International Journal of Pediatric Otorhinolaryngology 79 (2015) 157–160
Contents lists available at ScienceDirect
International Journal of Pediatric Otorhinolaryngology journal homepage: www.elsevier.com/locate/ijporl
Prevalence of smoke exposure amongst children who undergo tonsillectomy for recurrent tonsillitis Chelsey E. Straight a,*, Hetal H. Patel b, Erik B. Lehman c, Michele M. Carr d a
Penn State College of Medicine, 500 University Drive, Hershey, PA 17033-0850, USA Department of Surgery-Division of Otolaryngology, Penn State Milton S. Hershey Medical Center, 500 University Drive, Hershey, PA 17033-0850, USA c Department of Public Health Sciences, Penn State College of Medicine, 500 University Drive, Hershey, PA 17033-0850, USA d Department of Surgery and Department of Pediatrics, Penn State Milton S. Hershey Medical Center, 500 University Drive, Hershey, PA 17033-0850, USA b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 29 August 2014 Received in revised form 28 October 2014 Accepted 25 November 2014 Available online 3 December 2014
Purpose: The hypothesis tested was that smoke exposure has a detrimental effect on the developing upper respiratory tract. The purpose of this study was to determine if more children undergoing tonsillectomy for recurrent tonsillitis had smoke exposure in comparison to a control group of children undergoing hernia repair. Methods: This was a retrospective case-control study. Medical records of children less than 15 years of age that underwent tonsillectomy for recurrent tonsillitis at Penn State Hershey Medical Center from July 2009 to October 2012 were retrospectively reviewed to determine exposure to smoking contacts. Records of children less than 15 years of age that underwent hernia repair surgery at this facility during the same time, were also retrospectively reviewed for smoke exposure. Results: A total of 256 children who underwent tonsillectomy for recurrent tonsillitis and 241 children who underwent hernia repair surgery met the inclusion criteria. Of the children in the tonsillectomy for recurrent tonsillitis group, 121 (47.27%) had previous smoke exposure, compared to 67 (27.80%) in the hernia repair group. Further analysis of the data using logistic regression yielded an odds ratio of 2.49 (P = 0.004), indicating that children with smoke exposure had more than twice the odds of having tonsillectomy for recurrent tonsillitis compared to those with no exposure. Conclusions: Exposure to smoking contacts was more common in children who underwent tonsillectomy for recurrent tonsillitis than children who underwent hernia repair surgery. Future studies could address the relation of smoke exposure quantity to health outcomes in children. ß 2014 Elsevier Ireland Ltd. All rights reserved.
Keywords: Secondhand smoke Recurrent tonsillitis Children Tonsillectomy
1. Introduction A significant amount is known about the damaging effects that smoking tobacco has on the body, as smoking is associated with many diseases and reduced health, in general [1]. Not only is smoking detrimental to the smoker, but harmful effects of secondhand smoke, defined as the combination of smoke from the burning end of a cigarette and smoke exhaled by the smoker, are known to be harmful to bystanders, such as children. The Surgeon General’s 2006 report on involuntary smoking concluded
* Correspondence to: Penn State College of Medicine, 500 University Drive, Mail Code H091, Hershey, PA, 17033-0850, USA. Tel.: +1 814 730 8732. E-mail addresses: [email protected] (C.E. Straight), [email protected] (H.H. Patel), [email protected] (E.B. Lehman), [email protected] (M.M. Carr). http://dx.doi.org/10.1016/j.ijporl.2014.11.032 0165-5876/ß 2014 Elsevier Ireland Ltd. All rights reserved.
that there is no ‘‘safe’’ level of exposure to secondhand smoke. Additionally, thirdhand smoke, the residual tobacco smoke contaminants that remain after a cigarette is extinguished, also exposes nonsmoking individuals, such as children, to toxins in workplace and home environments when others smoke there [2,3]. The effects of cigarette smoke exposure on immune system function are complex and seemingly translate to many troublesome health problems in children. For example, evidence has shown that middle ear disease, such as recurrent otitis media and otitis media with effusion, is more common in children exposed to parental smoking [4]. Children’s respiratory system may also be adversely affected by passive inhalation of cigarette smoke toxins, as reactive oxygen species found in cigarette smoke have been implicated in damaging epithelial cells lining the airways via activation of intracellular signaling cascades that lead to immune cell recruitment and inflammation [5]. Additionally, studies have
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demonstrated that cigarette smoke extracts are involved in suppression of several proinflammatory cytokines normally involved in host defense against infections, such as interferon g (IFN-g). For example, levels of IFN-g were found to be reduced, with a significant inverse dose-response relationship to pack years, among children that had experienced parental smoke exposure during their first 11 years of life compared to children with nonsmoking parents [6]. Such complex effects on the immune system seem to play a role in making children more prone to breathing complications, like asthma, and recurrent respiratory infections, such as tonsillitis [2]. Throat infections, such as tonsillitis and pharyngitis, can contribute to missed days of school for children and account for over 10% of all office visits to primary care physicians as well as 50% of outpatient antibiotic use [7]. Recurrent episodes of throat infections, such as tonsillitis, may eventually warrant tonsillectomy as a treatment option, as this procedure has been shown to be effective at significantly reducing the number and severity of episodes in children who are severely affected [8]. Children are considered to be severely affected when they experience three or more episodes of recurrent infection in each of 3 years, five or more episodes in each of 2 years, or seven or more episodes in 1 year [9]. Tonsillectomy is one of the most commonly performed operations in children, it was estimated that 530,000 tonsillectomies were performed in children less than 15 years of age in the United States in 2006 [9]. Previous British and French studies attempted to determine if parental smoking is associated with increased occurrence of tonsillectomy in children, but the results were inconsistent [4]. We hypothesized that children’s respiratory systems are susceptible to environmental smoke exposure and those that underwent tonsillectomy for recurrent tonsillitis will have a higher prevalence of contacts with smoke compared to a control group of children that underwent hernia repair surgery. 2. Methods This was a retrospective case-control study that incorporated data contained in electronic medical records from July 2009 to October 2012, inclusive. Data used was from pediatric patients that were less than 15 years of age at the time they underwent tonsillectomy for recurrent tonsillitis or hernia repair surgery at Penn State Hershey Medical Center. This age was chosen to decrease the likelihood that patients were active smokers. Any patient noted to be an active smoker was excluded from the study. Additionally, patients with documented immunodeficiency were excluded, since such patients are more likely to develop recurrent infections, regardless of exposure to smoking contacts. To accommodate for unique living situations in which parents may not be the primary caregivers, documented smoke exposure from any household contact was included. Patient charts were reviewed for surgical indication, age, gender, and smoking exposure and data was recorded and coded using an Excel spreadsheet. Smoking exposure status was determined primarily by information from pediatric health assessment questionnaires completed by parents or caregivers. If this was not included in the patient’s record or the section regarding smoke exposure was incomplete, then provider documentation or any indication of a smoking contact included in the patients’ electronic medical records was used to determine exposure to smoking contacts. A statistical analysis of the above data was performed by the Public Health Services Biostatistics Department at Penn State Hershey. The prevalence of smoking contacts amongst children who underwent tonsillectomy for recurrent tonsillitis was compared to the prevalence observed in a control group, which was comprised of children who underwent hernia repair surgery during the same time period. The control group was selected on the
premise that, like the pediatric tonsillectomy patients, they also represented a common pediatric surgical population. The hernia surgery did not involve any component of the respiratory system and was presumably not indicated due to potential effects of exposure to smoking contacts. A logistic regression model was utilized for data analysis. The main independent variable of this model was smoke exposure and the main dependent variable was tonsillectomy for recurrent tonsillitis. Age and gender were identified as potential covariates. The association between the main dependent and independent variables was analyzed initially without any adjustment for covariates. The association between the dependent variable and each covariate was then analyzed independently. The association between the independent variable and each covariate was also analyzed independently. After demonstrating significance in the associations with each of the dependent and independent variables separately, the covariates were included for adjustment in a multivariable model used to determine the association between the dependent and main independent variables. Odds ratios were used to quantify the magnitude and direction of the associations. All analyses were carried out using SAS version 9.3 (SAS Institute, Cary, NC). Penn State Hershey Medical Center institutional review board (IRB) approval was obtained before research commenced. The IRB approval corresponds to protocol ID: 41237, entitled ‘‘Prevalence of Smoking Parents in Children that Undergo Tonsillectomy for recurrent tonsillitis.’’
3. Results A total of 269 children who underwent tonsillectomy for recurrent tonsillitis and 275 children who underwent hernia repair surgery during the time period were examined in this study. Of the 269 that had a tonsillectomy for recurrent tonsillitis, nine were excluded due to being outside the age criteria, one was excluded for documentation of being an active smoker, and three were excluded due to lack of documentation regarding their exposure to smoking contacts. Of the 275 that underwent hernia repair surgery, eight were excluded due to being outside the age criteria and 26 were excluded due to lack of documentation regarding their exposure to smoking contacts. No children were excluded from either group for documented immune deficiency syndrome, as no records that were reviewed indicated any child had such a condition. Therefore, a total of 256 children who underwent tonsillectomy for recurrent tonsillitis and 241 children who underwent hernia repair surgery met the inclusion criteria, had information regarding smoke exposure documented in their electronic record, and were included in the statistical analysis of the data. Differences in average age, gender, and smoke exposure were found to exist among the tonsillectomy for recurrent tonsillitis and hernia repair surgery groups, as summarized in Table 1. The average patient age in the tonsillectomy for recurrent tonsillitis group was 8.2 years (range: 1.80–14.90 years) compared to 2.9 years (range: 0.04–14.98 years) in the hernia repair surgery Table 1 Average age, gender, and smoke exposure by group.
Average age (years) Gender Smoke exposure
Tonsillectomy for recurrent tonsillitis group
Hernia repair group
8.2 (range: 1.80–14.90)
2.9 (range: 0.04–14.98)
Total Total Total Total
Total Total Total Total
males = 122 (43.75%) females = 144 (56.25%) negative = 135 (52.73%) positive = 121 (47.27%)
males = 194 (80.50%) females = 47 (19.50%) negative = 174 (72.20%) positive = 67 (27.80%)
C.E. Straight et al. / International Journal of Pediatric Otorhinolaryngology 79 (2015) 157–160
group. There were more females (144, or 56.3%) than males (112, or 43.8%) in the tonsillectomy for recurrent tonsillitis group. The opposite was observed in the hernia repair surgery group, as there was a male predominance (194 males, or 80.5%; 47 females, or 19.5%). Since hernias in children are more likely to occur in younger, predominantly male patients, these findings seem to reflect that [8]. Prior smoke exposure was more common among children in the tonsillectomy for recurrent tonsillitis group (121, or 47.3%) than in the hernia repair surgery group (67, or 27.8%). A logistic regression model was utilized to analyze the tonsillectomy for recurrent tonsillitis group by independent variable and/or covariates; the findings are included in Table 2. Both gender and age were determined to be significant covariates. To account for the variation that gender and age differences may have introduced to the association between smoke exposure and tonsillectomy for recurrent tonsillitis, age and gender were added to the logistic regression model. After this adjustment, the significant association remained, as children with smoke exposure were found to have 2.49 times the odds (95% CI: 1.50–4.11) of having tonsillectomy for recurrent tonsillitis than children with no smoke exposure (P < 0.001).
4. Discussion Previous British and French studies attempted to determine if parental smoking is associated with increased occurrence of tonsillectomy in children, but yielded inconsistent results [4]. This study sheds more light on the understanding of the relationship that exists between exposure to smoking contacts and the occurrence of tonsillectomy for recurrent tonsillitis in children in the United States. The results of this study make it evident that exposure to smoking contacts was prevalent amongst children who underwent tonsillectomy for recurrent tonsillitis and significantly more common than those that had hernia repair surgery during the same time period. According to the Centers for Disease Control and Prevention (CDC), tobacco use remains a heavy burden in the United States in terms of morbidity and mortality, as it is the single largest preventable cause of death and disease in this country. Not only is tobacco use costly purely in regards to its associated deleterious effects on health, but it also comprises a major source of financial expenditures. It is estimated that smoking alone costs the U.S. $96 billion in direct medical expenses and $97 billion in lost productivity annually [11]. Expenditures related to health care are an ever increasing concern in the U.S., since a sizeable portion of U.S. gross domestic product (GDP), 17.6% as of 2010, is dedicated to this area. The U.S. spends more on health care than any other country in the world, at a rate that is more than two-and-a-half times as much as other relatively rich, developed countries, such as France and the United Kingdom [12]. Smoking is an ideal target for health care professionals to focus educational efforts, since it is both preventable and a major contributing factor to burden of disease and financial strain in this country. Realizing the impact that decreasing the prevalence of smoking could make from both health and monetary standpoints, one of the Healthy People 2020 goals is Table 2 Results of the logistic regression of recurrent tonsillitis group by independent variable and/or covariate(s). Independent variable and/or covariate(s)
Odds ratio
95% Confidence intervals
P value
Smoke exposure Smoke exposure, gender and age
2.33 2.49
1.60–3.38 1.50–4.11
P < 0.0001 P = 0.0004
159
to achieve a drop in prevalence of cigarette smoking among adults in the U.S. to 12% by 2020 [11]. There is still a long way to go to reach such a goal, if the results of this study relating to smoking prevalence provide an accurate portrayal of the current prevalence of smoking. In order to put the data obtained from this study into perspective, it is useful to consider the national average smoking rate that existed during the course of the study period. Both 2010 and 2011 were full years included in the time frame of this study and serve as useful reference points for consideration of national rates during the same time. Overall, the national average smoking rate in the U.S. in 2011 was 19.0%, with no statistically significant change in adult smoking prevalence from 2010 (19.3%) to 2011 (19.0%). The highest prevalence of smoking among the population during 2011 was found in those aged 25–44 years, as the prevalence in this group was 22.1% [10]. This is important to recognize, as this age range that was observed to have the highest prevalence encompasses years when people typically start families and accordingly may have increased contact with children. In this study, the rate of smoking contacts in the hernia repair surgery group was similar to, but slightly higher than the national average values from 2010 and 2011. However, if one considers the higher prevalence among those aged 25–44 years that was observed in 2011 and assumes that many caregivers of children who were included in this study likely fell into that age range, the prevalence observed in the hernia repair surgery group seems to fit more closely with the national average. The prevalence of smoke exposure among the children in the tonsillectomy for recurrent tonsillitis group, on the other hand, was much higher than the national average, even if the higher prevalence among those aged 25–44 years is taken into consideration. Based upon these findings, it seems reasonable to conclude that there is an association between smoke exposure and recurrent tonsillitis requiring tonsillectomy in children. It is recognized that this study has several limitations. Age and gender differed among the two pediatric populations included in this study. Though a logistic regression model was utilized to account for these differences, it is possible that a future study incorporating age and gender matched controls may be a more suitable approach. Since the data obtained in this study was primarily in the form of parent or caregiver self-reported answers to a pediatric health questionnaire, it may not be a true reflection of the actual prevalence. It is possible that parents and caregivers may have underreported children’s exposure to smoking contacts to avoid criticism or judgment from health care professionals for a habit that is widely portrayed in a negative light in our culture. Alternatively, the prevalence may have been overestimated since this study took into account all contacts that were documented to potentially expose children. Despite recommendations that there is no ‘‘safe’’ level of exposure to smoke, it is unclear what amount of exposure leads to adverse health effects [3]. Therefore, it is difficult to put this factor into perspective and this study did not attempt to do so. Since self-reported data has the potential to be inaccurate, one way to perhaps gain a more accurate depiction of the true prevalence of children’s exposure to smoking contacts is by using urine cotinine as an indicator instead of parent or caregiver selfreported information. A major metabolite of nicotine, cotinine is considered to be the best laboratory measure to evaluate nicotine consumption. Following exposure to nicotine, cotinine can be found in various biological samples, such as blood, urine, saliva, semen, and hair. Since obtaining a urine sample is perceived as a typically non-invasive procedure associated with relatively no harm, this method of collection is often used when there is a desire to assess nicotine exposure [11]. A study by Boyaci et al. [13], compared the accuracy of parent or caregiver self-reported data
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pertaining to children’s exposure to environmental tobacco smoke with urine cotinine measures collected from the children. Based upon their findings, it was concluded that caregivers underreported children’s exposure to secondhand smoke as compared to urine cotinine. Although urine cotinine measures are more accurate, it is also a more costly approach to research. Urine cotinine measures were not evaluated in this study due to both cost and uncertainty as to whether or not it was a warranted approach, since nothing was yet known on the self-reported prevalence of smoking among parents/caregivers in the groups analyzed. Additionally, it is important to recognize that not every child that was included in this study that underwent tonsillectomy for recurrent tonsillitis had a history of smoke exposure. Therefore, although a relationship does seem to exist, it is clearly not the only variable that needs to be taken into consideration. Information pertaining to measures of socioeconomic status, such as insurance coverage, household income, and education level of caregivers, was not gathered, but conceivably may have been unknown confounders. Perhaps future studies to assess these variables in relation to the association between smoke exposure and tonsillectomy for recurrent tonsillitis could be performed. Other factors, including genetics, various stressors, and nutritional status, to name a few, also likely play an important role in a child’s susceptibility to recurrent tonsillitis requiring tonsillectomy. However, unlike some of the other factors, such as genetics, parents/caregivers have the ability to modify smoke exposure and eliminate its associated harmful effects. 5. Conclusion As children’s respiratory systems are developing throughout adolescence, they may be susceptible to adverse health outcomes following exposure to smoking contacts. Clinicians can use the findings of this study to better educate parents/caregivers about the risks of smoking not only for themselves, but also for children around them. Decreased smoke exposure could potentially translate to better health for children, as they would likely suffer fewer recurrent infections, and reduce healthcare costs, through fewer office visits, less antibiotic use, and fewer tonsillectomies performed. Additionally, reduction in the episodes of recurrent tonsillitis would also likely equate to fewer school absences and decreased missed days from work for parents/caregivers to take care of ill children and/or take them to appointments. In order to gain a better understanding of this particular topic, future research could attempt to determine whether or not the prevalence of smoking observed in this study is truly an accurate portrayal. This could be done by a prospective study comparing urine cotinine to
self-reported data amongst children who undergo tonsillectomy for recurrent tonsillitis. Determining whether or not the amount of exposure is correlated with increasingly adverse health effects could also be a potential future area of research study, but it would likely be difficult to measure a child’s cumulative exposure in many circumstances. Funding The authors have no financial relationships relevant to this article to disclose. Conflict of interest The authors have no conflict of interest to disclose. References [1] Centers for Disease Control, Prevention (CDC), Health effects of cigarette smoking, Smoking Tob. Use (2012), hwww.cdc.gov/tobacco/data_statistics/fact_sheets/ health_effects/effects_cig_smoking/i. (accessed 16.01.14). [2] Centers for Disease Control, Prevention, (CDC), Health effects of secondhand smoke, Smoking Tob. Use (2012) (accessed 16.01.12) www.cdc.gov/tobacco/ data_statistics/fact_sheets/secondhand_smoke/health_effects/index.htm. [3] J.P. Winickoff, J. Friebely, S.E. Tanski, C. Sherrod, G.E. Matt, M.F. Hovell, et al., Beliefs about the health effects of ‘‘thirdhand’’ smoke and home smoking bans, Pediatrics 123 (2009) e74–e79, http://dx.doi.org/10.1542/peds.2008-2184. [4] D.P. Strachan, D.G. Cook, Health effects of passive smoking. 4. Parental smoking, middle ear disease and adenotonsillectomy in children, Thorax 53 (1998) 50–56. [5] J. Lee, V. Taneja, R. Vassallo, Cigarette smoking and inflammation: cellular and molecular mechanisms, J. Dent. Res. 90 (2012) 142–149. [6] G. Tebow, D.L. Sherrill, I.C. Lohman, D.A. Stern, A.L. Wright, F.D. Martinez, et al., Effects of parental smoking on interferon g production in children, Pediatrics 121 (2008) e1563–e1569. [7] L.R. Lustig, J.S. Schindler, Ear, nose, & throat disorders, in: Current Medical Diagnosis & Treatment 2013, 2012 hwww.accessmedicine.com/content.aspx?.aID=2356i. (Chapter 8, accessed 18.01.12). [8] American Academy of Otolaryngology—Head and Neck Surgery, Tonsillectomy facts in the U.S.: from ENT doctors. hwww.entnet.org/HealthInformation/ TonsillectomyFactsFromENTs.cfm.i, 2012 (accessed 18.01.12.). [9] J.L. Paradise, Tonsillectomy and adenoidectomy in children. hwww.uptodate.com/ contents/tonsillectomy-and-adenoidectomy-in-childreni, 2014 (accessed 16.07.14.). [10] J.J. Aiken, K.T. Oldham, Inguinal hernias, in: Nelson Textbook of Pediatrics, 19th ed., 2013 hwww.mdconsult.com/books/page.do?.eid=4-u1.0-B978-1-4377-07557.00338-9&isbn=978-1-4377-0755-7&sid=1431388954&uniqId=4089450266#4-u1.0-B978-1-4377-0755-7.00338-9. 2011i. (Chapter 338, accessed 20.04.13). [11] Centers for Disease Control and Prevention (CDC), Current cigarette smoking among adults—United States, 2011, Morb. Mortal. Wkly. Rep. (2013), www.cdc.gov/mmwr/preview/mmwrhtml/mm6144a2.htm. (accessed 04.03.13). [12] J. Kane, Health costs: how the U.S. compares with other countries, Public Broadcasting Service (PBS) (2013), hwww.pbs.org/newshour/rundown/2012/10/healthcosts-how-the-us-compares-with-other-countries.html i. (accessed 20.04.13). [13] H. Boyaci, N. Etiler, C. Duman, I. Basyigit, A. Pala, Environmental tobacco exposure in school children: parent report and urine cotinine measures, Pediatr. Int. 48 (2006) 382–389.
Contents lists available at ScienceDirect
International Journal of Pediatric Otorhinolaryngology journal homepage: www.elsevier.com/locate/ijporl
Prevalence of smoke exposure amongst children who undergo tonsillectomy for recurrent tonsillitis Chelsey E. Straight a,*, Hetal H. Patel b, Erik B. Lehman c, Michele M. Carr d a
Penn State College of Medicine, 500 University Drive, Hershey, PA 17033-0850, USA Department of Surgery-Division of Otolaryngology, Penn State Milton S. Hershey Medical Center, 500 University Drive, Hershey, PA 17033-0850, USA c Department of Public Health Sciences, Penn State College of Medicine, 500 University Drive, Hershey, PA 17033-0850, USA d Department of Surgery and Department of Pediatrics, Penn State Milton S. Hershey Medical Center, 500 University Drive, Hershey, PA 17033-0850, USA b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 29 August 2014 Received in revised form 28 October 2014 Accepted 25 November 2014 Available online 3 December 2014
Purpose: The hypothesis tested was that smoke exposure has a detrimental effect on the developing upper respiratory tract. The purpose of this study was to determine if more children undergoing tonsillectomy for recurrent tonsillitis had smoke exposure in comparison to a control group of children undergoing hernia repair. Methods: This was a retrospective case-control study. Medical records of children less than 15 years of age that underwent tonsillectomy for recurrent tonsillitis at Penn State Hershey Medical Center from July 2009 to October 2012 were retrospectively reviewed to determine exposure to smoking contacts. Records of children less than 15 years of age that underwent hernia repair surgery at this facility during the same time, were also retrospectively reviewed for smoke exposure. Results: A total of 256 children who underwent tonsillectomy for recurrent tonsillitis and 241 children who underwent hernia repair surgery met the inclusion criteria. Of the children in the tonsillectomy for recurrent tonsillitis group, 121 (47.27%) had previous smoke exposure, compared to 67 (27.80%) in the hernia repair group. Further analysis of the data using logistic regression yielded an odds ratio of 2.49 (P = 0.004), indicating that children with smoke exposure had more than twice the odds of having tonsillectomy for recurrent tonsillitis compared to those with no exposure. Conclusions: Exposure to smoking contacts was more common in children who underwent tonsillectomy for recurrent tonsillitis than children who underwent hernia repair surgery. Future studies could address the relation of smoke exposure quantity to health outcomes in children. ß 2014 Elsevier Ireland Ltd. All rights reserved.
Keywords: Secondhand smoke Recurrent tonsillitis Children Tonsillectomy
1. Introduction A significant amount is known about the damaging effects that smoking tobacco has on the body, as smoking is associated with many diseases and reduced health, in general [1]. Not only is smoking detrimental to the smoker, but harmful effects of secondhand smoke, defined as the combination of smoke from the burning end of a cigarette and smoke exhaled by the smoker, are known to be harmful to bystanders, such as children. The Surgeon General’s 2006 report on involuntary smoking concluded
* Correspondence to: Penn State College of Medicine, 500 University Drive, Mail Code H091, Hershey, PA, 17033-0850, USA. Tel.: +1 814 730 8732. E-mail addresses: [email protected] (C.E. Straight), [email protected] (H.H. Patel), [email protected] (E.B. Lehman), [email protected] (M.M. Carr). http://dx.doi.org/10.1016/j.ijporl.2014.11.032 0165-5876/ß 2014 Elsevier Ireland Ltd. All rights reserved.
that there is no ‘‘safe’’ level of exposure to secondhand smoke. Additionally, thirdhand smoke, the residual tobacco smoke contaminants that remain after a cigarette is extinguished, also exposes nonsmoking individuals, such as children, to toxins in workplace and home environments when others smoke there [2,3]. The effects of cigarette smoke exposure on immune system function are complex and seemingly translate to many troublesome health problems in children. For example, evidence has shown that middle ear disease, such as recurrent otitis media and otitis media with effusion, is more common in children exposed to parental smoking [4]. Children’s respiratory system may also be adversely affected by passive inhalation of cigarette smoke toxins, as reactive oxygen species found in cigarette smoke have been implicated in damaging epithelial cells lining the airways via activation of intracellular signaling cascades that lead to immune cell recruitment and inflammation [5]. Additionally, studies have
158
C.E. Straight et al. / International Journal of Pediatric Otorhinolaryngology 79 (2015) 157–160
demonstrated that cigarette smoke extracts are involved in suppression of several proinflammatory cytokines normally involved in host defense against infections, such as interferon g (IFN-g). For example, levels of IFN-g were found to be reduced, with a significant inverse dose-response relationship to pack years, among children that had experienced parental smoke exposure during their first 11 years of life compared to children with nonsmoking parents [6]. Such complex effects on the immune system seem to play a role in making children more prone to breathing complications, like asthma, and recurrent respiratory infections, such as tonsillitis [2]. Throat infections, such as tonsillitis and pharyngitis, can contribute to missed days of school for children and account for over 10% of all office visits to primary care physicians as well as 50% of outpatient antibiotic use [7]. Recurrent episodes of throat infections, such as tonsillitis, may eventually warrant tonsillectomy as a treatment option, as this procedure has been shown to be effective at significantly reducing the number and severity of episodes in children who are severely affected [8]. Children are considered to be severely affected when they experience three or more episodes of recurrent infection in each of 3 years, five or more episodes in each of 2 years, or seven or more episodes in 1 year [9]. Tonsillectomy is one of the most commonly performed operations in children, it was estimated that 530,000 tonsillectomies were performed in children less than 15 years of age in the United States in 2006 [9]. Previous British and French studies attempted to determine if parental smoking is associated with increased occurrence of tonsillectomy in children, but the results were inconsistent [4]. We hypothesized that children’s respiratory systems are susceptible to environmental smoke exposure and those that underwent tonsillectomy for recurrent tonsillitis will have a higher prevalence of contacts with smoke compared to a control group of children that underwent hernia repair surgery. 2. Methods This was a retrospective case-control study that incorporated data contained in electronic medical records from July 2009 to October 2012, inclusive. Data used was from pediatric patients that were less than 15 years of age at the time they underwent tonsillectomy for recurrent tonsillitis or hernia repair surgery at Penn State Hershey Medical Center. This age was chosen to decrease the likelihood that patients were active smokers. Any patient noted to be an active smoker was excluded from the study. Additionally, patients with documented immunodeficiency were excluded, since such patients are more likely to develop recurrent infections, regardless of exposure to smoking contacts. To accommodate for unique living situations in which parents may not be the primary caregivers, documented smoke exposure from any household contact was included. Patient charts were reviewed for surgical indication, age, gender, and smoking exposure and data was recorded and coded using an Excel spreadsheet. Smoking exposure status was determined primarily by information from pediatric health assessment questionnaires completed by parents or caregivers. If this was not included in the patient’s record or the section regarding smoke exposure was incomplete, then provider documentation or any indication of a smoking contact included in the patients’ electronic medical records was used to determine exposure to smoking contacts. A statistical analysis of the above data was performed by the Public Health Services Biostatistics Department at Penn State Hershey. The prevalence of smoking contacts amongst children who underwent tonsillectomy for recurrent tonsillitis was compared to the prevalence observed in a control group, which was comprised of children who underwent hernia repair surgery during the same time period. The control group was selected on the
premise that, like the pediatric tonsillectomy patients, they also represented a common pediatric surgical population. The hernia surgery did not involve any component of the respiratory system and was presumably not indicated due to potential effects of exposure to smoking contacts. A logistic regression model was utilized for data analysis. The main independent variable of this model was smoke exposure and the main dependent variable was tonsillectomy for recurrent tonsillitis. Age and gender were identified as potential covariates. The association between the main dependent and independent variables was analyzed initially without any adjustment for covariates. The association between the dependent variable and each covariate was then analyzed independently. The association between the independent variable and each covariate was also analyzed independently. After demonstrating significance in the associations with each of the dependent and independent variables separately, the covariates were included for adjustment in a multivariable model used to determine the association between the dependent and main independent variables. Odds ratios were used to quantify the magnitude and direction of the associations. All analyses were carried out using SAS version 9.3 (SAS Institute, Cary, NC). Penn State Hershey Medical Center institutional review board (IRB) approval was obtained before research commenced. The IRB approval corresponds to protocol ID: 41237, entitled ‘‘Prevalence of Smoking Parents in Children that Undergo Tonsillectomy for recurrent tonsillitis.’’
3. Results A total of 269 children who underwent tonsillectomy for recurrent tonsillitis and 275 children who underwent hernia repair surgery during the time period were examined in this study. Of the 269 that had a tonsillectomy for recurrent tonsillitis, nine were excluded due to being outside the age criteria, one was excluded for documentation of being an active smoker, and three were excluded due to lack of documentation regarding their exposure to smoking contacts. Of the 275 that underwent hernia repair surgery, eight were excluded due to being outside the age criteria and 26 were excluded due to lack of documentation regarding their exposure to smoking contacts. No children were excluded from either group for documented immune deficiency syndrome, as no records that were reviewed indicated any child had such a condition. Therefore, a total of 256 children who underwent tonsillectomy for recurrent tonsillitis and 241 children who underwent hernia repair surgery met the inclusion criteria, had information regarding smoke exposure documented in their electronic record, and were included in the statistical analysis of the data. Differences in average age, gender, and smoke exposure were found to exist among the tonsillectomy for recurrent tonsillitis and hernia repair surgery groups, as summarized in Table 1. The average patient age in the tonsillectomy for recurrent tonsillitis group was 8.2 years (range: 1.80–14.90 years) compared to 2.9 years (range: 0.04–14.98 years) in the hernia repair surgery Table 1 Average age, gender, and smoke exposure by group.
Average age (years) Gender Smoke exposure
Tonsillectomy for recurrent tonsillitis group
Hernia repair group
8.2 (range: 1.80–14.90)
2.9 (range: 0.04–14.98)
Total Total Total Total
Total Total Total Total
males = 122 (43.75%) females = 144 (56.25%) negative = 135 (52.73%) positive = 121 (47.27%)
males = 194 (80.50%) females = 47 (19.50%) negative = 174 (72.20%) positive = 67 (27.80%)
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group. There were more females (144, or 56.3%) than males (112, or 43.8%) in the tonsillectomy for recurrent tonsillitis group. The opposite was observed in the hernia repair surgery group, as there was a male predominance (194 males, or 80.5%; 47 females, or 19.5%). Since hernias in children are more likely to occur in younger, predominantly male patients, these findings seem to reflect that [8]. Prior smoke exposure was more common among children in the tonsillectomy for recurrent tonsillitis group (121, or 47.3%) than in the hernia repair surgery group (67, or 27.8%). A logistic regression model was utilized to analyze the tonsillectomy for recurrent tonsillitis group by independent variable and/or covariates; the findings are included in Table 2. Both gender and age were determined to be significant covariates. To account for the variation that gender and age differences may have introduced to the association between smoke exposure and tonsillectomy for recurrent tonsillitis, age and gender were added to the logistic regression model. After this adjustment, the significant association remained, as children with smoke exposure were found to have 2.49 times the odds (95% CI: 1.50–4.11) of having tonsillectomy for recurrent tonsillitis than children with no smoke exposure (P < 0.001).
4. Discussion Previous British and French studies attempted to determine if parental smoking is associated with increased occurrence of tonsillectomy in children, but yielded inconsistent results [4]. This study sheds more light on the understanding of the relationship that exists between exposure to smoking contacts and the occurrence of tonsillectomy for recurrent tonsillitis in children in the United States. The results of this study make it evident that exposure to smoking contacts was prevalent amongst children who underwent tonsillectomy for recurrent tonsillitis and significantly more common than those that had hernia repair surgery during the same time period. According to the Centers for Disease Control and Prevention (CDC), tobacco use remains a heavy burden in the United States in terms of morbidity and mortality, as it is the single largest preventable cause of death and disease in this country. Not only is tobacco use costly purely in regards to its associated deleterious effects on health, but it also comprises a major source of financial expenditures. It is estimated that smoking alone costs the U.S. $96 billion in direct medical expenses and $97 billion in lost productivity annually [11]. Expenditures related to health care are an ever increasing concern in the U.S., since a sizeable portion of U.S. gross domestic product (GDP), 17.6% as of 2010, is dedicated to this area. The U.S. spends more on health care than any other country in the world, at a rate that is more than two-and-a-half times as much as other relatively rich, developed countries, such as France and the United Kingdom [12]. Smoking is an ideal target for health care professionals to focus educational efforts, since it is both preventable and a major contributing factor to burden of disease and financial strain in this country. Realizing the impact that decreasing the prevalence of smoking could make from both health and monetary standpoints, one of the Healthy People 2020 goals is Table 2 Results of the logistic regression of recurrent tonsillitis group by independent variable and/or covariate(s). Independent variable and/or covariate(s)
Odds ratio
95% Confidence intervals
P value
Smoke exposure Smoke exposure, gender and age
2.33 2.49
1.60–3.38 1.50–4.11
P < 0.0001 P = 0.0004
159
to achieve a drop in prevalence of cigarette smoking among adults in the U.S. to 12% by 2020 [11]. There is still a long way to go to reach such a goal, if the results of this study relating to smoking prevalence provide an accurate portrayal of the current prevalence of smoking. In order to put the data obtained from this study into perspective, it is useful to consider the national average smoking rate that existed during the course of the study period. Both 2010 and 2011 were full years included in the time frame of this study and serve as useful reference points for consideration of national rates during the same time. Overall, the national average smoking rate in the U.S. in 2011 was 19.0%, with no statistically significant change in adult smoking prevalence from 2010 (19.3%) to 2011 (19.0%). The highest prevalence of smoking among the population during 2011 was found in those aged 25–44 years, as the prevalence in this group was 22.1% [10]. This is important to recognize, as this age range that was observed to have the highest prevalence encompasses years when people typically start families and accordingly may have increased contact with children. In this study, the rate of smoking contacts in the hernia repair surgery group was similar to, but slightly higher than the national average values from 2010 and 2011. However, if one considers the higher prevalence among those aged 25–44 years that was observed in 2011 and assumes that many caregivers of children who were included in this study likely fell into that age range, the prevalence observed in the hernia repair surgery group seems to fit more closely with the national average. The prevalence of smoke exposure among the children in the tonsillectomy for recurrent tonsillitis group, on the other hand, was much higher than the national average, even if the higher prevalence among those aged 25–44 years is taken into consideration. Based upon these findings, it seems reasonable to conclude that there is an association between smoke exposure and recurrent tonsillitis requiring tonsillectomy in children. It is recognized that this study has several limitations. Age and gender differed among the two pediatric populations included in this study. Though a logistic regression model was utilized to account for these differences, it is possible that a future study incorporating age and gender matched controls may be a more suitable approach. Since the data obtained in this study was primarily in the form of parent or caregiver self-reported answers to a pediatric health questionnaire, it may not be a true reflection of the actual prevalence. It is possible that parents and caregivers may have underreported children’s exposure to smoking contacts to avoid criticism or judgment from health care professionals for a habit that is widely portrayed in a negative light in our culture. Alternatively, the prevalence may have been overestimated since this study took into account all contacts that were documented to potentially expose children. Despite recommendations that there is no ‘‘safe’’ level of exposure to smoke, it is unclear what amount of exposure leads to adverse health effects [3]. Therefore, it is difficult to put this factor into perspective and this study did not attempt to do so. Since self-reported data has the potential to be inaccurate, one way to perhaps gain a more accurate depiction of the true prevalence of children’s exposure to smoking contacts is by using urine cotinine as an indicator instead of parent or caregiver selfreported information. A major metabolite of nicotine, cotinine is considered to be the best laboratory measure to evaluate nicotine consumption. Following exposure to nicotine, cotinine can be found in various biological samples, such as blood, urine, saliva, semen, and hair. Since obtaining a urine sample is perceived as a typically non-invasive procedure associated with relatively no harm, this method of collection is often used when there is a desire to assess nicotine exposure [11]. A study by Boyaci et al. [13], compared the accuracy of parent or caregiver self-reported data
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pertaining to children’s exposure to environmental tobacco smoke with urine cotinine measures collected from the children. Based upon their findings, it was concluded that caregivers underreported children’s exposure to secondhand smoke as compared to urine cotinine. Although urine cotinine measures are more accurate, it is also a more costly approach to research. Urine cotinine measures were not evaluated in this study due to both cost and uncertainty as to whether or not it was a warranted approach, since nothing was yet known on the self-reported prevalence of smoking among parents/caregivers in the groups analyzed. Additionally, it is important to recognize that not every child that was included in this study that underwent tonsillectomy for recurrent tonsillitis had a history of smoke exposure. Therefore, although a relationship does seem to exist, it is clearly not the only variable that needs to be taken into consideration. Information pertaining to measures of socioeconomic status, such as insurance coverage, household income, and education level of caregivers, was not gathered, but conceivably may have been unknown confounders. Perhaps future studies to assess these variables in relation to the association between smoke exposure and tonsillectomy for recurrent tonsillitis could be performed. Other factors, including genetics, various stressors, and nutritional status, to name a few, also likely play an important role in a child’s susceptibility to recurrent tonsillitis requiring tonsillectomy. However, unlike some of the other factors, such as genetics, parents/caregivers have the ability to modify smoke exposure and eliminate its associated harmful effects. 5. Conclusion As children’s respiratory systems are developing throughout adolescence, they may be susceptible to adverse health outcomes following exposure to smoking contacts. Clinicians can use the findings of this study to better educate parents/caregivers about the risks of smoking not only for themselves, but also for children around them. Decreased smoke exposure could potentially translate to better health for children, as they would likely suffer fewer recurrent infections, and reduce healthcare costs, through fewer office visits, less antibiotic use, and fewer tonsillectomies performed. Additionally, reduction in the episodes of recurrent tonsillitis would also likely equate to fewer school absences and decreased missed days from work for parents/caregivers to take care of ill children and/or take them to appointments. In order to gain a better understanding of this particular topic, future research could attempt to determine whether or not the prevalence of smoking observed in this study is truly an accurate portrayal. This could be done by a prospective study comparing urine cotinine to
self-reported data amongst children who undergo tonsillectomy for recurrent tonsillitis. Determining whether or not the amount of exposure is correlated with increasingly adverse health effects could also be a potential future area of research study, but it would likely be difficult to measure a child’s cumulative exposure in many circumstances. Funding The authors have no financial relationships relevant to this article to disclose. Conflict of interest The authors have no conflict of interest to disclose. References [1] Centers for Disease Control, Prevention (CDC), Health effects of cigarette smoking, Smoking Tob. Use (2012), hwww.cdc.gov/tobacco/data_statistics/fact_sheets/ health_effects/effects_cig_smoking/i. (accessed 16.01.14). [2] Centers for Disease Control, Prevention, (CDC), Health effects of secondhand smoke, Smoking Tob. Use (2012) (accessed 16.01.12) www.cdc.gov/tobacco/ data_statistics/fact_sheets/secondhand_smoke/health_effects/index.htm. [3] J.P. Winickoff, J. Friebely, S.E. Tanski, C. Sherrod, G.E. Matt, M.F. Hovell, et al., Beliefs about the health effects of ‘‘thirdhand’’ smoke and home smoking bans, Pediatrics 123 (2009) e74–e79, http://dx.doi.org/10.1542/peds.2008-2184. [4] D.P. Strachan, D.G. Cook, Health effects of passive smoking. 4. Parental smoking, middle ear disease and adenotonsillectomy in children, Thorax 53 (1998) 50–56. [5] J. Lee, V. Taneja, R. Vassallo, Cigarette smoking and inflammation: cellular and molecular mechanisms, J. Dent. Res. 90 (2012) 142–149. [6] G. Tebow, D.L. Sherrill, I.C. Lohman, D.A. Stern, A.L. Wright, F.D. Martinez, et al., Effects of parental smoking on interferon g production in children, Pediatrics 121 (2008) e1563–e1569. [7] L.R. Lustig, J.S. Schindler, Ear, nose, & throat disorders, in: Current Medical Diagnosis & Treatment 2013, 2012 hwww.accessmedicine.com/content.aspx?.aID=2356i. (Chapter 8, accessed 18.01.12). [8] American Academy of Otolaryngology—Head and Neck Surgery, Tonsillectomy facts in the U.S.: from ENT doctors. hwww.entnet.org/HealthInformation/ TonsillectomyFactsFromENTs.cfm.i, 2012 (accessed 18.01.12.). [9] J.L. Paradise, Tonsillectomy and adenoidectomy in children. hwww.uptodate.com/ contents/tonsillectomy-and-adenoidectomy-in-childreni, 2014 (accessed 16.07.14.). [10] J.J. Aiken, K.T. Oldham, Inguinal hernias, in: Nelson Textbook of Pediatrics, 19th ed., 2013 hwww.mdconsult.com/books/page.do?.eid=4-u1.0-B978-1-4377-07557.00338-9&isbn=978-1-4377-0755-7&sid=1431388954&uniqId=4089450266#4-u1.0-B978-1-4377-0755-7.00338-9. 2011i. (Chapter 338, accessed 20.04.13). [11] Centers for Disease Control and Prevention (CDC), Current cigarette smoking among adults—United States, 2011, Morb. Mortal. Wkly. Rep. (2013), www.cdc.gov/mmwr/preview/mmwrhtml/mm6144a2.htm. (accessed 04.03.13). [12] J. Kane, Health costs: how the U.S. compares with other countries, Public Broadcasting Service (PBS) (2013), hwww.pbs.org/newshour/rundown/2012/10/healthcosts-how-the-us-compares-with-other-countries.html i. (accessed 20.04.13). [13] H. Boyaci, N. Etiler, C. Duman, I. Basyigit, A. Pala, Environmental tobacco exposure in school children: parent report and urine cotinine measures, Pediatr. Int. 48 (2006) 382–389.
