a significant increase in the
prevalence of symptoms of SDB in children exposed to in-
door biomass fuel pollution . However, the impact of
adherence to implementation and installation of higher
* Correspondence: firstname.lastname@example.org; email@example.com
1Laboratorio de Respiración del Instituto de Investigaciones de la Altura,
Universidad Peruana Cayetano Heredia, Lima, Perú
4Section of Pediatric Sleep Medicine, Department of Pediatrics, and Comer
Children’s Hospital, Pritzker School of Medicine, The University of Chicago,
Chicago, IL, USA
Full list of author information is available at the end of the article
© 2014 Accinelli et al.; licensee BioMed Central Ltd. This is an open access article distributed under the terms of the Creative
Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and
reproduction in any medium, provided the original work is properly cited.
Accinelli et al. BMC Pediatrics 2014, 14:12
efficiency home based stoves that reduce indoor pollution
was not examined. In this context, we took advantage of an
initiative aimed at replacing conventional home based
stoves with modified kitchen stoves that reduce biomass in-
door pollution by more than 95% to assess the impact of
such intervention on sleep and SDB symptoms, while mon-
itoring adherence to such intervention.
The study was approved by the Human Subject Ethics
Committee of the University Cayetano Heredia (registra-
tion code #56758). Informed consent was obtained from
the parents, and age appropriate assent was also obtained
from the children. We performed a prospective survey of
residents in Lliupapuquio, Andahuaylas-Peru, a small vil-
lage located at 3557 meters above sea level, who were
beneficiaries of Program Juntos, a Peruvian National ini-
tiative against poverty. We included children less than 15
years of age, who had a lifetime exposure to traditional
high biomass pollution generating home kitchen stoves. A
total of 56 families were identified during a pilot phase
intervention to install the Inkawasi stove, a Peruvian de-
signed stove with an external exhaust that has conclu-
sively been demonstrated to reduce particulate matter
concentrations (PM 2.5) by 74% when compared to
traditional stoves, while using 50% less wood combust-
ible material, as well as displaying a superior safety pro-
file during daily use .
Two years after the installation and after confirming the
adequate operation of the new stoves, we performed a
follow-up survey. In the village, a proportion of the fam-
ilies who received the Inkawasi stoves never used them
and preferred to continue using their traditional stoves. A
second group opted for the concomitant use of either the
traditional stoves or the new stoves, and a third group of
families exclusively used the new Inkawasi stoves.
Both pre- and post-intervention surveys were conducted
through a structured interview of the parents, using a pre-
viously validated questionnaire [32-34]. This questionnaire
is particularly focused on respiratory and sleep-associated
disorders and their symptoms. However, we did not imple-
ment any specific preferential weighting of questionnaire
items as previously reported in a US-based population
. The major questions for this study included whether
the child snored or not, and if so, the severity of snoring
(loudness and frequency). All sleep-related questions used
Likert-type responses “never” , “rarely” (once per week)
, “occasionally” (twice per week) , “frequently” (three
to four times per week) , and “almost always” (>4 times
per week)  for the preceding 3-month timeframe. The
overall scores to problems during sleep were designated
from each of the answers to questions pertaining to
sleep and divided by the number of questions. Other an-
swer categories of Likert-type order were for bedtime:
“7:00–8:00 p.m.,” “8:00–9:00 p.m.,” “9:00– 10 p.m.,”
“10:00–11:00 p.m.,” and “after 10 p.m.”; for wake up time:
“5:00–6:00 a.m.,” “6:00–6:30 a.m.,” “6:30–7 a.m.,” “7:00–
7:30 a.m.,” and “after 7:30 a.m.”; for loudness of snoring:
“mildly quiet” , “medium loud” , “loud” , “very loud”
, “extremely loud” ; for child’s room: “sleep alone,”
“share with 1,” “share with 2,” “share with 3,” and “share
with >3”; and for all other items binary answer categories
were applied. Likert values were treated as continuous vari-
ables for comparison purposes, and response scores ad-
dressing related symptoms were collapsed and treated as a
Questions on adherence regarding the use of new im-
proved stoves were developed and implemented only dur-
ing the follow-up visit.
Data were analyzed using SPSS statistical software (ver-
sion 17.0, Chicago, IL). McNemar tests or Chi-square test
with Fisher Exact correction were used to perform paired
comparisons of qualitative variables before and after kit-
chen stove change. A p-value of less than 0.05 was consid-
ered to be statistically significant.
Eighty-two children with lifetime exposures to biomass
fuel indoor pollution were included. The mean age was
8.3 ±3.2 years, ranging from 2 to 14 years, and the co-
hort included 40 boys (48.8%). Of the 82 children, 38 were in
households in which only the new Inkawasi stove stoves
were available, 19 had access to both the Inkawasi stoves and
traditional stoves operating concomitantly in their houses,
and 25 children continued to exclusively use the traditional
stoves despite having the new Inkawasi stoves installed.
The prevalence of respiratory symptoms for the whole
cohort was very high during the initial visit as follows:
nasal congestion (40%), frequent colds (41.3%), hyperactiv-
ity (26.9%), frequent repetitive movements during sleep
(35.4%), sore throat (38%), night time awakenings (42.3%),
daytime sleepiness (21.8%), and falling asleep at school
(11.7%). In follow-up survey, when the 25 children who
did not use the new Inkawasi kitchen stoves were omitted
from the analyses (Table 1), the remaining 57 children
demonstrated statistically significant reductions in the fre-
quency of sore throat (44.4% vs. 25.9%; p<0.05), headache
at awakening (43.4% vs. 22.6%; p<0.05), and nightmares
(48.1% vs. 25.9%; p<0.05). A statistically significant im-
provement in easiness to fall asleep was also found (29.6%
vs. 55.6% p<0.01). When the 19 children who were not
exclusively using the modified stove were further excluded
from the intervention group, the remaining 38 children
continued to demonstrate improvements in ease to fall
asleep (19.4% vs. 50%; p<0.02), and in the frequency of
sore throat symptoms (47.2% vs. 22.2%; p<0.05), as well
as improvements in the willingness to go to sleep (51.4%
vs. 77.1%; p<0.05) (Table 1). In fact, the children who
Accinelli et al. BMC Pediatrics 2014, 14:12
Page 2 of 5
exclusively used the improved Inkawasi kitchen stoves ex-
hibited significant improvements in the largest number of
questionnaires items (n=6/28; Table 1) compared to those
alternating use of the 2 stoves (n=1/28; p<0.05), as well
as those not using the improved stoves (0/28; p<0.02).
In the present study, we confirm previous findings that
children who have endured lifelong exposures to bio-
mass fuel indoor pollution display an inordinately high
prevalence of sleep and respiratory symptoms, including
SDB symptoms . Furthermore, we now show that
the magnitude of improvement in a selected number
of these symptoms, particularly sleep-related symptoms,
emerges only after changing the stoves to those with im-
proved, less polluting characteristics. Interestingly, even
partial use of the new and improved Inkawasi stove was as-
sociated with some degree of improvements, albeit not as
prominent or extensive as those occurring when the new
improved stoves were exclusively used.
In the context of the current study, we found a remark-
ably similar prevalence of respiratory and sleep symptoms
when compared to our previous study with the exception
of snoring (16.7% vs. 52.5%) . However, the magnitude
Table 1 Effects of frequency of use of improved Inkawasi cooking stoves on the itemized symptoms included in the
questionnaire before and 2 years after stove installation
Symptom Improved Inkawasi
stove use only
Mixed Inkawasi and
traditional stove use
(n= 38) (n=25)(n=19)
BeforeAfter p valueBeforeAfter p valueBeforeAfter p value
1647.115 44.1 1770.815 62.56 35.36 35.3
4 12.1515.22 9.54 193 16.700
18 54.5 11 33.311 45.8729.2211.1422.2
175013 38.2729.2937.5635.31 5.9
1648.5 1133.3 1354.2520.89 50527.8
1028.6 1131.47 289 364 22.2844.4
411.4411.47286242 11.14 22.2
Repetitive movements during sleep
1130.6 18 507 289 3610 55.68 44.4
Problems during sleep
20 53.91 2.6 <0.00055 20.85 20.810 52.61 5.3 <0.005
Respiratory effort during sleep
3 8.82 5.9003 12.5001 5.6
Stops breathing during sleep
4 11.82 5.91 4.22 8.31 5.62 11.1
Needs being shaken to breathe during sleep
26.14 12.12 8.73 1315.900
Ease falling asleep
411.15 13.9624416422.22 11.1
Wakes up to urinate
1335.1 1540.59 36 1352 1055.68 44.4
Easiness to wake up
21 56.830 80.7<0.05 1354.2 2187.5 <0.049 5010 55.6
Willingness to go to bed
1851.4 2777.1<0.05 21 8420 8012 66.7 1161.1
Not rested after sleep
1130.615 41.74166 242 11.1422.2
Wakes up during the night
1542.97209 3610409 50 1055.6
Speaks during sleep
1234.3 1028.61144 10 404 22.25 27.8
1 2.8 1.2.82814211.100
Sits while asleep
5 14.33 8.6520.8312.5211.13 16.7
17 47.2 10 27.812 488 329 50422.2
1541.7619.8<0.027 287288 47.1632.6
5 13.95 13.9283 122 11.100
720822.96 246 244 22.200
Sleepiness at school
4 11.838.84 163 121 5.600
Worried about sleep problems
3 8.84 11.8418.200002 11.1
Accinelli et al. BMC Pediatrics 2014, 14:12
Page 3 of 5
of the reduction of those symptoms in the present study
was not as prominent, even though the same survey tool
was used, and children in both studies had similar ages
and ethnicity. Therefore, it is possible that the differences
in response may reflect the mixed utilization patterns of
the new stoves in the present study compared to the com-
prehensive implementation of the Inkawasi stove in our
previous intervention .
In a parallel study of this population, the degree of in-
door pollution was markedly reduced when consistent,
correct, and exclusive use of the improved Inkawasi kit-
chen stoves was implemented. Compared to traditional
stoves, the particulate matter concentration levels de-
creased by 74% and the CO concentration level decreased
by 97%. Of the new stoves installed here, we found that
one year after installation, 78% had deteriorated grills, and
61% had deteriorated combustion chambers, both of these
factors clearly reducing the efficiency of the new stoves.
As such, the differences in the responses recorded in this
study and the preceding study probably reflect some of
these technical and equipment-related issues. Appropriate
utilization and maintenance of the higher efficiency stoves
are critically important factors for the correct operation of
the stoves, and for the anticipated emergence of improve-
ments in respiratory symptoms. In a study performed in
African children who intermittently cooked inside their
residences or outdoors, cooking with solid fuels in the ab-
sence of a chimney or hood was associated with a statisti-
cally significant adjusted hazard ratio of 2.68 (95% CI: 1.38
to 5.23) for the emergence of symptoms of respiratory in-
fection. Although outdoor cooking is less harmful than in-
door cooking, overall, stove ventilation efficiency emerges
as the most significant determinant of acute lower respira-
tory infection mortality . Similar studies have been re-
ported in other countries, such as in India , Nepal 
and Pakistan . In a 2011 meta-analysis of 25 studies,
the overall pooled odds ratios indicate significant associa-
tions between indoor biomass fuel pollution and acute re-
spiratory infection in children (OR 3.53, 95% CI 1.94 to
6.43) . In our study, a most salient finding was that
compliance in the use of the improved stoves was a major
determinant of the outcomes associated with the stove re-
placement intervention. In addition to the correct and ex-
clusive use of the Inkawasi stoves, appropriate maintenance
of such stoves over time appears to be important in secur-
ing improved outcomes.
Some limitations of the present study deserve mention.
First, the study did not implement any objective measures
of sleep or lung function, and such approach would clearly
be needed in future studies. Secondly, quantitative moni-
toring of environmental pollution in each of the house-
holds throughout the duration of the study would be
desirable and is planned in the context of subsequent ini-
tiatives aiming to further spread the implementation of
reduced biomass in-house pollution in poor villages. Fi-
nally, the study was not powered to identify differences in
most of the questionnaire items, since the frequency of
positive responses for several of the questionnaire items in
the pre-implementation group was low, and therefore
given the small number of children in all 3 groups, dem-
onstration of a statistically significant decrease would be
precluded under such circumstances.
In summary, the improvements in sleep-related symptoms
as previously observed following adequate and supervised
implementation of modified kitchen-stoves were not as
significant without the correct and exclusive use of such
less-polluting stoves. Reduced adherence to the use of im-
proved stoves for biomass fuels and inadequate operation
and maintenance of the stoves emerged as determining
factors associated with reduced effectiveness of the inter-
vention. There is no doubt that changing from traditional
biomass fuel stoves to improved less polluting stoves is of
main importance in reducing indoor air pollution associ-
ated symptoms. However, such interventions need to be
coupled with implementation of measures that will ensure
permanent and exclusive use of the new stoves along with
appropriate maintenance training. Otherwise, such well-
intentioned programs aiming to reduce sleep and respira-
tory morbidity due to biomass fuel indoor pollution may
either fail or underperform.
The authors declare that they have no competing interests.
All of the authors have made substantial contributions to the study. RAA:
conception and design of the study, interpretation of data, and drafting of
the article. OL: analysis and interpretation of data, and drafting the article. LL:
design of the study, acquisition of data, and drafting of the article. YB, VS,
ML, JN, MS-S, LZ, JS and FG: design of the study and acquisition of data. LKG
and DG performed critical evaluation and interpretation of the data, and
revised the manuscript critically for important intellectual content. All authors
have reviewed and approved the final version of the manuscript.
The study was funded by Deutsche Gesellschaft für Internationale
Zusammenarbeit GIZ (German Society for International Cooperation), National
Programme for support the poorest-JUNTOS (Government of Peru) and Global
Cooperation Energy and Climate Change (Government of Holland). The funder
did not have any role in the study design, analysis, interpretation or
dissemination of research findings.
1Laboratorio de Respiración del Instituto de Investigaciones de la Altura,
Universidad Peruana Cayetano Heredia, Lima, Perú.2Hospital Nacional
Cayetano Heredia, Lima, Perú.3Facultad de Medicina Alberto Hurtado,
Universidad Peruana Cayetano Heredia, Lima, Perú.4Section of Pediatric
Sleep Medicine, Department of Pediatrics, and Comer Children’s Hospital,
Pritzker School of Medicine, The University of Chicago, Chicago, IL, USA.
5Department of Pediatrics, University of Chicago, 5721 S. Maryland Avenue,
MC 8000, Suite K-160, Chicago, IL 60637, USA.
Received: 15 August 2013 Accepted: 14 January 2014
Published: 17 January 2014
Accinelli et al. BMC Pediatrics 2014, 14:12
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Cite this article as: Accinelli et al.: Adherence to reduced-polluting biomass
fuel stoves improves respiratory and sleep symptoms in children. BMC Pediatrics
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