Abstract
This study examined the association between home tobacco smoke exposure (TSE) status and gastrointestinal problems in the past 12-months among U.S. children. We conducted a secondary analysis of the 2018–2019 National Survey of Children’s Health cross-sectional data including 20,149 children ages 4–10 years. Weighted logistic regression models unadjusted and adjusted for child and family covariates were fitted. Overall, 12.3% of children had home thirdhand smoke (THS) exposure only and 1.8% had home secondhand smoke (SHS) and THS exposure. Unadjusted (OR=1.70, 95%CI=1.32,2.20) and adjusted (AOR=1.151, 95%CI=1.14, 1.99) logistic regression results indicated that relative to children with no home TSE, children with home THS exposure only were at increased odds of having frequent or chronic difficulty with gastrointestinal problems over the past 12-months. Interventions are critically needed to promote smoking cessation among household members who live with children in order to reduce levels of SHS and THS in their homes.
Keywords: tobacco smoke pollution, secondhand smoke, thirdhand smoke, stomach, National Survey of Children’s Health
Introduction
There are many known risks associated with involuntary exposure to tobacco smoke.1 Although the prevalence of tobacco smoke exposure (TSE) has declined since 1988,2 it remains at about 38% among children ages 3–11 years.3 Exposure to tobacco smoke consists of both secondhand smoke (SHS) and thirdhand smoke (THS); both sources contain toxic chemicals. Specifically, SHS is the mixture of mainstream smoke exhaled from smokers and sidestream smoke emitted from burning tobacco products that contain over 7,000 chemicals (e.g., nicotine, lead, cadmium, arsenic) including around 70 chemicals that can cause cancer (e.g., benzene, formaldehyde).4 THS pollution consists of a mixture of residual SHS pollutants that remain in environments after active smoking of tobacco products has ceased. THS pollutants re-emit into the gas phase and react with ambient oxidants and other compounds to yield secondary chemicals including those that also increase cancer risk (e.g., tobacco-specific nitrosamines).5
Homes are the predominant locations of TSE among children.1 Despite legislative smoking bans in public places that have promoted voluntary smoking bans in private places,6 there is a need to improve the implementation of these smoke-free rules in private locations such as homes that are not supported by legislation. Specifically, 4-in-10 homes in which smokers and at least one child reside have not implemented a voluntary home smoking ban.7 Thus, children living with household members who smoke tobacco products inside their homes are at risk of inhaling SHS and inhaling, dermally absorbing, or ingesting THS. Unfortunately, home smoking bans alone do not fully protect children from THS exposure and associated clinical risks.8
Active and passive smoking have been causally associated with respiratory- and cardiovascular-related effects such as increased risk of asthma, endothelial dysfunction, and arterial stiffness.9,10 Additionally, mounting research indicates that active smoking may induce pathogenic and carcinogenic effects that cause gastrointestinal disorders such as peptic ulcer disease and inflammatory bowel disease.11–14 There is also sufficient evidence that active tobacco smoking can cause cancer of the stomach.10,15 However, much less is known on the association between TSE and gastrointestinal problems. About 23% of U.S. children four years of age and older have a functional gastrointestinal disorder with functional constipation, abdominal migraine, aerophagia, and irritable bowel syndrome (IBS) being the most prevalent.16 Gastrointestinal problems such as functional gastrointestinal disorders and recurrent abdominal pain are associated with additional nongastrointestinal-related physical and mental health morbidities and increased healthcare utilization.17–19 Therefore, it is important to assess the potential association between child TSE and gastrointestinal problems.
The current study examined the association between home TSE status and gastrointestinal problems among U.S. children 4–10 years old. We posited that children who lived with a household smoker, that did (SHS and THS exposure) or did not (THS exposure) smoke inside the home would be at increased odds of having parent-reported frequent or chronic difficulty with gastrointestinal problems over the past 12-months compared to children who did not live with a household smoker (no home TSE).
Materials and Methods
Participants and Procedures
A secondary analysis of the 2018–2019 National Survey of Children’s Health (NSCH) data was conducted.20 A total of 20,149 children ages 4–10 years were included in this study. Children <4 years old were excluded due to their non-specific symptoms (e.g., crying) and the difficulty in distinguishing normal behaviors (e.g., infant reflux) from gastrointestinal symptoms and diagnoses.21,22 Children ages >10 years were excluded due to the onset of puberty that may be the etiology causing gastrointestinal problems.23,24 The NSCH, an annual survey that collects broad information on U.S. child health and well-being, is sponsored and led by the U.S. Health Resources and Services Administration’s Maternal and Child Health Bureau, and administered by the U.S. Census Bureau.25,26 The University of Cincinnati’s institutional review board (IRB) exempted the current study from review due to using publicly available NSCH data with no identifiers (IRB #: 2021–0262). Participant informed consent was collected as part of the original NSCH study.
The NSCH methodology is available in detail elsewhere.25,26 As a brief overview, households were mailed invitations asking a household adult, usually the parent, to complete a short screener questionnaire online or by mail. The screener asked adults to identify all 0–17-year-olds living in the household, and one household child was randomly selected to be the study participant for the age-specific questionnaire completed by the household adult. The weighted response rate of the 2018 NSCH, conducted from June 2018 to January 2019, was 43.1% (N=30,530).25,26 The weighted response rate of the 2019 NSCH, conducted from June 2019 to January 2020, was 42.4% (N=29,433).
Measures
Child Home TSE Status
Adult respondents reported whether the child lived with anyone who smoked cigarettes, cigars, or pipe tobacco (no/yes). If the adult respondents answered “yes” and the child lived with a smoker, then they reported whether anyone smoked inside the home (no/yes). Both no/yes questions’ responses were combined to classify children by their home TSE status: (1) no home TSE- the child did not live with a household smoker; (2) home THS exposure only- the child lived with a household smoker who did not smoke inside the home; and (3) home SHS and THS exposure- the child lived with a household smoker who smoked inside the home.
Child Gastrointestinal Problems
Adult respondents reported whether the child had frequent or chronic difficulty with digesting food, including stomach or gastrointestinal problems, diarrhea, or constipation in the past 12-months (no/yes).
Child and Family Covariates
Child and family covariates included in this study were: child age, sex, race/ethnicity (non-Hispanic White, non-Hispanic Black, non-Hispanic Other/Multiracial, and Hispanic), premature birth, overweight status, current anxiety problems, and current depression; parent education level (≤high school graduate or equivalent, some college, ≥college degree); family household structure (two currently married parents, two not currently married parents, single parent, and other family household structure), and federal poverty level (0–199%, 200–299%, 300–399%, and ≥400%). Federal poverty level was calculated by the NSCH for public-use to protect households’ confidentiality by using publicly unavailable data on family income and family size including the number of 0–17-year-olds to calculate levels based on State Children’s Health Insurance Program groupings.27
Child premature birth was defined as whether the child was born >3 weeks prior to the due date (no/yes). Child overweight status, defined as whether a healthcare provider told adult respondents that the child was overweight (no/yes), was included in the current study since overweight/obese weight status has been associated with gastrointestinal symptoms and disorders (e.g., gastroesophageal reflux, constipation, and irritable bowel syndrome).28 Current depression and anxiety problems, defined as the child having a current healthcare provider-diagnosed condition, were included since these diagnoses have been linked to gastrointestinal problems starting in childhood29,30 and continuing throughout life.31,32
Statistical Analysis
Sampling weights were applied to all study analyses to adjust for screener and questionnaire nonresponse and to match and provide general estimates of U.S. noninstitutionalized 4–10-year-olds’ sociodemographic characteristics. Unweighted counts and weighted percentages were calculated for home TSE and child and family covariates overall, and by gastrointestinal problems. To answer our study objective, a weighted unadjusted logistic regression model was built to examine the association between home TSE status and gastrointestinal problems. A weighted adjusted logistic regression model was then built while adding the child and family covariates to gain an understanding of how these additional variables attenuated the crude association. Missing data were removed prior to analyses. SPSS Complex Samples (version 28.0) was used and p<0.05 indicated statistical significance.
Results
Of the 20,149 children 4–10 years old, their mean age was 7.05 (SE=0.03) years and 49.1% were female (Table 1). About half (51.1%) were non-Hispanic White, 24.6% were Hispanic, 13.1% were non-Hispanic Black, and 11.2% were non-Hispanic Other race or Multiracial. About 12% of children were born premature, 6.7% were overweight, 5.7% had current anxiety problems, and 1.2% had current depression. The majority of children had parents with an education level of ≥college degree (50.8%) and lived with two currently married parents (64.2%). A total of 39.9% of children were in the lowest federal poverty level of 0–199% and 31.4% were in the highest federal poverty level of ≥400%. Concerning home TSE status, 12.3% of children had home THS exposure only and 1.8% had home SHS and THS exposure.
Table 1.
Child and Family Characteristics of U.S. Children 4–10 Years Old, 2018–2019 NSCH
Overall (N=20,149) | |
---|---|
Child and Family Covariate | n (%)a |
| |
Child Age, M (SE) | 7.05 (0.03) |
Child Sex | |
Male | 10,495 (50.9) |
Female | 9,654 (49.1) |
Child Race/Ethnicity | |
Non-Hispanic White | 13,812 (51.1) |
Non-Hispanic Black | 1,285 (13.1) |
Hispanic | 2,458 (24.6) |
Non-Hispanic Other or Multiracial | 2,594 (11.2) |
Child Premature Birth | |
No | 17,931 (88.5) |
Yes | 2,218 (11.5) |
Child Overweight Status | |
No | 19,112 (93.3) |
Yes | 1,037 (6.7) |
Child Current Anxiety Problems | |
No | 18,732 (94.3) |
Yes | 1,417 (5.7) |
Child Current Depression | |
No | 19,886 (98.8) |
Yes | 263 (1.2) |
Parent Education Level | |
≤High school graduate/GED | 2,972 (26.8) |
Some College | 4,727 (22.4) |
≥College Degree | 12,450 (50.8) |
Family Household Structure | |
2-parents, currently married | 14,012 (64.2) |
2-parents, not currently married | 1,455 (8.7) |
Single parent | 3,582 (20.3) |
Other family type | 1,100 (6.8) |
Federal Poverty Level | |
0–199% | 5,742 (39.9) |
200%−299% | 3,381 (16.4) |
300%−399% | 2,988 (12.3) |
≥400% | 8,038 (31.4) |
Child Home TSE Status | |
No Home TSE | 17,240 (85.9) |
Home THS Exposure Only | 2,602 (12.3) |
Home SHS and THS Exposure | 307 (1.8) |
Abbreviations: NSCH, National Survey of Children’s Health; SE, standard error; TSE, tobacco smoke exposure; THS, thirdhand smoke exposure; SHS, secondhand smoke exposure.
n refers to unweighted count and % refers to weighted column percent, unless otherwise noted.
Parent-Reported Child Home TSE Status and Gastrointestinal Problems
Overall, 9.0% (n=1,851) of children had reports of frequent or chronic difficulty with gastrointestinal problems over the past 12-months. By home TSE status, 13.5% and 7.2% of children with home THS exposure only and home SHS and THS exposure, respectively, had frequent or chronic difficulty with gastrointestinal problems (Table 2). Weighted unadjusted model results indicated that relative to children with no home TSE, children with home THS exposure only were at 1.70 increased odds (95%CI=1.32, 2.20) of having frequent or chronic difficulty with gastrointestinal problems over the past 12-months. Similarly, weighted adjusted model results indicated that when compared to children with no home TSE, children with home THS exposure only were at 1.51 increased odds (95%CI=1.14, 1.99) of having frequent or chronic difficulty with gastrointestinal problems, independent of child age, sex, race/ethnicity, premature birth, overweight status, current anxiety problems, and current depression; parent education level; family household structure, and federal poverty level. Significant covariates in the adjusted model were child age (adjusted odds ratio [AOR]=1.06, 95%CI=1.01, 1.11), premature birth (AOR=1.39, 95%CI=1.06, 1.82), overweight status (AOR=1.66, 95%CI=1.02, 2.71), and current anxiety problems (AOR=3.08, 95%CI=2.32, 4.09).
Table 2.
Home TSE Status and Frequent or Chronic Difficulty with Gastrointestinal Problems among Children 4–10 Years Old, 2018–2019 NSCH
Child Gastrointestinal Problems (n=1,851) | Unadjusted Logistic Regression | Adjusted Logistic Regression | |||||
---|---|---|---|---|---|---|---|
|
|||||||
n (weighted %)a | OR | 95% CI | p-value | AORb | 95% CI | p-value | |
Child Home TSE Status | |||||||
No Home TSE | 1511 (8.4) | Ref | Ref | Ref | Ref | Ref | Ref |
Home THS Exposure Only | 306 (13.5) | 1.70 | 1.32, 2.20 | <0.001 | 1.51 | 1.14, 1.99 | 0.004 |
Home SHS and THS Exposure | 34 (7.2) | 0.85 | 0.52, 1.41 | 0.537 | 0.64 | 0.37, 1.09 | 0.099 |
Child Age, M (SE) | 7.38 (0.08) | - | - | - | 1.06 | 1.01, 1.11 | 0.009 |
Child Sex | |||||||
Male | 920 (8.9) | - | - | - | Ref | Ref | Ref |
Female | 931 (9.0) | - | - | - | 1.03 | 0.85, 1.24 | 0.773 |
Child Race/Ethnicity | |||||||
Non-Hispanic White | 1,282 (9.2) | - | - | - | Ref | Ref | Ref |
Non-Hispanic Black | 118 (9.3) | - | - | - | 0.94 | 0.69, 1.29 | 0.699 |
Hispanic | 242 (9.3) | - | - | - | 1.00 | 0.74, 1.36 | 0.985 |
Non-Hispanic Other or Multiracial | 209 (6.8) | - | - | - | 0.78 | 0.60, 1.02 | 0.070 |
Child Premature Birth | |||||||
No | 1,577 (8.5) | - | - | - | Ref | Ref | Ref |
Yes | 274 (12.3) | - | - | - | 1.39 | 1.06, 1.82 | 0.019 |
Child Overweight Status | |||||||
No | 1,687 (8.6) | - | - | - | Ref | Ref | Ref |
Yes | 164 (14.7) | - | - | - | 1.66 | 1.02, 2.71 | 0.042 |
Child Current Anxiety Problems | |||||||
No | 1,510 (8.0) | - | - | - | Ref | Ref | Ref |
Yes | 341 (24.2) | - | - | - | 3.08 | 2.32, 4.09 | <0.001 |
Child Current Depression | |||||||
No | 1,777 (8.8) | - | - | - | Ref | Ref | Ref |
Yes | 74 (27.0) | - | - | - | 1.17 | 0.67, 2.05 | 0.587 |
Parent Education Level | |||||||
≤High school graduate/GED | 311 (9.1) | - | - | - | 0.91 | 0.67, 1.22 | 0.525 |
Some College | 498 (11.0) | - | - | - | 1.12 | 0.88, 1.43 | 0.354 |
≥College Degree | 1,042 (8.0) | - | - | - | Ref | Ref | Ref |
Family Household Structure | |||||||
2-parents, currently married | 1,180 (8.2) | - | - | - | Ref | Ref | Ref |
2-parents, not currently married | 159 (11.6) | - | - | - | 1.25 | 0.84, 1.85 | 0.267 |
Single parent | 396 (10.4) | - | - | - | 1.16 | 0.90, 1.50 | 0.255 |
Other family type | 116 (8.9) | - | - | - | 0.99 | 0.69, 1.43 | 0.971 |
Federal Poverty Level | |||||||
0–199% | 627 (10.0) | - | - | - | 1.27 | 0.97, 1.66 | 0.087 |
200%−299% | 328 (9.8) | - | - | - | 1.28 | 0.95, 1.72 | 0.103 |
300%−399% | 284 (9.5) | - | - | - | 1.32 | 0.98, 1.78 | 0.072 |
≥400% | 612 (7.1) | - | - | - | Ref | Ref | Ref |
Abbreviations: NSCH, National Survey of Children’s Health; OR, odds ratio; CI, confidence interval; AOR, adjusted odds ratio; Ref, reference group; TSE, tobacco smoke exposure; THS, thirdhand smoke exposure; SHS, secondhand smoke exposure.
n refers to unweighted count and % refers to weighted column percent, unless otherwise noted.
Logistic regression adjusting for child age, sex, race/ethnicity, premature birth, overweight status, current anxiety problems, and current depression; parent education level, family household structure, and federal poverty level. Bold font indicates statistical significance p<0.05.
Discussion
The current study found that home TSE status was associated with frequent or chronic difficulty with gastrointestinal problems in the past 12-months among U.S. children 4–10 years old. Specifically, we found that children who lived in homes in which smoking was not allowed inside the home, and who thus were exposed to home THS only, were at increased likelihood of having frequent or chronic difficulty with gastrointestinal problems compared to children with no home TSE, even after adjustment for important child and family covariates. It is important to highlight that the home THS exposure only group’s effect sizes remained similar in the unadjusted and adjusted models. However, no differences were found between the child home SHS and THS exposure group and gastrointestinal problems, likely due to the smaller group size. While more research is needed to assess biologic plausibility, our findings suggest that child exposure to home THS pollution which includes exposure to nicotine, the predominant constituent of THS,5 may potentially impact children’s gastrointestinal tracts. Further, adult respondents may have under-reported children’s TSE status inside of their homes, which may partially explain the lack of associations of having gastrointestinal problems between children with home SHS and THS exposure versus no home TSE.
Functional gastrointestinal disorders can occur in combination with physiological and morphologic abnormalities including gut motility disturbances and visceral hypersensitivity, as well as alterations of gut microbiota, mucosal and immune function, and central nervous system processing.33 Recently, a review of the literature indicated that the gut microbiome can differ between children with gastrointestinal disorders such as IBS compared to those without IBS.34 Further, we found that children with a parent-reported overweight status were over 1.5 times more likely to have frequent or chronic difficulty with gastrointestinal problems. This finding aligns with other research that suggests gut microbiota, dietary habits, and psychosocial disorders play a role in the pathogenesis of gastrointestinal problems among 4–18-year-olds who are overweight and obese.35 Concerning environmental exposures, a prior review of the literature connected toxic environmental exposures to gut microbiome-associated gastrointestinal problems (e.g., IBS).36 Budding animal and human research studies indicate that active tobacco smoking has been associated with gut microbiome modifications that can lead to several gastrointestinal problems.37,38 Additionally, it is has been reported that exposure to toxicants found in cigarette smoke can effect gut microbiota.39 Distinct from SHS exposure, THS pollution can be ingested, which may have direct implications to children’s gut microbiomes, and in turn, may result in gastrointestinal problems. Specific to THS, recent human studies have indicated an association between THS exposure and gut microbiome alterations in infants40 and preschool children.41 This preliminary evidence suggests that THS exposure may alter children’s microbiomes, which may be related to pediatric pathologies. The current study contributes to this growing body of work and fills a gap in the evidence base.
The current study’s findings highlight that limiting exposure to TSE such as through voluntary home smoking bans does not protect children from the associated health risks. These results align with other previously published research studies that have focused on the associations between TSE and a wide range of children’s health outcomes including respiratory illnesses,8 oral health problems,42 and inadequate sleep.43 Therefore, tobacco cessation should be promoted among households with smokers and children across the U.S. In addition to focusing on screening for and reducing child SHS exposure, it is also important to include information on THS exposure, especially among smokers who have implemented smoke-free home rules. Encouragingly, one study found that when parents who smoked agreed that THS is harmful to their child’s health, they were more likely to make quitting attempts, use tobacco cessation assistance such as nicotine replacement therapy, and enforce strict home and car smoking bans.44
The use of NSCH data has several strengths including the inclusion of a large, nationally representative sample of U.S. children that participated in the 2018 and 2019 surveys. However, limitations should be outlined. The NSCH is cross-sectional and this study could not establish longitudinal or causal relationships of home TSE status with gastrointestinal problems. Adult respondents provided answers for their child, which may have been under- or overestimated due to recall bias or inaccurately answered due to social desirability bias. Additionally, only two questions about home TSE status were included on the 2018 and 2019 NSCH questionnaires. Therefore, objectively measured TSE status among children via biomarkers (e.g., cotinine45) and environmental markers (e.g., hand nicotine46) should be considered in future research. Further, since only one question about gastrointestinal problems was included on the 2018 and 2019 NSCH questionnaires, we were unable to assess specific gastrointestinal symptoms or disorders such as functional constipation among children in this study. Thus, objective confirmation of specific gastrointestinal problems via healthcare provider reports or medical record review is warranted in future studies. Another suggestion for future work is to assess the child’s diet and microbiome, which was not assessed by the NSCH. Additionally, child overweight status was asked among all ages and used in the current study’s analysis, but body mass index was not made publicly available for <10-year-olds. Therefore, we were unable to differentiate between overweight and obese status, which is an important distinction as body mass indices indicative of obesity and severe obesity have been associated with a high prevalence of gastrointestinal problems such as functional constipation among 4–17-year-olds.47
Interventions are critically needed to promote tobacco cessation among household smokers who live with children. Efforts should also promote voluntary smoking bans in order to reduce child TSE. Specifically, parents and other household members who smoke should be educated on THS exposure and how smoking outside of the home does not completely protect their children from TSE-associated risks. Additionally, THS remediation information (e.g., cleaning protocols) should be offered to provide households with the tools needed to reduce and potentially eliminate home THS pollution. Future longitudinal research should consider using objective measures of TSE and gastrointestinal problems to further assess this relationship, and to provide insights into the potential impact chronic THS pollution exposure may have on the development and persistence of gastrointestinal problems during childhood and beyond.
Acknowledgements:
This work was supported by the National Institute on Drug Abuse (NIH Grant Number K01DA044313) and the National Institute of Environmental Health Sciences (NIH Grant Numbers R21ES032161, R01ES030743, and R01ES027815). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.
Footnotes
Declaration of Conflicting Interests: The Authors declare that there is no conflict of interest.
References
- 1.National Center for Chronic Disease Prevention and Health Promotion; Office on Smoking and Health. The health consequences of involuntary exposure to tobacco smoke: a report of the Surgeon General. Atlanta (GA): Centers for Disease Control and Prevention (US); 2006. [PubMed] [Google Scholar]
- 2.Tsai J, Homa DM, Gentzke AS, et al. Exposure to secondhand smoke among nonsmokers - United States, 1988–2014. MMWR Morb Mortal Wkly Rep. 2018;67(48):1342–1346. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Brody DJ, Lu Z, Tsai J. Secondhand smoke exposure among nonsmoking youth: United States, 2013–2016. NCHS Data Brief. 2019;(348):1–8. [PubMed] [Google Scholar]
- 4.National Center for Chronic Disease Prevention and Health Promotion; Office on Smoking and Health. How tobacco smoke causes disease: the biology and behavioral basis for smoking-attributable disease: a report of the Surgeon General. Atlanta (GA): Centers for Disease Control and Prevention (US); 2010. [PubMed] [Google Scholar]
- 5.Jacob P, Benowitz NL, Destaillats H, et al. Thirdhand smoke: new evidence, challenges, and future directions. Chem Res Toxicol. 2017;30(1):270–294. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Monson E, Arsenault N. Effects of enactment of legislative (public) smoking bans on voluntary home smoking restrictions: a review. Nicotine Tob Res. 2017;19(2):141–148. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.King BA, Patel R, Babb SD, Hartman AM, Freeman A. National and state prevalence of smoke-free rules in homes with and without children and smokers: two decades of progress. Prev Med. 2016;82:51–58. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Mahabee-Gittens EM, Merianos AL, Jandarov RA, Quintana PJE, Hoh E, Matt GE. Differential associations of hand nicotine and urinary cotinine with children’s exposure to tobacco smoke and clinical outcomes. Environ Res. 2021;202:111722. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Raghuveer G, White DA, Hayman LL, et al. Cardiovascular consequences of childhood secondhand tobacco smoke exposure: prevailing evidence, burden, and racial and socioeconomic disparities: a scientific statement from the American Heart Association. Circulation. 2016;134(16):e336–e359. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.National Center for Chronic Disease Prevention and Health Promotion; Office on Smoking and Health. The health consequences of smoking—50 years of progress: a report of the Surgeon General. Atlanta (GA): Centers for Disease Control and Prevention; 2014. [Google Scholar]
- 11.Berkowitz L, Schultz BM, Salazar GA, et al. Impact of cigarette smoking on the gastrointestinal tract inflammation: opposing effects in Crohn’s disease and ulcerative colitis. Front Immunol. 2018;9:74. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Li LF, Chan RL, Lu L, et al. Cigarette smoking and gastrointestinal diseases: the causal relationship and underlying molecular mechanisms (review). Int J Mol Med. 2014;34(2):372–380. [DOI] [PubMed] [Google Scholar]
- 13.Chu K, Cho CH, Shin VY. Nicotine and gastrointestinal disorders: its role in ulceration and cancer development. Curr Pharm Des. 2013;19(1):5–10. [DOI] [PubMed] [Google Scholar]
- 14.Zhang L, Ren JW, Wong CCM, et al. Effects of cigarette smoke and its active components on ulcer formation and healing in the gastrointestinal mucosa. Curr Med Chem. 2012;19(1):63–69. [DOI] [PubMed] [Google Scholar]
- 15.IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Personal habits and indoor combustions. Volume 100 E. A review of human carcinogens. IARC Monogr Eval Carcinog Risks Hum. 2012;100(Pt E):1–538. [PMC free article] [PubMed] [Google Scholar]
- 16.Lewis ML, Palsson OS, Whitehead WE, van Tilburg MAL. Prevalence of functional gastrointestinal disorders in children and adolescents. J Pediatr. 2016;177:39–43.e3. [DOI] [PubMed] [Google Scholar]
- 17.Nightingale S, Sharma A. Functional gastrointestinal disorders in children: what is new? J Paediatr Child Health. 2020;56(11):1724–1730. [DOI] [PubMed] [Google Scholar]
- 18.Spee LA, Lisman-van Leeuwen Y, Benninga MA, et al. Predictors of chronic abdominal pain affecting the well-being of children in primary care. Ann Fam Med. 2015;13(2):158–163. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Jarrett M, Heitkemper M, Czyzewski DI, Shulman R. Recurrent abdominal pain in children: forerunner to adult irritable bowel syndrome? J Spec Pediatr Nurs. 2003;8(3):81–89. [DOI] [PubMed] [Google Scholar]
- 20.Child and Adolescent Health Measurement Initiative. 2018–2019 National Survey of Children’s Health (2 years combined data set): SPSS data set. Data Resource Center for Child and Adolescent Health supported by Cooperative Agreement U59MC27866 from the U.S. Department of Health and Human Services, Health Resources and Services Administration, Maternal and Child Health Bureau; 2021. [Google Scholar]
- 21.Vernon-Roberts A, Alexander I, Day AS. Systematic review of pediatric functional gastrointestinal disorders (Rome IV Criteria). J Clin Med. 2021;10(21):5087. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Benninga MA, Faure C, Hyman PE, St. James Roberts I, Schechter NL, Nurko S. Childhood functional gastrointestinal disorders: neonate/toddler. Gastroenterology. 2016;150(6):1443–1455.e2. [DOI] [PubMed] [Google Scholar]
- 23.Hijaz NM, Friesen CA. Managing acute abdominal pain in pediatric patients: current perspectives. Pediatric Health Med Ther. 2017;8:83–91. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Rosenfield RL, Lipton RB, Drum ML. Thelarche, pubarche, and menarche attainment in children with normal and elevated body mass index. Pediatrics. 2009;123(1):84–88. [DOI] [PubMed] [Google Scholar]
- 25.U.S. Census Bureau. 2018 National Survey of Children’s Health methodology report. Available at: https://www.childhealthdata.org/learn-about-the-nsch/methods
- 26.U.S. Census Bureau. 2019 National Survey of Children’s Health methodology report. Available at: https://www.childhealthdata.org/learn-about-the-nsch/methods
- 27.Child and Adolescent Health Measurement Initiative. 2018–2019 National Survey of Children’s Health (2 Years Combined Data Set): child and family health measures, national performance and outcome measures, and subgroups, SPSS codebook, version 1.0. Data Resource Center for Child and Adolescent Health supported by Cooperative Agreement U59MC27866 from the U.S. Department of Health and Human Services, Health Resources and Services Administration, Maternal and Child Health Bureau; 2021. [Google Scholar]
- 28.Phatak UP, Pashankar DS. Obesity and gastrointestinal disorders in children. J Pediatr Gastroenterol Nutr. 2015;60(4):441–445. [DOI] [PubMed] [Google Scholar]
- 29.Campo JV, Bridge J, Ehmann M, et al. Recurrent abdominal pain, anxiety, and depression in primary care. Pediatrics. 2004;113(4):817–824. [DOI] [PubMed] [Google Scholar]
- 30.Korterink JJ, Diederen K, Benninga MA, Tabbers MM. Epidemiology of pediatric functional abdominal pain disorders: a meta-analysis. PloS one. 2015;10(5):e0126982. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31.Horst S, Shelby G, Anderson J, et al. Predicting persistence of functional abdominal pain from childhood into young adulthood. Clin Gastroenterol Hepatol. 2014;12(12):2026–2032. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 32.Shelby GD, Shirkey KC, Sherman AL, et al. Functional abdominal pain in childhood and long-term vulnerability to anxiety disorders. Pediatrics. 2013;132(3):475–482. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33.Drossman DA. Functional gastrointestinal disorders: history, pathophysiology, clinical features, and Rome IV. Gastroenterology. 2016;150(6):1262–1279.e2. [DOI] [PubMed] [Google Scholar]
- 34.Shin A, Preidis GA, Shulman R, Kashyap PC. The gut microbiome in adult and pediatric functional gastrointestinal disorders. Clin Gastroenterol Hepatol. 2019;17(2):256–274. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 35.Tambucci R, Quitadamo P, Ambrosi M, et al. Association between obesity/overweight and functional gastrointestinal disorders in children. J Pediatr Gastroenterol Nutr. 2019;68(4):517–520. [DOI] [PubMed] [Google Scholar]
- 36.Tu P, Chi L, Bodnar W, et al. Gut microbiome toxicity: connecting the environment and gut microbiome-associated diseases. Toxics. 2020;8(1):19. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37.Huang C, Shi G. Smoking and microbiome in oral, airway, gut and some systemic diseases. J Transl Med. 2019;17(1):225. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 38.Savin Z, Kivity S, Yonath H, Yehuda S. Smoking and the intestinal microbiome. Arch Microbiol. 2018;200(5):677–684. [DOI] [PubMed] [Google Scholar]
- 39.Gui X, Yang Z, Li MD. Effect of cigarette smoke on gut microbiota: state of knowledge. Front Physiol. 2021;12:673341. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 40.Northrup TF, Stotts AL, Suchting R, et al. Thirdhand smoke associations with the gut microbiomes of infants admitted to a neonatal intensive care unit: an observational study. Environ Res. 2021;197:111180. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 41.Kelley ST, Liu W, Quintana PJE, et al. Altered microbiomes in thirdhand smoke-exposed children and their home environments. Pediatr Res. 2021;90(6):1153–1160. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 42.Mahabee-Gittens EM, Smith HA, Merianos AL. Disparities in dental health issues and oral health care visits in US children with tobacco smoke exposure. J Am Dental Assoc. 2022: S0002–8177(21)00579–1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 43.Merianos AL, Mahabee-Gittens EM, Choi K. Tobacco smoke exposure and inadequate sleep among U.S. school-aged children. Sleep Med. 2021;86:99–105. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 44.Drehmer JE, Ossip DJ, Nabi-Burza E, et al. Thirdhand smoke beliefs of parents. Pediatrics. 2014;133(4):e850–e856. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 45.Mahabee-Gittens EM, Matt GE, Ding L, Merianos AL. Comparison of levels of three tobacco smoke exposure biomarkers in children of smokers. Int J Environ Res Public Health. 2021;18(22):11803. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 46.Mahabee-Gittens EM, Quintana PJE, Hoh E, et al. Collecting hand wipe samples to assess thirdhand smoke exposure. Front Public Health. 2021;9:770505. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 47.Pashankar DS, Loening-Baucke V. Increased prevalence of obesity in children with functional constipation evaluated in an academic medical center. Pediatrics. 2005;116(3):e377–e380. [DOI] [PubMed] [Google Scholar]