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Cigarette smoke exposure and increased risks of stunting among under-five children

Published:March 12, 2020DOI:https://doi.org/10.1016/j.cegh.2020.02.029

      Abstract

      Background

      Stunting describes the condition of chronic malnutrition in children under the age of five, especially in the first 1000 days of life, so that it has an impact on increasing morbidity and mortality. The objective of this study was to analyze the relationship between passive smoking and stunting in children 25–59 months old.

      Method

      This cross-sectional study used a stratified random sampling technique in 123 children 25–59 months old. Exposure of cigarette smoke is assessed from the length of exposure to cigarette smoke using The Secondhand Smoke Exposure Scale questionnaire.

      Results

      Bivariate statistical test with Chi-Square and Fisher's Exact Test showed the relationship of stunting to length of cigarette smoke exposure (p-value <0.000; OR 10.316), water source (p-value 0.040; OR 0.145), hygiene (p-value 0.028; OR 2.742), exclusive breastfeeding (p-value 0.041; OR 0.396), history of pregnancy disorders (p-value 0.035; OR 2.791), and recurrent respiratory infections (p-value <0.000; OR 21,368). Logistic regression analysis showed that the length of smoking increases the risk of stunting (p-value <0.000; OR 13,49), and the most influential variable was recurrent respiratory infections (p-value <0.000; OR 30.57).

      Conclusion

      Length of exposure of more than 3 h a day increases the risk of stunting by 10,316 times. Public policy needs to provide health education in the community and family about the effects of cigarette smoke exposure on the increased risk of stunting in children.

      Keywords

      1. Introduction

      Stunting is one of the global health problems to be addressed immediately, illustrates the condition of chronic malnutrition, especially in the first thousand days of life. Hence, it causes the child height growth to be disrupted.
      • Dorsey J.L.
      • Manohar S.
      • Neupane S.
      • Shrestha B.
      • Klemm R.D.W.
      • West K.P.
      Individual, household, and community level risk factors of stunting in children younger than 5 years: findings from a national surveillance system in Nepal.
      Chronic malnutrition has a long-term impact on cognitive development, as well as on the increase of child morbidity and mortality.
      • Vilcins D.
      • Sly P.D.
      • Jagals P.
      Environmental risk factors associated with child stunting: a systematic review of the literature.
      The incidence of stunting in the world is estimated at 156 million,
      • Hall C.
      • Bennett C.
      • Crookston B.
      • et al.
      Maternal knowledge of stunting in rural Indonesia.
      while in Indonesia, it reaches 30.8%, according to the 2018 Basic Health Research.
      • Ministry of Health of the Republic of Indonesia
      Perkembangan PISPK (Program Indonesia Sehat Dengan Pendekatan Keluarga).
      The causes of stunting in children are, however, complex, not only solely about malnutrition.
      • Cumming O.
      • Cairncross S.
      Can water, sanitation and hygiene help eliminate stunting? Current evidence and policy implications.
      The study stated that knowledge of Indonesian people, especially mothers, about the causes of stunting is still low.
      • Haines A.C.
      • Jones A.C.
      • Kriser H.
      • et al.
      Analysis of rural Indonesian mothers knowledge, attitudes, and beliefs regarding stunting.
      Misinformation about the origins of stunting is related to wrong perceptions and behavior in preventing it. Research on the causes of stunting is usually only associated with nutritional factors; therefore, other factors such as exposure to cigarette smoke are still limited. More comprehensive research on the causes of stunting is needed to provide appropriate information to the public in determining efforts to promote health prevention of stunting.
      • Hall C.
      • Bennett C.
      • Crookston B.
      • et al.
      Maternal knowledge of stunting in rural Indonesia.
      Smoking is one of the health problems faced in Indonesia. In the Healthy Indonesia Program with the Family Approach, the achievement of the indicator is still low at 44.74%, meaning that only about 44.74% of family members do not smoke.
      • Ministry of Health of the Republic of Indonesia
      Perkembangan PISPK (Program Indonesia Sehat Dengan Pendekatan Keluarga).
      This shows that there are still many family members in Indonesia who smoke, which in turn directly increases cigarette smoke exposure to both mother and child. Shah et al.
      • Shah S.
      • Kanaan M.
      • Huque R.
      • et al.
      Secondhand smoke exposure in primary school children: a survey in Dhaka, Bangladesh.
      revealed evidence that 40% of children under the age of five are exposed to cigarette smoke, and the majority of sources of exposure come from their fathers.
      Pregnant women who smoke have a short-term impact on fetal growth
      • Ramadani M.
      • Utomo B.
      • Achadi E.L.
      • Gunardi H.
      Prenatal secondhand smoke exposure: correlation between.
      ,
      • Quelhas D.
      • Kompala C.
      • Wittenbrink B.
      • et al.
      The association between active tobacco use during pregnancy and growth outcomes of children under five years of age: a systematic review and meta-analysis.
      and a long-term effect on children's height.
      • Muraro A.P.
      • Gonçalves-Silva R.M.V.
      • Moreira N.F.
      • et al.
      Effect of tobacco smoke exposure during pregnancy and preschool age on growth from birth to adolescence: a cohort study.
      That is due to the nicotine contained in cigarette smoke inhaled by the mother during pregnancy causes impaired embryonic and bone growth, and enters the baby's body during the breastfeeding process.
      • Goyal N.
      • Canning D.
      Exposure to ambient fine particulate air pollution in utero as a risk factor for child stunting in Bangladesh.
      However, the research has only shown the effect of cigarette smoke exposure on fetal development during pregnancy but has not examined further the relationship of cigarette smoke exposure to the incidence of stunting in under-five children.
      The phenomenon explained the importance of research on the causes of stunting for the prevention of stunting in children. This study aimed to analyze the relationship between cigarette smoke exposure and stunting in children 25–59 months. Researchers applied the Health Promotion Model Theory by Nola J. Pender to answer the research question, “Is exposure to cigarette smoke-related to the incidence of stunting in children 25–59 months?".

      2. Method

      This quantitative study used a cross-sectional approach conducted in a rural village, Surakarta City, Indonesia, in July–August 2019. The sample size was 123 children aged 25–59 months. This research used a stratified random sampling technique. The determination of strata based on the study area was divided administratively by the government into 37 community units (RW). Then each RW was taken 3–4 families randomly.
      The number of samples in this study will use the following formula:
      n=NZ1α22P(1P)Nd2+Z1α22P(1P)


      Based on the method above, the sample with an estimated population of 691 children can be calculated as follows:
      n=691(1.96)20.5(10.5)691(0.1)2+(1.96)20.5(10.5)=84,32becomes85


      The researcher anticipates the drop out by adding 10% of the total sample so that the minimum sample size was 93 children. In this study, 123 children exceeded the minimum sample.
      The criteria for inclusion were families with children aged 24–59 months, living in the study area for a minimum of 2 years, having a health record book for mothers and children, willing to become study respondents represented by the parents. Children with a history of chronic cancer and the nephrotic syndrome were excluded from the study. The dependent variable in this study was stunting in children aged 25–59 months, while the independent variable is exposure to cigarette smoke.
      Exposure to cigarette smoke is assessed by the duration of cigarette smoke exposure in children with the questions in the questionnaire. The modified Secondhand Smoke Exposure Scale (SHSES) questionnaire from Shah et al.
      • Shah S.
      • Kanaan M.
      • Huque R.
      • et al.
      Secondhand smoke exposure in primary school children: a survey in Dhaka, Bangladesh.
      was used with validity and reliability to be tested in 30 families with Cronbach's Alpha 0.935. The SHSES questionnaire consisted of a history of child exposure, a history of maternal exposure during pregnancy, and the smoking characteristics of parents. The intended cigarette smoke exposure is a cigarette made from tobacco. Anthropometric data assessment was done by calculating Z-scores and processed by the WHO's World Health Organization Anthro program to assess z-scores. Z-score is assessed with WAZ (weight based on age), WHZ (weight based on height), and HAZ (height based on age).
      The questionnaire also consisted of parental identity, history of childbirth, history of exclusive breastfeeding, family income, history of infection, immunization status, family density, and environmental health (Water, Sanitation, and Hygiene/WASH). Water consists of water sources, the distance of water sources with latrines, and drinking water cooking habits. Sanitation consists of ownership of family toilets, requirements for healthy latrines, management of family waste, use of fuel for cooking. Hygiene consists of family hand hygiene habits.
      Secondary research data were obtained from maternal and child health books. Data retrieval was done by conducting home visits by following the time contract with the family. The statistical tests used were Chi-Square and Fisher's Exact Test, as well as multivariate logistic regression analysis. The validation of the results was carried out by the expert or the expert in charge of the Nutrition Program at the public health center (PHC) in the study area. The ethical review was conducted by the Ethics Committee of Local Hospital numbered 642/V/HREC/2019.

      3. Result

      The prevalence of stunting in children aged 25–59 months was estimated at 33 (26.83%) children. Exposure to cigarette smoke in this study is assessed from the length of exposure to cigarette smoke for a day. The duration of cigarette smoke exposure had a significant relationship with stunting in children 25–59 months (p-value = 0.000; OR = 10.316; 95% CI 3.509–30.323) (Table 1). Long exposure to cigarette smoke more than 3 h per day could increase the risk of stunting by 10.316 times. The majority of cigarette smoke exposure originated from paternal (father) as many as 21 (63.6%), and the majority of father's smoking for more than three years was 77 (97.5%).
      Table 1The relationship of the exposure of cigarette smoke exposure and stunting in children 25–59 Months (n = 123).
      VariableStuntingTotalp-valueOR (CI 95%)
      Yes (%)No (%)f (%)
      1. Exposure to Cigarette Smoke in Children
       a. Duration
      ≥3 h per day14 (42.4)6 (6.7)20 (16.3)<0.000
      Bivariate Test Results with Chi-Square.
      10.316 (3.509–30.323)
      <3 h per day19 (57.6)84 (93.3)103 (83.7)
      Total33 (100)90(100)123 (100)
       b. Source
      Home21 (63.7)56 (62.2)77 (62.6)1.000
      Bivariate Test Results with Chi-Square.
      1.063 (0.464–2.430)
      Public places12 (36.3)34 (37.8)46 (37.4)
      Total33 (100)90 (100)123 (100)
      2. Exposure to Cigarette Smoke in Pregnant Women
       a. History
      Yes22 (66.7)70 (77.8)92 (74.8)0.306
      Bivariate Test Results with Chi-Square.
      0.571 (0.238–1.375)
      No11 (33.3)20 (22.2)31 (25.2)
      Total33 (100)90 (100)123 (100)
       b. Source
      Home15 (45.5)49 (54.4)64 (52)0.496
      Bivariate Test Results with Chi-Square.
      0.697 (0.313–1.553)
      Public places18 (54.5)41 (45.5)59 (48)
      Total33 (100)90 (100)123 (100)
      3. Description of The Smoking Father
       a. Smoker father
      Yes21 (63.6)58 (64.4)79 (64.2)1.00
      Bivariate Test Results with Chi-Square.
      0.966 (0.421–2.215)
      No12 (36.4)32 (35.6)44 (35.8)
      Total33 (100)90 (100)123 (100)
       b. Duration
      <3 yr2 (9.5)0 (0)2 (2.5)0.068
      Bivariate Test Results with Fisher's Exact Test.
      0.247 (0.167–0.365)
      ≥3 yr19 (90.5)58 (100)77 (97.5)
      Total21 (100)58 (100)79 (100)
       c. Frequency
      <3 x per day0 (0)3 (5.2)3 (3.8)0.561
      Bivariate Test Results with Fisher's Exact Test.
      0.724 (0.630–0.832)
      ≥3 x per day21 (100)55 (94.8)76 (96.2)
      Total21 (100)58 (100)79 (100)
      Note:
      a Bivariate Test Results with Chi-Square.
      b Bivariate Test Results with Fisher's Exact Test.
      This study did not analyze the relationship between nutrition and stunting. The variables that had a significant relationship with stunting in 25–59 months (Table 2) in this study were exclusive breastfeeding (p-value = 0.041; OR = 0.396; 95% CI 0.175–0.895), a history of pregnancy disorders (p-value = 0.035; OR = 2.791; 95% CI 1.163–6.698), recurrent respiratory infections (p-value = 0.000; OR = 21,368; 95% CI 5584–81,778), water source (p-value = 0.040; OR = 0.145; 95% CI 0.018–1.137) and hygiene or hand washing habits (p-value = 0.028; OR = 2.742; 95% CI 1.194–6.293).
      Table 2Factors related to stunting in children 25–59 Months (n = 123).
      VariableStuntingTotalp-valueOR (CI 95%)
      Yes (%)No (%)f (%)
      Individual Factor
      1. Sex
       a. Male18 (54.5)45 (50)63 (51.2)0.808
      Bivariate Test Results with Chi-Square.
      1.200 (0.539–2.6710
       b. Female15 (45.5)45 (50)60 (48.8)
      Total33 (100)90 (100)123 (100)
      2. Age
       a. 25–36 months12 (36.4)31 (34.4)43 (35)1.000
      Bivariate Test Results with Chi-Square.
      1.088 (0.473–2.499)
       b. 37–60 months21 (63.6)59 (65.6)80 (65)
      Total33 (100)90 (100)123 (100)
      3. History of preterm birth
       a. Gestational age <37 weeks3 (9.09)3 (3.33)6 (4.9)0.341
      Bivariate Test Results with Fisher's Exact Test.
      2.900 (0.555–15.149)
       b. Gestational age ≥37 weeks30 (90.91)87 (96.67)117 (95.1)
      Total33 (100)90 (100)123 (100)
      4. History of Low Birth Weight
       a. Yes3 (9.09)9 (10)12 (9.8)1.000
      Bivariate Test Results with Chi-Square.
      0.900 (0.228–3.549)
       b. No30 (90.91)81 (90)111 (90.2)
      Total33 (100)90 (100)123 (100)
      5. Body length
       a. Birth length <48 cm11 (33.33)25 (27.8)36 (29.3)0.707
      Bivariate Test Results with Chi-Square.
      1.300 (0.551–3.067)
       b. Birth length ≥48 cm22 (66.67)65 (72.22)87 (70.7)
      Total33 (100)90 (100)123 (100)
      6. Exclusive breastfeeding
       a. No18 (54.55)29 (32.22)47 (38.2)0.041
      Bivariate Test Results with Chi-Square.
      0.396 (0.175–0.895)
       b. Yes15 (45.45)61 (67.78)76 (61.8)
      Total33 (100)90 (100)123 (100)
      7. Duration of breastfeeding
       a. < 2 yr17 (51.51)48 (53.33)65 (52.8)1.000
      Bivariate Test Results with Chi-Square.
      0.930 (0.418–2.066)
       b. ≥ 2 yr16 (48.89)42 (46.67)58 (47.2)
      Total33 (100)90 (100)123 (100)
      Maternal and Paternal Factor
      8. Gestational age
       a. At risk (<20 yr or >35 yr)6 (18.18)12 (13.33)18 (14.6)0.699
      Bivariate Test Results with Chi-Square.
      1.444 (0.494–4.225)
       b. Not at risk (20–35 yr)27 (81.82)78 (86.67)105 (85.4)
      Total33 (100)90 (100)123 (100)
      9. History of chronic energy deficiency
       a. Yes (Mid Upper Arm Circumference/MUAC < 23,5 cm)5 (15.15)6 (6.67)11 (8.9)0.269
      Bivariate Test Results with Chi-Square.
      2.500 (0.708–8.827)
       b. No (MUAC ≥ 23,5 cm28 (84.85)84 (93.33)112 (91.1)
      Total33 (100)90 (100)123 (100)
      10. History of pregnancy disorder
       a. Yes13 (39.39)17 (18.89)30 (24.4)0.035
      Bivariate Test Results with Chi-Square.
      2.791 (1.163–6.698)
       b. No20 (60.61)73 (81.11)93 (75.6)
      Total33 (100)90 (100)123 (100)
      11. Parents' body height
       a. Father
      <155 cm0 (0)0 (0)0 (0)
      ≥155 cm33 (100)90 (100)123 (100)
      Total33 (100)90 (100)123 (100)
       b. Mother
      <150 cm5 (15.15)5 (5.56)10 (8.1)0.176
      Bivariate Test Results with Chi-Square.
      3.036 (0.818–11.263)
      ≥150 cm28 (84.85)85 (94.44)113 (91.9)
      Total33 (100)90 (100)123 (100)
      Infection Factor
      12. Recurrent respiratory tract infections
       a. ≥ 3 x in a year14 (42.42)3 (3.33)17 (13.8)<0.000
      Bivariate Test Results with Chi-Square.
      21.368 (5.584–81.778)
       b. < 3 x in a year19 (57.58)87 (96.67)106 (86.2)
      Total33 (100)90 (100)123 (100)
      13. Recurrent digestive tract infections
       a. ≥ 3 x in a year0 (0)8 (88.89)10 (8.1)0.174
      Bivariate Test Results with Fisher's Exact Test.
      1.402 (1.249–1.575)
       b. < 3 x in a year33 (100)82 (91.11)113 (91.9)
      Total33 (100)90 (100)123 (100)
      14. History of basic immunization
       a. Not complete4 (12.12)5 (5.56)9 (7.3)0.396
      Bivariate Test Results with Chi-Square.
      0.426 (0.107–1.696)
       b. Complete29 (87.88)85 (94.44)114 (92.7)
      Total33 (100)90 (100)123 (100)
      Home Environment Factor
      15. Level of family income
       a. < Rp 1.802.700,00 (Low Income)4 (12.12)8 (8.89)12 (9.8)0.847
      Bivariate Test Results with Chi-Square.
      1.414 (0.396–5.048)
       b. ≥ Rp 1.802.700,00 (Above Standards Income)29 (87.88)82 (91.11)111 (90.2)
      Total33 (100)90 (100)123 (100)
      16. Family member
       a. > 5 persons24 (72.73)69 (76.67)93 (75.6)0.831
      Bivariate Test Results with Chi-Square.
      1.232 (0.497–3.057)
       b. ≤ 5 persons9 (27.27)21 (23.33)30 (24.4)
      Total33 (100)90 (100)123 (100)
      17. Stimulation of growth and development
       a. Less13 (39.39)20 (22.22)33 (26.8)0.940
      Bivariate Test Results with Chi-Square.
      2.275 (0.966–5.360)
       b. Appropriate20 (60.61)70 (77.78)90 (73.2)
      Total33 (100)90 (100)123 (100)
      18. Mother's education
       a. Elementary3 (9.09)13 (14.44)16 (13)0.632
      Bivariate Test Results with Chi-Square.
      0.592 (0.158–2.227)
       b. Middle-senior high30 (90.91)77 (85.56)107(87)
      Total33 (100)90 (100)123 (100)
      19. Father's education
       a. Elementary3 (9.09)15 (16.67)18 (14.6)0.444
      Bivariate Test Results with Chi-Square.
      0.500 (0.135–1.853)
       b. Middle-senior high30 (90.91)75 (83.33)105 (85.4)
      Total33 (100)90 (100)123 (100)
      20. Water (clean water source)
       a. Not good1 (3)16 (17.77)17 (13.8)0.040
      Bivariate Test Results with Fisher's Exact Test.
      0.145 (0.018–1.137)
       b. Good32 (97)74 (82.23)106 (86.2)
      Total33 (100)90 (100)123 (100)
      21. Sanitation (facility of environmental health)
       a. Not good9 (27.27)17 (18.89)26 (21.1)0.447
      Bivariate Test Results with Chi-Square.
      1.610 (0.635–4.083)
       b. Good24 (72.73)73 (81.11)97 (78.9)
      Total33 (100)90 (100)123 (100)
      22. Hygiene (handwashing)
       a. Not good16 (48.48)23 (25.56)39 (31.7)0.028
      Bivariate Test Results with Chi-Square.
      2.742 (1.194–6.293)
       b. Good17 (51.52)67 (74.44)84 (68.3)
      Total33 (100)90 (100)123 (100)
      23. Anthropometric Value
       a. WAZ-score
      <-2 SD and > +2 SD7 (21.21)11(12.22)18(14.63)0.3360.517 (0.182–1.472)
      −2 SD until + 2 SD26 (78.79)79(87.78)105(85.37)
      Total33 (100)90 (100)123 (100)
       b. WHZ-score
      <-2 SD and > +2 SD2 (06.06)11(12.22)13(10.57)0.5132.158 (0.452–10.300)
      −2 SD until + 2 SD31 (93.94)79 (87.78)110 (89.43)
      Total33 (100)90 (100)123 (100)
      Note:
      a Bivariate Test Results with Chi-Square.
      b Bivariate Test Results with Fisher's Exact Test.
      Exposure to cigarette smoke is a long exposure to cigarette smoke more than 3 h a day, which continually occurs, especially in the first 1000 days of life. Recurrent respiratory infections are respiratory infections more than three times a month caused by the risk of exposure to cigarette smoke, such as acute respiratory infection (ARI) and pneumonia. A history of pregnancy disorders is a pregnancy disorder that may be caused by exposure to cigarette smoke, such as intrauterine growth restriction (IUGR). Exclusive breastfeeding is defined as breastfeeding for infants from birth to 6 months of age without providing additional food. Water sources are assessed from the distance of drinking water sources with family toilets and protection from chemical and fecal contamination. Hygiene is evaluated from families having handwashing facilities, the habit of handwashing with running water and soap after defecation, before eating, and preparing food.
      Table 3 Describes the results of the logistic regression test to find out the factors most related with stunting in under-five children. The variables that influenced the incidence of stunting were recurrent respiratory infections (p-value = 0.000; OR 30.57; 95% CI 5.40–172.93), duration of exposure to cigarette smoke (p-value = 0.000; OR = 13.49; CI 95% 3.55–51.33), and water sources (p-value = 0.041; OR = 0.024; CI 95% 0.01–0.85). However, the most related to the incidence of stunting was recurrent respiratory infections.
      Table 3Factors that are Most Associated with Stunting in Children 25–59 Months (n = 123).
      VariableCoefficientS.EWalddfp valueORCI 95% (min-max)
      Recurrent diarrhea−0.3901.1790.11010.7410.680.067–6.82
      Recurrent respiratory infections3.4200.88414.9661<0.00030.575.40–172.93
      History of Pregnancy Disorders1.0390.7202.08210.1492.820.69–11.58
      Exclusive breastfeeding0.7250.6141.39510.2382.060.62–6.87
      Mother's Height−0.9070.9910.83710.3600.4040.06–2.82
      Water (clean water source)−3.7381.8274.18410.0410.0240.01–0.85
      Hygiene1.2240.6563.48310.0623.400.94–12.30
      Exposure length to cigarette smoke in children2.6020.68214.5661<0.00013.493.55–51.33
      Constant−2.8070.51729.45610.0000.060

      4. Discussion

      4.1 Characteristics of children and families related to stunting

      The results of this study showed that the sex of the child was not associated with stunting in children. The results of other studies showed that boys had a strong relationship with the incidence of stunting.
      • Cruz L.M.G.
      • Azpeitia G.G.
      • Súarez D.R.
      • Rodríguez A.S.
      • Ferrer J.F.L.
      This may be related to cultural issues, gender preferences, and differences in eating practices between boys and girls. Boys are biologically more vulnerable to morbidity and mortality.
      • Dake S.K.
      • Solomon F.B.
      • Bobe T.M.
      • Tekle H.A.
      Predictors of stunting among children 6–59 months of age in Sodo Zuria District,South Ethiopia: a community based crosssectional study.
      In this study, the majority of families had an income above the standards set by the government. Children who had non-smoking fathers had less growth disturbance compared to children with smoking fathers. In families with non-smoking fathers, the possibility to consume foods with various nutrients needed by children is higher such as animal protein, which is considered expensive. The results also showed that fathers who smoke spend money to smoke the same value as to buy food such as eggs, meat, milk, oil, and vegetables.
      • Wijaya-Erhardt M.
      Nutritional status of Indonesian children in low-income households with fathers that smoke.
      The results of the study showed that the majority of parents had high middle-senior level education. Parental education may be related to knowledge about stunting. Research results in Indonesia state that only 66 (2.1%) hear, read, and know about stunting.
      • Hall C.
      • Bennett C.
      • Crookston B.
      • et al.
      Maternal knowledge of stunting in rural Indonesia.
      Lack of knowledge will lead to low access to health facilities.
      • Thakur B.
      • Kar S.
      • Pathak M.
      • Thakur N.
      Public-private share in maternal health care services utilization in India: a multinomial logistic regression analysis from three consecutive survey data.
      This showed that public knowledge about stunting still needs to be improved to form behaviors that support stunting prevention.
      • Haines A.C.
      • Jones A.C.
      • Kriser H.
      • et al.
      Analysis of rural Indonesian mothers knowledge, attitudes, and beliefs regarding stunting.

      4.2 Cigarette smoke exposure and increased risks of stunting

      In this current study, the duration of cigarette smoke exposure had a significant relationship with stunting in children 25–59 months. Exposure to cigarette smoke more than 3 h per day increased the incidence of stunting by 10.316 times. However, a study result stated that exposure to cigarette smoke from the environment does not have a significant relationship with the prevalence of stunting.
      • Dadras O.
      • Chapman R.S.
      Biomass fuel smoke and stunting in early childhood : finding from a national survey in Nepal.
      The difference in the results may be due to the length of exposure to cigarette smoke. Prolonged exposure to cigarette smoke causes increased levels of nicotine in the body. Nicotine can reduce the 30–40% oxygen supply and disturb the absorption of nutrients such as calcium, minerals, and vitamin C that are important for the height growth of children.
      • Ramadani M.
      • Utomo B.
      • Achadi E.L.
      • Gunardi H.
      Prenatal secondhand smoke exposure: correlation between.
      The majority of children with stunting in this study had a smoker father with more than three years of smoking and a frequency of smoking more than three times a day. This showed that the exposure to cigarette smoke was constant and a long period of time, especially in the early 1000 days of a child's life (golden period of growth). Exposure to cigarette smoke in the first 1000 days of life increases the risk of stunting by 2.04 times.
      • Pem D.
      Factors affecting early childhood growth and development: golden 1000 days.
      The majority of families did not have a smoking ban at home. A study by Shah et al.
      • Shah S.
      • Kanaan M.
      • Huque R.
      • et al.
      Secondhand smoke exposure in primary school children: a survey in Dhaka, Bangladesh.
      showed that children who lived with smokers had higher nicotine levels of 0.36 ng/mL compared to those who did not live with smokers.
      A history of pregnancy disorders in mothers had a significant relationship with stunting in children in this current study.
      • Young M.F.
      • Nguyen P.H.
      • Casanova I.G.
      • et al.
      Role of maternal preconception nutrition on offspring growth and risk of stunting across the first 1000 days in Vietnam: a prospective cohort study.
      stated that the disturbance in the preconception period and maternal pregnancy is related to the incidence of stunting in children. Exposure to cigarette smoke during pregnancy can increase IUGR, premature birth, and low birth weight. Exposure to cigarette smoke causes the mediator of insulin-like growth factor (IGF), insulin-like growth factor binding protein 2 (IGFBP-3) to be disrupted. This harms children's growth.
      • de Brito M.L.
      • Nunes M.
      • Bernardi J.R.
      • Bosa V.L.
      • Goldani M.Z.
      • da Silva C.H.
      Somatic growth in the first six months of life of infants exposed to maternal smoking in pregnancy.
      There was a relationship between recurrent respiratory infections and stunting in children. One of the effects of exposure to cigarette smoke in children is to reduce the function of cilia and changes in the colonization of normal flora bacteria that function as the body's defenses.
      • Bugova G.
      • Janickova M.
      • Uhliarova B.
      • Babela R.
      • Jesenak M.
      The effect of passive smoking on bacterial colonisation of the upper airways and selected laboratory parameters in children.
      The impaired function causes the child to be vulnerable to respiratory infections such as ARI and pneumonia.
      • Verhagen L.M.
      • Hermsen M.
      • Rivera-Olivero I.A.
      • et al.
      Nasopharyngeal carriage of respiratory pathogens in Warao Amerindians: significant relationship with stunting.
      Recurrent respiratory infections cause inflammatory processes and fever, which increase nutritional requirements for metabolism, and the child experiences a decrease in appetite.
      • Tazinya A.A.
      • Halle-Ekane G.E.
      • Mbuagbaw L.T.
      • Abanda M.
      • Atashili J.
      • Obama M.T.
      Risk factors for acute respiratory infections in children under five years attending the Bamenda regional hospital in Cameroon.
      The bivariate test result shows that exclusive breastfeeding was a protective factor for stunting in children. It was supported by a study by
      • Muldiasman M.
      • Kusharisupeni K.
      • Laksminingsih E.
      • Besral B.
      Can early initiation to breastfeeding prevent stunting in 6–59 months old children?.
      that breast milk prevented stunting by 1.3 times. Early breastfeeding will make children get colostrums, which is rich in nutrients for long-term child development. The provision of maternal colostrum in the first week of life affects the maturation of the gastrointestinal tract and increases the body's immunity.
      • Muraro A.P.
      • Gonçalves-Silva R.M.V.
      • Moreira N.F.
      • et al.
      Effect of tobacco smoke exposure during pregnancy and preschool age on growth from birth to adolescence: a cohort study.
      stated that nicotine could enter a baby's body during the breastfeeding process, thus interfering with the absorption of nutrients in breast milk, especially zinc, thereby increasing the risk of growth disorders.
      In this study, another variable related to stunting in children was environmental health. The source of clean water and handwashing had a relationship with the incidence of stunting in children.
      • Saxton J.
      • Rath S.
      • Nair N.
      • et al.
      Handwashing, sanitation and family planning practices are the strongest underlying determinants of child stunting in rural indigenous communities of Jharkhand and Odisha, Eastern India: a cross-sectional study.
      stated that water, sanitation, and hygiene had a strong relationship with the incidence of stunting in children. Unclean water sources cause the gastrointestinal tract to be exposed to bacteria and produce enterotoxins that interfere with the barrier layer of the digestive tract (environmental enteric dysfunction/EED). Washing hands prevents oral-fecal transmission in the first 1000 days of life in both pregnant women and children.
      • Mbuya M.N.N.
      • Humphrey J.H.
      Preventing environmental enteric dysfunction through improved water, sanitation and hygiene: an opportunity for stunting reduction in developing countries.
      The variables associated with the incidence of stunting from the multivariate analysis were exposed to cigarette smoke, clean water sources, and respiratory tract infections. These three variables might be interconnected. Inadequate environmental health causes children to be vulnerable to diarrhea and diarrhea might cause inadequate nutritional intake in children, so that they experience decreased endurance and are susceptible to respiratory infections.
      • DeBoer M.D.
      • Scharf R.J.
      • Leite A.M.
      • et al.
      Systemic inflammation, growth factors, and linear growth in the setting of infection and malnutrition.
      This might give an idea for a further study on a relationship between environmental health and respiratory infections to the incidence of stunting.
      This study provides fundamental knowledge that the incidence of stunting in children is not only caused by factors directly related to nutrition such as exclusive breastfeeding and nutritional status but also due to other factors such as exposure to cigarette smoke. Health Promotion Model Theory by Nola J. Pender stated that people's perceptions influence public health behavior in looking at health problems, especially the occurrence of stunting in children. Increased knowledge about the occurrence of stunting can improve people's perception, which subsequently forms positive behavior towards efforts to prevent stunting in children.
      The research method used in this study was still weak, so the results of the study may not be generalizable. The limitation of this study is the observation of the relationship between risk factors and effects may not be done at the same time. Exposure to cigarette smoke may have occurred in the past, but the assessment is carried out at this time. Therefore, further research on the occurrence of stunting can be done with a case-control or prospective approach. This study also provides recommendations for experimental research on methods of providing health promotion for the prevention of stunting.

      5. Conclusion

      In addition to nutrition, it turns out there are several other factors that can cause stunting in children 25–59 months old such as exclusive breastfeeding, water source, hygiene, prolonged exposure to cigarette smoke, and recurrent respiratory infections. This study concludes that the duration of cigarette smoke exposure has a significant relationship with stunting in children 25–59 months old. The study recommends that health policies in Indonesia for handling stunting pay attention to not only issues of nutrition, sanitation, education, health services, and social protection, but also the handling of family members who smoke. Providing education to the community and family about the impact of cigarette smoke exposure on the increased risk of stunting in children.

      Financial Support

      We express our gratitude to the Directure of Health Polytechnic of Health Ministry Surakarta for permitting and supporting this study.

      Authorship

      Dyah Dwi Astuti as a research leader (pediatric nursing spesialist).
      Tri Widyastuti Handayani as co leader (community nursing spesialist).
      Duwi Pudji Astuti as co leader (contribution about statistic method).

      Ethical standards disclosure

      Manuscripts describing research involving human participants must include the following statement: “This study was conducted according to the guidelines laid down in the Declaration of Helsinki and all procedures involving research study participants were approved by the Ethics Committee of Dr. Moewardi Local Hospital numbered 642/V/HREC/2019. Written informed consent was obtained from all subjects/patients.” Where verbal consent was obtained, this must be followed by a statement such as: “Verbal consent was witnessed and formally recorded."

      Declaration of competing interest

      There are no conflict interest on this study.

      Acknowledgements

      Thank you to the Directure of Health Polytechnic of Health Ministry Surakarta for funding this research (financial support).

      Appendix A. Supplementary data

      The following are the supplementary data to this article:

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