Published online November 1, 2006
PEDIATRICS
Vol. 118
No. 5
November 2006, pp.
1925-1931
(doi:10.1542/peds.2006-1555)
Recurrent Respiratory Papillomatosis in Children: Masquerader of Common Respiratory Diseases
Michael C. Zacharisen, MD, FAAPa and
Stephen F. Conley, MD, FAAPb
a Department of Pediatrics, Section of Allergy and Immunology
b Department of Otolaryngology and Communication Sciences, Division of Pediatric Otolaryngology, Medical College of Wisconsin, Milwaukee, Wisconsin
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ABSTRACT
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BACKGROUND. Recurrent respiratory papillomatosis in children is an uncommon but potentially life-threatening benign tumor of the respiratory tract with laryngeal predilection. The diagnosis of recurrent respiratory papillomatosis may be challenging unless there is a high index of suspicion and awareness of the variable presentations.
METHODS. We reviewed the medical charts of children with recurrent respiratory papillomatosis treated at a tertiary children’s hospital. The presentation of recurrent respiratory papillomatosis is illustrated by a series of case reports. We provide a paradigm to assist in the early diagnosis of children with recurrent respiratory papillomatosis.
RESULTS. Five patients, aged 2 to 6 years, were erroneously diagnosed with recurrent croup, asthma, laryngeal hemangioma, and tracheomalacia after presenting with variable degrees of chronic dyspnea, cough, stridor, dysphonia, weak cry, and syncope. Once the diagnosis of recurrent respiratory papillomatosis was made, recurring surgical ablation of papillomata was initiated.
CONCLUSIONS. Any child presenting with a voice disturbance with or without stridor is recommended to have diagnostic flexible fiber-optic laryngoscopy. Recurrent respiratory papillomatosis should be considered in children when other common pediatric airway diseases either do not follow the natural history or do not respond to treatment of the common disorder.
Key Words: pediatric • recurrent respiratory papillomatosis • human papilloma virus • asthma • croup • stridor • hoarseness
Abbreviations: RRP—recurrent respiratory papillomatosis • HPV—human papillomavirus • ED—emergency department • URI—upper respiratory infection • FFL—flexible fiberoptic laryngoscopy
Recurrent respiratory papillomatosis (RRP) is the most common benign neoplasm to affect the larynx in children.1 It is estimated that 
6000 active cases of RRP were present in 1995 with >2300 new cases.2 The incidence of RRP in the US pediatric population is estimated at 4.3 per 100000 children and 1.8 per 100000 adults.3 The etiology of RRP is infection of the upper airway with human papillomavirus (HPV) types 6 and 11. Although there are several dozen HPV DNA types; types 6 and 11 have a predilection for mucocutaneous surfaces including not only the larynx but also external genital infections in both men and women, mucosal infection of the vagina and cervix termed condyloma acuminata, and oral papillomas of the tongue and oral mucosa.4 HPV 11 infections are more likely to have greater disease severity and more frequent surgeries, need adjuvant therapies, develop tracheal and pulmonary disease, and require a tracheostomy.5
The classic presenting symptom of pediatric RRP is persistent hoarseness or weak cry occurring between 2 and 4 years of age. The only other more frequent cause of hoarseness in children is voice overuse with secondary vocal cord nodules, a localized laryngitis. Nearly 75% of RRP patients are diagnosed before their fifth birthday and nearly all before 7 years old. If the diagnosis is delayed, the wart-like masses will progressively grow leading to aphonia and then upper airway obstruction.6 Although the definitive diagnosis is made by an experienced pediatric otolaryngologist or pediatric pulmonologist, inevitably, primary care or emergency department (ED) physicians will be evaluating these children. Other subspecialists may also be involved if the patient presents with atypical symptoms.
Common pediatric respiratory disorders may be erroneously diagnosed before the recognition of RRP. The causes of "noisy breathing" in children are numerous and can be classified as infectious or congenital and subdivided into intrathoracic or extrathoracic.7 The presence of a high-pitched noise (stridor) versus a low-pitched noise (stertor) aids in determining a diagnosis as does the breathing noise relationship to the phase of respiration: inspiratory, expiratory, or biphasic. Other less common disorders that affect the vocal cords resulting in hoarseness include vocal cord paralysis (unilateral or bilateral), cysts, polyps, arytenoid fixation, and Arnold-Chiari syndrome. Other causes of pediatric airway obstruction that should be considered based on the level of obstruction include the following: nasal lesion (choanal stenosis/atresia, pyriform aperture stenosis, adenoid hypertrophy, nasal tumors, neonatal rhinitis, and foreign body), pharyngeal obstruction (nasopharyngeal stenosis, tonsillar hypertrophy, large tongue related to lymphatic malformation, trisomy 21, or Beckwith-Wiedemann syndrome and craniofacial abnormalities, such as mandibular and midfacial hypoplasia), laryngeal obstruction (laryngomalacia, vocal cord granulomas, foreign body, web, angioedema, infectious laryngitis, diphtheria, and epiglottitis), subglottic airway obstruction (congenital or acquired stenosis, hemangioma, and trauma), and tracheal airway obstruction (congenital tracheal stenosis, tracheomalacia, complete tracheal rings, foreign body, and extrinsic compression from a neoplasm or anomalous vascular structures). A variety of diagnostic techniques are available to arrive at a correct diagnosis.
Treatment
Treatment of pediatric RRP depends on the degree of airway involvement. If the child presents with acute respiratory distress from upper airway obstruction, then tracheostomy may be necessary. Tracheostomy was performed in 14% of pediatric cases compared with only 6% of adult-onset papillomatosis.2 The most common current methods of treatment are CO2 laser excision or endolaryngeal microdebrider papilloma excision via direct laryngoscopy.
Many treatments have been used in the past with only limited success. These include ultrasound, cryosurgery, hormones, steroids, and chemotherapeutic agents, such as methotrexate, autogenous vaccine, transfer factor, isotretinoin, and interferon.8–10 Antiviral therapy with intralesional cidofovir has had variable success.11 These studies lacked control groups and enrolled small numbers of patients. Photodynamic therapy uses intravenous dihematoporphyrin ether, a photosensitizing agent that, when activated by light at the appropriate wavelength, selectively destroys those cells that contain the dihematoporphyrin ether. Thirty-three patients (9 children) treated with this therapy had 50% decrease in the average rate of laryngeal papilloma growth.12 The use of excision by microdebrider was comparable to CO2 laser in a prospective trial for immediate postoperative results.13 Laryngeal webs can be a soft-tissue complication from surgery in the context of laryngopharyngeal acid reflux.14 Treatment for acid reflux may improve outcome. Gene expression research is underway, and a vaccine to prevent HPV infection has been approved recently. The recombinant quadrivalent HPV vaccine contains types 6, 11, 16, and 18.15–17 The anticipated effect of this new vaccine on RRP caused by these disease types is promising, because 90% of genital warts are caused by these types.
Descriptive Cases
We describe 5 children with respiratory papillomatosis with special emphasis on the presenting symptoms to highlight the spectrum of presentations and identify masqueraders of laryngeal RRP.
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METHODS
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We identified patients with RRP treated at Children’s Hospital of Wisconsin through a medical chart review. The human research review committee approved this review. The medical charts of patients were reviewed for demographic data, presenting symptoms including onset and duration, initial pediatric diagnoses, past history, operative findings, and treatment.
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RESULTS
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The following 5 cases are illustrative.
Case 1
A 17-month-old white boy was referred by his pediatrician to the allergist for an evaluation for asthma. The "lifelong" history of noisy breathing and now chronic cough that occurred with exertion and upper respiratory infections (URIs) did not respond to albuterol. One year before this visit, he was seen by a pediatric cardiologist for evaluation of a heart murmur and mild cardiomegaly viewed on a chest radiograph. Although a complete cardiac evaluation was unremarkable, moderate upper airway sounds were noted on examination, and he was diagnosed with tracheomalacia. He had been diagnosed with croup once. On the allergist’s examination, he was noted to have a hoarse, weakened cry and monophasic inspiratory and expiratory stridor. Lungs were clear to auscultation. A lateral neck radiograph revealed diminished anterior-posterior dimension of the tracheal air column reflecting tracheomalacia. A contrast upper gastrointestinal study was normal. Although arrangements were being made for outpatient bronchoscopy by the pediatric pulmonologist, he presented to the ED with a 3-day history of the following URI symptoms: "croupy" cough, stridor, and increased work of breathing. He was diagnosed with croup and treated with nebulized epinephrine. A chest radiograph revealed mild hyperaeration, and lateral neck radiograph revealed enlarged adenoids, subglottic airway edema, and a "lobular density at the level of the vocal cords," which was interpreted to be "either motion artifact or a true lesion." Rigid bronchoscopy was performed within 4 weeks, and 90% airway obstruction was noted with papillomas observed on the anterior true vocal cords, posterior ventricle, anterior commissure, and subchordal region. Pinpoint lesions were noted in the trachea. He underwent CO2 laser ablation and surgical debulking with significant symptom improvement. The common respiratory diagnoses made in this patient include tracheomalacia and croup with an erroneous diagnosis of asthma. It is conceivable that even the croup diagnosis/symptoms were related to the papillomas as opposed to infectious (viral) or spasmodic croup.
Case 2
A 2-year-old boy had a 1-year history of progressive dyspnea with new-onset pronounced stridor. He presented to the ED with a barky cough, fever, tachypnea, tachycardia, coarse breath sounds, and faint wheezing. A chest radiograph was normal. He was discharged from the hospital with a diagnosis of croup. Three weeks later he was diagnosed again with croup in the ED after presenting with "noisy" and labored breathing, especially with excitement or exertion, and syncopal episodes over the preceding week. On examination, he exhibited stridor with crying, and lungs were clear to auscultation. A lateral neck radiograph was normal, and a chest radiograph showed slight overexpansion with patchy increased density in the central portions consistent with a lower respiratory viral infection. Eight months later he again presented to the ED with a 1-week history of barky cough, URI symptoms, and intermittent stridor while sleeping with brief apneic episodes. The day before admission he had a syncopal episode with perioral cyanosis. On examination, he was in severe respiratory distress, tachypneic, stridorous, and retracting. Lungs were clear to auscultation. A diagnosis of infectious croup was made, and he was treated with nebulized epinephrine and oral dexamethasone. A lateral neck radiograph revealed a 6-mm soft tissue density in the region of the aryepiglottic folds consistent with a cyst or foreign body. There was no drooling, dysphagia, or fever. Otolaryngology consultation was obtained, and a flexible nasopharyngoscopy revealed grape-like clusters of tissues in the supraglottic area. He was taken to the operating room emergently. During mask induction in the operating room, the airway was lost, requiring emergent direct laryngoscopy and rigid bronchoscopy to reestablish ventilation of the patient. The papillomas had completely obstructed the airway. Surgical debulking followed by CO2 laser ablation successfully opened the airway. Recurrent croup, syncope, apnea, and stridor were this patient’s presenting symptoms. The papillomas may partially or even completely explain the respiratory symptoms in this child.
Case 3
A 7-year-old white boy with a history of asthma that did not improve with albuterol or beclomethasone inhaler was assessed. On further questioning, he had a 1-year history of dysphonia, noisy breathing, and mild inspiratory stridor. Chest radiograph was normal, and a lateral neck radiograph revealed a mass lesion in the subglottic space with 75% narrowing of the airway and aryepiglottic fold irregularity. Flexible laryngoscopy revealed a large mass of papillomas involving the supraglottic and true vocal cords bilaterally. After biopsy and treatment with surgical debulking, followed by CO2 laser ablation, he improved. Pulmonary function tests were normal. He was not compliant with follow-up visits and 8 months later presented to the ED in severe respiratory distress and obstructive laryngeal symptoms requiring emergent bronchoscopy. He underwent laser therapy twice after this episode but was again lost to follow-up until 7 months later when he suddenly collapsed outside his house after walking home from school. He received mouth-to-mouth resuscitation from his mother and required emergency surgery. At anesthesia induction, the airway was obstructed, and he required rigid bronchoscopy for airway control. He was found to have severe airway obstruction related to multiple large laryngeal papillomas. It is unlikely that he indeed had asthma in light of the lack of response to ß-2 agonists, normal lung function, and lack of other symptoms. However, a methacholine challenge test was not performed. His severe case eventually prompted initiation of Cidofovir therapy with an excellent clinical response.
Case 4
A 4-year-old black female with a history of asthma and a weak cry since 3 months of age was first brought to medical attention at age 4 months. She was referred by her primary physician to an otolaryngologist for a lack of vocalizations when she cried. A physical examination without laryngoscopy was performed, and she was treated with decongestant-antihistamine combination and cefaclor. Chest radiograph revealed nonspecific mild bilateral hilar accentuation. At 7 months old, she was transported to the ED after experiencing repeated syncopal episodes at day care. She had experienced a weaker cry for 1 week. Chest radiograph revealed a right lower lobe infiltrate, and a lateral neck radiograph revealed subglottic narrowing with a protrusion near the vocal cords. She was treated for pneumonia with intravenous antibiotics and scheduled for outpatient flexible bronchoscopy to evaluate for laryngeal hemangioma. Two weeks later, she developed severe difficulty breathing and suffered a respiratory arrest. Emergency rescue personnel administered mouth-to-mouth respirations. She was cyanotic and exhibiting deep retractions when paramedics arrived. She improved slightly with bag-and-mask-assisted ventilation. The ED physician was unable to intubate her, and eventually an anesthesiologist tracheally intubated her albeit with difficulty. She suffered hypoxemia and seizures. She was transported to the intensive care unit and at flexible bronchoscopy was found to have a large exophytic papilloma in the laryngeal vestibule. She was referred to pediatric otolaryngology with surgical debulking and laser CO2 treatments performed expeditiously. She subsequently required 24 laser treatments. Repeat laryngoscopy performed at intervals revealed recurrence of papilloma growth. Previous diagnoses included asthma, aphonia, possible hemangioma, and respiratory arrest.
Case 5
A 2-year-old white boy born by cesarean section had a history of recurrent croup since 6 months of age after general anesthesia and endotracheal intubation for a minor surgical procedure. He had not responded to antibiotics and developed gradually progressive inspiratory stridor with exertion, a weak voice, 11-kg weight loss, and decreased appetite. Significant hoarseness and respiratory distress over 10 days prompted an evaluation for inhaled foreign body. A chest radiograph and upper gastrointestinal contrast study were normal. A lateral neck radiograph revealed supraglottic and subglottic masses. He was admitted directly from the clinic, and operative direct laryngoscopy revealed massive papillomas. He has since undergone multiple laser ablations and now at 10 years old is stable and in remission. His previous diagnoses were recurrent croup and laryngeal foreign body.
Figure 1 illustrates the typical findings at diagnosis. After treatment, laryngoscopy is essentially normal (Fig 2).
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FIGURE 1 Laryngoscopic view of multiple papillomas surrounding the vocal cords and impinging on the airway.
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FIGURE 2 Laryngoscopic view of the laryngeal airway after surgical debridement and CO2 laser ablation revealing a patent airway.
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DISCUSSION
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Although laryngeal RRP is the most common benign tumor to affect the larynx in children, the prevalence is low with an estimated 2000 to 2500 new cases each year and 6000 children in the United States treated annually for this disease.1,2 Nearly all of the affected patients in our series with laryngeal papillomatosis carried the diagnosis of croup, tracheomalacia, or asthma. Whether asthma was indeed the case is doubtful, because no patients went on to exhibit persistent or recurrent symptoms after treatment of their papillomas. All of the patients eventually had symptoms directly attributed to the area of the vocal cords, such as hoarseness, and a weak cry, although this was not the chief complaint. Unfortunately, it is not possible to retrospectively interpret the diagnosis of croup, although a history of "recurrent croup" should raise awareness of a potential underlying condition.
RRP, formerly referred to as juvenile laryngeal papillomas, is characterized by recurrent growth of benign papillomas along the epithelium of the respiratory tract and usually concentrates at the mucocutaneous margin of the true vocal cords where the squamous epithelium of the vocal cord contacts the respiratory epithelium of the larynx. Other affected areas include the false vocal cords, anterior commissure, arytenoids, subglottis, ventricle, and trachea.
Typically, the physical examination is normal in otherwise healthy children. Early RRP can present solely with voice disturbance (hoarseness, weak cry, and aphonia), which must be differentiated from true vocal cord nodules, a localized laryngitis that is the most common cause of childhood voice disturbance. The classic presentation of gradual progressive stridor leading to upper airway obstruction was not seen in these patients. Children may have considerable morbidity, because the papillomas grow relentlessly even after seemingly thorough surgical excision. In these examples, the age of symptom onset ranged from "birth" to 6 years old. The duration of symptoms before definitive diagnosis ranged from 2 months to >2 years. Patients are typically first-born children by vaginal delivery. A maternal history of known perineal warts was present in only 1 patient, and he was delivered by cesarean section because of maternal preeclampsia and fetal distress. Routine cesarean section delivery for birth canal or perineal warts is not recommended.18 Although nonsexual transmission of HPV can occur, children who present with anogenital warts at >4 years of age should be referred to Child Protective Services.19 Compared with children, adults with papillomata have been diagnosed with reflux esophagitis and vocal fold nodules.20
The confusion with asthma and croup is not surprising, because acute asthma exacerbation is the most frequent inpatient diagnosis in most children’s hospitals. A 3-year-old child was presumed to have steroid-dependent asthma for a year before the diagnosis of RRP.21 Similarly, both croup and asthma are very common ED diagnoses, with most children returning home. Unfortunately, most of these children present at an age where formal lung function testing is not feasible, thereby relying on characteristic symptoms, supporting radiographs, and response to asthma or croup treatment to help elucidate the diagnosis. Lower airway papillomatosis is an uncommon but serious complication of RRP that can present with recurrent pneumonia, emphysema, or atelectasis and also be confused with asthma.22 The lower frequency of tracheal disease may be because of lower frequency of activation, because latent infection in biopsy samples similar to laryngeal tissue can be demonstrated.23
Confirmatory diagnosis of RRP is made by direct laryngoscopy and biopsy for tissue diagnosis and viral typing, because type 11 has a more severe prognosis.5 In our series, all of the patients had primary care providers, and some patients were evaluated by specialists; nonetheless, a number of months elapsed before the final diagnosis was made. Figure 3 is a paradigm summarizing our recommendations for a timely (<4 weeks) referral to an otolaryngologist for diagnostic flexible fiberoptic laryngoscopy (FFL). Because of airway concerns, time should not be wasted on radiographic studies before FFL can be obtained. If inspiratory stridor at rest is present, then a referral within 48 hours is recommended because of the risk of significant (>80%) airway obstruction. If the FFL is negative, then dynamic airway fluoroscopy provides a greater sensitivity than plain films (lateral neck radiograph) in diagnosing the site of airway obstruction below the vocal cords.24
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CONCLUSIONS
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Pediatricians, family physicians, allergists, pulmonologists, and even otolaryngologists who have less exposure to young children need to be keenly aware that recurrent or progressive respiratory symptoms consistent with common diagnoses of asthma and croup may be presentations of papillomas. Asthma is not usually associated with any type of voice disturbance. Any child with such a presentation warrants prompt visualization of the laryngeal structures, especially if there is no clinical response to appropriate asthma therapies. The need for early diagnosis and prompt treatment is evident, because complete airway obstruction may occur. These benign yet dangerous upper airway tumors require repeated definitive treatment, such as surgical debulking and CO2 laser ablation. Because RRP have a tendency to grow in size and number, a high index of suspicion by all clinicians is required to accurately diagnose and treat this potentially life-threatening disorder.
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ACKNOWLEDGMENTS
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We thank Dr Arun Kadambi for his contribution in data collection.
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FOOTNOTES
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Accepted Jun 13, 2006.
Address correspondence to Michael C. Zacharisen, MD, 9000 W Wisconsin Ave, Suite 411, Milwaukee, WI 5322. E-mail: mzach{at}mcw.edu
Financial Disclosure: Dr Zacharisen is on the speakers bureau of Merck, Inc, in relation to asthma and allergies, not vaccines. This relationship has no impact upon the article submitted or its conclusions. Dr Conley participates in the speakers bureau of Abbott Laboratories. This relationship has no impact on the article submitted or its conclusions.
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PEDIATRICS (ISSN 1098-4275). ©2006 by the American Academy of Pediatrics
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ABSTRACT
METHODS
