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Juvenile onset recurrent respiratory papillomatosis (JRRP) is a rare and often chronic disease.[[1–4]] It is characterised by benign but potentially aggressive recurring laryngeal epithelial lesions[[5]] caused by the human papilloma virus (HPV), most likely by vertical transmission.[[6]] Being the first-born child with a maternal age younger than 20 years increases the risk.[[6]] Children can present with dysphonia, chronic coughing or with signs of compromised airways including stridor.[[5]] Multiple procedures to debulk the recurrent lesions to maintain voice and airway patency are often required. More severely affected patients may require a tracheostomy. Mortality has been reported.[[5]]

A quadrivalent vaccine which protects against HPV subtypes 6, 11, 16 and 18 was added to the national immunisation schedule for females aged 12 years in 2008.[[7]] Females up to the age of 20 were later eligible as part of a catch-up programme between 2009 to 2016.[[7]] A nonavalent vaccine replaced this in 2017, which also protects against subtypes 31, 33, 45, 52 and 58. At the same time the immunisation schedule was extended to include males and females aged 9 to 26 years.[[8]] This vaccination protects against high-risk HPV types responsible for cervical cancer, but also offers protection against HPV types 6 and 11, which cause the majority of JRRP.[[9]]

As the number of individuals protected against HPV increases, the incidence and prevalence of JRRP could be expected to decrease. There are few studies reviewing the incidence of JRRP following the introduction of an HPV vaccination programme.[[10]] In Australia, an estimated incidence of 0.16 per 100,000 per year declining to 0.02 per 100,000 per year after the introduction of the vaccine has been reported.[[10]] Preliminary data from the US and Canada show similar trends.[[11]] Trends in New Zealand are unknown.

Aim

To review and compare the incidence of JRRP at Starship Children’s Hospital (SSH) before and after the introduction of a national HPV vaccination programme.

Study design

This is a single-centre retrospective review of children managed for JRRP at SSH. Children aged up to and including 14 years were included. This age cut-off was chosen to align with census data. As the HPV vaccination was introduced on 1 September 2007, a study year is counted from 1 September to 31 August. It took 1 year for the first cohort of children to complete their vaccination. As a result, children treated between 1 September 1998 and 31 August 2008 (before vaccination) were compared with those diagnosed between 1 September 2008 and 31 August 2022 (after vaccination).

Children without histopathological confirmation of laryngeal papillomatosis were excluded.

All New Zealand hospitals with otolaryngology (ORL) departments were contacted regarding their referral patterns. ORL departments that referred children with JRRP to SSH exclusively were included. Children were excluded when SSH was not the exclusive referral hospital.

This study (AH22479) was approved by Auckland Health Research Ethics Committee (AHREC) on 14 May 2021.

Method

A retrospective review of the electronic clinical records was performed at Starship Children’s Hospital. Children were identified by searching for ICD-10 code D14.1 (benign lesions of the larynx).

A survey was emailed to all ORL departments’ clinical directors and/or paediatric otolaryngology leads in New Zealand. Follow-up emails and phone calls were made where additional information was required. All New Zealand hospital ORL departments that referred patients with JRRP to SSH exclusively were included.

Population data by age and district were extracted from Statistics New Zealand.[[12]] These data were interpolated to calculate the population at risk of JRRP between 1998 and 2022. All data were analysed using a generalised linear model, modelling the observed counts data as having a Poisson distribution. A p-value of <0.05 was considered statistically significant.

The mean of the incidence over the 10 years prior to the introduction of the HPV vaccination was compared with the mean of the incidence after its introduction. Further analysis was performed from 2016 when the vaccination programme was made more widely available. Statistical analyses were carried out using SAS 9.4 and R statistical program version 4.1.2.[[13,14]]

Results

The SSH paediatric ORL department received referrals from hospitals throughout the North Island and from one hospital in the South Island. All ORL departments contacted completed the survey.

A total of 31 children with JRRP treated at SSH were identified between 1 September 2008 and 31 August 2022. This included patients from our catchment in central Auckland, as well as hospitals that referred to SSH exclusively. These included Northland, Waitamatā, Counties Manukau, MidCentral, Whanganui and Bay of Plenty (Figure 1). Eight children were excluded as their primary hospitals did not refer JRRP patients to SSH exclusively. These include Lakes, Taranaki, Hawkes Bay, Tairāwhiti, Capital Coast, Hutt Valley, Wairarapa and Nelson.

The paediatric populations of the qualifying districts were included in the analysis (Figure 1). This included 44 to 49% of the total New Zealand population of children. The incidence over the study period is displayed in Figure 2.

View Figures 1–2 and Tables 1–2.

The mean incidence of JRRP prior to the introduction of the HPV vaccination was 0.21 per 100,000 children per year. There was no change after the introduction of the vaccination with a rate of 0.23 per 100,000 children per year observed (Table 1).

The mean incidence over the last 6 years (2017 to 2022) was 0.15 per 100,000 children per year. Compared to the baseline, there was a non-significant reduction by 0.06 per 100,000 children per year (p=0.56) (Table 2).

Discussion

The introduction of the HPV vaccine has not resulted in a significant reduction in the incidence of JRRP in New Zealand to date. Between 1998 and 2008, before the introduction of the HPV vaccine, the incidence of children with JRRP in the SSH catchment area was 0.21 per 100,000 children per year. This is comparable to the baseline incidence of 0.24 in Canada.[[15]] The reported incidence range varies from 4.3 per 100,000 persons under 14 years per year in the US[[16]] to a much lower incidence of 0.17 per 100,000 persons under 18 years per year in Norway.[[4]] An Australian study could not determine the incidence but estimated the pre-vaccination prevalence of JRRP to have been between 0.6–1.1 per 100,000 persons under 20 years.[[3]]

There has been a reduction in the incidence of JRRP to 0.15 per 100,000 children per year in the most past 6 years. This decline compared to the pre-vaccination incidence remained non-significant (Table 2). Females who received their HPV vaccination in 2008 are now 26 years old and those eligible as part of the “catch-up” cohort are now 31 and 32 years old. The median age of first-time mothers has been between 29.9 and 30.5 years in New Zealand over the past decade,[[17]] therefore, many of the vaccinated women may not have borne children. As a greater number of vaccinated women become mothers, a further reduction in the incidence may be observed.[[15]] Additionally, the earlier cohorts included a heterogenous age group of 12- to 20-year-olds. As the effectiveness of the vaccine relies upon being vaccinated prior to sexual debut, a greater proportion of the earlier cohort may not be protected.

Australia reported a declining incidence from 0.16 per 100,000 children per year in 2012 to 0.02 in 2016.[[10]] The incidence rate in our cohort between 2016 and 2022 is comparable to the incidence rate in Australia a decade ago,[[10]] with more recent Australian results far lower than the SSH figures (Figure 2). Australia introduced a national HPV programme at a similar time to New Zealand.[[18]] At least half of Australia’s female population aged 12–26 years were fully vaccinated in the year of the vaccination programme being introduced in 2007.[[19]] The Australian vaccination rates at age 15 have been above 78% since 2015.[[18,19]] It had increased to over 80% in females and 78% in males in 2020.[[19]] The roll out and uptake of the vaccine has been slower in New Zealand[[8]] with between 60 to 67% of eligible females vaccinated in the birth cohorts up until 2003.[[20]] According to the Immunisation Advisory Centre, the rate for females increased to 69–70% in the 2007 and 2008 cohorts.[[21]] Data beyond the 2008 birth cohort are not available. The vaccine uptake rate for males in New Zealand has been modelled to be 53%.[[22]] A rate of 75% is considered necessary for “herd immunity”.[[7]] Our non-significant results may be due to this lower HPV vaccine coverage in our population.

Attitudes toward childhood vaccinations are becoming increasingly polarised in New Zealand.[[23]] There is a stigma around HPV being a sexually transmitted infection (STI).[[24]] The HPV vaccination programme brings together two demanding and confronting areas in promoting vaccination and sexual health.[[24]] Attempts to desexualise HPV vaccination failed overseas and high-profile public debate ensued with political, cultural and religious divide on the matter, which continues today.[[24]] Similar issues may have contributed to the low uptake of the HPV vaccination in New Zealand. Efforts are concentrated on improving coverage.[[7]]

Strengths of our study include the use of the International Classification of Disease code D14.1 (benign neoplasm of the larynx). This has been shown to be a very sensitive and specific ICD-10 code for identifying JRRP (PPV 98.1%).[[2]] We were able to obtain 100% feedback from referral centres and ORL departments around the country, which enabled more accurate estimates of the catchment population. Although a single-centre study, the referral population represents nearly half of the New Zealand population, which should provide a good proxy for the true incidence of JRRP in New Zealand. Limitations of the study include this being a single-centre study, the high number of patients that were excluded and the relatively low absolute numbers due to this being a rare disease.

A future study will be a national study with the aim to address these shortcomings. The establishment of a national database will allow continual monitoring of JRRP and provide more certainty about its incidence and disease patterns, which may in turn reduce the need of referrals to tertiary centres.

Conclusion

The mean incidence of JRRP before and after the introduction of HPV has remained unchanged in children treated at SSH. More recently, there has been a reduction in incidence—although this is based on small numbers. The low HPV vaccination rate (≤70%) may explain why a significant reduction in the incidence of JRRP seen overseas has not been observed in New Zealand. Ongoing surveillance and a national study would provide more insight into the true incidence and evolving trends.

Summary

Abstract

Aim

To review and compare the incidence of juvenile onset recurrent respiratory papillomatosis (JRRP) at Starship Children’s Hospital (SSH) before and after the introduction of a national HPV vaccination programme.

Method

Patients treated for JRRP at SSH were identified retrospectively using ICD-10 code D14.1 over a 14-year period. The incidence of JRRP in the 10-year period prior to the introduction of HPV vaccination (1 September 1998 to 31 August 2008) was compared with the incidence after its introduction. A second comparison was made between the pre-vaccination incidence with the incidence over the most recent 6 years when the vaccination became more widely available. All New Zealand hospital ORL departments that referred children with JRRP to SSH exclusively were included.

Results

SSH manages about half of the New Zealand paediatric population with JRRP. The incidence of JRRP before the introduction of the HPV vaccination programme was 0.21 per 100,000 per year in children 14 years of age and younger. This remained stable between 2008 and 2022 (0.23 vs 0.21 per 100,000 per year). The mean incidence in the later post-vaccination period was 0.15 per 100,000 per year based on small numbers.

Conclusion

The mean incidence of JRRP before and after the introduction of HPV has remained unchanged in children treated at SSH. More recently, a reduction in incidence has been noted, although this is based on small numbers. The low HPV vaccination rate (≤70%) may explain why a significant reduction in the incidence of JRRP seen overseas has not been observed in New Zealand. Ongoing surveillance and a national study would provide more insight into the true incidence and evolving trends.

Author Information

Dora Blair: ORL Registrar, Department of Paediatric Otorhinolaryngology, Starship Children’s Hospital, Auckland, New Zealand. Evelyn Lamble: House Officer, Department of Paediatric Otorhinolaryngology, Starship Children’s Hospital, Auckland, New Zealand. Graeme van der Meer: ORL Surgeon: Department of Paediatric Otorhinolaryngology, Starship Children’s Hospital, Auckland, New Zealand. Edward Toll: ORL Surgeon, Department of Paediatric Otorhinolaryngology, Starship Children’s Hospital, Auckland, New Zealand. Craig McCaffer: ORL Surgeon, Department of Paediatric Otorhinolaryngology, Starship Children’s Hospital, Auckland, New Zealand. Colin Barber: ORL Surgeon, Department of Paediatric Otorhinolaryngology, Starship Children’s Hospital, Auckland, New Zealand; Honorary Senior Lecturer, Department of Surgery, The University of Auckland, Auckland, New Zealand. Nikki Mills: ORL Surgeon, Department of Otorhinolaryngology, Nelson Hospital, New Zealand. Michel Neeff: ORL Surgeon, Department of Paediatric Otorhinolaryngology, Starship Children’s Hospital, Auckland, New Zealand; Senior Lecturer, Department of Surgery, The University of Auckland, Auckland, New Zealand.

Acknowledgements

We would like to thank Dr Dug Yeo Han, Clinical Research Biostatistician at Starship Research & Innovation and Dr Sandro Leite, ORL Surgeon and Honorary Senior Lecturer at The University of Auckland for their assistance in statistical analysis. In addition, we would also like to thank Professor Nikki Turner, Medical Director and Dr Anna Howe, Research and Policy Analyst at Immunisation Advisory Centre, New Zealand for their insight into HPV vaccination in New Zealand.

Correspondence

Dora Blair: ORL Registrar, Department of Paediatric Otorhinolaryngology, Starship Children’s Hospital, Auckland, New Zealand.

Correspondence Email

E: drdorablair@gmail.com

Competing Interests

Nil.

1)      Marsico M, Mehta V, Chastek B, et al. Estimating the incidenceand prevalence of juvenile-onset recurrent respiratory papillomatosis in publiclyand privately insured claims databases in the United States. Sex Transm Dis. 2014May 1;41(5):300-5. doi: 10.1097/OLQ.0000000000000115.

2)      Novakovic D, Cheng AT, Baguley K, et al. Juvenile recurrent respiratorypapillomatosis: 10‐year audit and Australian prevalence estimates. Laryngoscope.2016 Dec;126(12):2827-32. doi: 10.1002/lary.26005.

3)      Seedat RY. The incidence and prevalence of juvenile-onset recurrentrespiratory papillomatosis in the Free State province of South Africa and Lesotho.Int J Pediatr Otorhinolaryngol. 2014 Dec 1;78(12):2113-5. doi:10.1016/j.ijporl.2014.09.017.

4)      Omland T, Akre H, Vårdal M, Brøndbo K. Epidemiological aspectsof recurrent respiratory papillomatosis: a population‐based study. Laryngoscope.2012 Jul;122(7):1595-9. doi: 10.1002/lary.23327.

5)      LindebergH, Elbrønd O. Laryngeal papillomas: clinical aspects in a seriesof 231 patients. Clin Otolaryngol Allied Sci. 1989 Aug;14(4):333-42. doi:10.1111/j.1365-2273.1989.tb00381.x.

6)      Niyibizi J, Rodier C, Wassef M, Trottier H. Risk factors for thedevelopment and severity of juvenile-onset recurrent respiratory papillomatosis:a systematic review. Int J Pediatr Otorhinolaryngol. 2014 Feb 1;78(2):186-97. doi:10.1016/j.ijporl.2013.11.036.

7)      Best Practice Advocacy Centre New Zealand. HPV vaccination: gettingthe programme back on track [Internet]. 2019 Mar 29 [cited 2021 Apr 5].Available from: https://bpac.org.nz/2019/hpv.aspx.

8)      Manatū Hauora – Ministry of Health. History of the HPV immunsationprogramme [Internet].2014 Apr 9 [cited 2021 Jun 4]. Available from: https://www.health.govt.nz/our-work/preventative-health-wellness/immunisation/hpv-immunisation-programme/history-hpv-immunisation-programme.

9)      Gissmann L, Diehl V, Schultz-Coulon HJ, zur Hausen H. Molecularcloning and characterization of human papilloma virus DNA derived from a laryngealpapilloma. J Virol. 1982 Oct;44(1):393-400. doi: 10.1128/JVI.44.1.393-400.1982.

10)   Novakovic D, Cheng AT, Zurynski Y, et al. A Prospective Studyof the Incidence of Juvenile-Onset Recurrent Respiratory Papillomatosis AfterImplementation of a National HPV Vaccination Program. J Infect Dis. 2018 Jan 4;217(2):208-12.doi: 10.1093/infdis/jix498.

11)   Benedict JJ, Derkay CS. Recurrent respiratory papillomatosis:A 2020 perspective. Laryngoscope Investig Otolaryngol. 2021;6(2):340-5. doi:10.1002/lio2.545.

12)   Stats NZ – Tatauranga Aotearoa. Subnational population estimates(DHB, DHB constituency), by age and sex, at 30 June 1996-2022 (2015 boundaries)[Internet]. [cited 2022 Nov 12.] Available from: https://nzdotstat.stats.govt.nz/wbos/Index.aspx?DataSetCode=TABLECODE7509

13)   SAS Institute Inc. SAS software version 9.4 [software]. Cary,NC, USA.

14)   R Foundation for Statistical Computing. R: A language and environmentfor statistical computing [software].  Vienna,Austria; 2019. Available from: https://www.R-project.org/.

15)   Campisi P, Hawkes M, Simpson K; Canadian Juvenile Onset RecurrentRespiratory Papillomatosis Working Group. The epidemiology of juvenile onset recurrentrespiratory papillomatosis derived from a population level national database. Laryngoscope.2010 Jun;120(6):1233-45. doi: 10.1002/lary.20901.

16)   Derkay CS. Task force on recurrent respiratory papillomas: A preliminaryreport. Arch Otolaryngol Head Neck Surg. 1995 Dec;121(12):1386-91. doi:10.1001/archotol.1995.01890120044008.

17)   Stats NZ – Tatauranga Aotearoa. Parenting and fertility trendsin New Zealand: 2018 [Internet].2019 Oct 24 [cited 2022 Nov 20]. Available from: https://www.stats.govt.nz/reports/parenting-and-fertility-trends-in-new-zealand-2018.

18)   Brotherton JM, Liu B, Donovan B, et al. Human papillomavirus (HPV)vaccination coverage in young Australian women is higher than previously estimated:independent estimates from a nationally representative mobile phone survey. Vaccine.2014 Jan 23;32(5):592-7. doi: 10.1016/j.vaccine.2013.11.075.

19)   Australian Government – Department of Health and Aged Care. NationalHPV 3 dose vaccination coverage for all adolescents turning 15 years of age fromyear of program commencement [Internet]. 2019 Dec 4 [cited: 2022, Nov 20 2022].Available from:  https://www.health.gov.au/resources/publications/national-hpv-3-dose-vaccination-coverage-for-all-adolescents-turning-15-years-of-age-from-year-of-program-commencement.

20)   Manatū Hauora – Ministry of Health. HPV immunisation programme[Internet]. 2021 Aug 13 [cited 2022 Nov 20]. Available from: https://www.health.govt.nz/our-work/preventative-health-wellness/immunisation/hpv-immunisation-programme.

21)   Howe, A. Research and Policy Analyst at Immunisation AdvisoryCentre (IMAC), New Zealand. Email to: Dora Blair (ORL Registrar, Starship Children’sHospital) Re: HPV vaccination coverage. 2021, Nov 1.

22)   Smith MA, Hall M, Lew JB, Canfell K. Potential for HPV vaccinationand primary HPV screening to reduce cervical cancer disparities: Example from NewZealand. Vaccine. 2018 Oct 8;36(42):6314-24. doi:10.1016/j.vaccine.2018.08.063.

23)   Lee CH, Sibley CG. Attitudes toward vaccinations are becomingmore polarized in New Zealand: Findings from a longitudinal survey. EClinicalMedicine.2020 Jun;23:100387. doi: 10.1016/j.eclinm.2020.100387.

24)   Velan B, Yadgar Y. On the implications of desexualizing vaccinesagainst sexually transmitted diseases: health policy challenges in a multiculturalsociety. Isr J Health Policy Res. 2017 Dec;6(1):1-2.

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Juvenile onset recurrent respiratory papillomatosis (JRRP) is a rare and often chronic disease.[[1–4]] It is characterised by benign but potentially aggressive recurring laryngeal epithelial lesions[[5]] caused by the human papilloma virus (HPV), most likely by vertical transmission.[[6]] Being the first-born child with a maternal age younger than 20 years increases the risk.[[6]] Children can present with dysphonia, chronic coughing or with signs of compromised airways including stridor.[[5]] Multiple procedures to debulk the recurrent lesions to maintain voice and airway patency are often required. More severely affected patients may require a tracheostomy. Mortality has been reported.[[5]]

A quadrivalent vaccine which protects against HPV subtypes 6, 11, 16 and 18 was added to the national immunisation schedule for females aged 12 years in 2008.[[7]] Females up to the age of 20 were later eligible as part of a catch-up programme between 2009 to 2016.[[7]] A nonavalent vaccine replaced this in 2017, which also protects against subtypes 31, 33, 45, 52 and 58. At the same time the immunisation schedule was extended to include males and females aged 9 to 26 years.[[8]] This vaccination protects against high-risk HPV types responsible for cervical cancer, but also offers protection against HPV types 6 and 11, which cause the majority of JRRP.[[9]]

As the number of individuals protected against HPV increases, the incidence and prevalence of JRRP could be expected to decrease. There are few studies reviewing the incidence of JRRP following the introduction of an HPV vaccination programme.[[10]] In Australia, an estimated incidence of 0.16 per 100,000 per year declining to 0.02 per 100,000 per year after the introduction of the vaccine has been reported.[[10]] Preliminary data from the US and Canada show similar trends.[[11]] Trends in New Zealand are unknown.

Aim

To review and compare the incidence of JRRP at Starship Children’s Hospital (SSH) before and after the introduction of a national HPV vaccination programme.

Study design

This is a single-centre retrospective review of children managed for JRRP at SSH. Children aged up to and including 14 years were included. This age cut-off was chosen to align with census data. As the HPV vaccination was introduced on 1 September 2007, a study year is counted from 1 September to 31 August. It took 1 year for the first cohort of children to complete their vaccination. As a result, children treated between 1 September 1998 and 31 August 2008 (before vaccination) were compared with those diagnosed between 1 September 2008 and 31 August 2022 (after vaccination).

Children without histopathological confirmation of laryngeal papillomatosis were excluded.

All New Zealand hospitals with otolaryngology (ORL) departments were contacted regarding their referral patterns. ORL departments that referred children with JRRP to SSH exclusively were included. Children were excluded when SSH was not the exclusive referral hospital.

This study (AH22479) was approved by Auckland Health Research Ethics Committee (AHREC) on 14 May 2021.

Method

A retrospective review of the electronic clinical records was performed at Starship Children’s Hospital. Children were identified by searching for ICD-10 code D14.1 (benign lesions of the larynx).

A survey was emailed to all ORL departments’ clinical directors and/or paediatric otolaryngology leads in New Zealand. Follow-up emails and phone calls were made where additional information was required. All New Zealand hospital ORL departments that referred patients with JRRP to SSH exclusively were included.

Population data by age and district were extracted from Statistics New Zealand.[[12]] These data were interpolated to calculate the population at risk of JRRP between 1998 and 2022. All data were analysed using a generalised linear model, modelling the observed counts data as having a Poisson distribution. A p-value of <0.05 was considered statistically significant.

The mean of the incidence over the 10 years prior to the introduction of the HPV vaccination was compared with the mean of the incidence after its introduction. Further analysis was performed from 2016 when the vaccination programme was made more widely available. Statistical analyses were carried out using SAS 9.4 and R statistical program version 4.1.2.[[13,14]]

Results

The SSH paediatric ORL department received referrals from hospitals throughout the North Island and from one hospital in the South Island. All ORL departments contacted completed the survey.

A total of 31 children with JRRP treated at SSH were identified between 1 September 2008 and 31 August 2022. This included patients from our catchment in central Auckland, as well as hospitals that referred to SSH exclusively. These included Northland, Waitamatā, Counties Manukau, MidCentral, Whanganui and Bay of Plenty (Figure 1). Eight children were excluded as their primary hospitals did not refer JRRP patients to SSH exclusively. These include Lakes, Taranaki, Hawkes Bay, Tairāwhiti, Capital Coast, Hutt Valley, Wairarapa and Nelson.

The paediatric populations of the qualifying districts were included in the analysis (Figure 1). This included 44 to 49% of the total New Zealand population of children. The incidence over the study period is displayed in Figure 2.

View Figures 1–2 and Tables 1–2.

The mean incidence of JRRP prior to the introduction of the HPV vaccination was 0.21 per 100,000 children per year. There was no change after the introduction of the vaccination with a rate of 0.23 per 100,000 children per year observed (Table 1).

The mean incidence over the last 6 years (2017 to 2022) was 0.15 per 100,000 children per year. Compared to the baseline, there was a non-significant reduction by 0.06 per 100,000 children per year (p=0.56) (Table 2).

Discussion

The introduction of the HPV vaccine has not resulted in a significant reduction in the incidence of JRRP in New Zealand to date. Between 1998 and 2008, before the introduction of the HPV vaccine, the incidence of children with JRRP in the SSH catchment area was 0.21 per 100,000 children per year. This is comparable to the baseline incidence of 0.24 in Canada.[[15]] The reported incidence range varies from 4.3 per 100,000 persons under 14 years per year in the US[[16]] to a much lower incidence of 0.17 per 100,000 persons under 18 years per year in Norway.[[4]] An Australian study could not determine the incidence but estimated the pre-vaccination prevalence of JRRP to have been between 0.6–1.1 per 100,000 persons under 20 years.[[3]]

There has been a reduction in the incidence of JRRP to 0.15 per 100,000 children per year in the most past 6 years. This decline compared to the pre-vaccination incidence remained non-significant (Table 2). Females who received their HPV vaccination in 2008 are now 26 years old and those eligible as part of the “catch-up” cohort are now 31 and 32 years old. The median age of first-time mothers has been between 29.9 and 30.5 years in New Zealand over the past decade,[[17]] therefore, many of the vaccinated women may not have borne children. As a greater number of vaccinated women become mothers, a further reduction in the incidence may be observed.[[15]] Additionally, the earlier cohorts included a heterogenous age group of 12- to 20-year-olds. As the effectiveness of the vaccine relies upon being vaccinated prior to sexual debut, a greater proportion of the earlier cohort may not be protected.

Australia reported a declining incidence from 0.16 per 100,000 children per year in 2012 to 0.02 in 2016.[[10]] The incidence rate in our cohort between 2016 and 2022 is comparable to the incidence rate in Australia a decade ago,[[10]] with more recent Australian results far lower than the SSH figures (Figure 2). Australia introduced a national HPV programme at a similar time to New Zealand.[[18]] At least half of Australia’s female population aged 12–26 years were fully vaccinated in the year of the vaccination programme being introduced in 2007.[[19]] The Australian vaccination rates at age 15 have been above 78% since 2015.[[18,19]] It had increased to over 80% in females and 78% in males in 2020.[[19]] The roll out and uptake of the vaccine has been slower in New Zealand[[8]] with between 60 to 67% of eligible females vaccinated in the birth cohorts up until 2003.[[20]] According to the Immunisation Advisory Centre, the rate for females increased to 69–70% in the 2007 and 2008 cohorts.[[21]] Data beyond the 2008 birth cohort are not available. The vaccine uptake rate for males in New Zealand has been modelled to be 53%.[[22]] A rate of 75% is considered necessary for “herd immunity”.[[7]] Our non-significant results may be due to this lower HPV vaccine coverage in our population.

Attitudes toward childhood vaccinations are becoming increasingly polarised in New Zealand.[[23]] There is a stigma around HPV being a sexually transmitted infection (STI).[[24]] The HPV vaccination programme brings together two demanding and confronting areas in promoting vaccination and sexual health.[[24]] Attempts to desexualise HPV vaccination failed overseas and high-profile public debate ensued with political, cultural and religious divide on the matter, which continues today.[[24]] Similar issues may have contributed to the low uptake of the HPV vaccination in New Zealand. Efforts are concentrated on improving coverage.[[7]]

Strengths of our study include the use of the International Classification of Disease code D14.1 (benign neoplasm of the larynx). This has been shown to be a very sensitive and specific ICD-10 code for identifying JRRP (PPV 98.1%).[[2]] We were able to obtain 100% feedback from referral centres and ORL departments around the country, which enabled more accurate estimates of the catchment population. Although a single-centre study, the referral population represents nearly half of the New Zealand population, which should provide a good proxy for the true incidence of JRRP in New Zealand. Limitations of the study include this being a single-centre study, the high number of patients that were excluded and the relatively low absolute numbers due to this being a rare disease.

A future study will be a national study with the aim to address these shortcomings. The establishment of a national database will allow continual monitoring of JRRP and provide more certainty about its incidence and disease patterns, which may in turn reduce the need of referrals to tertiary centres.

Conclusion

The mean incidence of JRRP before and after the introduction of HPV has remained unchanged in children treated at SSH. More recently, there has been a reduction in incidence—although this is based on small numbers. The low HPV vaccination rate (≤70%) may explain why a significant reduction in the incidence of JRRP seen overseas has not been observed in New Zealand. Ongoing surveillance and a national study would provide more insight into the true incidence and evolving trends.

Summary

Abstract

Aim

To review and compare the incidence of juvenile onset recurrent respiratory papillomatosis (JRRP) at Starship Children’s Hospital (SSH) before and after the introduction of a national HPV vaccination programme.

Method

Patients treated for JRRP at SSH were identified retrospectively using ICD-10 code D14.1 over a 14-year period. The incidence of JRRP in the 10-year period prior to the introduction of HPV vaccination (1 September 1998 to 31 August 2008) was compared with the incidence after its introduction. A second comparison was made between the pre-vaccination incidence with the incidence over the most recent 6 years when the vaccination became more widely available. All New Zealand hospital ORL departments that referred children with JRRP to SSH exclusively were included.

Results

SSH manages about half of the New Zealand paediatric population with JRRP. The incidence of JRRP before the introduction of the HPV vaccination programme was 0.21 per 100,000 per year in children 14 years of age and younger. This remained stable between 2008 and 2022 (0.23 vs 0.21 per 100,000 per year). The mean incidence in the later post-vaccination period was 0.15 per 100,000 per year based on small numbers.

Conclusion

The mean incidence of JRRP before and after the introduction of HPV has remained unchanged in children treated at SSH. More recently, a reduction in incidence has been noted, although this is based on small numbers. The low HPV vaccination rate (≤70%) may explain why a significant reduction in the incidence of JRRP seen overseas has not been observed in New Zealand. Ongoing surveillance and a national study would provide more insight into the true incidence and evolving trends.

Author Information

Dora Blair: ORL Registrar, Department of Paediatric Otorhinolaryngology, Starship Children’s Hospital, Auckland, New Zealand. Evelyn Lamble: House Officer, Department of Paediatric Otorhinolaryngology, Starship Children’s Hospital, Auckland, New Zealand. Graeme van der Meer: ORL Surgeon: Department of Paediatric Otorhinolaryngology, Starship Children’s Hospital, Auckland, New Zealand. Edward Toll: ORL Surgeon, Department of Paediatric Otorhinolaryngology, Starship Children’s Hospital, Auckland, New Zealand. Craig McCaffer: ORL Surgeon, Department of Paediatric Otorhinolaryngology, Starship Children’s Hospital, Auckland, New Zealand. Colin Barber: ORL Surgeon, Department of Paediatric Otorhinolaryngology, Starship Children’s Hospital, Auckland, New Zealand; Honorary Senior Lecturer, Department of Surgery, The University of Auckland, Auckland, New Zealand. Nikki Mills: ORL Surgeon, Department of Otorhinolaryngology, Nelson Hospital, New Zealand. Michel Neeff: ORL Surgeon, Department of Paediatric Otorhinolaryngology, Starship Children’s Hospital, Auckland, New Zealand; Senior Lecturer, Department of Surgery, The University of Auckland, Auckland, New Zealand.

Acknowledgements

We would like to thank Dr Dug Yeo Han, Clinical Research Biostatistician at Starship Research & Innovation and Dr Sandro Leite, ORL Surgeon and Honorary Senior Lecturer at The University of Auckland for their assistance in statistical analysis. In addition, we would also like to thank Professor Nikki Turner, Medical Director and Dr Anna Howe, Research and Policy Analyst at Immunisation Advisory Centre, New Zealand for their insight into HPV vaccination in New Zealand.

Correspondence

Dora Blair: ORL Registrar, Department of Paediatric Otorhinolaryngology, Starship Children’s Hospital, Auckland, New Zealand.

Correspondence Email

E: drdorablair@gmail.com

Competing Interests

Nil.

1)      Marsico M, Mehta V, Chastek B, et al. Estimating the incidenceand prevalence of juvenile-onset recurrent respiratory papillomatosis in publiclyand privately insured claims databases in the United States. Sex Transm Dis. 2014May 1;41(5):300-5. doi: 10.1097/OLQ.0000000000000115.

2)      Novakovic D, Cheng AT, Baguley K, et al. Juvenile recurrent respiratorypapillomatosis: 10‐year audit and Australian prevalence estimates. Laryngoscope.2016 Dec;126(12):2827-32. doi: 10.1002/lary.26005.

3)      Seedat RY. The incidence and prevalence of juvenile-onset recurrentrespiratory papillomatosis in the Free State province of South Africa and Lesotho.Int J Pediatr Otorhinolaryngol. 2014 Dec 1;78(12):2113-5. doi:10.1016/j.ijporl.2014.09.017.

4)      Omland T, Akre H, Vårdal M, Brøndbo K. Epidemiological aspectsof recurrent respiratory papillomatosis: a population‐based study. Laryngoscope.2012 Jul;122(7):1595-9. doi: 10.1002/lary.23327.

5)      LindebergH, Elbrønd O. Laryngeal papillomas: clinical aspects in a seriesof 231 patients. Clin Otolaryngol Allied Sci. 1989 Aug;14(4):333-42. doi:10.1111/j.1365-2273.1989.tb00381.x.

6)      Niyibizi J, Rodier C, Wassef M, Trottier H. Risk factors for thedevelopment and severity of juvenile-onset recurrent respiratory papillomatosis:a systematic review. Int J Pediatr Otorhinolaryngol. 2014 Feb 1;78(2):186-97. doi:10.1016/j.ijporl.2013.11.036.

7)      Best Practice Advocacy Centre New Zealand. HPV vaccination: gettingthe programme back on track [Internet]. 2019 Mar 29 [cited 2021 Apr 5].Available from: https://bpac.org.nz/2019/hpv.aspx.

8)      Manatū Hauora – Ministry of Health. History of the HPV immunsationprogramme [Internet].2014 Apr 9 [cited 2021 Jun 4]. Available from: https://www.health.govt.nz/our-work/preventative-health-wellness/immunisation/hpv-immunisation-programme/history-hpv-immunisation-programme.

9)      Gissmann L, Diehl V, Schultz-Coulon HJ, zur Hausen H. Molecularcloning and characterization of human papilloma virus DNA derived from a laryngealpapilloma. J Virol. 1982 Oct;44(1):393-400. doi: 10.1128/JVI.44.1.393-400.1982.

10)   Novakovic D, Cheng AT, Zurynski Y, et al. A Prospective Studyof the Incidence of Juvenile-Onset Recurrent Respiratory Papillomatosis AfterImplementation of a National HPV Vaccination Program. J Infect Dis. 2018 Jan 4;217(2):208-12.doi: 10.1093/infdis/jix498.

11)   Benedict JJ, Derkay CS. Recurrent respiratory papillomatosis:A 2020 perspective. Laryngoscope Investig Otolaryngol. 2021;6(2):340-5. doi:10.1002/lio2.545.

12)   Stats NZ – Tatauranga Aotearoa. Subnational population estimates(DHB, DHB constituency), by age and sex, at 30 June 1996-2022 (2015 boundaries)[Internet]. [cited 2022 Nov 12.] Available from: https://nzdotstat.stats.govt.nz/wbos/Index.aspx?DataSetCode=TABLECODE7509

13)   SAS Institute Inc. SAS software version 9.4 [software]. Cary,NC, USA.

14)   R Foundation for Statistical Computing. R: A language and environmentfor statistical computing [software].  Vienna,Austria; 2019. Available from: https://www.R-project.org/.

15)   Campisi P, Hawkes M, Simpson K; Canadian Juvenile Onset RecurrentRespiratory Papillomatosis Working Group. The epidemiology of juvenile onset recurrentrespiratory papillomatosis derived from a population level national database. Laryngoscope.2010 Jun;120(6):1233-45. doi: 10.1002/lary.20901.

16)   Derkay CS. Task force on recurrent respiratory papillomas: A preliminaryreport. Arch Otolaryngol Head Neck Surg. 1995 Dec;121(12):1386-91. doi:10.1001/archotol.1995.01890120044008.

17)   Stats NZ – Tatauranga Aotearoa. Parenting and fertility trendsin New Zealand: 2018 [Internet].2019 Oct 24 [cited 2022 Nov 20]. Available from: https://www.stats.govt.nz/reports/parenting-and-fertility-trends-in-new-zealand-2018.

18)   Brotherton JM, Liu B, Donovan B, et al. Human papillomavirus (HPV)vaccination coverage in young Australian women is higher than previously estimated:independent estimates from a nationally representative mobile phone survey. Vaccine.2014 Jan 23;32(5):592-7. doi: 10.1016/j.vaccine.2013.11.075.

19)   Australian Government – Department of Health and Aged Care. NationalHPV 3 dose vaccination coverage for all adolescents turning 15 years of age fromyear of program commencement [Internet]. 2019 Dec 4 [cited: 2022, Nov 20 2022].Available from:  https://www.health.gov.au/resources/publications/national-hpv-3-dose-vaccination-coverage-for-all-adolescents-turning-15-years-of-age-from-year-of-program-commencement.

20)   Manatū Hauora – Ministry of Health. HPV immunisation programme[Internet]. 2021 Aug 13 [cited 2022 Nov 20]. Available from: https://www.health.govt.nz/our-work/preventative-health-wellness/immunisation/hpv-immunisation-programme.

21)   Howe, A. Research and Policy Analyst at Immunisation AdvisoryCentre (IMAC), New Zealand. Email to: Dora Blair (ORL Registrar, Starship Children’sHospital) Re: HPV vaccination coverage. 2021, Nov 1.

22)   Smith MA, Hall M, Lew JB, Canfell K. Potential for HPV vaccinationand primary HPV screening to reduce cervical cancer disparities: Example from NewZealand. Vaccine. 2018 Oct 8;36(42):6314-24. doi:10.1016/j.vaccine.2018.08.063.

23)   Lee CH, Sibley CG. Attitudes toward vaccinations are becomingmore polarized in New Zealand: Findings from a longitudinal survey. EClinicalMedicine.2020 Jun;23:100387. doi: 10.1016/j.eclinm.2020.100387.

24)   Velan B, Yadgar Y. On the implications of desexualizing vaccinesagainst sexually transmitted diseases: health policy challenges in a multiculturalsociety. Isr J Health Policy Res. 2017 Dec;6(1):1-2.

For the PDF of this article,
contact nzmj@nzma.org.nz

View Article PDF

Juvenile onset recurrent respiratory papillomatosis (JRRP) is a rare and often chronic disease.[[1–4]] It is characterised by benign but potentially aggressive recurring laryngeal epithelial lesions[[5]] caused by the human papilloma virus (HPV), most likely by vertical transmission.[[6]] Being the first-born child with a maternal age younger than 20 years increases the risk.[[6]] Children can present with dysphonia, chronic coughing or with signs of compromised airways including stridor.[[5]] Multiple procedures to debulk the recurrent lesions to maintain voice and airway patency are often required. More severely affected patients may require a tracheostomy. Mortality has been reported.[[5]]

A quadrivalent vaccine which protects against HPV subtypes 6, 11, 16 and 18 was added to the national immunisation schedule for females aged 12 years in 2008.[[7]] Females up to the age of 20 were later eligible as part of a catch-up programme between 2009 to 2016.[[7]] A nonavalent vaccine replaced this in 2017, which also protects against subtypes 31, 33, 45, 52 and 58. At the same time the immunisation schedule was extended to include males and females aged 9 to 26 years.[[8]] This vaccination protects against high-risk HPV types responsible for cervical cancer, but also offers protection against HPV types 6 and 11, which cause the majority of JRRP.[[9]]

As the number of individuals protected against HPV increases, the incidence and prevalence of JRRP could be expected to decrease. There are few studies reviewing the incidence of JRRP following the introduction of an HPV vaccination programme.[[10]] In Australia, an estimated incidence of 0.16 per 100,000 per year declining to 0.02 per 100,000 per year after the introduction of the vaccine has been reported.[[10]] Preliminary data from the US and Canada show similar trends.[[11]] Trends in New Zealand are unknown.

Aim

To review and compare the incidence of JRRP at Starship Children’s Hospital (SSH) before and after the introduction of a national HPV vaccination programme.

Study design

This is a single-centre retrospective review of children managed for JRRP at SSH. Children aged up to and including 14 years were included. This age cut-off was chosen to align with census data. As the HPV vaccination was introduced on 1 September 2007, a study year is counted from 1 September to 31 August. It took 1 year for the first cohort of children to complete their vaccination. As a result, children treated between 1 September 1998 and 31 August 2008 (before vaccination) were compared with those diagnosed between 1 September 2008 and 31 August 2022 (after vaccination).

Children without histopathological confirmation of laryngeal papillomatosis were excluded.

All New Zealand hospitals with otolaryngology (ORL) departments were contacted regarding their referral patterns. ORL departments that referred children with JRRP to SSH exclusively were included. Children were excluded when SSH was not the exclusive referral hospital.

This study (AH22479) was approved by Auckland Health Research Ethics Committee (AHREC) on 14 May 2021.

Method

A retrospective review of the electronic clinical records was performed at Starship Children’s Hospital. Children were identified by searching for ICD-10 code D14.1 (benign lesions of the larynx).

A survey was emailed to all ORL departments’ clinical directors and/or paediatric otolaryngology leads in New Zealand. Follow-up emails and phone calls were made where additional information was required. All New Zealand hospital ORL departments that referred patients with JRRP to SSH exclusively were included.

Population data by age and district were extracted from Statistics New Zealand.[[12]] These data were interpolated to calculate the population at risk of JRRP between 1998 and 2022. All data were analysed using a generalised linear model, modelling the observed counts data as having a Poisson distribution. A p-value of <0.05 was considered statistically significant.

The mean of the incidence over the 10 years prior to the introduction of the HPV vaccination was compared with the mean of the incidence after its introduction. Further analysis was performed from 2016 when the vaccination programme was made more widely available. Statistical analyses were carried out using SAS 9.4 and R statistical program version 4.1.2.[[13,14]]

Results

The SSH paediatric ORL department received referrals from hospitals throughout the North Island and from one hospital in the South Island. All ORL departments contacted completed the survey.

A total of 31 children with JRRP treated at SSH were identified between 1 September 2008 and 31 August 2022. This included patients from our catchment in central Auckland, as well as hospitals that referred to SSH exclusively. These included Northland, Waitamatā, Counties Manukau, MidCentral, Whanganui and Bay of Plenty (Figure 1). Eight children were excluded as their primary hospitals did not refer JRRP patients to SSH exclusively. These include Lakes, Taranaki, Hawkes Bay, Tairāwhiti, Capital Coast, Hutt Valley, Wairarapa and Nelson.

The paediatric populations of the qualifying districts were included in the analysis (Figure 1). This included 44 to 49% of the total New Zealand population of children. The incidence over the study period is displayed in Figure 2.

View Figures 1–2 and Tables 1–2.

The mean incidence of JRRP prior to the introduction of the HPV vaccination was 0.21 per 100,000 children per year. There was no change after the introduction of the vaccination with a rate of 0.23 per 100,000 children per year observed (Table 1).

The mean incidence over the last 6 years (2017 to 2022) was 0.15 per 100,000 children per year. Compared to the baseline, there was a non-significant reduction by 0.06 per 100,000 children per year (p=0.56) (Table 2).

Discussion

The introduction of the HPV vaccine has not resulted in a significant reduction in the incidence of JRRP in New Zealand to date. Between 1998 and 2008, before the introduction of the HPV vaccine, the incidence of children with JRRP in the SSH catchment area was 0.21 per 100,000 children per year. This is comparable to the baseline incidence of 0.24 in Canada.[[15]] The reported incidence range varies from 4.3 per 100,000 persons under 14 years per year in the US[[16]] to a much lower incidence of 0.17 per 100,000 persons under 18 years per year in Norway.[[4]] An Australian study could not determine the incidence but estimated the pre-vaccination prevalence of JRRP to have been between 0.6–1.1 per 100,000 persons under 20 years.[[3]]

There has been a reduction in the incidence of JRRP to 0.15 per 100,000 children per year in the most past 6 years. This decline compared to the pre-vaccination incidence remained non-significant (Table 2). Females who received their HPV vaccination in 2008 are now 26 years old and those eligible as part of the “catch-up” cohort are now 31 and 32 years old. The median age of first-time mothers has been between 29.9 and 30.5 years in New Zealand over the past decade,[[17]] therefore, many of the vaccinated women may not have borne children. As a greater number of vaccinated women become mothers, a further reduction in the incidence may be observed.[[15]] Additionally, the earlier cohorts included a heterogenous age group of 12- to 20-year-olds. As the effectiveness of the vaccine relies upon being vaccinated prior to sexual debut, a greater proportion of the earlier cohort may not be protected.

Australia reported a declining incidence from 0.16 per 100,000 children per year in 2012 to 0.02 in 2016.[[10]] The incidence rate in our cohort between 2016 and 2022 is comparable to the incidence rate in Australia a decade ago,[[10]] with more recent Australian results far lower than the SSH figures (Figure 2). Australia introduced a national HPV programme at a similar time to New Zealand.[[18]] At least half of Australia’s female population aged 12–26 years were fully vaccinated in the year of the vaccination programme being introduced in 2007.[[19]] The Australian vaccination rates at age 15 have been above 78% since 2015.[[18,19]] It had increased to over 80% in females and 78% in males in 2020.[[19]] The roll out and uptake of the vaccine has been slower in New Zealand[[8]] with between 60 to 67% of eligible females vaccinated in the birth cohorts up until 2003.[[20]] According to the Immunisation Advisory Centre, the rate for females increased to 69–70% in the 2007 and 2008 cohorts.[[21]] Data beyond the 2008 birth cohort are not available. The vaccine uptake rate for males in New Zealand has been modelled to be 53%.[[22]] A rate of 75% is considered necessary for “herd immunity”.[[7]] Our non-significant results may be due to this lower HPV vaccine coverage in our population.

Attitudes toward childhood vaccinations are becoming increasingly polarised in New Zealand.[[23]] There is a stigma around HPV being a sexually transmitted infection (STI).[[24]] The HPV vaccination programme brings together two demanding and confronting areas in promoting vaccination and sexual health.[[24]] Attempts to desexualise HPV vaccination failed overseas and high-profile public debate ensued with political, cultural and religious divide on the matter, which continues today.[[24]] Similar issues may have contributed to the low uptake of the HPV vaccination in New Zealand. Efforts are concentrated on improving coverage.[[7]]

Strengths of our study include the use of the International Classification of Disease code D14.1 (benign neoplasm of the larynx). This has been shown to be a very sensitive and specific ICD-10 code for identifying JRRP (PPV 98.1%).[[2]] We were able to obtain 100% feedback from referral centres and ORL departments around the country, which enabled more accurate estimates of the catchment population. Although a single-centre study, the referral population represents nearly half of the New Zealand population, which should provide a good proxy for the true incidence of JRRP in New Zealand. Limitations of the study include this being a single-centre study, the high number of patients that were excluded and the relatively low absolute numbers due to this being a rare disease.

A future study will be a national study with the aim to address these shortcomings. The establishment of a national database will allow continual monitoring of JRRP and provide more certainty about its incidence and disease patterns, which may in turn reduce the need of referrals to tertiary centres.

Conclusion

The mean incidence of JRRP before and after the introduction of HPV has remained unchanged in children treated at SSH. More recently, there has been a reduction in incidence—although this is based on small numbers. The low HPV vaccination rate (≤70%) may explain why a significant reduction in the incidence of JRRP seen overseas has not been observed in New Zealand. Ongoing surveillance and a national study would provide more insight into the true incidence and evolving trends.

Summary

Abstract

Aim

To review and compare the incidence of juvenile onset recurrent respiratory papillomatosis (JRRP) at Starship Children’s Hospital (SSH) before and after the introduction of a national HPV vaccination programme.

Method

Patients treated for JRRP at SSH were identified retrospectively using ICD-10 code D14.1 over a 14-year period. The incidence of JRRP in the 10-year period prior to the introduction of HPV vaccination (1 September 1998 to 31 August 2008) was compared with the incidence after its introduction. A second comparison was made between the pre-vaccination incidence with the incidence over the most recent 6 years when the vaccination became more widely available. All New Zealand hospital ORL departments that referred children with JRRP to SSH exclusively were included.

Results

SSH manages about half of the New Zealand paediatric population with JRRP. The incidence of JRRP before the introduction of the HPV vaccination programme was 0.21 per 100,000 per year in children 14 years of age and younger. This remained stable between 2008 and 2022 (0.23 vs 0.21 per 100,000 per year). The mean incidence in the later post-vaccination period was 0.15 per 100,000 per year based on small numbers.

Conclusion

The mean incidence of JRRP before and after the introduction of HPV has remained unchanged in children treated at SSH. More recently, a reduction in incidence has been noted, although this is based on small numbers. The low HPV vaccination rate (≤70%) may explain why a significant reduction in the incidence of JRRP seen overseas has not been observed in New Zealand. Ongoing surveillance and a national study would provide more insight into the true incidence and evolving trends.

Author Information

Dora Blair: ORL Registrar, Department of Paediatric Otorhinolaryngology, Starship Children’s Hospital, Auckland, New Zealand. Evelyn Lamble: House Officer, Department of Paediatric Otorhinolaryngology, Starship Children’s Hospital, Auckland, New Zealand. Graeme van der Meer: ORL Surgeon: Department of Paediatric Otorhinolaryngology, Starship Children’s Hospital, Auckland, New Zealand. Edward Toll: ORL Surgeon, Department of Paediatric Otorhinolaryngology, Starship Children’s Hospital, Auckland, New Zealand. Craig McCaffer: ORL Surgeon, Department of Paediatric Otorhinolaryngology, Starship Children’s Hospital, Auckland, New Zealand. Colin Barber: ORL Surgeon, Department of Paediatric Otorhinolaryngology, Starship Children’s Hospital, Auckland, New Zealand; Honorary Senior Lecturer, Department of Surgery, The University of Auckland, Auckland, New Zealand. Nikki Mills: ORL Surgeon, Department of Otorhinolaryngology, Nelson Hospital, New Zealand. Michel Neeff: ORL Surgeon, Department of Paediatric Otorhinolaryngology, Starship Children’s Hospital, Auckland, New Zealand; Senior Lecturer, Department of Surgery, The University of Auckland, Auckland, New Zealand.

Acknowledgements

We would like to thank Dr Dug Yeo Han, Clinical Research Biostatistician at Starship Research & Innovation and Dr Sandro Leite, ORL Surgeon and Honorary Senior Lecturer at The University of Auckland for their assistance in statistical analysis. In addition, we would also like to thank Professor Nikki Turner, Medical Director and Dr Anna Howe, Research and Policy Analyst at Immunisation Advisory Centre, New Zealand for their insight into HPV vaccination in New Zealand.

Correspondence

Dora Blair: ORL Registrar, Department of Paediatric Otorhinolaryngology, Starship Children’s Hospital, Auckland, New Zealand.

Correspondence Email

E: drdorablair@gmail.com

Competing Interests

Nil.

1)      Marsico M, Mehta V, Chastek B, et al. Estimating the incidenceand prevalence of juvenile-onset recurrent respiratory papillomatosis in publiclyand privately insured claims databases in the United States. Sex Transm Dis. 2014May 1;41(5):300-5. doi: 10.1097/OLQ.0000000000000115.

2)      Novakovic D, Cheng AT, Baguley K, et al. Juvenile recurrent respiratorypapillomatosis: 10‐year audit and Australian prevalence estimates. Laryngoscope.2016 Dec;126(12):2827-32. doi: 10.1002/lary.26005.

3)      Seedat RY. The incidence and prevalence of juvenile-onset recurrentrespiratory papillomatosis in the Free State province of South Africa and Lesotho.Int J Pediatr Otorhinolaryngol. 2014 Dec 1;78(12):2113-5. doi:10.1016/j.ijporl.2014.09.017.

4)      Omland T, Akre H, Vårdal M, Brøndbo K. Epidemiological aspectsof recurrent respiratory papillomatosis: a population‐based study. Laryngoscope.2012 Jul;122(7):1595-9. doi: 10.1002/lary.23327.

5)      LindebergH, Elbrønd O. Laryngeal papillomas: clinical aspects in a seriesof 231 patients. Clin Otolaryngol Allied Sci. 1989 Aug;14(4):333-42. doi:10.1111/j.1365-2273.1989.tb00381.x.

6)      Niyibizi J, Rodier C, Wassef M, Trottier H. Risk factors for thedevelopment and severity of juvenile-onset recurrent respiratory papillomatosis:a systematic review. Int J Pediatr Otorhinolaryngol. 2014 Feb 1;78(2):186-97. doi:10.1016/j.ijporl.2013.11.036.

7)      Best Practice Advocacy Centre New Zealand. HPV vaccination: gettingthe programme back on track [Internet]. 2019 Mar 29 [cited 2021 Apr 5].Available from: https://bpac.org.nz/2019/hpv.aspx.

8)      Manatū Hauora – Ministry of Health. History of the HPV immunsationprogramme [Internet].2014 Apr 9 [cited 2021 Jun 4]. Available from: https://www.health.govt.nz/our-work/preventative-health-wellness/immunisation/hpv-immunisation-programme/history-hpv-immunisation-programme.

9)      Gissmann L, Diehl V, Schultz-Coulon HJ, zur Hausen H. Molecularcloning and characterization of human papilloma virus DNA derived from a laryngealpapilloma. J Virol. 1982 Oct;44(1):393-400. doi: 10.1128/JVI.44.1.393-400.1982.

10)   Novakovic D, Cheng AT, Zurynski Y, et al. A Prospective Studyof the Incidence of Juvenile-Onset Recurrent Respiratory Papillomatosis AfterImplementation of a National HPV Vaccination Program. J Infect Dis. 2018 Jan 4;217(2):208-12.doi: 10.1093/infdis/jix498.

11)   Benedict JJ, Derkay CS. Recurrent respiratory papillomatosis:A 2020 perspective. Laryngoscope Investig Otolaryngol. 2021;6(2):340-5. doi:10.1002/lio2.545.

12)   Stats NZ – Tatauranga Aotearoa. Subnational population estimates(DHB, DHB constituency), by age and sex, at 30 June 1996-2022 (2015 boundaries)[Internet]. [cited 2022 Nov 12.] Available from: https://nzdotstat.stats.govt.nz/wbos/Index.aspx?DataSetCode=TABLECODE7509

13)   SAS Institute Inc. SAS software version 9.4 [software]. Cary,NC, USA.

14)   R Foundation for Statistical Computing. R: A language and environmentfor statistical computing [software].  Vienna,Austria; 2019. Available from: https://www.R-project.org/.

15)   Campisi P, Hawkes M, Simpson K; Canadian Juvenile Onset RecurrentRespiratory Papillomatosis Working Group. The epidemiology of juvenile onset recurrentrespiratory papillomatosis derived from a population level national database. Laryngoscope.2010 Jun;120(6):1233-45. doi: 10.1002/lary.20901.

16)   Derkay CS. Task force on recurrent respiratory papillomas: A preliminaryreport. Arch Otolaryngol Head Neck Surg. 1995 Dec;121(12):1386-91. doi:10.1001/archotol.1995.01890120044008.

17)   Stats NZ – Tatauranga Aotearoa. Parenting and fertility trendsin New Zealand: 2018 [Internet].2019 Oct 24 [cited 2022 Nov 20]. Available from: https://www.stats.govt.nz/reports/parenting-and-fertility-trends-in-new-zealand-2018.

18)   Brotherton JM, Liu B, Donovan B, et al. Human papillomavirus (HPV)vaccination coverage in young Australian women is higher than previously estimated:independent estimates from a nationally representative mobile phone survey. Vaccine.2014 Jan 23;32(5):592-7. doi: 10.1016/j.vaccine.2013.11.075.

19)   Australian Government – Department of Health and Aged Care. NationalHPV 3 dose vaccination coverage for all adolescents turning 15 years of age fromyear of program commencement [Internet]. 2019 Dec 4 [cited: 2022, Nov 20 2022].Available from:  https://www.health.gov.au/resources/publications/national-hpv-3-dose-vaccination-coverage-for-all-adolescents-turning-15-years-of-age-from-year-of-program-commencement.

20)   Manatū Hauora – Ministry of Health. HPV immunisation programme[Internet]. 2021 Aug 13 [cited 2022 Nov 20]. Available from: https://www.health.govt.nz/our-work/preventative-health-wellness/immunisation/hpv-immunisation-programme.

21)   Howe, A. Research and Policy Analyst at Immunisation AdvisoryCentre (IMAC), New Zealand. Email to: Dora Blair (ORL Registrar, Starship Children’sHospital) Re: HPV vaccination coverage. 2021, Nov 1.

22)   Smith MA, Hall M, Lew JB, Canfell K. Potential for HPV vaccinationand primary HPV screening to reduce cervical cancer disparities: Example from NewZealand. Vaccine. 2018 Oct 8;36(42):6314-24. doi:10.1016/j.vaccine.2018.08.063.

23)   Lee CH, Sibley CG. Attitudes toward vaccinations are becomingmore polarized in New Zealand: Findings from a longitudinal survey. EClinicalMedicine.2020 Jun;23:100387. doi: 10.1016/j.eclinm.2020.100387.

24)   Velan B, Yadgar Y. On the implications of desexualizing vaccinesagainst sexually transmitted diseases: health policy challenges in a multiculturalsociety. Isr J Health Policy Res. 2017 Dec;6(1):1-2.

Contact diana@nzma.org.nz
for the PDF of this article

View Article PDF

Juvenile onset recurrent respiratory papillomatosis (JRRP) is a rare and often chronic disease.[[1–4]] It is characterised by benign but potentially aggressive recurring laryngeal epithelial lesions[[5]] caused by the human papilloma virus (HPV), most likely by vertical transmission.[[6]] Being the first-born child with a maternal age younger than 20 years increases the risk.[[6]] Children can present with dysphonia, chronic coughing or with signs of compromised airways including stridor.[[5]] Multiple procedures to debulk the recurrent lesions to maintain voice and airway patency are often required. More severely affected patients may require a tracheostomy. Mortality has been reported.[[5]]

A quadrivalent vaccine which protects against HPV subtypes 6, 11, 16 and 18 was added to the national immunisation schedule for females aged 12 years in 2008.[[7]] Females up to the age of 20 were later eligible as part of a catch-up programme between 2009 to 2016.[[7]] A nonavalent vaccine replaced this in 2017, which also protects against subtypes 31, 33, 45, 52 and 58. At the same time the immunisation schedule was extended to include males and females aged 9 to 26 years.[[8]] This vaccination protects against high-risk HPV types responsible for cervical cancer, but also offers protection against HPV types 6 and 11, which cause the majority of JRRP.[[9]]

As the number of individuals protected against HPV increases, the incidence and prevalence of JRRP could be expected to decrease. There are few studies reviewing the incidence of JRRP following the introduction of an HPV vaccination programme.[[10]] In Australia, an estimated incidence of 0.16 per 100,000 per year declining to 0.02 per 100,000 per year after the introduction of the vaccine has been reported.[[10]] Preliminary data from the US and Canada show similar trends.[[11]] Trends in New Zealand are unknown.

Aim

To review and compare the incidence of JRRP at Starship Children’s Hospital (SSH) before and after the introduction of a national HPV vaccination programme.

Study design

This is a single-centre retrospective review of children managed for JRRP at SSH. Children aged up to and including 14 years were included. This age cut-off was chosen to align with census data. As the HPV vaccination was introduced on 1 September 2007, a study year is counted from 1 September to 31 August. It took 1 year for the first cohort of children to complete their vaccination. As a result, children treated between 1 September 1998 and 31 August 2008 (before vaccination) were compared with those diagnosed between 1 September 2008 and 31 August 2022 (after vaccination).

Children without histopathological confirmation of laryngeal papillomatosis were excluded.

All New Zealand hospitals with otolaryngology (ORL) departments were contacted regarding their referral patterns. ORL departments that referred children with JRRP to SSH exclusively were included. Children were excluded when SSH was not the exclusive referral hospital.

This study (AH22479) was approved by Auckland Health Research Ethics Committee (AHREC) on 14 May 2021.

Method

A retrospective review of the electronic clinical records was performed at Starship Children’s Hospital. Children were identified by searching for ICD-10 code D14.1 (benign lesions of the larynx).

A survey was emailed to all ORL departments’ clinical directors and/or paediatric otolaryngology leads in New Zealand. Follow-up emails and phone calls were made where additional information was required. All New Zealand hospital ORL departments that referred patients with JRRP to SSH exclusively were included.

Population data by age and district were extracted from Statistics New Zealand.[[12]] These data were interpolated to calculate the population at risk of JRRP between 1998 and 2022. All data were analysed using a generalised linear model, modelling the observed counts data as having a Poisson distribution. A p-value of <0.05 was considered statistically significant.

The mean of the incidence over the 10 years prior to the introduction of the HPV vaccination was compared with the mean of the incidence after its introduction. Further analysis was performed from 2016 when the vaccination programme was made more widely available. Statistical analyses were carried out using SAS 9.4 and R statistical program version 4.1.2.[[13,14]]

Results

The SSH paediatric ORL department received referrals from hospitals throughout the North Island and from one hospital in the South Island. All ORL departments contacted completed the survey.

A total of 31 children with JRRP treated at SSH were identified between 1 September 2008 and 31 August 2022. This included patients from our catchment in central Auckland, as well as hospitals that referred to SSH exclusively. These included Northland, Waitamatā, Counties Manukau, MidCentral, Whanganui and Bay of Plenty (Figure 1). Eight children were excluded as their primary hospitals did not refer JRRP patients to SSH exclusively. These include Lakes, Taranaki, Hawkes Bay, Tairāwhiti, Capital Coast, Hutt Valley, Wairarapa and Nelson.

The paediatric populations of the qualifying districts were included in the analysis (Figure 1). This included 44 to 49% of the total New Zealand population of children. The incidence over the study period is displayed in Figure 2.

View Figures 1–2 and Tables 1–2.

The mean incidence of JRRP prior to the introduction of the HPV vaccination was 0.21 per 100,000 children per year. There was no change after the introduction of the vaccination with a rate of 0.23 per 100,000 children per year observed (Table 1).

The mean incidence over the last 6 years (2017 to 2022) was 0.15 per 100,000 children per year. Compared to the baseline, there was a non-significant reduction by 0.06 per 100,000 children per year (p=0.56) (Table 2).

Discussion

The introduction of the HPV vaccine has not resulted in a significant reduction in the incidence of JRRP in New Zealand to date. Between 1998 and 2008, before the introduction of the HPV vaccine, the incidence of children with JRRP in the SSH catchment area was 0.21 per 100,000 children per year. This is comparable to the baseline incidence of 0.24 in Canada.[[15]] The reported incidence range varies from 4.3 per 100,000 persons under 14 years per year in the US[[16]] to a much lower incidence of 0.17 per 100,000 persons under 18 years per year in Norway.[[4]] An Australian study could not determine the incidence but estimated the pre-vaccination prevalence of JRRP to have been between 0.6–1.1 per 100,000 persons under 20 years.[[3]]

There has been a reduction in the incidence of JRRP to 0.15 per 100,000 children per year in the most past 6 years. This decline compared to the pre-vaccination incidence remained non-significant (Table 2). Females who received their HPV vaccination in 2008 are now 26 years old and those eligible as part of the “catch-up” cohort are now 31 and 32 years old. The median age of first-time mothers has been between 29.9 and 30.5 years in New Zealand over the past decade,[[17]] therefore, many of the vaccinated women may not have borne children. As a greater number of vaccinated women become mothers, a further reduction in the incidence may be observed.[[15]] Additionally, the earlier cohorts included a heterogenous age group of 12- to 20-year-olds. As the effectiveness of the vaccine relies upon being vaccinated prior to sexual debut, a greater proportion of the earlier cohort may not be protected.

Australia reported a declining incidence from 0.16 per 100,000 children per year in 2012 to 0.02 in 2016.[[10]] The incidence rate in our cohort between 2016 and 2022 is comparable to the incidence rate in Australia a decade ago,[[10]] with more recent Australian results far lower than the SSH figures (Figure 2). Australia introduced a national HPV programme at a similar time to New Zealand.[[18]] At least half of Australia’s female population aged 12–26 years were fully vaccinated in the year of the vaccination programme being introduced in 2007.[[19]] The Australian vaccination rates at age 15 have been above 78% since 2015.[[18,19]] It had increased to over 80% in females and 78% in males in 2020.[[19]] The roll out and uptake of the vaccine has been slower in New Zealand[[8]] with between 60 to 67% of eligible females vaccinated in the birth cohorts up until 2003.[[20]] According to the Immunisation Advisory Centre, the rate for females increased to 69–70% in the 2007 and 2008 cohorts.[[21]] Data beyond the 2008 birth cohort are not available. The vaccine uptake rate for males in New Zealand has been modelled to be 53%.[[22]] A rate of 75% is considered necessary for “herd immunity”.[[7]] Our non-significant results may be due to this lower HPV vaccine coverage in our population.

Attitudes toward childhood vaccinations are becoming increasingly polarised in New Zealand.[[23]] There is a stigma around HPV being a sexually transmitted infection (STI).[[24]] The HPV vaccination programme brings together two demanding and confronting areas in promoting vaccination and sexual health.[[24]] Attempts to desexualise HPV vaccination failed overseas and high-profile public debate ensued with political, cultural and religious divide on the matter, which continues today.[[24]] Similar issues may have contributed to the low uptake of the HPV vaccination in New Zealand. Efforts are concentrated on improving coverage.[[7]]

Strengths of our study include the use of the International Classification of Disease code D14.1 (benign neoplasm of the larynx). This has been shown to be a very sensitive and specific ICD-10 code for identifying JRRP (PPV 98.1%).[[2]] We were able to obtain 100% feedback from referral centres and ORL departments around the country, which enabled more accurate estimates of the catchment population. Although a single-centre study, the referral population represents nearly half of the New Zealand population, which should provide a good proxy for the true incidence of JRRP in New Zealand. Limitations of the study include this being a single-centre study, the high number of patients that were excluded and the relatively low absolute numbers due to this being a rare disease.

A future study will be a national study with the aim to address these shortcomings. The establishment of a national database will allow continual monitoring of JRRP and provide more certainty about its incidence and disease patterns, which may in turn reduce the need of referrals to tertiary centres.

Conclusion

The mean incidence of JRRP before and after the introduction of HPV has remained unchanged in children treated at SSH. More recently, there has been a reduction in incidence—although this is based on small numbers. The low HPV vaccination rate (≤70%) may explain why a significant reduction in the incidence of JRRP seen overseas has not been observed in New Zealand. Ongoing surveillance and a national study would provide more insight into the true incidence and evolving trends.

Summary

Abstract

Aim

To review and compare the incidence of juvenile onset recurrent respiratory papillomatosis (JRRP) at Starship Children’s Hospital (SSH) before and after the introduction of a national HPV vaccination programme.

Method

Patients treated for JRRP at SSH were identified retrospectively using ICD-10 code D14.1 over a 14-year period. The incidence of JRRP in the 10-year period prior to the introduction of HPV vaccination (1 September 1998 to 31 August 2008) was compared with the incidence after its introduction. A second comparison was made between the pre-vaccination incidence with the incidence over the most recent 6 years when the vaccination became more widely available. All New Zealand hospital ORL departments that referred children with JRRP to SSH exclusively were included.

Results

SSH manages about half of the New Zealand paediatric population with JRRP. The incidence of JRRP before the introduction of the HPV vaccination programme was 0.21 per 100,000 per year in children 14 years of age and younger. This remained stable between 2008 and 2022 (0.23 vs 0.21 per 100,000 per year). The mean incidence in the later post-vaccination period was 0.15 per 100,000 per year based on small numbers.

Conclusion

The mean incidence of JRRP before and after the introduction of HPV has remained unchanged in children treated at SSH. More recently, a reduction in incidence has been noted, although this is based on small numbers. The low HPV vaccination rate (≤70%) may explain why a significant reduction in the incidence of JRRP seen overseas has not been observed in New Zealand. Ongoing surveillance and a national study would provide more insight into the true incidence and evolving trends.

Author Information

Dora Blair: ORL Registrar, Department of Paediatric Otorhinolaryngology, Starship Children’s Hospital, Auckland, New Zealand. Evelyn Lamble: House Officer, Department of Paediatric Otorhinolaryngology, Starship Children’s Hospital, Auckland, New Zealand. Graeme van der Meer: ORL Surgeon: Department of Paediatric Otorhinolaryngology, Starship Children’s Hospital, Auckland, New Zealand. Edward Toll: ORL Surgeon, Department of Paediatric Otorhinolaryngology, Starship Children’s Hospital, Auckland, New Zealand. Craig McCaffer: ORL Surgeon, Department of Paediatric Otorhinolaryngology, Starship Children’s Hospital, Auckland, New Zealand. Colin Barber: ORL Surgeon, Department of Paediatric Otorhinolaryngology, Starship Children’s Hospital, Auckland, New Zealand; Honorary Senior Lecturer, Department of Surgery, The University of Auckland, Auckland, New Zealand. Nikki Mills: ORL Surgeon, Department of Otorhinolaryngology, Nelson Hospital, New Zealand. Michel Neeff: ORL Surgeon, Department of Paediatric Otorhinolaryngology, Starship Children’s Hospital, Auckland, New Zealand; Senior Lecturer, Department of Surgery, The University of Auckland, Auckland, New Zealand.

Acknowledgements

We would like to thank Dr Dug Yeo Han, Clinical Research Biostatistician at Starship Research & Innovation and Dr Sandro Leite, ORL Surgeon and Honorary Senior Lecturer at The University of Auckland for their assistance in statistical analysis. In addition, we would also like to thank Professor Nikki Turner, Medical Director and Dr Anna Howe, Research and Policy Analyst at Immunisation Advisory Centre, New Zealand for their insight into HPV vaccination in New Zealand.

Correspondence

Dora Blair: ORL Registrar, Department of Paediatric Otorhinolaryngology, Starship Children’s Hospital, Auckland, New Zealand.

Correspondence Email

E: drdorablair@gmail.com

Competing Interests

Nil.

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