- Email: [email protected]
Risk factors for pediatric post-tonsillectomy hemorrhage
International Journal of Pediatric Otorhinolaryngology 84 (2016) 151–155
Contents lists available at ScienceDirect
International Journal of Pediatric Otorhinolaryngology journal homepage: www.elsevier.com/locate/ijporl
Risk factors for pediatric post-tonsillectomy hemorrhage§ Zorik Spektor a,b,c, Sandra Saint-Victor b, David J. Kay a,b,c, David L. Mandell a,b,c,* a b c
Center for Pediatric ENT—Head and Neck Surgery, 10150 Hagen Ranch Road, Boynton Beach, FL 33437, USA Department of Otolaryngology, Miller School of Medicine, 1600 NW 10th Ave #1140, Miami, FL 33136, USA Florida Atlantic University, Charles E. Schmidt College of Medicine, 777 Glades Road, Boca Raton, FL 33431, USA
A R T I C L E I N F O
A B S T R A C T
Article history: Received 7 January 2016 Received in revised form 4 March 2016 Accepted 7 March 2016 Available online 18 March 2016
Objectives: To determine pre-operative risk factors for post-tonsillectomy secondary hemorrhage in children, and quantify the magnitude of their risk. Materials and methods: Retrospective case-control study of all pediatric tonsillectomy patients experiencing post-operative bleeding from 2005 to 2010 in a community practice consisting of three fellowship-trained pediatric otolaryngologists were identified. The 91 cases were matched with 151 controls that underwent tonsillectomy by the same surgeon on the same day as each identified case. All charts were reviewed, and 41 pre-operative variables were extracted and statistically analyzed with contingency and regression analysis to calculate significance and odds ratios. Results: Three significant predictors of post-operative bleeding were identified. Performing a tonsillectomy on a child with recurrent tonsillitis (vs. other indications) increased the risk of postoperative hemorrhage by 4.5 times (p < 0.0001, 95% confidence intervals 2.41–8.38). Performing a tonsillectomy on a child with attention deficit hyperactivity disorder (ADHD) increased the risk by 8.7 times (p = 0.029, 95%CI 1.4–53.6). Older children were more predisposed to post-operative bleeding. For every increase in age by one year, the hemorrhage risk increased by 1.1 times (p = 0.0025, 95%CI 1.032– 1.162). Children 11 years of age and older had double the risk of bleeding compared to younger children (odds ratio 1.98, p = 0.0381, 95%CI 1.04–3.79). None of the remaining 38 variables showed significant differences between cases and controls. Conclusions: The risk of post-tonsillectomy hemorrhage is significantly increased in older children and those with recurrent tonsillitis and ADHD. ß 2016 Elsevier Ireland Ltd. All rights reserved.
Keywords: Pediatric tonsillectomy Hemorrhage Risk factors
1. Introduction Tonsillectomy (often combined with adenoidectomy) is among the most common pediatric surgical procedures performed in the United States, with 530,000 tonsillectomies performed in patients <15 years of age in 2006 [1]. While traditional extra-capsular adenotonsillectomy is a routine and effective procedure, it is associated with significant post-operative morbidities such as pain, dehydration, and hemorrhage. Post-operative bleeding can
§ Presented at the 27th annual meeting of the American Society of Pediatric Otolaryngology, San Diego, CA, April 21, 2012. * Corresponding author at: Center for Pediatric ENT, 10301 Hagen Ranch Road, Suite B-900, Boynton Beach, FL 33437, USA. Tel.: +1 561 736 8141; fax: +1 561 736 5662. E-mail addresses: [email protected] (Z. Spektor), [email protected] (S. Saint-Victor), [email protected] (D.J. Kay), [email protected] (D.L. Mandell).
http://dx.doi.org/10.1016/j.ijporl.2016.03.005 0165-5876/ß 2016 Elsevier Ireland Ltd. All rights reserved.
be potentially life-threatening and may require control under general anesthesia. 1.1. Rate of post-tonsillectomy hemorrhage The rate of post-tonsillectomy oropharyngeal hemorrhage across all age groups ranges from 2.1% to 12% [2–4], with the overall rate of secondary surgery to stop hemorrhage ranging from 1.2% to 6% [3,4]. The wide variation seen in reported rates of posttonsillectomy hemorrhage are likely due to diverse definitions and criteria for identifying and reporting such incidents [4]. 1.2. Risk factors for post-tonsillectomy hemorrhage Due to the inability in most cases to predict which patients will go on to experience post-tonsillectomy hemorrhage; many studies have attempted to identify risk factors that might predispose patients to this complication. Much has been written on comparison of different surgical techniques as potential causes
152
Z. Spektor et al. / International Journal of Pediatric Otorhinolaryngology 84 (2016) 151–155
This project was a retrospective cohort study that was compliant with the Health Insurance Portability and Accountability Act (HIPAA) and was granted an exemption by the Western Institutional Review Board (IRB).
upon weight, to be used as-needed for severe pain unresponsive to over-the-counter analgesics. All patients were instructed to report any bleeding to the physician group immediately via telephone contact, at which time they were instructed to either present to the hospital or to the office of the practice on the same day, depending on the clinical information reported. It is possible that there could have been bleeding episodes the providers were not aware of (such as if caregivers had never called the practice about it), and there may have been bleeding episodes that caregivers called about afterhours for which billing documentation wasn’t possible, and were minor enough that caregivers didn’t decide to make a visit. Given the retrospective nature of the study, all we could do was search records for ICD-9 coded cases of post-operative hemorrhage. Not all bleeding was actually witnessed by the providers, as many patients who were seen as a result of bleeding had already stopped bleeding by the time the physician evaluated them. Still, these were known cases, and were included. Other similar studies have also only been able to include cases of bleeding that reached a level where they either visited a hospital or emergency room, or were included in state ambulatory surgery databases in which only cases of bleeding the resulted in a re-visit to the provider were included [2,3]. Post-tonsillectomy hemorrhage can be classified as either primary (<24 h after tonsillectomy) or secondary (>24 h after tonsillectomy) [7]. All episodes in the present study were noted to be secondary in nature.
2.1. Data collection
2.3. Study design
The electronic medical records of the Center for Pediatric ENT— Head and Neck Surgery were searched from January 1, 2005 to January 1, 2010 to identify any patient who had undergone a procedure with the Current Procedural Terminology (CPT) codes 42820 (tonsillectomy and adenoidectomy, under age 12), 42821 (tonsillectomy and adenoidectomy, age 12 or over), 42825 (tonsillectomy, primary or secondary under age 12), or 42826 (tonsillectomy, primary or secondary age 12 or over). The records were further searched to determine which patients experienced a post-operative bleeding episode by searching for ICD-9 (International Classification of Diseases 9th Edition) code 998.11 (hemorrhage complicating a procedure). All procedures were performed by one of the three fellowship-trained pediatric otolaryngologists in the practice. The age ranges studied ranged from 15 months to 19 years old. A de-identified database was constructed including each patient’s age at the time of tonsillectomy, concurrent procedures at the time of the tonsillectomy, as well as pre-operative medical conditions, medications and coagulation studies (if performed). A history of personal and family tendencies toward easy bruising was obtained for every patient, and if the history was positive, preoperative coagulation studies were performed, which included complete blood count with platelet levels, prothrombin time, partial thromboplastin time, and a screening for Von Willebrand disease.
A total of forty-one (41) pre-operative variables were recorded for each patient. Body mass index percentiles were calculated for children over 2 years old using National Heart Lung and Blood Institute Body Mass Index calculator [8], and weight percentiles for children less than two were calculated using World Health Organization Clinical Growth Charts [9]. Any episode of postoperative bleeding was recorded, as were the methods of management. Similar data was recorded for any additional bleeding events subsequent to the first one. The case-control study was performed by matching all ‘‘failures’’ (i.e. patients experiencing a post-tonsillectomy bleed) with all ‘‘successes’’ (i.e. tonsillectomy patients not experiencing a postoperative bleed) who had their surgeries performed on the same day by the same surgeon. Demographic and surgical data were obtained for the control patients in a similar fashion to that of the study subjects. We intentionally did not match controls for age or gender, since age and gender were two of the pre-operative variables that were being studied as potential risk factors for posttonsillectomy hemorrhage.
of postoperative bleeding [5], with no one technique emerging as being universally-accepted as superior to the others. According to U.S. national guidelines, the rate of post-tonsillectomy hemorrhage is generally not affected by whether or not peri-operative antibiotics are used, or by the use of post-operative ibuprofen [6]. Some of the risk factors for post-operative hemorrhage that have been identified in prior reports have included patient ages between 15 and 30 years old [7], chronic/cryptic tonsillitis [4,7], and lower median household incomes [2]. 1.3. Purpose of present study The purpose of the present study was to retrospectively assess and quantify risk factors that may be associated with postoperative hemorrhage. The surgical outcomes of three fellowship-trained pediatric otolaryngologists in a single tertiary level pediatric otolaryngology practice were analyzed, with surgery having been performed under the same settings with identical perioperative care protocols.
2. Materials and methods
2.2. Surgical technique and post-operative care All tonsillectomies were extra-capsular dissections performed using bipolar radiofrequency ablation (Coblation, Arthrocare, Inc. Austin, TX). All patients received an intra-operative dose of steroids (Decadron 0.5 mg/kg with a maximum of 12 mg) [6]. Patients were discharged home the same day as the surgery, and were encouraged to use over-the-counter ibuprofen every 6 h as-needed, acetaminophen every 4 h as-needed, and were given a prescription for acetaminophen and hydrocodone, dosed based
2.4. Statistical analysis Statistical evaluation was performed by using contingency table analysis to identify significant risk factors associated with tonsillectomy, with odds ratios calculated for the binary variables, and logistic regression calculated for the continuous variables. The criterion for significance was determined by a two-tailed t-test with significance (alpha) of 0.050. The statistical software utilized was from StataCorp, LP, College Station, TX, USA. 3. Results During the 5 year study period, 2237 tonsillectomy procedures fitting the inclusion criteria for this study were evaluated. Within this group, 91 patients (4.07%) were identified who experienced any form of bleeding after surgery, and they were matched with
Z. Spektor et al. / International Journal of Pediatric Otorhinolaryngology 84 (2016) 151–155
153
3.2. Recurrent tonsillitis as a risk factor
151 control patients who underwent tonsillectomies on the same day by the same surgeon, but did not experience a bleeding episode. Their descriptive characteristics regarding gender, age and surgical indications are presented in Table 1. The patients ranged in age from 15 months to 19 years old, and were evenly divided between males and females.
The data analysis demonstrated that subjects undergoing tonsillectomy for recurrent tonsillitis (vs. any other indication) had a 4.5 times greater risk of experiencing post-operative hemorrhage (95% confidence intervals 2.41 to 8.38).
3.1. Age as a risk factor
3.3. ADHD as a risk factor
The children who experienced post-operative bleeding were significantly older that those who did not (mean 8.3 vs. mean 6.5 years old, p = 0.0022). For every increase in age by one year, the risk of bleeding post-operatively significantly increased by 1.1 times (p = 0.0025, 95% confidence intervals 1.032 to 1.162). In comparing those patients age 12 or older (CPT codes 42821 and 42826) to those who were under age 12 (CPT codes 42820 and 42825), the older children were 1.6 times more likely to bleed postoperatively, but this did not meet statistical significance (p = 0.17).
Tonsillectomy patients with a history of attention-deficit hyperactivity disorder (ADHD) were found to have an 8.7 times greater risk of experiencing post-operative hemorrhage (95% confidence intervals 1.4 to 53.6, p = 0.0293). No other surgical indications, past medical history, hematological history, preoperative medications, or concurrent surgeries were noted to have any significant effects on the post-operative bleeding rates.
Table 1 Comparison of the hemorrhage group vs. the control group.
Number of patients (n) Age (mean, years) Tonsil size (0+ to 4+, mean)
Gender Males Females Tonsillectomy indication Recurrent tonsillitis UAO/OSA Prior PTA R/O lymphoma Medical History Seizure disorder ADHD Down Syndrome Other craniofacial sydrome Asthma Weight Overweight (>85th %ile BMI) Obese (>95th %ile BMI) Morbidly obese (>99th) Underweight (<5th %ile BMI) Hematology History Family Hx bleeding D/O Von Willebrand Disease Hemophilia Other bleeding disorder Pre-op labs done Pre-op labs abnormal Pre-operative medications Any Nasal steroids Inhaled steroids Oral steroids Antihistamines Singulair ADHD medication OCPs Anti-Seizure meds Bronchodilators Antibiotics Other Concurrent Surgery BMT Turbinate reduction Any other a b
Controls
Cases (post tonsillectomy bleed)
151 6.5 3.4
91 8.3 3.3
n (%)
n (%)
78 (52) 73 (48) (19) (83) (3) (2)
46 73 4 1
(51) (80) (4) (1)
4 1 0 1 18
(3) (1) (0) (1) (12)
2 5 0 1 18
(2) (5) (0) (1) (20)
56 42 30 6
(37) (28) (20) (4)
40 23 12 3
(44) (25) (13) (3)
49 26 7 1 13 8 1 2 4 14 12 11
(2) (1) (0) (0) (3) (1) (32) (17) (5) (1) (9) (5) (1) (1) (3) (9) (8) (7)
21 (14) 6 (4) 8 (5)
Two-sample t test with equal variances. 2-sided Fischer’s exact test.
0.0022a
49 (54) 42 (46)
28 126 5 3
3 1 0 0 4 1
p-Value
3 0 0 1 8 2 31 16 6 1 7 3 3 1 0 11 6 11
(3) (0) (0) (1) (9) (2) (34) (18) (7) (1) (8) (3) (3) (1) (0) (12) (7) (12)
5 (5) 4 (4) 11 (12)
<0.0001b
0.029b
3.4. Management of post-operative hemorrhage A summary of the patients who experienced post-operative hemorrhage and how they were managed is depicted in Fig. 1. Of the 91 patients experiencing any post-operative tonsil bleeding, 21 patients (23%) were taken to the operating room for surgical control of the bleeding. In all cases, control of hemorrhage was achieved with meticulous suction electrocautery. Although suture ligature is an option if needed, it wasn’t used in this cohort, nor was it decided to close the tonsillar fossa. Compared to all the other patients, those children returning to the operating room were more likely to be older (mean of 9.2 years vs. 6.96 years, p = 0.0261) and have a diagnosis of recurrent tonsillitis (p = 0.044). Among the 91 patients who experienced any postoperative bleeding, 37 of them (41%) were admitted to the hospital for overnight observation without requiring surgery, of which 6 of them were cauterized at the bedside with silver nitrate. The remaining 33 post-tonsillectomy hemorrhage patients (36%) were managed conservatively at the office without requiring hospitalization, of which 13 were cauterized with silver nitrate. Post-tonsillectomy hemorrhage episodes occurred most commonly on the 8th post-operative day. Fig. 2 demonstrates the full distribution of post-operative days on which bleeding occurred. There were no significant differences regarding the post-operative day that bleeding occurred among the different management groups (office management, hospitalized for observation, or surgical control of hemorrhage). 3.5. Repeated bleeding episodes Of the 91 patients experiencing any post-tonsillectomy bleeding, 11 experienced a second bleeding episode. Compared to all the other patients, those children experiencing a second bleeding episode were more likely to have a diagnosis of recurrent tonsillitis (p = 0.004). The age difference between the multiplebleed group was not statistically different than the other patients (mean of 9.63 years vs. 7.05 years, p = 0.071). There were no significant risk factors identified among the patients experiencing a second bleed when compared to those experiencing only an initial bleed. Of those children with a second bleeding episode, 4 were taken to the operating room for surgical control of the bleeding. An additional 3 patients who experienced a second posttonsillectomy bleeding episode were admitted to the hospital for overnight observation without requiring surgery, of which one of them was cauterized at the bedside with silver nitrate. The remaining 4 patients were managed conservatively in the office without requiring hospitalization, and all 4 of them were cauterized with silver nitrate.
154
Z. Spektor et al. / International Journal of Pediatric Otorhinolaryngology 84 (2016) 151–155
3.6. Patients with ‘‘hematologic history’’ When reviewing the data, we found that there were 8 of 91 patients (9%) in the bleeding group and 4 of 151 patients (3%) in the control group who had undergone pre-operative hematological lab tests to screen for coagulopathy, and labs were reported as abnormal in 2 of the post-tonsillectomy hemorrhage patients and 1 of the control patients. The difference in the number of patients who underwent this analysis between groups was not significant (p = 0.062, 2-sided Fischer’s exact test). In order to determine if inclusion of these patients could have affected the results, the statistical analyses were repeated after removing all subjects who underwent pre-operative hematological testing from the database. This led to 83 subjects who experienced post-tonsillectomy bleeding and 147 controls. With this new analysis, there was still a significant age difference between the control group (mean age of 6.5) vs. the hemorrhage group (mean age of 7.8) (p = 0.0292). This new analysis also still demonstrated a significant association between a history of recurrent tonsillitis and post-operative hemorrhage, with 46 (55%) of hemorrhage cases compared to 27 (18%) of controls having a history of recurrent tonsillitis (p < 0.0001). Finally, 5 (6%) of hemorrhage cases vs. 1 (1%) of control subjects had a history of ADHD, which remained significant (p = 0.024). None of the other pre-operative factors showed significant differences between groups.
4. Discussion In the present study, using a case-control methodology, the following risk factors for post-tonsillectomy hemorrhage were identified in our pediatric study population: history of recurrent tonsillitis, patient age of 11 years and older, and the presence of ADHD (attention deficit hyperactivity disorder). None of the other 38 pre-operative variables were shown to have an impact on the risk of post-tonsillectomy hemorrhage, including other medical comorbidities, patient body habitus, pre-operative medications, concurrent surgeries, or hematological history. 4.1. Chronic tonsillitis as a risk factor for post-tonsillectomy hemorrhage One independent risk factor that has been reported in prior research to have an association with post-tonsillectomy hemorrhage
Fig. 2. Distribution of post-tonsillectomy bleeding based on the post-operative day bleeding occurred.
is chronic tonsillitis [4]. Furthermore, in a recent histopathologic study, it has been found that cryptic tonsillitis and actinomyces infection within the tonsils are significantly correlated with posttonsillectomy hemorrhage [7]. A recent meta-analysis of adenotonsillectomy complications in children found that secondary hemorrhage was significantly less likely to occur in patients who underwent tonsillectomy for obstructive sleep apnea (compared to patients with other indications such as tonsillitis) (OR = 0.41, CI: 0.23–0.74) [10]. 4.2. Patient age as a risk factor for post-tonsillectomy hemorrhage Patient age has also been identified as a risk factor in numerous studies, with hemorrhage occurring in adults more often than children [11]. A recent large series reported a linear rate of postprocedural hemorrhage after tonsillectomy associated with increasing age [3]. The rate of post-tonsillectomy bleeding in adults has been reported to be as high as 8.6% to 10% [4,7] vs. children (2.1% to 5.0% [2,3,7], with significantly more bleeding episodes in 15–30 year olds [7] and in patients over the age of 25 years [4], or over the age of 12 years [12]. Our study echoes these findings, with children aged 11 years and older having a higher risk of post-tonsillectomy hemorrhage. Some theoretical explanations for this age-dependent increased risk of bleeding may be that a longer duration of chronic tonsillitis in older patients predisposes
Fig. 1. Management approaches utilized for post-tonsillectomy hemorrhage patients.
Z. Spektor et al. / International Journal of Pediatric Otorhinolaryngology 84 (2016) 151–155
to this complication, or perhaps that older patients (who may not have parents looking over their care as closely) may be less compliant with postoperative management recommendations such as dietary intake and rest. 4.3. ADHD as a risk factor for post-tonsillectomy hemorrhage A significant finding in the current study is that the medical comorbidity of ADHD was an independent predictor of posttonsillectomy hemorrhage. We were unable to find any prior clinical research to explain this relationship; thus, we can only theorize as to the reasons for this association. We could hypothesize that patients with ADHD might have increased physical activity and decreased compliance with postoperative instructions postoperatively, but this is only conjecture at this point. A future study exploring this association in more detail would be helpful. At the very least, we have found that the increased expectation of this potential complication in this group of patients has been added to our preoperative education of families.
155
history of recurrent tonsillitis were 4.5 times more likely to experience post-tonsillectomy bleeding than those who had surgery for other indications. Also, patients with the co-morbid condition of ADHD were almost 9 times more likely to experience post-tonsillectomy bleeding than children without ADHD. Future prospective studies would be recommended to help either confirm or refute the associations identified in this study and search for other factors that would be predictive of tonsillectomy complications. Conflict of Interest statement None. Submission declaration This work described in this article has not been published previously. It was presented at the American Society of Pediatric Otolaryngology 27th Annual Meeting, San Diego, CA, April 21, 2012.
4.4. Other risk factors for post-tonsillectomy hemorrhage Authorship Regarding body habitus, a recent study found that the risk of post-tonsillectomy hemorrhage was not increased in overweight children compared to children of normal weight [12]. The present study found similar results. There was also a significantly lower risk of post-operative bleeding in females (OR 0.77) [2], a finding echoed in a study from Germany looking at patients ages 15–44 [4]. Gender was not a risk factor for post-tonsillectomy hemorrhage in the present study. 4.5. Study weaknesses A weakness of the present study is that it is a retrospective casecontrolled study which has to potential for type 2 beta errors given the sample size. It is possible that more than three of the 41 preoperative variables actually are significant, but the present study did not have adequate power to detect them. The present study focused on pre-operative potential risk factors for post-operative hemorrhage. Intra-operative factors (such as presence of fibrosis and degree of difficulty in identifying surgical tissue planes) weren’t included as risk factors to be studied, in part because this particular level of detail was not consistently available in operative reports, given the retrospective nature of the study. Other recent studies on risk factors for posttonsillectomy hemorrhage also have not addressed this topic [3,4,7]. Similarly, the present study did not assess whether or not there was a correlation between the amount of intra-operative bleeding and the risk of post-operative hemorrhage. Incidentally, review of operative reports in this study demonstrated that estimated blood loss was 10 mL or less in all cases. Certainly there may be intra-operative anatomical features unique to each case that could be risk factors for post-operative hemorrhage, and this is a topic that could be addressed in a future study. 5. Conclusion The present study identified and quantified patient factors that were associated with an increased likelihood of post-tonsillectomy bleeding. Children 11 years old and above were twice as likely to experience postoperative bleeding. Children who presented with a
All authors have made substantial contributions to all of the following: (1) the conception and design of the study, acquisition of data, and analysis and interpretation of data, (2) drafting the article or revising it critically for important intellectual content, and (3) final approval of the version to be submitted. Acknowledgements None. References [1] K.A. Cullen, M.J. Hall, A. Golosinskiy, Ambulatory surgery in the United States, Natl. Health Stat. Rep. 11 (2009) 1–25. [2] N. Bhattacharyya, N.L. Shapiro, Associations between socioeconomic status and race with complications after tonsillectomy in children, Otolaryngol. Head. Neck. Surg. 151 (6) (2014) 1055–1060. [3] M. Duval, J. Wilkes, K. Korgenski, R. Srivastava, J. Meier, Causes, costs, and risk factors for unplanned return visits after adenotonsillectomy in children, Int. J. Pediatr. Otorhinolaryngol. 79 (2015) 1640–1646. [4] J. Mueller, D. Boeger, J. Buentzel, D. Esser, K. Hoffmann, P. Jecker, et al., Populationbased analysis of tonsil surgery and postoperative hemorrhage, Eur. Arch. Otorhinolaryngol 272 (2015) 3769–3777. [5] D. Lowe, J. van der Meulen, National Postoperative Tonsillectomy Audit, Lancet 364 (2004) 697–702. [6] R.F. Baugh, S.M. Archer, R.B. Mitchell, et al., Clinical practice guideline: tonsillectomy in children, Otolaryngol. Head. Neck. Surg. 144 (15) (2011) S1–S30. [7] A. Schrock, T. Send, L. Heukamp, A.O. Gerstner, F. Bootz, M. Jakob, The role of histology and other risk factors for post-tonsillectomy haemorrhage, Eur. Arch. Otorhinolaryngol. 266 (2009) 1983–1987. [8] National Heart, Lung and Blood Institute, Calculate Your Body Mass Index, National Institutes of Health, Department of Health and Human Services, USA.gov, 2015 hhttp://www.nhlbi.nih.gov/health/educational/lose_wt/BMI/bmicalc.htmi [accessed December 27, 2015]. [9] Centers for Disease Control and Prevention, National Center for Health Statistics, Standards Are Recommended for Use in the U.S. for Infants and Children 0 to 2 Years of Age, Centers for Disease Control and Prevention, National Center for Health Statistics, 2010. [10] G. De Luca Canto, C. Pacheco-Periera, S. Aydinoz, et al., Adenotonsillectomy complications: a meta-analysis, Pediatrics 136 (4) (2015) 702–718. [11] D.W. Kim, J.W. Koo, S.H. Ahn, C.H. Lee, J.W. Kim, Difference of delayed posttonsillectomy bleeding between children and adults, Auris Nasus Larynx 37 (2010) 456–460. [12] H. Riechelmann, E.C. Blassnigg, C. Profanter, K. Greier, F. Kral, B. Bender, No association between obesity and post-tonsillectomy haemorrhage, J. Laryngol. Otol. 128 (2014) 463–467.
Contents lists available at ScienceDirect
International Journal of Pediatric Otorhinolaryngology journal homepage: www.elsevier.com/locate/ijporl
Risk factors for pediatric post-tonsillectomy hemorrhage§ Zorik Spektor a,b,c, Sandra Saint-Victor b, David J. Kay a,b,c, David L. Mandell a,b,c,* a b c
Center for Pediatric ENT—Head and Neck Surgery, 10150 Hagen Ranch Road, Boynton Beach, FL 33437, USA Department of Otolaryngology, Miller School of Medicine, 1600 NW 10th Ave #1140, Miami, FL 33136, USA Florida Atlantic University, Charles E. Schmidt College of Medicine, 777 Glades Road, Boca Raton, FL 33431, USA
A R T I C L E I N F O
A B S T R A C T
Article history: Received 7 January 2016 Received in revised form 4 March 2016 Accepted 7 March 2016 Available online 18 March 2016
Objectives: To determine pre-operative risk factors for post-tonsillectomy secondary hemorrhage in children, and quantify the magnitude of their risk. Materials and methods: Retrospective case-control study of all pediatric tonsillectomy patients experiencing post-operative bleeding from 2005 to 2010 in a community practice consisting of three fellowship-trained pediatric otolaryngologists were identified. The 91 cases were matched with 151 controls that underwent tonsillectomy by the same surgeon on the same day as each identified case. All charts were reviewed, and 41 pre-operative variables were extracted and statistically analyzed with contingency and regression analysis to calculate significance and odds ratios. Results: Three significant predictors of post-operative bleeding were identified. Performing a tonsillectomy on a child with recurrent tonsillitis (vs. other indications) increased the risk of postoperative hemorrhage by 4.5 times (p < 0.0001, 95% confidence intervals 2.41–8.38). Performing a tonsillectomy on a child with attention deficit hyperactivity disorder (ADHD) increased the risk by 8.7 times (p = 0.029, 95%CI 1.4–53.6). Older children were more predisposed to post-operative bleeding. For every increase in age by one year, the hemorrhage risk increased by 1.1 times (p = 0.0025, 95%CI 1.032– 1.162). Children 11 years of age and older had double the risk of bleeding compared to younger children (odds ratio 1.98, p = 0.0381, 95%CI 1.04–3.79). None of the remaining 38 variables showed significant differences between cases and controls. Conclusions: The risk of post-tonsillectomy hemorrhage is significantly increased in older children and those with recurrent tonsillitis and ADHD. ß 2016 Elsevier Ireland Ltd. All rights reserved.
Keywords: Pediatric tonsillectomy Hemorrhage Risk factors
1. Introduction Tonsillectomy (often combined with adenoidectomy) is among the most common pediatric surgical procedures performed in the United States, with 530,000 tonsillectomies performed in patients <15 years of age in 2006 [1]. While traditional extra-capsular adenotonsillectomy is a routine and effective procedure, it is associated with significant post-operative morbidities such as pain, dehydration, and hemorrhage. Post-operative bleeding can
§ Presented at the 27th annual meeting of the American Society of Pediatric Otolaryngology, San Diego, CA, April 21, 2012. * Corresponding author at: Center for Pediatric ENT, 10301 Hagen Ranch Road, Suite B-900, Boynton Beach, FL 33437, USA. Tel.: +1 561 736 8141; fax: +1 561 736 5662. E-mail addresses: [email protected] (Z. Spektor), [email protected] (S. Saint-Victor), [email protected] (D.J. Kay), [email protected] (D.L. Mandell).
http://dx.doi.org/10.1016/j.ijporl.2016.03.005 0165-5876/ß 2016 Elsevier Ireland Ltd. All rights reserved.
be potentially life-threatening and may require control under general anesthesia. 1.1. Rate of post-tonsillectomy hemorrhage The rate of post-tonsillectomy oropharyngeal hemorrhage across all age groups ranges from 2.1% to 12% [2–4], with the overall rate of secondary surgery to stop hemorrhage ranging from 1.2% to 6% [3,4]. The wide variation seen in reported rates of posttonsillectomy hemorrhage are likely due to diverse definitions and criteria for identifying and reporting such incidents [4]. 1.2. Risk factors for post-tonsillectomy hemorrhage Due to the inability in most cases to predict which patients will go on to experience post-tonsillectomy hemorrhage; many studies have attempted to identify risk factors that might predispose patients to this complication. Much has been written on comparison of different surgical techniques as potential causes
152
Z. Spektor et al. / International Journal of Pediatric Otorhinolaryngology 84 (2016) 151–155
This project was a retrospective cohort study that was compliant with the Health Insurance Portability and Accountability Act (HIPAA) and was granted an exemption by the Western Institutional Review Board (IRB).
upon weight, to be used as-needed for severe pain unresponsive to over-the-counter analgesics. All patients were instructed to report any bleeding to the physician group immediately via telephone contact, at which time they were instructed to either present to the hospital or to the office of the practice on the same day, depending on the clinical information reported. It is possible that there could have been bleeding episodes the providers were not aware of (such as if caregivers had never called the practice about it), and there may have been bleeding episodes that caregivers called about afterhours for which billing documentation wasn’t possible, and were minor enough that caregivers didn’t decide to make a visit. Given the retrospective nature of the study, all we could do was search records for ICD-9 coded cases of post-operative hemorrhage. Not all bleeding was actually witnessed by the providers, as many patients who were seen as a result of bleeding had already stopped bleeding by the time the physician evaluated them. Still, these were known cases, and were included. Other similar studies have also only been able to include cases of bleeding that reached a level where they either visited a hospital or emergency room, or were included in state ambulatory surgery databases in which only cases of bleeding the resulted in a re-visit to the provider were included [2,3]. Post-tonsillectomy hemorrhage can be classified as either primary (<24 h after tonsillectomy) or secondary (>24 h after tonsillectomy) [7]. All episodes in the present study were noted to be secondary in nature.
2.1. Data collection
2.3. Study design
The electronic medical records of the Center for Pediatric ENT— Head and Neck Surgery were searched from January 1, 2005 to January 1, 2010 to identify any patient who had undergone a procedure with the Current Procedural Terminology (CPT) codes 42820 (tonsillectomy and adenoidectomy, under age 12), 42821 (tonsillectomy and adenoidectomy, age 12 or over), 42825 (tonsillectomy, primary or secondary under age 12), or 42826 (tonsillectomy, primary or secondary age 12 or over). The records were further searched to determine which patients experienced a post-operative bleeding episode by searching for ICD-9 (International Classification of Diseases 9th Edition) code 998.11 (hemorrhage complicating a procedure). All procedures were performed by one of the three fellowship-trained pediatric otolaryngologists in the practice. The age ranges studied ranged from 15 months to 19 years old. A de-identified database was constructed including each patient’s age at the time of tonsillectomy, concurrent procedures at the time of the tonsillectomy, as well as pre-operative medical conditions, medications and coagulation studies (if performed). A history of personal and family tendencies toward easy bruising was obtained for every patient, and if the history was positive, preoperative coagulation studies were performed, which included complete blood count with platelet levels, prothrombin time, partial thromboplastin time, and a screening for Von Willebrand disease.
A total of forty-one (41) pre-operative variables were recorded for each patient. Body mass index percentiles were calculated for children over 2 years old using National Heart Lung and Blood Institute Body Mass Index calculator [8], and weight percentiles for children less than two were calculated using World Health Organization Clinical Growth Charts [9]. Any episode of postoperative bleeding was recorded, as were the methods of management. Similar data was recorded for any additional bleeding events subsequent to the first one. The case-control study was performed by matching all ‘‘failures’’ (i.e. patients experiencing a post-tonsillectomy bleed) with all ‘‘successes’’ (i.e. tonsillectomy patients not experiencing a postoperative bleed) who had their surgeries performed on the same day by the same surgeon. Demographic and surgical data were obtained for the control patients in a similar fashion to that of the study subjects. We intentionally did not match controls for age or gender, since age and gender were two of the pre-operative variables that were being studied as potential risk factors for posttonsillectomy hemorrhage.
of postoperative bleeding [5], with no one technique emerging as being universally-accepted as superior to the others. According to U.S. national guidelines, the rate of post-tonsillectomy hemorrhage is generally not affected by whether or not peri-operative antibiotics are used, or by the use of post-operative ibuprofen [6]. Some of the risk factors for post-operative hemorrhage that have been identified in prior reports have included patient ages between 15 and 30 years old [7], chronic/cryptic tonsillitis [4,7], and lower median household incomes [2]. 1.3. Purpose of present study The purpose of the present study was to retrospectively assess and quantify risk factors that may be associated with postoperative hemorrhage. The surgical outcomes of three fellowship-trained pediatric otolaryngologists in a single tertiary level pediatric otolaryngology practice were analyzed, with surgery having been performed under the same settings with identical perioperative care protocols.
2. Materials and methods
2.2. Surgical technique and post-operative care All tonsillectomies were extra-capsular dissections performed using bipolar radiofrequency ablation (Coblation, Arthrocare, Inc. Austin, TX). All patients received an intra-operative dose of steroids (Decadron 0.5 mg/kg with a maximum of 12 mg) [6]. Patients were discharged home the same day as the surgery, and were encouraged to use over-the-counter ibuprofen every 6 h as-needed, acetaminophen every 4 h as-needed, and were given a prescription for acetaminophen and hydrocodone, dosed based
2.4. Statistical analysis Statistical evaluation was performed by using contingency table analysis to identify significant risk factors associated with tonsillectomy, with odds ratios calculated for the binary variables, and logistic regression calculated for the continuous variables. The criterion for significance was determined by a two-tailed t-test with significance (alpha) of 0.050. The statistical software utilized was from StataCorp, LP, College Station, TX, USA. 3. Results During the 5 year study period, 2237 tonsillectomy procedures fitting the inclusion criteria for this study were evaluated. Within this group, 91 patients (4.07%) were identified who experienced any form of bleeding after surgery, and they were matched with
Z. Spektor et al. / International Journal of Pediatric Otorhinolaryngology 84 (2016) 151–155
153
3.2. Recurrent tonsillitis as a risk factor
151 control patients who underwent tonsillectomies on the same day by the same surgeon, but did not experience a bleeding episode. Their descriptive characteristics regarding gender, age and surgical indications are presented in Table 1. The patients ranged in age from 15 months to 19 years old, and were evenly divided between males and females.
The data analysis demonstrated that subjects undergoing tonsillectomy for recurrent tonsillitis (vs. any other indication) had a 4.5 times greater risk of experiencing post-operative hemorrhage (95% confidence intervals 2.41 to 8.38).
3.1. Age as a risk factor
3.3. ADHD as a risk factor
The children who experienced post-operative bleeding were significantly older that those who did not (mean 8.3 vs. mean 6.5 years old, p = 0.0022). For every increase in age by one year, the risk of bleeding post-operatively significantly increased by 1.1 times (p = 0.0025, 95% confidence intervals 1.032 to 1.162). In comparing those patients age 12 or older (CPT codes 42821 and 42826) to those who were under age 12 (CPT codes 42820 and 42825), the older children were 1.6 times more likely to bleed postoperatively, but this did not meet statistical significance (p = 0.17).
Tonsillectomy patients with a history of attention-deficit hyperactivity disorder (ADHD) were found to have an 8.7 times greater risk of experiencing post-operative hemorrhage (95% confidence intervals 1.4 to 53.6, p = 0.0293). No other surgical indications, past medical history, hematological history, preoperative medications, or concurrent surgeries were noted to have any significant effects on the post-operative bleeding rates.
Table 1 Comparison of the hemorrhage group vs. the control group.
Number of patients (n) Age (mean, years) Tonsil size (0+ to 4+, mean)
Gender Males Females Tonsillectomy indication Recurrent tonsillitis UAO/OSA Prior PTA R/O lymphoma Medical History Seizure disorder ADHD Down Syndrome Other craniofacial sydrome Asthma Weight Overweight (>85th %ile BMI) Obese (>95th %ile BMI) Morbidly obese (>99th) Underweight (<5th %ile BMI) Hematology History Family Hx bleeding D/O Von Willebrand Disease Hemophilia Other bleeding disorder Pre-op labs done Pre-op labs abnormal Pre-operative medications Any Nasal steroids Inhaled steroids Oral steroids Antihistamines Singulair ADHD medication OCPs Anti-Seizure meds Bronchodilators Antibiotics Other Concurrent Surgery BMT Turbinate reduction Any other a b
Controls
Cases (post tonsillectomy bleed)
151 6.5 3.4
91 8.3 3.3
n (%)
n (%)
78 (52) 73 (48) (19) (83) (3) (2)
46 73 4 1
(51) (80) (4) (1)
4 1 0 1 18
(3) (1) (0) (1) (12)
2 5 0 1 18
(2) (5) (0) (1) (20)
56 42 30 6
(37) (28) (20) (4)
40 23 12 3
(44) (25) (13) (3)
49 26 7 1 13 8 1 2 4 14 12 11
(2) (1) (0) (0) (3) (1) (32) (17) (5) (1) (9) (5) (1) (1) (3) (9) (8) (7)
21 (14) 6 (4) 8 (5)
Two-sample t test with equal variances. 2-sided Fischer’s exact test.
0.0022a
49 (54) 42 (46)
28 126 5 3
3 1 0 0 4 1
p-Value
3 0 0 1 8 2 31 16 6 1 7 3 3 1 0 11 6 11
(3) (0) (0) (1) (9) (2) (34) (18) (7) (1) (8) (3) (3) (1) (0) (12) (7) (12)
5 (5) 4 (4) 11 (12)
<0.0001b
0.029b
3.4. Management of post-operative hemorrhage A summary of the patients who experienced post-operative hemorrhage and how they were managed is depicted in Fig. 1. Of the 91 patients experiencing any post-operative tonsil bleeding, 21 patients (23%) were taken to the operating room for surgical control of the bleeding. In all cases, control of hemorrhage was achieved with meticulous suction electrocautery. Although suture ligature is an option if needed, it wasn’t used in this cohort, nor was it decided to close the tonsillar fossa. Compared to all the other patients, those children returning to the operating room were more likely to be older (mean of 9.2 years vs. 6.96 years, p = 0.0261) and have a diagnosis of recurrent tonsillitis (p = 0.044). Among the 91 patients who experienced any postoperative bleeding, 37 of them (41%) were admitted to the hospital for overnight observation without requiring surgery, of which 6 of them were cauterized at the bedside with silver nitrate. The remaining 33 post-tonsillectomy hemorrhage patients (36%) were managed conservatively at the office without requiring hospitalization, of which 13 were cauterized with silver nitrate. Post-tonsillectomy hemorrhage episodes occurred most commonly on the 8th post-operative day. Fig. 2 demonstrates the full distribution of post-operative days on which bleeding occurred. There were no significant differences regarding the post-operative day that bleeding occurred among the different management groups (office management, hospitalized for observation, or surgical control of hemorrhage). 3.5. Repeated bleeding episodes Of the 91 patients experiencing any post-tonsillectomy bleeding, 11 experienced a second bleeding episode. Compared to all the other patients, those children experiencing a second bleeding episode were more likely to have a diagnosis of recurrent tonsillitis (p = 0.004). The age difference between the multiplebleed group was not statistically different than the other patients (mean of 9.63 years vs. 7.05 years, p = 0.071). There were no significant risk factors identified among the patients experiencing a second bleed when compared to those experiencing only an initial bleed. Of those children with a second bleeding episode, 4 were taken to the operating room for surgical control of the bleeding. An additional 3 patients who experienced a second posttonsillectomy bleeding episode were admitted to the hospital for overnight observation without requiring surgery, of which one of them was cauterized at the bedside with silver nitrate. The remaining 4 patients were managed conservatively in the office without requiring hospitalization, and all 4 of them were cauterized with silver nitrate.
154
Z. Spektor et al. / International Journal of Pediatric Otorhinolaryngology 84 (2016) 151–155
3.6. Patients with ‘‘hematologic history’’ When reviewing the data, we found that there were 8 of 91 patients (9%) in the bleeding group and 4 of 151 patients (3%) in the control group who had undergone pre-operative hematological lab tests to screen for coagulopathy, and labs were reported as abnormal in 2 of the post-tonsillectomy hemorrhage patients and 1 of the control patients. The difference in the number of patients who underwent this analysis between groups was not significant (p = 0.062, 2-sided Fischer’s exact test). In order to determine if inclusion of these patients could have affected the results, the statistical analyses were repeated after removing all subjects who underwent pre-operative hematological testing from the database. This led to 83 subjects who experienced post-tonsillectomy bleeding and 147 controls. With this new analysis, there was still a significant age difference between the control group (mean age of 6.5) vs. the hemorrhage group (mean age of 7.8) (p = 0.0292). This new analysis also still demonstrated a significant association between a history of recurrent tonsillitis and post-operative hemorrhage, with 46 (55%) of hemorrhage cases compared to 27 (18%) of controls having a history of recurrent tonsillitis (p < 0.0001). Finally, 5 (6%) of hemorrhage cases vs. 1 (1%) of control subjects had a history of ADHD, which remained significant (p = 0.024). None of the other pre-operative factors showed significant differences between groups.
4. Discussion In the present study, using a case-control methodology, the following risk factors for post-tonsillectomy hemorrhage were identified in our pediatric study population: history of recurrent tonsillitis, patient age of 11 years and older, and the presence of ADHD (attention deficit hyperactivity disorder). None of the other 38 pre-operative variables were shown to have an impact on the risk of post-tonsillectomy hemorrhage, including other medical comorbidities, patient body habitus, pre-operative medications, concurrent surgeries, or hematological history. 4.1. Chronic tonsillitis as a risk factor for post-tonsillectomy hemorrhage One independent risk factor that has been reported in prior research to have an association with post-tonsillectomy hemorrhage
Fig. 2. Distribution of post-tonsillectomy bleeding based on the post-operative day bleeding occurred.
is chronic tonsillitis [4]. Furthermore, in a recent histopathologic study, it has been found that cryptic tonsillitis and actinomyces infection within the tonsils are significantly correlated with posttonsillectomy hemorrhage [7]. A recent meta-analysis of adenotonsillectomy complications in children found that secondary hemorrhage was significantly less likely to occur in patients who underwent tonsillectomy for obstructive sleep apnea (compared to patients with other indications such as tonsillitis) (OR = 0.41, CI: 0.23–0.74) [10]. 4.2. Patient age as a risk factor for post-tonsillectomy hemorrhage Patient age has also been identified as a risk factor in numerous studies, with hemorrhage occurring in adults more often than children [11]. A recent large series reported a linear rate of postprocedural hemorrhage after tonsillectomy associated with increasing age [3]. The rate of post-tonsillectomy bleeding in adults has been reported to be as high as 8.6% to 10% [4,7] vs. children (2.1% to 5.0% [2,3,7], with significantly more bleeding episodes in 15–30 year olds [7] and in patients over the age of 25 years [4], or over the age of 12 years [12]. Our study echoes these findings, with children aged 11 years and older having a higher risk of post-tonsillectomy hemorrhage. Some theoretical explanations for this age-dependent increased risk of bleeding may be that a longer duration of chronic tonsillitis in older patients predisposes
Fig. 1. Management approaches utilized for post-tonsillectomy hemorrhage patients.
Z. Spektor et al. / International Journal of Pediatric Otorhinolaryngology 84 (2016) 151–155
to this complication, or perhaps that older patients (who may not have parents looking over their care as closely) may be less compliant with postoperative management recommendations such as dietary intake and rest. 4.3. ADHD as a risk factor for post-tonsillectomy hemorrhage A significant finding in the current study is that the medical comorbidity of ADHD was an independent predictor of posttonsillectomy hemorrhage. We were unable to find any prior clinical research to explain this relationship; thus, we can only theorize as to the reasons for this association. We could hypothesize that patients with ADHD might have increased physical activity and decreased compliance with postoperative instructions postoperatively, but this is only conjecture at this point. A future study exploring this association in more detail would be helpful. At the very least, we have found that the increased expectation of this potential complication in this group of patients has been added to our preoperative education of families.
155
history of recurrent tonsillitis were 4.5 times more likely to experience post-tonsillectomy bleeding than those who had surgery for other indications. Also, patients with the co-morbid condition of ADHD were almost 9 times more likely to experience post-tonsillectomy bleeding than children without ADHD. Future prospective studies would be recommended to help either confirm or refute the associations identified in this study and search for other factors that would be predictive of tonsillectomy complications. Conflict of Interest statement None. Submission declaration This work described in this article has not been published previously. It was presented at the American Society of Pediatric Otolaryngology 27th Annual Meeting, San Diego, CA, April 21, 2012.
4.4. Other risk factors for post-tonsillectomy hemorrhage Authorship Regarding body habitus, a recent study found that the risk of post-tonsillectomy hemorrhage was not increased in overweight children compared to children of normal weight [12]. The present study found similar results. There was also a significantly lower risk of post-operative bleeding in females (OR 0.77) [2], a finding echoed in a study from Germany looking at patients ages 15–44 [4]. Gender was not a risk factor for post-tonsillectomy hemorrhage in the present study. 4.5. Study weaknesses A weakness of the present study is that it is a retrospective casecontrolled study which has to potential for type 2 beta errors given the sample size. It is possible that more than three of the 41 preoperative variables actually are significant, but the present study did not have adequate power to detect them. The present study focused on pre-operative potential risk factors for post-operative hemorrhage. Intra-operative factors (such as presence of fibrosis and degree of difficulty in identifying surgical tissue planes) weren’t included as risk factors to be studied, in part because this particular level of detail was not consistently available in operative reports, given the retrospective nature of the study. Other recent studies on risk factors for posttonsillectomy hemorrhage also have not addressed this topic [3,4,7]. Similarly, the present study did not assess whether or not there was a correlation between the amount of intra-operative bleeding and the risk of post-operative hemorrhage. Incidentally, review of operative reports in this study demonstrated that estimated blood loss was 10 mL or less in all cases. Certainly there may be intra-operative anatomical features unique to each case that could be risk factors for post-operative hemorrhage, and this is a topic that could be addressed in a future study. 5. Conclusion The present study identified and quantified patient factors that were associated with an increased likelihood of post-tonsillectomy bleeding. Children 11 years old and above were twice as likely to experience postoperative bleeding. Children who presented with a
All authors have made substantial contributions to all of the following: (1) the conception and design of the study, acquisition of data, and analysis and interpretation of data, (2) drafting the article or revising it critically for important intellectual content, and (3) final approval of the version to be submitted. Acknowledgements None. References [1] K.A. Cullen, M.J. Hall, A. Golosinskiy, Ambulatory surgery in the United States, Natl. Health Stat. Rep. 11 (2009) 1–25. [2] N. Bhattacharyya, N.L. Shapiro, Associations between socioeconomic status and race with complications after tonsillectomy in children, Otolaryngol. Head. Neck. Surg. 151 (6) (2014) 1055–1060. [3] M. Duval, J. Wilkes, K. Korgenski, R. Srivastava, J. Meier, Causes, costs, and risk factors for unplanned return visits after adenotonsillectomy in children, Int. J. Pediatr. Otorhinolaryngol. 79 (2015) 1640–1646. [4] J. Mueller, D. Boeger, J. Buentzel, D. Esser, K. Hoffmann, P. Jecker, et al., Populationbased analysis of tonsil surgery and postoperative hemorrhage, Eur. Arch. Otorhinolaryngol 272 (2015) 3769–3777. [5] D. Lowe, J. van der Meulen, National Postoperative Tonsillectomy Audit, Lancet 364 (2004) 697–702. [6] R.F. Baugh, S.M. Archer, R.B. Mitchell, et al., Clinical practice guideline: tonsillectomy in children, Otolaryngol. Head. Neck. Surg. 144 (15) (2011) S1–S30. [7] A. Schrock, T. Send, L. Heukamp, A.O. Gerstner, F. Bootz, M. Jakob, The role of histology and other risk factors for post-tonsillectomy haemorrhage, Eur. Arch. Otorhinolaryngol. 266 (2009) 1983–1987. [8] National Heart, Lung and Blood Institute, Calculate Your Body Mass Index, National Institutes of Health, Department of Health and Human Services, USA.gov, 2015 hhttp://www.nhlbi.nih.gov/health/educational/lose_wt/BMI/bmicalc.htmi [accessed December 27, 2015]. [9] Centers for Disease Control and Prevention, National Center for Health Statistics, Standards Are Recommended for Use in the U.S. for Infants and Children 0 to 2 Years of Age, Centers for Disease Control and Prevention, National Center for Health Statistics, 2010. [10] G. De Luca Canto, C. Pacheco-Periera, S. Aydinoz, et al., Adenotonsillectomy complications: a meta-analysis, Pediatrics 136 (4) (2015) 702–718. [11] D.W. Kim, J.W. Koo, S.H. Ahn, C.H. Lee, J.W. Kim, Difference of delayed posttonsillectomy bleeding between children and adults, Auris Nasus Larynx 37 (2010) 456–460. [12] H. Riechelmann, E.C. Blassnigg, C. Profanter, K. Greier, F. Kral, B. Bender, No association between obesity and post-tonsillectomy haemorrhage, J. Laryngol. Otol. 128 (2014) 463–467.