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Across the world, the impact of the COVID-19 pandemic on access to cancer diagnosis and subsequent clinical services has been profound. In regions with widespread community transmission of the disease, this impact endured throughout 2020 and into 2021, and has resulted in a significant backlog of under-diagnosed and under-treated disease in these regions.[[1–6]]

In countries like New Zealand that have pursued an elimination approach to COVID-19, the impact has to date been less intense and shorter-lasting, largely concentrated to those times of national or regional lockdown.[[7–9]] Early in the pandemic, New Zealand’s national Cancer Control Agency, Te Aho o Te Kahu, engaged widely with clinicians, researchers and other stakeholders to plan the cancer-related response to the anticipated upheavals to usual healthcare provision caused by COVID-19. As noted elsewhere,[[10,11]] a focus on preventing exacerbation of inequity was a core element of this response, which included the ongoing monitoring of inequities in access to diagnosis, and partnership with Hei Āhuru Mōwai (National Māori Cancer Leadership Group) and other Māori researchers to develop an Equity Response Framework.[[10]] This framework aimed to identify the likely impact of the pandemic on existing inequities, and what actions could be taken to mitigate them. These actions, along with strong Māori-focused public health messaging from organisations such as Te Rōpū Whakakaupapa Urutā (the National Māori Pandemic Group), reduced the likelihood that the COVID-19 pandemic would have a differential impact on cancer diagnosis and treatment for Māori.

As part of ongoing monitoring across 2020, Te Aho o Te Kahu provided detailed analysis and reports and engaged with decision-makers to disseminate key findings. These reports outlined changes in cancer registration, diagnostic procedures and treatment (surgery, systemic therapy and radiation therapy).[[12–17]] These reports compared the occurrence of these events on a month-by-month basis across 2020 against the same period in 2018 and 2019, and presented results separately for the total population and for Māori. While the reduction in these events during the national lockdown of late March and April 2020 was dramatic—for example, cancer registrations dropped by more than 40% over this period compared to previous years[[16]]—these reports found little evidence of disparities in the magnitude of these downturns between Māori and non-Māori patients. In other words, it appeared that the pandemic had impacted access to diagnosis and treatment in much the same way for Māori as for the rest of the population.

The sole exception to this absence of disparity was found in the diagnosis and treatment of lung cancer—by far the most common cause of cancer death for Māori.[[18]] As noted in one of the reports, the number of lung cancer registrations, bronchoscopies and surgeries appeared to have dropped more substantially for Māori patients than the rest of the population.[[17]] Disparities in the pandemic’s impact on lung cancer registrations among Māori compared to the rest of the population is particularly concerning, since it may indicate that Māori patients with symptoms of lung cancer are experiencing greater delays to diagnosis than non-Māori patients, with subsequent ramifications on quality of life and survival.

However, because data were only available up until the end of October for the Te Aho o Te Kahu report,[[17]] and since that report only presented absolute numbers of cases compared to previous years, two key factors remain unclear: 1) whether disparities in the downturn of registrations (and related procedures) continued for the remainder of 2020, or were “correcting” toward the end of the year; and 2) whether expressing the numbers of events relative to their underlying ethnic-specific population, as well as adjusting rates for differences between Māori and non-Māori in terms of age, will impact our understanding of what happened regarding this disparity. In addition, it remains unclear whether delays to diagnosis during 2020 have resulted in an overall shift in the distribution of disease stage at diagnosis, and whether these changes have inequitably impacted Māori patients.

In this article, we examine age-standardised lung cancer registrations, diagnostic procedures (bronchoscopy) and surgical treatment separately by ethnic group for the years 2018–2020, and we express the number of these events relative to their ethnic-specific underlying population. We also examine patterns of stage of diagnosis by ethnic groups across these years, in order to assess whether the COVID-19 pandemic has resulted in a shift in stage distribution for Māori (and/or non-Māori) patients with lung cancer. We have focussed our comparisons to Māori and non-Māori/non-Pacific populations, to ensure adequate numbers of patients in our month-on-month stratified analyses.

Methods

Participants and data sources

Numerators

This study included three participant cohorts. Firstly, when assessing the impact of COVID-19 on lung cancer registrations, we extracted all those who were diagnosed with lung cancer (ICD code C34) on the New Zealand Cancer Registry (NZCR) between 1 January 2018 to 31 December 2020 (N = 6,679; 1,497 Māori, 5,182 non-Māori/non-Pacific). Secondly, when assessing the impact on access to bronchoscopy, we extracted data for all New Zealanders (irrespective of subsequent lung cancer status) who underwent a bronchoscopy over this same period from the National Non-Admitted Patient Collection (NNPAC; purchase unit code MS02003; N = 7,281; 1,143 Māori, 6,138 non-Māori/non-Pacific). Thirdly, when assessing the impact on lung cancer surgery, we extracted data for all New Zealanders who underwent a publicly-funded lung resection as an inpatient, and who had a diagnosis of cancer on the same admission, from the National Minimum Dataset (NMDS; see Appendix 1  for procedures and ICD codes; N = 1,030; 168 Māori, 862 non-Māori/non-Pacific).

Denominators

When describing rates of lung cancer registration, bronchoscopy and surgery, we used the ethnicity-stratified total estimated residential population of New Zealand for each of 2018, 2019 and 2020 as the denominator, with this data derived from Stats NZ.[[19]] When describing the distribution of stage of disease at diagnosis, we used the total number of patients diagnosed with lung cancer on the NZCR as the denominator.

Variables

For the purposes of age standardisation, patient age at either the time of diagnosis (in the case of lung cancer registration) or procedure (in the case of bronchoscopy and lung surgery) was defined using their date of birth and the data of diagnosis or procedure, respectively. Age was categorised as <50 years, 50–64, 65–74, and 75+. Patient ethnicity (Māori, Pacific or non-Māori/non-Pacific) was defined using prioritised ethnicity, as recorded on the NZCR (for registration), NNPAC (for bronchoscopy) or NMDS (for surgery). To prevent misinterpretation of data due to low numbers of diagnoses and procedures, Pacific data were not analysed for this manuscript. Month and year of diagnosis or procedure were derived from the date of diagnosis or procedure from each respective dataset. Stage of disease was extracted for each lung cancer registration from the NZCR, and was defined according to the SEER staging system (Local, Regional, Advanced and Unstaged).

Statistical analysis

For our descriptive analysis, we described the number and rate of lung cancer registration, bronchoscopy and lung surgery. Crude and age-standardised rates were described per 100,000 Māori or non-Māori/non-Pacific New Zealanders, using the denominator data derived from Stats NZ. To adjust for differences between Māori and non-Māori/non-Pacific peoples in terms of population age structure, we used direct standardisation techniques to describe age-adjusted rates of diagnosis or procedure, using the 2001 Māori Census population as the standard population.[[20, 21]] When describing the distribution of stage at diagnosis, we expressed the number of diagnoses within each respective stage (Local, Regional, Advanced, Unstaged) as a proportion (%) of the total number of all combined stages, separately for each year and for Māori and non-Māori/non-Pacific patients. In terms of ensuring the study’s responsiveness to Māori, this study was led by a Māori epidemiologist (JG), supported by Māori public servants, academics and clinicians (MM, MR, SC, GL).

Results

Cancer registrations

The cumulative age-standardised rate of lung cancer registrations is shown in Figure 1, stratified by year and ethnicity, with full tabulated data including confidence limits shown in Appendix 2. The rate of lung cancer registrations trended toward being lower in 2020 compared to the previous two years for Māori, but not for non-Māori/non-Pacific peoples. For Māori the cumulative registration rate in 2020 had increased by December to draw close to that observed by the end of 2019, although this may reflect a general downturn between September–December 2019 relative to the same period in 2018. Rates of lung cancer registration for non-Māori/non-Pacific peoples were indiscernible between 2018–2020.

Figure 1: Cumulative age-standardised rate of lung cancer registrations by month and year (2018–2020) per 100,000 New Zealanders, for Māori (left) and non-Māori/non-Pacific (right).

The distribution of stage at diagnosis among lung cancer registrations between 2018–2020 is shown in Figure 2, separately for Māori and non-Māori/non-Pacific patients. For Māori, there was no clear change in stage distribution over the three-year period: the proportion of advanced cancers remained at 47% each year, while the proportion of Unstaged cancers ranged between 29–33% across the three years. Variation between years was somewhat greater for non-Māori/non-Pacific patients, although the stage distribution remained broadly similar across the three-year period.

Figure 2: Stacked bar chart showing the crude distribution of local, regional, advanced and unstaged lung cancer on the New Zealand Cancer Registry, by year (2018–2020), separately for Māori and non-Māori/non-Pacific patients.

Bronchoscopy

The cumulative age-standardised rate of bronchoscopies is shown in Figure 3, stratified by year and ethnicity, with full tabulated data including confidence limits shown in Appendix 3. The bronchoscopy rate trended toward being lower in 2020 compared to the previous two years for both Māori and non-Māori/non-Pacific peoples, with an abrupt decline occurring between March and April of 2020 (coinciding with the onset of the first national lockdown in New Zealand). The cumulative bronchoscopy rate remained substantially below that observed in previous years by the end of 2020, particularly so for Māori.

Figure 3: Cumulative age-standardised rate of bronchoscopy by month and year (2018–2020) per 100,000 New Zealanders, for Māori (left) and non-Māori/non-Pacific (right).

Access to lung surgery

The cumulative age-standardised rate of lung surgery is shown in Figure 4, stratified by year and ethnicity, with full tabulated data including confidence limits shown in Appendix 4. For Māori patients, rates of lung surgery trended toward being lower from July of 2020 compared to the same period from previous two years, although this was based on low numbers of procedures and should therefore be interpreted with caution. Rates of lung cancer surgery for non-Māori/non-Pacific peoples were indiscernible between 2018–2020.

Figure 4: Cumulative age-standardised rate of lung surgery by month and year (2018-2020) per 100,000 New Zealanders, for Māori (left) and non-Māori/non-Pacific (right).

Discussion

Beginning in March 2020, there was a trend toward a downturn in the rate of lung cancer registration for Māori (but not non-Māori/non-Pacific) New Zealanders compared to previous years —although the cumulative rate of registration for Māori appeared to be returning to 2019 levels by the end of 2020. There was no apparent shift in the distribution of stage at diagnosis across the three-year period. Rates of bronchoscopy abruptly dropped for both Māori and non-Māori/non-Pacific patients in 2020 relative to previous years (but to a greater extent for Māori), while rates of lung cancer surgery appeared somewhat lower in 2020 for Māori patients, although this was based on a small number of procedures and thus should be interpreted with caution.

What do these findings mean?

Cancer registrations in general decreased during the early phases of the COVID-19 pandemic when there were national lock downs both in New Zealand and internationally. A downturn in lung cancer registrations might be an expected consequence of the COVID-19 pandemic for the following reasons. Firstly, because of the strong public health messaging which advised people to remain home if feeling unwell, it is likely that some patients who may have otherwise sought care for their symptoms were dissuaded from doing so. Secondly, given the overlap between COVID-19 and lung cancer in common presenting respiratory symptoms, it is plausible that among those who sought care the symptoms of their lung cancer were either not differentiable from symptoms of COVID-19, or a diagnostic bias towards excluding COVID-19 resulted in limited consideration of other causes for their symptoms—with both of these impacting on clinical work-up and subsequent delays to lung cancer diagnosis. Similarly, it is plausible that the reduction in the incidence of seasonal respiratory conditions such as influenza [[22]] resulted in fewer opportunistic diagnoses of lung cancer among those with respiratory symptoms. Thirdly, the disruptions caused to normal clinical pathways by the pandemic and associated national and regional lockdowns likely impacted access to diagnostic services—including likely difficulties in obtaining community-based tests such as chest x-rays. We noted earlier that there was an abrupt downturn in the rate of bronchoscopy for both Māori and non-Māori/non-Pacific patients from April 2020 compared to previous years, due to a purposeful reduction in bronchoscopy services during the early stages of the COVID-19 pandemic. Unlike lung cancer registrations, we may not expect the cumulative rate of bronchoscopy to “catch-up” with that observed in previous years, since it is possible that in early 2020 other forms of investigation (such as CT-guided biopsy) may have been preferred to bronchoscopy, in order to reduce potential aerosolisation of the SARS-CoV-2 virus.[[23–27]]

In order to drive the differential impact of COVID-19 on lung cancer diagnosis observed in this study, one or more of the above factors must have acted differently for Māori than they did for non-Māori/non-Pacific peoples. In other words, it is possible that Māori with symptoms of lung cancer were more likely to heed public health advice to remain in-place in spite of symptoms, whether out of hesitancy around the virus and/or a sense of duty to their community; and/or more likely to have their symptoms not differentiable for COVID-19; and/or less likely to gain access to diagnostic services to assist in the diagnosis of their lung cancer. The first two of these factors require further investigation with more granular data than were available for this study: for example, it would be valuable to learn the extent to which patients diagnosed with lung cancer during the national or regional lockdowns of 2020 delayed seeking care, and/or sought care but investigations were delayed, for their early symptoms due to COVID-related barriers;[[28, 29]] how this compares to patients diagnosed post-lockdowns; and how this experience differs for Māori compared to other ethnic groups.

In terms of access to diagnostic services, it does appear that the cumulative rate of bronchoscopy was somewhat more severely impacted for Māori than it was for non-Māori/non-Pacific peoples (Figure 3), with this reduced access potentially contributing to the differential impact on lung cancer registrations. Such an observation must be interpreted alongside the healthcare access-related factors discussed above. In addition, it is important to bear in mind that the data reported in this study refers to all bronchoscopies performed in the general population, which was likely impacted by reductions in seasonal respiratory illness due to the 2020 lockdowns—which means that it is not straightforward to presume that differential cumulative reductions for Māori correspond to differential access for Māori with symptoms of lung cancer. In terms of future research, it would be useful to view these bronchoscopy data alongside data on CT-guided lung biopsy access during the national and regional lockdowns, and to compare this access between Māori and non-Māori/non-Pacific peoples. Currently these data are not readily available at a national level, but may be reviewed within regions with granular data around lung cancer management (see below).

Related to diagnostic service access is the pathway by which patients enter the cancer care system. We noted in a recent report that the number and proportion of lung cancers referred through the Faster Cancer Treatment (FCT) pathway seemed to be unaffected by the COVID-19 pandemic, for both Māori and non-Māori.[[17]] The FCT pathway provides monitoring for patients referred with a high risk of cancer, with targets related to timing of first treatment. Around half of Māori lung cancer patients nationwide go through the FCT pathway,[[17]] although this proportion varies by region.[[30]]  The fact this pathway was unaffected might suggest that Māori patients who were not diagnosed or had their diagnosis delayed due to the pandemic would likely have entered via other pathways such as emergency rooms and incidental findings during hospital admissions.[[17]] A review of lung cancer registrations between 2015–2018 found that Māori patients were more likely to be diagnosed through emergency presentation than non-Māori patients.[[31]] During COVID-related lockdowns, emergency room use was substantially impacted, which may be a factor in creating greater delays to lung cancer registrations for Māori than it would for other ethnic groups.[[31]] The same rationale exists for inpatient diagnoses: it is plausible that Māori—who are more likely to be hospitalised than non-Māori [[32]]—are more likely to have their lung cancer diagnosed in an inpatient setting (possibly incidentally when hospitalised for another condition), and if COVID-19 reduced access to inpatient care, then this would differentially impact lung cancer registrations for Māori. The extent of incidental diagnosis (particularly for Māori) remains unknown in New Zealand, but international evidence suggests that 9–40% of lung cancers are diagnosed in this way [[33,34]]—reinforcing the potential importance of this pathway (particularly for Māori).

There was no apparent shift in the distribution of stage at diagnosis across the three years, for either Māori or non-Māori/non-Pacific patients. Crucially, the proportion of advanced (i.e., metastasised) diagnoses remained relatively stable over this period (particularly for Māori patients), suggesting that, at least by the end of 2020, the downturn in lung cancer registrations for Māori patients does not appear to have led to an increase in the relative proportion of metastasised disease. However, there are two caveats to this observation: firstly, the high proportion of unstaged lung cancer registrations on the NZCR means that the actual proportion of advanced diagnoses is likely to be higher than that observed in this study, although the relative difference between years (and ethnicities) is still likely to be accurate.[[35]] Future analyses could include datasets such as the Midland and Northern regional registers, which include more granular (and complete) staging information.[[36]] Secondly, it may be that we do not yet have sufficient data to fully capture the impact of the 2020 downturn in lung cancer registrations on stage distribution for Māori; in other words, such an impact may only become clear once full data are available for multiple years following the onset of the pandemic.

Why just lung cancer?

As noted in the introduction, there has been little evidence that the disturbances to cancer diagnoses caused by the COVID-19 pandemic have differentially impacted Māori, with the exception of lung cancer. As such, it would seem likely that the factors driving the disparity in the downturn of lung cancer registrations for Māori are likely to be unique to lung cancer, rather than applicable to other contexts.

Firstly, it is also important to note that bronchoscopy has the capacity to substantially increase the risk of SARS-CoV-2 spread between patients and clinicians. This, possibly combined with the impact of reductions in bronchoscopy due to reductions in seasonal respiratory illnesses, resulted in stark reductions in its use—reductions which appear to have been at least somewhat worse for Māori. Secondly, as noted above, the pathway toward lung cancer diagnosis is not necessarily the same for Māori patients as it is for non-Māori/non-Pacific patients, and which might have led to fewer Māori registrations over 2020. While the latter factor might also apply to other cancer contexts (e.g., colorectal cancer, where Māori patients are more likely to be diagnosed following emergency presentation than non-Māori patients),[[37]] perhaps it is the combination of all three factors which ultimately drove the observed differential impact of COVID-19 on lung cancer registrations.

What have we learned?

There are three key lessons to be drawn from our observations of the impact of COVID-19 on lung cancer registrations and treatment. Firstly, the likelihood that the pathway to diagnosis and treatment may differ between Māori and non-Māori/non-Pacific patients means that we need to understand more about the pathways outside of the Faster Cancer Treatment pathway and their associated barriers. The absence of changes in diagnoses through the Faster Cancer Treatment pathway for Māori (and non-Māori) suggests that these other pathways (including emergency presentation and inpatient, incidental diagnoses) may be where the majority of inequities in the lung cancer pathway occur—not just in the context of COVID-19. These inequities reflect implicit bias within the healthcare system, wherein the system is more accessible for non-Māori patients than it is for Māori patients.[[38]]

Secondly, our observations in all other cancer contexts illustrates that it is not necessarily inevitable that a significant health event such as the COVID-19 pandemic will lead to the exacerbation of health inequities; rather, these can be avoided by deliberate prioritisation of the equitable provision of healthcare within the population, and in particular the preferential allocation of time and resources toward protecting the health of Māori.

Finally, in light of recent evidence suggesting that primary care communication and national messaging may have diverted attention away from other health conditions,[[28,29]] there is need for more deliberate focus at a national and regional level on timely access to non-COVID-19 related healthcare. In the context of lung cancer, this focus could be first directed toward high-risk groups (such as Māori smokers and ex-smokers).

Strengths and limitations

The data used in the current study includes all lung cancer registrations reported the New Zealand Cancer Registry (NZCR) over the follow-up period, ensuring national generalisability. We note that we purposefully did not conduct statistical tests on the data, since we note that tests (such as a Cochran-Mantel-Haenszel test for trend) would only tell us if something was different between years, but provide little additional information with which to interpret the data. We also note that, in recent years, there has been renewed emphasis on departing from a reliance on statistical tests and p-values when interpreting differences between groups.[[39]]

Conclusions

Using national-level data, we observed a downturn in the rate of lung cancer registration for Māori (but not non-Māori/non-Pacific) New Zealanders in 2020 compared to 2018 and 2019. There was no apparent shift in the distribution of stage at diagnosis across the three-year period. Rates of bronchoscopy abruptly dropped for both Māori and non-Māori/non-Pacific patients in 2020 relative to previous years, with this drop appearing to be greatest for Māori. Rates of lung cancer surgery appeared somewhat lower in 2020 for Māori patients, although this was based on a small number of procedures. While other cancer contexts have illustrated that the impact of COVID-19 on access to and through cancer services does not necessarily need to occur inequitably between Māori and non-Māori patients, disparities observed in the lung cancer context suggest that a) we need to ensure that Māori with respiratory symptoms receive best practice care for their symptoms, and b) we need to better quantify and monitor the pathways by which Māori patients with symptoms of lung cancer are entering the healthcare system.

View Appendices.

Summary

Abstract

Aim

The purpose of this article is to examine disparities in the impact of the COVID-19 pandemic on access to lung cancer diagnosis and access to clinical services between Māori and non-Māori.

Method

Using national-level data, we examined age-standardised lung cancer registrations, diagnostic procedures (bronchoscopy) and lung surgeries separately by ethnic group for the years 2018–2020, as well as patterns of stage of diagnosis.

Results

We found a trend toward a reduction in rates of lung cancer registration in Māori (but not non-Māori/non-Pacific) New Zealanders in 2020 compared to 2018 and 2019, but no apparent shift in the distribution of stage at diagnosis. We found a trend toward a reduction in rates of bronchoscopy for both Māori and non-Māori/non-Pacific patients, with the largest reduction observed for Māori. Rates of lung cancer surgery appeared to have reduced for Māori patients, although this was based on a small number of procedures.

Conclusion

We observed disparities between Māori and non-Māori/non-Pacific patients in lung cancer registration and bronchoscopy as a result of the COVID-19 pandemic.

Author Information

Jason K Gurney: Te Aho o Te Kahu – Cancer Control Agency, Wellington, New Zealand; Department of Public Health, University of Otago, Wellington, New Zealand. Alex Dunn: Te Aho o Te Kahu – Cancer Control Agency, Wellington, New Zealand. Michelle Liu: Te Aho o Te Kahu – Cancer Control Agency, Wellington, New Zealand. Michelle Mako: Te Aho o Te Kahu – Cancer Control Agency, Wellington, New Zealand. Elinor Millar: Te Aho o Te Kahu – Cancer Control Agency, Wellington, New Zealand. Myra Ruka: Te Aho o Te Kahu – Cancer Control Agency, Wellington, New Zealand. Sue Crengle: Department of Preventive and Social Medicine, University of Otago, Dunedin, New Zealand Paul Dawkins: Counties-Manukau District Health Board, Auckland, New Zealand. Christopher Jackson: Southern District Health Board, Dunedin, New Zealand; Department of Medicine, University of Otago, Dunedin, New Zealand. George Laking: Auckland District Health Board, Auckland, New Zealand; Northland District Health Board, Whangārei, New Zealand. Diana Sarfati: Te Aho o Te Kahu – Cancer Control Agency, Wellington, New Zealand.

Acknowledgements

We would like to thank Vahid Arabneiad from the Te Aho o Te Kahu Data Monitoring and Reporting team for the rapid provision of data for this study. This work was funded by Te Aho o Te Kahu – Cancer Control Agency.

Correspondence

Jason K Gurney: Department of Public Health, University of Otago, Wellington, New Zealand, PO Box 7343, Wellington, New Zealand. +64 21 279 3597

Correspondence Email

jason.gurney@otago.ac.nz

Competing Interests

Nil.

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33) Kocher F, Lunger F, Seeber A, Amann A, Pircher A, Hilbe W, Fiegl M. Incidental Diagnosis of Asymptomatic Non-Small-Cell Lung Cancer: A Registry-Based Analysis. Clinical lung cancer. 2016;17(1):62-7.e1.

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35) Gurney J, Stanley J, Jackson C, Sarfati D. Stage at diagnosis for Maori cancer patients: disparities, similarities and data limitations. New Zealand Medical Journal. 2020;133:43-64.

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Across the world, the impact of the COVID-19 pandemic on access to cancer diagnosis and subsequent clinical services has been profound. In regions with widespread community transmission of the disease, this impact endured throughout 2020 and into 2021, and has resulted in a significant backlog of under-diagnosed and under-treated disease in these regions.[[1–6]]

In countries like New Zealand that have pursued an elimination approach to COVID-19, the impact has to date been less intense and shorter-lasting, largely concentrated to those times of national or regional lockdown.[[7–9]] Early in the pandemic, New Zealand’s national Cancer Control Agency, Te Aho o Te Kahu, engaged widely with clinicians, researchers and other stakeholders to plan the cancer-related response to the anticipated upheavals to usual healthcare provision caused by COVID-19. As noted elsewhere,[[10,11]] a focus on preventing exacerbation of inequity was a core element of this response, which included the ongoing monitoring of inequities in access to diagnosis, and partnership with Hei Āhuru Mōwai (National Māori Cancer Leadership Group) and other Māori researchers to develop an Equity Response Framework.[[10]] This framework aimed to identify the likely impact of the pandemic on existing inequities, and what actions could be taken to mitigate them. These actions, along with strong Māori-focused public health messaging from organisations such as Te Rōpū Whakakaupapa Urutā (the National Māori Pandemic Group), reduced the likelihood that the COVID-19 pandemic would have a differential impact on cancer diagnosis and treatment for Māori.

As part of ongoing monitoring across 2020, Te Aho o Te Kahu provided detailed analysis and reports and engaged with decision-makers to disseminate key findings. These reports outlined changes in cancer registration, diagnostic procedures and treatment (surgery, systemic therapy and radiation therapy).[[12–17]] These reports compared the occurrence of these events on a month-by-month basis across 2020 against the same period in 2018 and 2019, and presented results separately for the total population and for Māori. While the reduction in these events during the national lockdown of late March and April 2020 was dramatic—for example, cancer registrations dropped by more than 40% over this period compared to previous years[[16]]—these reports found little evidence of disparities in the magnitude of these downturns between Māori and non-Māori patients. In other words, it appeared that the pandemic had impacted access to diagnosis and treatment in much the same way for Māori as for the rest of the population.

The sole exception to this absence of disparity was found in the diagnosis and treatment of lung cancer—by far the most common cause of cancer death for Māori.[[18]] As noted in one of the reports, the number of lung cancer registrations, bronchoscopies and surgeries appeared to have dropped more substantially for Māori patients than the rest of the population.[[17]] Disparities in the pandemic’s impact on lung cancer registrations among Māori compared to the rest of the population is particularly concerning, since it may indicate that Māori patients with symptoms of lung cancer are experiencing greater delays to diagnosis than non-Māori patients, with subsequent ramifications on quality of life and survival.

However, because data were only available up until the end of October for the Te Aho o Te Kahu report,[[17]] and since that report only presented absolute numbers of cases compared to previous years, two key factors remain unclear: 1) whether disparities in the downturn of registrations (and related procedures) continued for the remainder of 2020, or were “correcting” toward the end of the year; and 2) whether expressing the numbers of events relative to their underlying ethnic-specific population, as well as adjusting rates for differences between Māori and non-Māori in terms of age, will impact our understanding of what happened regarding this disparity. In addition, it remains unclear whether delays to diagnosis during 2020 have resulted in an overall shift in the distribution of disease stage at diagnosis, and whether these changes have inequitably impacted Māori patients.

In this article, we examine age-standardised lung cancer registrations, diagnostic procedures (bronchoscopy) and surgical treatment separately by ethnic group for the years 2018–2020, and we express the number of these events relative to their ethnic-specific underlying population. We also examine patterns of stage of diagnosis by ethnic groups across these years, in order to assess whether the COVID-19 pandemic has resulted in a shift in stage distribution for Māori (and/or non-Māori) patients with lung cancer. We have focussed our comparisons to Māori and non-Māori/non-Pacific populations, to ensure adequate numbers of patients in our month-on-month stratified analyses.

Methods

Participants and data sources

Numerators

This study included three participant cohorts. Firstly, when assessing the impact of COVID-19 on lung cancer registrations, we extracted all those who were diagnosed with lung cancer (ICD code C34) on the New Zealand Cancer Registry (NZCR) between 1 January 2018 to 31 December 2020 (N = 6,679; 1,497 Māori, 5,182 non-Māori/non-Pacific). Secondly, when assessing the impact on access to bronchoscopy, we extracted data for all New Zealanders (irrespective of subsequent lung cancer status) who underwent a bronchoscopy over this same period from the National Non-Admitted Patient Collection (NNPAC; purchase unit code MS02003; N = 7,281; 1,143 Māori, 6,138 non-Māori/non-Pacific). Thirdly, when assessing the impact on lung cancer surgery, we extracted data for all New Zealanders who underwent a publicly-funded lung resection as an inpatient, and who had a diagnosis of cancer on the same admission, from the National Minimum Dataset (NMDS; see Appendix 1  for procedures and ICD codes; N = 1,030; 168 Māori, 862 non-Māori/non-Pacific).

Denominators

When describing rates of lung cancer registration, bronchoscopy and surgery, we used the ethnicity-stratified total estimated residential population of New Zealand for each of 2018, 2019 and 2020 as the denominator, with this data derived from Stats NZ.[[19]] When describing the distribution of stage of disease at diagnosis, we used the total number of patients diagnosed with lung cancer on the NZCR as the denominator.

Variables

For the purposes of age standardisation, patient age at either the time of diagnosis (in the case of lung cancer registration) or procedure (in the case of bronchoscopy and lung surgery) was defined using their date of birth and the data of diagnosis or procedure, respectively. Age was categorised as <50 years, 50–64, 65–74, and 75+. Patient ethnicity (Māori, Pacific or non-Māori/non-Pacific) was defined using prioritised ethnicity, as recorded on the NZCR (for registration), NNPAC (for bronchoscopy) or NMDS (for surgery). To prevent misinterpretation of data due to low numbers of diagnoses and procedures, Pacific data were not analysed for this manuscript. Month and year of diagnosis or procedure were derived from the date of diagnosis or procedure from each respective dataset. Stage of disease was extracted for each lung cancer registration from the NZCR, and was defined according to the SEER staging system (Local, Regional, Advanced and Unstaged).

Statistical analysis

For our descriptive analysis, we described the number and rate of lung cancer registration, bronchoscopy and lung surgery. Crude and age-standardised rates were described per 100,000 Māori or non-Māori/non-Pacific New Zealanders, using the denominator data derived from Stats NZ. To adjust for differences between Māori and non-Māori/non-Pacific peoples in terms of population age structure, we used direct standardisation techniques to describe age-adjusted rates of diagnosis or procedure, using the 2001 Māori Census population as the standard population.[[20, 21]] When describing the distribution of stage at diagnosis, we expressed the number of diagnoses within each respective stage (Local, Regional, Advanced, Unstaged) as a proportion (%) of the total number of all combined stages, separately for each year and for Māori and non-Māori/non-Pacific patients. In terms of ensuring the study’s responsiveness to Māori, this study was led by a Māori epidemiologist (JG), supported by Māori public servants, academics and clinicians (MM, MR, SC, GL).

Results

Cancer registrations

The cumulative age-standardised rate of lung cancer registrations is shown in Figure 1, stratified by year and ethnicity, with full tabulated data including confidence limits shown in Appendix 2. The rate of lung cancer registrations trended toward being lower in 2020 compared to the previous two years for Māori, but not for non-Māori/non-Pacific peoples. For Māori the cumulative registration rate in 2020 had increased by December to draw close to that observed by the end of 2019, although this may reflect a general downturn between September–December 2019 relative to the same period in 2018. Rates of lung cancer registration for non-Māori/non-Pacific peoples were indiscernible between 2018–2020.

Figure 1: Cumulative age-standardised rate of lung cancer registrations by month and year (2018–2020) per 100,000 New Zealanders, for Māori (left) and non-Māori/non-Pacific (right).

The distribution of stage at diagnosis among lung cancer registrations between 2018–2020 is shown in Figure 2, separately for Māori and non-Māori/non-Pacific patients. For Māori, there was no clear change in stage distribution over the three-year period: the proportion of advanced cancers remained at 47% each year, while the proportion of Unstaged cancers ranged between 29–33% across the three years. Variation between years was somewhat greater for non-Māori/non-Pacific patients, although the stage distribution remained broadly similar across the three-year period.

Figure 2: Stacked bar chart showing the crude distribution of local, regional, advanced and unstaged lung cancer on the New Zealand Cancer Registry, by year (2018–2020), separately for Māori and non-Māori/non-Pacific patients.

Bronchoscopy

The cumulative age-standardised rate of bronchoscopies is shown in Figure 3, stratified by year and ethnicity, with full tabulated data including confidence limits shown in Appendix 3. The bronchoscopy rate trended toward being lower in 2020 compared to the previous two years for both Māori and non-Māori/non-Pacific peoples, with an abrupt decline occurring between March and April of 2020 (coinciding with the onset of the first national lockdown in New Zealand). The cumulative bronchoscopy rate remained substantially below that observed in previous years by the end of 2020, particularly so for Māori.

Figure 3: Cumulative age-standardised rate of bronchoscopy by month and year (2018–2020) per 100,000 New Zealanders, for Māori (left) and non-Māori/non-Pacific (right).

Access to lung surgery

The cumulative age-standardised rate of lung surgery is shown in Figure 4, stratified by year and ethnicity, with full tabulated data including confidence limits shown in Appendix 4. For Māori patients, rates of lung surgery trended toward being lower from July of 2020 compared to the same period from previous two years, although this was based on low numbers of procedures and should therefore be interpreted with caution. Rates of lung cancer surgery for non-Māori/non-Pacific peoples were indiscernible between 2018–2020.

Figure 4: Cumulative age-standardised rate of lung surgery by month and year (2018-2020) per 100,000 New Zealanders, for Māori (left) and non-Māori/non-Pacific (right).

Discussion

Beginning in March 2020, there was a trend toward a downturn in the rate of lung cancer registration for Māori (but not non-Māori/non-Pacific) New Zealanders compared to previous years —although the cumulative rate of registration for Māori appeared to be returning to 2019 levels by the end of 2020. There was no apparent shift in the distribution of stage at diagnosis across the three-year period. Rates of bronchoscopy abruptly dropped for both Māori and non-Māori/non-Pacific patients in 2020 relative to previous years (but to a greater extent for Māori), while rates of lung cancer surgery appeared somewhat lower in 2020 for Māori patients, although this was based on a small number of procedures and thus should be interpreted with caution.

What do these findings mean?

Cancer registrations in general decreased during the early phases of the COVID-19 pandemic when there were national lock downs both in New Zealand and internationally. A downturn in lung cancer registrations might be an expected consequence of the COVID-19 pandemic for the following reasons. Firstly, because of the strong public health messaging which advised people to remain home if feeling unwell, it is likely that some patients who may have otherwise sought care for their symptoms were dissuaded from doing so. Secondly, given the overlap between COVID-19 and lung cancer in common presenting respiratory symptoms, it is plausible that among those who sought care the symptoms of their lung cancer were either not differentiable from symptoms of COVID-19, or a diagnostic bias towards excluding COVID-19 resulted in limited consideration of other causes for their symptoms—with both of these impacting on clinical work-up and subsequent delays to lung cancer diagnosis. Similarly, it is plausible that the reduction in the incidence of seasonal respiratory conditions such as influenza [[22]] resulted in fewer opportunistic diagnoses of lung cancer among those with respiratory symptoms. Thirdly, the disruptions caused to normal clinical pathways by the pandemic and associated national and regional lockdowns likely impacted access to diagnostic services—including likely difficulties in obtaining community-based tests such as chest x-rays. We noted earlier that there was an abrupt downturn in the rate of bronchoscopy for both Māori and non-Māori/non-Pacific patients from April 2020 compared to previous years, due to a purposeful reduction in bronchoscopy services during the early stages of the COVID-19 pandemic. Unlike lung cancer registrations, we may not expect the cumulative rate of bronchoscopy to “catch-up” with that observed in previous years, since it is possible that in early 2020 other forms of investigation (such as CT-guided biopsy) may have been preferred to bronchoscopy, in order to reduce potential aerosolisation of the SARS-CoV-2 virus.[[23–27]]

In order to drive the differential impact of COVID-19 on lung cancer diagnosis observed in this study, one or more of the above factors must have acted differently for Māori than they did for non-Māori/non-Pacific peoples. In other words, it is possible that Māori with symptoms of lung cancer were more likely to heed public health advice to remain in-place in spite of symptoms, whether out of hesitancy around the virus and/or a sense of duty to their community; and/or more likely to have their symptoms not differentiable for COVID-19; and/or less likely to gain access to diagnostic services to assist in the diagnosis of their lung cancer. The first two of these factors require further investigation with more granular data than were available for this study: for example, it would be valuable to learn the extent to which patients diagnosed with lung cancer during the national or regional lockdowns of 2020 delayed seeking care, and/or sought care but investigations were delayed, for their early symptoms due to COVID-related barriers;[[28, 29]] how this compares to patients diagnosed post-lockdowns; and how this experience differs for Māori compared to other ethnic groups.

In terms of access to diagnostic services, it does appear that the cumulative rate of bronchoscopy was somewhat more severely impacted for Māori than it was for non-Māori/non-Pacific peoples (Figure 3), with this reduced access potentially contributing to the differential impact on lung cancer registrations. Such an observation must be interpreted alongside the healthcare access-related factors discussed above. In addition, it is important to bear in mind that the data reported in this study refers to all bronchoscopies performed in the general population, which was likely impacted by reductions in seasonal respiratory illness due to the 2020 lockdowns—which means that it is not straightforward to presume that differential cumulative reductions for Māori correspond to differential access for Māori with symptoms of lung cancer. In terms of future research, it would be useful to view these bronchoscopy data alongside data on CT-guided lung biopsy access during the national and regional lockdowns, and to compare this access between Māori and non-Māori/non-Pacific peoples. Currently these data are not readily available at a national level, but may be reviewed within regions with granular data around lung cancer management (see below).

Related to diagnostic service access is the pathway by which patients enter the cancer care system. We noted in a recent report that the number and proportion of lung cancers referred through the Faster Cancer Treatment (FCT) pathway seemed to be unaffected by the COVID-19 pandemic, for both Māori and non-Māori.[[17]] The FCT pathway provides monitoring for patients referred with a high risk of cancer, with targets related to timing of first treatment. Around half of Māori lung cancer patients nationwide go through the FCT pathway,[[17]] although this proportion varies by region.[[30]]  The fact this pathway was unaffected might suggest that Māori patients who were not diagnosed or had their diagnosis delayed due to the pandemic would likely have entered via other pathways such as emergency rooms and incidental findings during hospital admissions.[[17]] A review of lung cancer registrations between 2015–2018 found that Māori patients were more likely to be diagnosed through emergency presentation than non-Māori patients.[[31]] During COVID-related lockdowns, emergency room use was substantially impacted, which may be a factor in creating greater delays to lung cancer registrations for Māori than it would for other ethnic groups.[[31]] The same rationale exists for inpatient diagnoses: it is plausible that Māori—who are more likely to be hospitalised than non-Māori [[32]]—are more likely to have their lung cancer diagnosed in an inpatient setting (possibly incidentally when hospitalised for another condition), and if COVID-19 reduced access to inpatient care, then this would differentially impact lung cancer registrations for Māori. The extent of incidental diagnosis (particularly for Māori) remains unknown in New Zealand, but international evidence suggests that 9–40% of lung cancers are diagnosed in this way [[33,34]]—reinforcing the potential importance of this pathway (particularly for Māori).

There was no apparent shift in the distribution of stage at diagnosis across the three years, for either Māori or non-Māori/non-Pacific patients. Crucially, the proportion of advanced (i.e., metastasised) diagnoses remained relatively stable over this period (particularly for Māori patients), suggesting that, at least by the end of 2020, the downturn in lung cancer registrations for Māori patients does not appear to have led to an increase in the relative proportion of metastasised disease. However, there are two caveats to this observation: firstly, the high proportion of unstaged lung cancer registrations on the NZCR means that the actual proportion of advanced diagnoses is likely to be higher than that observed in this study, although the relative difference between years (and ethnicities) is still likely to be accurate.[[35]] Future analyses could include datasets such as the Midland and Northern regional registers, which include more granular (and complete) staging information.[[36]] Secondly, it may be that we do not yet have sufficient data to fully capture the impact of the 2020 downturn in lung cancer registrations on stage distribution for Māori; in other words, such an impact may only become clear once full data are available for multiple years following the onset of the pandemic.

Why just lung cancer?

As noted in the introduction, there has been little evidence that the disturbances to cancer diagnoses caused by the COVID-19 pandemic have differentially impacted Māori, with the exception of lung cancer. As such, it would seem likely that the factors driving the disparity in the downturn of lung cancer registrations for Māori are likely to be unique to lung cancer, rather than applicable to other contexts.

Firstly, it is also important to note that bronchoscopy has the capacity to substantially increase the risk of SARS-CoV-2 spread between patients and clinicians. This, possibly combined with the impact of reductions in bronchoscopy due to reductions in seasonal respiratory illnesses, resulted in stark reductions in its use—reductions which appear to have been at least somewhat worse for Māori. Secondly, as noted above, the pathway toward lung cancer diagnosis is not necessarily the same for Māori patients as it is for non-Māori/non-Pacific patients, and which might have led to fewer Māori registrations over 2020. While the latter factor might also apply to other cancer contexts (e.g., colorectal cancer, where Māori patients are more likely to be diagnosed following emergency presentation than non-Māori patients),[[37]] perhaps it is the combination of all three factors which ultimately drove the observed differential impact of COVID-19 on lung cancer registrations.

What have we learned?

There are three key lessons to be drawn from our observations of the impact of COVID-19 on lung cancer registrations and treatment. Firstly, the likelihood that the pathway to diagnosis and treatment may differ between Māori and non-Māori/non-Pacific patients means that we need to understand more about the pathways outside of the Faster Cancer Treatment pathway and their associated barriers. The absence of changes in diagnoses through the Faster Cancer Treatment pathway for Māori (and non-Māori) suggests that these other pathways (including emergency presentation and inpatient, incidental diagnoses) may be where the majority of inequities in the lung cancer pathway occur—not just in the context of COVID-19. These inequities reflect implicit bias within the healthcare system, wherein the system is more accessible for non-Māori patients than it is for Māori patients.[[38]]

Secondly, our observations in all other cancer contexts illustrates that it is not necessarily inevitable that a significant health event such as the COVID-19 pandemic will lead to the exacerbation of health inequities; rather, these can be avoided by deliberate prioritisation of the equitable provision of healthcare within the population, and in particular the preferential allocation of time and resources toward protecting the health of Māori.

Finally, in light of recent evidence suggesting that primary care communication and national messaging may have diverted attention away from other health conditions,[[28,29]] there is need for more deliberate focus at a national and regional level on timely access to non-COVID-19 related healthcare. In the context of lung cancer, this focus could be first directed toward high-risk groups (such as Māori smokers and ex-smokers).

Strengths and limitations

The data used in the current study includes all lung cancer registrations reported the New Zealand Cancer Registry (NZCR) over the follow-up period, ensuring national generalisability. We note that we purposefully did not conduct statistical tests on the data, since we note that tests (such as a Cochran-Mantel-Haenszel test for trend) would only tell us if something was different between years, but provide little additional information with which to interpret the data. We also note that, in recent years, there has been renewed emphasis on departing from a reliance on statistical tests and p-values when interpreting differences between groups.[[39]]

Conclusions

Using national-level data, we observed a downturn in the rate of lung cancer registration for Māori (but not non-Māori/non-Pacific) New Zealanders in 2020 compared to 2018 and 2019. There was no apparent shift in the distribution of stage at diagnosis across the three-year period. Rates of bronchoscopy abruptly dropped for both Māori and non-Māori/non-Pacific patients in 2020 relative to previous years, with this drop appearing to be greatest for Māori. Rates of lung cancer surgery appeared somewhat lower in 2020 for Māori patients, although this was based on a small number of procedures. While other cancer contexts have illustrated that the impact of COVID-19 on access to and through cancer services does not necessarily need to occur inequitably between Māori and non-Māori patients, disparities observed in the lung cancer context suggest that a) we need to ensure that Māori with respiratory symptoms receive best practice care for their symptoms, and b) we need to better quantify and monitor the pathways by which Māori patients with symptoms of lung cancer are entering the healthcare system.

View Appendices.

Summary

Abstract

Aim

The purpose of this article is to examine disparities in the impact of the COVID-19 pandemic on access to lung cancer diagnosis and access to clinical services between Māori and non-Māori.

Method

Using national-level data, we examined age-standardised lung cancer registrations, diagnostic procedures (bronchoscopy) and lung surgeries separately by ethnic group for the years 2018–2020, as well as patterns of stage of diagnosis.

Results

We found a trend toward a reduction in rates of lung cancer registration in Māori (but not non-Māori/non-Pacific) New Zealanders in 2020 compared to 2018 and 2019, but no apparent shift in the distribution of stage at diagnosis. We found a trend toward a reduction in rates of bronchoscopy for both Māori and non-Māori/non-Pacific patients, with the largest reduction observed for Māori. Rates of lung cancer surgery appeared to have reduced for Māori patients, although this was based on a small number of procedures.

Conclusion

We observed disparities between Māori and non-Māori/non-Pacific patients in lung cancer registration and bronchoscopy as a result of the COVID-19 pandemic.

Author Information

Jason K Gurney: Te Aho o Te Kahu – Cancer Control Agency, Wellington, New Zealand; Department of Public Health, University of Otago, Wellington, New Zealand. Alex Dunn: Te Aho o Te Kahu – Cancer Control Agency, Wellington, New Zealand. Michelle Liu: Te Aho o Te Kahu – Cancer Control Agency, Wellington, New Zealand. Michelle Mako: Te Aho o Te Kahu – Cancer Control Agency, Wellington, New Zealand. Elinor Millar: Te Aho o Te Kahu – Cancer Control Agency, Wellington, New Zealand. Myra Ruka: Te Aho o Te Kahu – Cancer Control Agency, Wellington, New Zealand. Sue Crengle: Department of Preventive and Social Medicine, University of Otago, Dunedin, New Zealand Paul Dawkins: Counties-Manukau District Health Board, Auckland, New Zealand. Christopher Jackson: Southern District Health Board, Dunedin, New Zealand; Department of Medicine, University of Otago, Dunedin, New Zealand. George Laking: Auckland District Health Board, Auckland, New Zealand; Northland District Health Board, Whangārei, New Zealand. Diana Sarfati: Te Aho o Te Kahu – Cancer Control Agency, Wellington, New Zealand.

Acknowledgements

We would like to thank Vahid Arabneiad from the Te Aho o Te Kahu Data Monitoring and Reporting team for the rapid provision of data for this study. This work was funded by Te Aho o Te Kahu – Cancer Control Agency.

Correspondence

Jason K Gurney: Department of Public Health, University of Otago, Wellington, New Zealand, PO Box 7343, Wellington, New Zealand. +64 21 279 3597

Correspondence Email

jason.gurney@otago.ac.nz

Competing Interests

Nil.

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23) Houston SA, McDonald CM, Tyan C-C, Fortin M, Sakr L, Gillson A-ME, Myers R, Bendiak GN, Dumoulin E, Gonzalez AV, Hergott CA. Bronchoscopy during the COVID-19 pandemic: A Canadian Thoracic Society position statement. Canadian Journal of Respiratory, Critical Care, and Sleep Medicine. 2021:1-7.

24) Pritchett MA, Oberg CL, Belanger A, Cardenas JD, Cheng G, Nacheli GC, Franco-Paredes C, Singh J, Toth J, Zgoda M, Folch E. Society for Advanced Bronchoscopy Consensus Statement and Guidelines for bronchoscopy and airway management amid the COVID-19 pandemic. Journal of Thoracic Disease. 2020;12(5):1781-98.

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Across the world, the impact of the COVID-19 pandemic on access to cancer diagnosis and subsequent clinical services has been profound. In regions with widespread community transmission of the disease, this impact endured throughout 2020 and into 2021, and has resulted in a significant backlog of under-diagnosed and under-treated disease in these regions.[[1–6]]

In countries like New Zealand that have pursued an elimination approach to COVID-19, the impact has to date been less intense and shorter-lasting, largely concentrated to those times of national or regional lockdown.[[7–9]] Early in the pandemic, New Zealand’s national Cancer Control Agency, Te Aho o Te Kahu, engaged widely with clinicians, researchers and other stakeholders to plan the cancer-related response to the anticipated upheavals to usual healthcare provision caused by COVID-19. As noted elsewhere,[[10,11]] a focus on preventing exacerbation of inequity was a core element of this response, which included the ongoing monitoring of inequities in access to diagnosis, and partnership with Hei Āhuru Mōwai (National Māori Cancer Leadership Group) and other Māori researchers to develop an Equity Response Framework.[[10]] This framework aimed to identify the likely impact of the pandemic on existing inequities, and what actions could be taken to mitigate them. These actions, along with strong Māori-focused public health messaging from organisations such as Te Rōpū Whakakaupapa Urutā (the National Māori Pandemic Group), reduced the likelihood that the COVID-19 pandemic would have a differential impact on cancer diagnosis and treatment for Māori.

As part of ongoing monitoring across 2020, Te Aho o Te Kahu provided detailed analysis and reports and engaged with decision-makers to disseminate key findings. These reports outlined changes in cancer registration, diagnostic procedures and treatment (surgery, systemic therapy and radiation therapy).[[12–17]] These reports compared the occurrence of these events on a month-by-month basis across 2020 against the same period in 2018 and 2019, and presented results separately for the total population and for Māori. While the reduction in these events during the national lockdown of late March and April 2020 was dramatic—for example, cancer registrations dropped by more than 40% over this period compared to previous years[[16]]—these reports found little evidence of disparities in the magnitude of these downturns between Māori and non-Māori patients. In other words, it appeared that the pandemic had impacted access to diagnosis and treatment in much the same way for Māori as for the rest of the population.

The sole exception to this absence of disparity was found in the diagnosis and treatment of lung cancer—by far the most common cause of cancer death for Māori.[[18]] As noted in one of the reports, the number of lung cancer registrations, bronchoscopies and surgeries appeared to have dropped more substantially for Māori patients than the rest of the population.[[17]] Disparities in the pandemic’s impact on lung cancer registrations among Māori compared to the rest of the population is particularly concerning, since it may indicate that Māori patients with symptoms of lung cancer are experiencing greater delays to diagnosis than non-Māori patients, with subsequent ramifications on quality of life and survival.

However, because data were only available up until the end of October for the Te Aho o Te Kahu report,[[17]] and since that report only presented absolute numbers of cases compared to previous years, two key factors remain unclear: 1) whether disparities in the downturn of registrations (and related procedures) continued for the remainder of 2020, or were “correcting” toward the end of the year; and 2) whether expressing the numbers of events relative to their underlying ethnic-specific population, as well as adjusting rates for differences between Māori and non-Māori in terms of age, will impact our understanding of what happened regarding this disparity. In addition, it remains unclear whether delays to diagnosis during 2020 have resulted in an overall shift in the distribution of disease stage at diagnosis, and whether these changes have inequitably impacted Māori patients.

In this article, we examine age-standardised lung cancer registrations, diagnostic procedures (bronchoscopy) and surgical treatment separately by ethnic group for the years 2018–2020, and we express the number of these events relative to their ethnic-specific underlying population. We also examine patterns of stage of diagnosis by ethnic groups across these years, in order to assess whether the COVID-19 pandemic has resulted in a shift in stage distribution for Māori (and/or non-Māori) patients with lung cancer. We have focussed our comparisons to Māori and non-Māori/non-Pacific populations, to ensure adequate numbers of patients in our month-on-month stratified analyses.

Methods

Participants and data sources

Numerators

This study included three participant cohorts. Firstly, when assessing the impact of COVID-19 on lung cancer registrations, we extracted all those who were diagnosed with lung cancer (ICD code C34) on the New Zealand Cancer Registry (NZCR) between 1 January 2018 to 31 December 2020 (N = 6,679; 1,497 Māori, 5,182 non-Māori/non-Pacific). Secondly, when assessing the impact on access to bronchoscopy, we extracted data for all New Zealanders (irrespective of subsequent lung cancer status) who underwent a bronchoscopy over this same period from the National Non-Admitted Patient Collection (NNPAC; purchase unit code MS02003; N = 7,281; 1,143 Māori, 6,138 non-Māori/non-Pacific). Thirdly, when assessing the impact on lung cancer surgery, we extracted data for all New Zealanders who underwent a publicly-funded lung resection as an inpatient, and who had a diagnosis of cancer on the same admission, from the National Minimum Dataset (NMDS; see Appendix 1  for procedures and ICD codes; N = 1,030; 168 Māori, 862 non-Māori/non-Pacific).

Denominators

When describing rates of lung cancer registration, bronchoscopy and surgery, we used the ethnicity-stratified total estimated residential population of New Zealand for each of 2018, 2019 and 2020 as the denominator, with this data derived from Stats NZ.[[19]] When describing the distribution of stage of disease at diagnosis, we used the total number of patients diagnosed with lung cancer on the NZCR as the denominator.

Variables

For the purposes of age standardisation, patient age at either the time of diagnosis (in the case of lung cancer registration) or procedure (in the case of bronchoscopy and lung surgery) was defined using their date of birth and the data of diagnosis or procedure, respectively. Age was categorised as <50 years, 50–64, 65–74, and 75+. Patient ethnicity (Māori, Pacific or non-Māori/non-Pacific) was defined using prioritised ethnicity, as recorded on the NZCR (for registration), NNPAC (for bronchoscopy) or NMDS (for surgery). To prevent misinterpretation of data due to low numbers of diagnoses and procedures, Pacific data were not analysed for this manuscript. Month and year of diagnosis or procedure were derived from the date of diagnosis or procedure from each respective dataset. Stage of disease was extracted for each lung cancer registration from the NZCR, and was defined according to the SEER staging system (Local, Regional, Advanced and Unstaged).

Statistical analysis

For our descriptive analysis, we described the number and rate of lung cancer registration, bronchoscopy and lung surgery. Crude and age-standardised rates were described per 100,000 Māori or non-Māori/non-Pacific New Zealanders, using the denominator data derived from Stats NZ. To adjust for differences between Māori and non-Māori/non-Pacific peoples in terms of population age structure, we used direct standardisation techniques to describe age-adjusted rates of diagnosis or procedure, using the 2001 Māori Census population as the standard population.[[20, 21]] When describing the distribution of stage at diagnosis, we expressed the number of diagnoses within each respective stage (Local, Regional, Advanced, Unstaged) as a proportion (%) of the total number of all combined stages, separately for each year and for Māori and non-Māori/non-Pacific patients. In terms of ensuring the study’s responsiveness to Māori, this study was led by a Māori epidemiologist (JG), supported by Māori public servants, academics and clinicians (MM, MR, SC, GL).

Results

Cancer registrations

The cumulative age-standardised rate of lung cancer registrations is shown in Figure 1, stratified by year and ethnicity, with full tabulated data including confidence limits shown in Appendix 2. The rate of lung cancer registrations trended toward being lower in 2020 compared to the previous two years for Māori, but not for non-Māori/non-Pacific peoples. For Māori the cumulative registration rate in 2020 had increased by December to draw close to that observed by the end of 2019, although this may reflect a general downturn between September–December 2019 relative to the same period in 2018. Rates of lung cancer registration for non-Māori/non-Pacific peoples were indiscernible between 2018–2020.

Figure 1: Cumulative age-standardised rate of lung cancer registrations by month and year (2018–2020) per 100,000 New Zealanders, for Māori (left) and non-Māori/non-Pacific (right).

The distribution of stage at diagnosis among lung cancer registrations between 2018–2020 is shown in Figure 2, separately for Māori and non-Māori/non-Pacific patients. For Māori, there was no clear change in stage distribution over the three-year period: the proportion of advanced cancers remained at 47% each year, while the proportion of Unstaged cancers ranged between 29–33% across the three years. Variation between years was somewhat greater for non-Māori/non-Pacific patients, although the stage distribution remained broadly similar across the three-year period.

Figure 2: Stacked bar chart showing the crude distribution of local, regional, advanced and unstaged lung cancer on the New Zealand Cancer Registry, by year (2018–2020), separately for Māori and non-Māori/non-Pacific patients.

Bronchoscopy

The cumulative age-standardised rate of bronchoscopies is shown in Figure 3, stratified by year and ethnicity, with full tabulated data including confidence limits shown in Appendix 3. The bronchoscopy rate trended toward being lower in 2020 compared to the previous two years for both Māori and non-Māori/non-Pacific peoples, with an abrupt decline occurring between March and April of 2020 (coinciding with the onset of the first national lockdown in New Zealand). The cumulative bronchoscopy rate remained substantially below that observed in previous years by the end of 2020, particularly so for Māori.

Figure 3: Cumulative age-standardised rate of bronchoscopy by month and year (2018–2020) per 100,000 New Zealanders, for Māori (left) and non-Māori/non-Pacific (right).

Access to lung surgery

The cumulative age-standardised rate of lung surgery is shown in Figure 4, stratified by year and ethnicity, with full tabulated data including confidence limits shown in Appendix 4. For Māori patients, rates of lung surgery trended toward being lower from July of 2020 compared to the same period from previous two years, although this was based on low numbers of procedures and should therefore be interpreted with caution. Rates of lung cancer surgery for non-Māori/non-Pacific peoples were indiscernible between 2018–2020.

Figure 4: Cumulative age-standardised rate of lung surgery by month and year (2018-2020) per 100,000 New Zealanders, for Māori (left) and non-Māori/non-Pacific (right).

Discussion

Beginning in March 2020, there was a trend toward a downturn in the rate of lung cancer registration for Māori (but not non-Māori/non-Pacific) New Zealanders compared to previous years —although the cumulative rate of registration for Māori appeared to be returning to 2019 levels by the end of 2020. There was no apparent shift in the distribution of stage at diagnosis across the three-year period. Rates of bronchoscopy abruptly dropped for both Māori and non-Māori/non-Pacific patients in 2020 relative to previous years (but to a greater extent for Māori), while rates of lung cancer surgery appeared somewhat lower in 2020 for Māori patients, although this was based on a small number of procedures and thus should be interpreted with caution.

What do these findings mean?

Cancer registrations in general decreased during the early phases of the COVID-19 pandemic when there were national lock downs both in New Zealand and internationally. A downturn in lung cancer registrations might be an expected consequence of the COVID-19 pandemic for the following reasons. Firstly, because of the strong public health messaging which advised people to remain home if feeling unwell, it is likely that some patients who may have otherwise sought care for their symptoms were dissuaded from doing so. Secondly, given the overlap between COVID-19 and lung cancer in common presenting respiratory symptoms, it is plausible that among those who sought care the symptoms of their lung cancer were either not differentiable from symptoms of COVID-19, or a diagnostic bias towards excluding COVID-19 resulted in limited consideration of other causes for their symptoms—with both of these impacting on clinical work-up and subsequent delays to lung cancer diagnosis. Similarly, it is plausible that the reduction in the incidence of seasonal respiratory conditions such as influenza [[22]] resulted in fewer opportunistic diagnoses of lung cancer among those with respiratory symptoms. Thirdly, the disruptions caused to normal clinical pathways by the pandemic and associated national and regional lockdowns likely impacted access to diagnostic services—including likely difficulties in obtaining community-based tests such as chest x-rays. We noted earlier that there was an abrupt downturn in the rate of bronchoscopy for both Māori and non-Māori/non-Pacific patients from April 2020 compared to previous years, due to a purposeful reduction in bronchoscopy services during the early stages of the COVID-19 pandemic. Unlike lung cancer registrations, we may not expect the cumulative rate of bronchoscopy to “catch-up” with that observed in previous years, since it is possible that in early 2020 other forms of investigation (such as CT-guided biopsy) may have been preferred to bronchoscopy, in order to reduce potential aerosolisation of the SARS-CoV-2 virus.[[23–27]]

In order to drive the differential impact of COVID-19 on lung cancer diagnosis observed in this study, one or more of the above factors must have acted differently for Māori than they did for non-Māori/non-Pacific peoples. In other words, it is possible that Māori with symptoms of lung cancer were more likely to heed public health advice to remain in-place in spite of symptoms, whether out of hesitancy around the virus and/or a sense of duty to their community; and/or more likely to have their symptoms not differentiable for COVID-19; and/or less likely to gain access to diagnostic services to assist in the diagnosis of their lung cancer. The first two of these factors require further investigation with more granular data than were available for this study: for example, it would be valuable to learn the extent to which patients diagnosed with lung cancer during the national or regional lockdowns of 2020 delayed seeking care, and/or sought care but investigations were delayed, for their early symptoms due to COVID-related barriers;[[28, 29]] how this compares to patients diagnosed post-lockdowns; and how this experience differs for Māori compared to other ethnic groups.

In terms of access to diagnostic services, it does appear that the cumulative rate of bronchoscopy was somewhat more severely impacted for Māori than it was for non-Māori/non-Pacific peoples (Figure 3), with this reduced access potentially contributing to the differential impact on lung cancer registrations. Such an observation must be interpreted alongside the healthcare access-related factors discussed above. In addition, it is important to bear in mind that the data reported in this study refers to all bronchoscopies performed in the general population, which was likely impacted by reductions in seasonal respiratory illness due to the 2020 lockdowns—which means that it is not straightforward to presume that differential cumulative reductions for Māori correspond to differential access for Māori with symptoms of lung cancer. In terms of future research, it would be useful to view these bronchoscopy data alongside data on CT-guided lung biopsy access during the national and regional lockdowns, and to compare this access between Māori and non-Māori/non-Pacific peoples. Currently these data are not readily available at a national level, but may be reviewed within regions with granular data around lung cancer management (see below).

Related to diagnostic service access is the pathway by which patients enter the cancer care system. We noted in a recent report that the number and proportion of lung cancers referred through the Faster Cancer Treatment (FCT) pathway seemed to be unaffected by the COVID-19 pandemic, for both Māori and non-Māori.[[17]] The FCT pathway provides monitoring for patients referred with a high risk of cancer, with targets related to timing of first treatment. Around half of Māori lung cancer patients nationwide go through the FCT pathway,[[17]] although this proportion varies by region.[[30]]  The fact this pathway was unaffected might suggest that Māori patients who were not diagnosed or had their diagnosis delayed due to the pandemic would likely have entered via other pathways such as emergency rooms and incidental findings during hospital admissions.[[17]] A review of lung cancer registrations between 2015–2018 found that Māori patients were more likely to be diagnosed through emergency presentation than non-Māori patients.[[31]] During COVID-related lockdowns, emergency room use was substantially impacted, which may be a factor in creating greater delays to lung cancer registrations for Māori than it would for other ethnic groups.[[31]] The same rationale exists for inpatient diagnoses: it is plausible that Māori—who are more likely to be hospitalised than non-Māori [[32]]—are more likely to have their lung cancer diagnosed in an inpatient setting (possibly incidentally when hospitalised for another condition), and if COVID-19 reduced access to inpatient care, then this would differentially impact lung cancer registrations for Māori. The extent of incidental diagnosis (particularly for Māori) remains unknown in New Zealand, but international evidence suggests that 9–40% of lung cancers are diagnosed in this way [[33,34]]—reinforcing the potential importance of this pathway (particularly for Māori).

There was no apparent shift in the distribution of stage at diagnosis across the three years, for either Māori or non-Māori/non-Pacific patients. Crucially, the proportion of advanced (i.e., metastasised) diagnoses remained relatively stable over this period (particularly for Māori patients), suggesting that, at least by the end of 2020, the downturn in lung cancer registrations for Māori patients does not appear to have led to an increase in the relative proportion of metastasised disease. However, there are two caveats to this observation: firstly, the high proportion of unstaged lung cancer registrations on the NZCR means that the actual proportion of advanced diagnoses is likely to be higher than that observed in this study, although the relative difference between years (and ethnicities) is still likely to be accurate.[[35]] Future analyses could include datasets such as the Midland and Northern regional registers, which include more granular (and complete) staging information.[[36]] Secondly, it may be that we do not yet have sufficient data to fully capture the impact of the 2020 downturn in lung cancer registrations on stage distribution for Māori; in other words, such an impact may only become clear once full data are available for multiple years following the onset of the pandemic.

Why just lung cancer?

As noted in the introduction, there has been little evidence that the disturbances to cancer diagnoses caused by the COVID-19 pandemic have differentially impacted Māori, with the exception of lung cancer. As such, it would seem likely that the factors driving the disparity in the downturn of lung cancer registrations for Māori are likely to be unique to lung cancer, rather than applicable to other contexts.

Firstly, it is also important to note that bronchoscopy has the capacity to substantially increase the risk of SARS-CoV-2 spread between patients and clinicians. This, possibly combined with the impact of reductions in bronchoscopy due to reductions in seasonal respiratory illnesses, resulted in stark reductions in its use—reductions which appear to have been at least somewhat worse for Māori. Secondly, as noted above, the pathway toward lung cancer diagnosis is not necessarily the same for Māori patients as it is for non-Māori/non-Pacific patients, and which might have led to fewer Māori registrations over 2020. While the latter factor might also apply to other cancer contexts (e.g., colorectal cancer, where Māori patients are more likely to be diagnosed following emergency presentation than non-Māori patients),[[37]] perhaps it is the combination of all three factors which ultimately drove the observed differential impact of COVID-19 on lung cancer registrations.

What have we learned?

There are three key lessons to be drawn from our observations of the impact of COVID-19 on lung cancer registrations and treatment. Firstly, the likelihood that the pathway to diagnosis and treatment may differ between Māori and non-Māori/non-Pacific patients means that we need to understand more about the pathways outside of the Faster Cancer Treatment pathway and their associated barriers. The absence of changes in diagnoses through the Faster Cancer Treatment pathway for Māori (and non-Māori) suggests that these other pathways (including emergency presentation and inpatient, incidental diagnoses) may be where the majority of inequities in the lung cancer pathway occur—not just in the context of COVID-19. These inequities reflect implicit bias within the healthcare system, wherein the system is more accessible for non-Māori patients than it is for Māori patients.[[38]]

Secondly, our observations in all other cancer contexts illustrates that it is not necessarily inevitable that a significant health event such as the COVID-19 pandemic will lead to the exacerbation of health inequities; rather, these can be avoided by deliberate prioritisation of the equitable provision of healthcare within the population, and in particular the preferential allocation of time and resources toward protecting the health of Māori.

Finally, in light of recent evidence suggesting that primary care communication and national messaging may have diverted attention away from other health conditions,[[28,29]] there is need for more deliberate focus at a national and regional level on timely access to non-COVID-19 related healthcare. In the context of lung cancer, this focus could be first directed toward high-risk groups (such as Māori smokers and ex-smokers).

Strengths and limitations

The data used in the current study includes all lung cancer registrations reported the New Zealand Cancer Registry (NZCR) over the follow-up period, ensuring national generalisability. We note that we purposefully did not conduct statistical tests on the data, since we note that tests (such as a Cochran-Mantel-Haenszel test for trend) would only tell us if something was different between years, but provide little additional information with which to interpret the data. We also note that, in recent years, there has been renewed emphasis on departing from a reliance on statistical tests and p-values when interpreting differences between groups.[[39]]

Conclusions

Using national-level data, we observed a downturn in the rate of lung cancer registration for Māori (but not non-Māori/non-Pacific) New Zealanders in 2020 compared to 2018 and 2019. There was no apparent shift in the distribution of stage at diagnosis across the three-year period. Rates of bronchoscopy abruptly dropped for both Māori and non-Māori/non-Pacific patients in 2020 relative to previous years, with this drop appearing to be greatest for Māori. Rates of lung cancer surgery appeared somewhat lower in 2020 for Māori patients, although this was based on a small number of procedures. While other cancer contexts have illustrated that the impact of COVID-19 on access to and through cancer services does not necessarily need to occur inequitably between Māori and non-Māori patients, disparities observed in the lung cancer context suggest that a) we need to ensure that Māori with respiratory symptoms receive best practice care for their symptoms, and b) we need to better quantify and monitor the pathways by which Māori patients with symptoms of lung cancer are entering the healthcare system.

View Appendices.

Summary

Abstract

Aim

The purpose of this article is to examine disparities in the impact of the COVID-19 pandemic on access to lung cancer diagnosis and access to clinical services between Māori and non-Māori.

Method

Using national-level data, we examined age-standardised lung cancer registrations, diagnostic procedures (bronchoscopy) and lung surgeries separately by ethnic group for the years 2018–2020, as well as patterns of stage of diagnosis.

Results

We found a trend toward a reduction in rates of lung cancer registration in Māori (but not non-Māori/non-Pacific) New Zealanders in 2020 compared to 2018 and 2019, but no apparent shift in the distribution of stage at diagnosis. We found a trend toward a reduction in rates of bronchoscopy for both Māori and non-Māori/non-Pacific patients, with the largest reduction observed for Māori. Rates of lung cancer surgery appeared to have reduced for Māori patients, although this was based on a small number of procedures.

Conclusion

We observed disparities between Māori and non-Māori/non-Pacific patients in lung cancer registration and bronchoscopy as a result of the COVID-19 pandemic.

Author Information

Jason K Gurney: Te Aho o Te Kahu – Cancer Control Agency, Wellington, New Zealand; Department of Public Health, University of Otago, Wellington, New Zealand. Alex Dunn: Te Aho o Te Kahu – Cancer Control Agency, Wellington, New Zealand. Michelle Liu: Te Aho o Te Kahu – Cancer Control Agency, Wellington, New Zealand. Michelle Mako: Te Aho o Te Kahu – Cancer Control Agency, Wellington, New Zealand. Elinor Millar: Te Aho o Te Kahu – Cancer Control Agency, Wellington, New Zealand. Myra Ruka: Te Aho o Te Kahu – Cancer Control Agency, Wellington, New Zealand. Sue Crengle: Department of Preventive and Social Medicine, University of Otago, Dunedin, New Zealand Paul Dawkins: Counties-Manukau District Health Board, Auckland, New Zealand. Christopher Jackson: Southern District Health Board, Dunedin, New Zealand; Department of Medicine, University of Otago, Dunedin, New Zealand. George Laking: Auckland District Health Board, Auckland, New Zealand; Northland District Health Board, Whangārei, New Zealand. Diana Sarfati: Te Aho o Te Kahu – Cancer Control Agency, Wellington, New Zealand.

Acknowledgements

We would like to thank Vahid Arabneiad from the Te Aho o Te Kahu Data Monitoring and Reporting team for the rapid provision of data for this study. This work was funded by Te Aho o Te Kahu – Cancer Control Agency.

Correspondence

Jason K Gurney: Department of Public Health, University of Otago, Wellington, New Zealand, PO Box 7343, Wellington, New Zealand. +64 21 279 3597

Correspondence Email

jason.gurney@otago.ac.nz

Competing Interests

Nil.

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