Head and neck
Published: 2024-04-30
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Changes in Management of Head and Neck Malignancies during the COVID-19 Pandemic

Department of Otorhinolaryngology, Head and Neck Surgery, Medical University of Vienna, Vienna, Austria
Department of Otorhinolaryngology, University Clinical Center Tuzla, Tuzla, Bosnia and Herzegovina
Department of Otorhinolaryngology, Head and Neck Surgery, Medical University of Vienna, Vienna, Austria
Department of Otorhinolaryngology, Head and Neck Surgery, Medical University of Vienna, Vienna, Austria
Department of Otorhinolaryngology, University Clinical Center Tuzla, Tuzla, Bosnia and Herzegovina
Department of Otorhinolaryngology, University Clinical Center Tuzla, Tuzla, Bosnia and Herzegovina
Department of Otorhinolaryngology, University Clinical Center Tuzla, Tuzla, Bosnia and Herzegovina
Department of Otorhinolaryngology, University Clinical Center Tuzla, Tuzla, Bosnia and Herzegovina
Department of Otorhinolaryngology, Head and Neck Surgery, Medical University of Vienna, Vienna, Austria
Department of Otorhinolaryngology, Head and Neck Surgery, Medical University of Vienna, Vienna, Austria
COVID-19 pandemic head and neck cancer Bosnia and Herzegovina

Abstract

Objective. Despite multiple studies from high-income countries, reports from low- and middle-income countries on the impact of COVID-19 on head and neck cancer care remain sparse. This study aimed to assess the effects of the COVID-19 pandemic on head and neck cancer patients at a tertiary reference centre in Bosnia and Herzegovina.
Methods. We included 228 patients with malignant head and neck tumours evaluated and treated between January 1, 2019, and December 31, 2021. Patient demographics, histological characteristics, and treatment modalities were retrospectively obtained and compared between the pre-pandemic period (pre-COVID-19 group) and the period after the implementation of COVID-19 restrictive measures (COVID-19 group).
Results. Patients were significantly older during the COVID-19 pandemic. In particular, 63 patients (44.7%) were under 65 and 78 (55.3%) were 65 or older, while in the pre- COVID-19 period, 53 patients (60.9%) were under 65 and 34 (39.1%) were 65 or older (p = 0.017). The pre-COVID-19 and COVID-19 groups did not significantly differ regarding other patient- and tumour characteristics, or primary treatment modalities.
Conclusions. During the COVID-19 pandemic, significantly fewer patients were under 65 at the time of initial work-up, potentially reflecting the more enhanced disease-related anxiety of the younger population. Future studies are warranted to address this population’s specific educational and psychological needs to ensure appropriate cancer care.

Introduction

Since the onset of the COVID-19 pandemic in 2020, high mortality rates relative to other respiratory infectious diseases, coupled with the emergence of new variants, have continued to strain healthcare providers worldwide 1. Furthermore, recent studies have demonstrated that pandemic-related restrictions have severely compromised the timely and comprehensive provision of cancer care 2,3. Notably, nations with well-resourced healthcare systems, including sufficient hospital capacity, medical personnel, and essential medical equipment, generally managed the pandemic better than countries with limited resources 4. However, the majority of current literature investigating the impact of COVID-19 on cancer care originates from high-income countries and lacks the perspective of low- and middle-income countries 5.

The first case of COVID-19 in Bosnia and Herzegovina (B&H) was reported on March 5, 2020 6. By May 16, 2020, the number of confirmed COVID-19 cases had surged to 2,236, prompting the government to implement widespread restrictive measures, including movement restrictions, closure of public institutions, cafes, bars, and restaurants, as well as restrictions in public spaces and airports 6. By March 31, 2022, B&H had documented 249,495 COVID-19 cases and 8,845 COVID-19-associated deaths 7. Nearly a year later, a combination of low vaccine acceptance rates, limited health care resources and fatigued healthcare workers, created a challenging environment for B&H to effectively manage the ongoing COVID-19 pandemic 8-10. The combination of these factors, along with patient-centred variables such as fear and uncertainty surrounding COVID-19, led to patients presenting with more advanced stages of head and neck cancer during the pandemic 11,12. Certainly, identifying disparities to inform national healthcare policies is crucial to improve the management of cancer care during the pandemic, especially in light of future pandemic developments.

The data on the impact of the COVID-19 pandemic on head and neck cancer care in low- or middle-income countries remain sparse. Therefore, the aim of this study was to assess the impact of the pandemic on patients who presented with head and neck malignancies at a tertiary referral centre in B&H. In particular, we compared patient characteristics, including demographics, tumour characteristics and treatment modalities, between patients who presented before and during the pandemic.

Methods

Study population and study design

This retrospective cohort study included all patients with malignant tumours of the head and neck region who received treatment at the Department of Otorhinolaryngology at the University Clinical Center Tuzla, B&H, from January 1, 2019, to December 31, 2021. Patients with incomplete medical records were excluded from the analysis. The study period was divided into two periods: the pre-COVID-19 period, spanning from January 1, 2019, to March 15, 2020, and the COVID-19 period, spanning from March 16, 2020, to December 31, 2021, following the implementation of the first governmental restrictions in B&H. Patient demographics, tumour characteristics and treatment modalities were compared between the two time periods. Tumour characteristics included information on the primary site, histotype, TNM-classification, clinical staging, grading, and subsite. Staging was performed using the 8th edition of the American Joint Committee on Cancer (AJCC) staging manual 13. The therapeutic modalities were primary surgery with or without postoperative radiotherapy (RT), primary RT, chemotherapy (CHT), radio-chemotherapy (RCHT), and palliative therapy. Due to the recency of the COVID-19 pandemic, the follow-up periods were different between the two cohorts. Therefore, survival analyses were omitted.

Statistical analysis

All categorical variables are presented as numbers and percentages. We used Pearson’s chi-squared test to examine differences between groups. For groups with less than 5 patients, Fisher’s exact test was used. A p value of ≤ 0.05 was considered statistically significant. Statistical analyses were performed using STATA (Version 14, StataCorp LLC, College Station, Texas USA).

Results

A total of 228 patients with head and neck malignancies were treated during the study period. In particular, the pre-COVID-19 group included 87 patients (38.2%), while 141 patients (61.8%) received treatment during the COVID-19 pandemic.

Patient demographics

Our cohort comprised 116 patients (50.9%) under the age of 65 and 112 (49.1%) over 65. In terms of gender, 161 (70.6%) patients were males and 67 (29.4%) females (Tab. I). Interestingly, during the pre-COVID-19 period, significantly fewer patients aged under 65 at the time of the initial work-up (p = 0.017). In particular, 53 patients (60.9%) were under the age of 65 in the pre-COVID-19 group, while during the COVID-19 period, 63 patients (44.7%) were under 65. There were no significant differences in gender distribution between the two time periods (p = 0.282).

Tumour characteristics

Table II summarises the tumour characteristics before and during the COVID-19 pandemic. Histopathological analysis revealed that 161 patients (70.6%) presented with squamous cell carcinoma, while four (1.8%) and two (0.9%) presented with myoepithelial and adenoid cystic carcinoma, respectively. Moreover, one patient (1.8%) presented with invasive ductal carcinoma of the salivary gland. Regarding thyroid cancers, 37 patients (16.2%) presented with papillary thyroid carcinoma, six (2.6%) with follicular thyroid carcinoma, and two (0.9%) with medullary thyroid carcinoma. Additionally, seven (3.1%) patients presented with basal cell carcinoma, while three (1.3%) were diagnosed with a malignant melanoma of the skin. We did not observe a significant difference between the pre-COVID-19 and the COVID-19 periods regarding the distribution of histopathological diagnoses (p = 0.712).

In 155 patients (68%), the primary cancer site was the head and neck mucosa, in 47 (20.6%) the thyroid gland and in 26 (11.4%) the skin. Specifically, within the head and neck region, 103 (45.2%), 47 (20.6%), 26 (11.4%), six (2.6%), one (0.4%), five (2.2%), and five (2.2%) patients had carcinomas located in the larynx, thyroid gland, oropharynx, hypopharynx, nasopharynx, sinonasal, and salivary glands, respectively. Nine patients (3.9%) presented with cancer of unknown primary (CUP). No significant differences were observed when comparing the distribution of primary tumour sites and head and neck cancer subsites before and during the pandemic (p = 0.886 and p = 0.565, respectively).

Moreover, we did not observe a significant difference in the distribution of the T (p = 0.566) or N category (p = 0.067). Only one patient (0.7%), treated during the pandemic, had distant metastases at the initial check-up.

Lastly, the groups showed no significant differences in tumour stage (p = 0.802) or grade (p = 0.609).

Impact of the COVID-19 pandemic on treatment modalities

Throughout the entire study period, 187 patients (81.6%) underwent a primary surgical resection. Eight patients (3.5%) were treated with primary definitive RT and four patients (1.8%) received RCHT. Furthermore, one patient (0.4%) received CHT. Overall, 17 patients (7.5%) were admitted to palliative best-supportive care, and the primary treatment modality was missing in 12 patients (5.3%). Notably, no significant differences in the distribution of treatment modalities between the pre- and COVID-19 period was observed (p = 0.975; Table III).

Discussion

The present study provides first insights into the impact of the COVID-19 pandemic on demographics, tumour characteristics, and treatment modalities of head and neck cancer patients in a tertiary academic centre in B&H. As the main finding of our study, patients were significantly older at initial presentation after the introduction of COVID-19 restrictions in March 2020.

Other than patient age, we found no differences in tumour characteristics, primary sites, and clinical staging between the two time periods. In particular, tumours were not more advanced during the pandemic. These results contradict most studies about the impact of COVID-19 on head and neck cancer care. The COVIDSurg collaborative multicentre study 14 and several other studies revealed a trend toward larger tumours, higher stages and aggravated nodal status during the COVID-19 pandemic 12,15. Similar observations were noted for other cancer entities 2. However, the impact of COVID-19 on head and neck cancer care differed among countries. For example, studies from France showed no change in tumour stage during the pandemic 16. Even within high-income countries, contradictory results have been observed. While a study from California by Solis et al. 12 noted more extensive tumours and higher T categories, a study from Tennessee by Stevens et al. 17 reported no such differences. Although the lack of generalisability of single-centre studies is considered a limitation, we believe that studies from different areas are essential to reflect the different needs of the specific local population.

As aforementioned, the cohort was significantly older during the pandemic, compared to the pre-COVID-19 group, which might have been caused due to fear of transmission by the younger population. Undoubtedly, the COVID-19 outbreak had an unprecedented effect on healthcare providers worldwide. Especially in the early phase, the COVID-19 pandemic was associated with uncertainties regarding transmission, severity of the disease, and mortality rates. Recent studies proved that the fear of COVID-19 infection and transmission caused patients to cancel elective surgeries to avoid hospital admissions 18. Furthermore, in patients with oncologic diseases, gaps in oncologic care and isolation during the COVID-19 pandemic severely aggravated those fears 11,19. At the beginning of the pandemic, it was suspected that due to poor survival rates, higher numbers of physical and psychological comorbidities, and social isolation, older people would be significantly more affected by COVID-19-related fear 20. However, the current literature shows a trend towards lower levels of COVID-19 related anxiety and depression in older people than in younger people. A study from Brazil showed, despite higher chances of severe disease and higher mortality, that people over 60 had a significant decrease in fear of infection or transmission 19. This age-related protective effect of COVID-19-related fear was also shown in studies from Qatar, Spain, and China 20-22. A nationwide multicentre study by Wang et al., involving 19,372 individuals, revealed that those aged 35-49 had more severe depressive and anxiety symptoms compared to other age groups, especially those aged 65 and above 20. We therefore suggest that higher fear in younger people might have led to fewer hospital presentations during the COVID-19 pandemic. Nevertheless, cultural differences regarding beliefs and values around health and illness, social norms like mask-wearing and social distancing, trust in authorities, communal responsibility, and obedience to governmental restrictions, might significantly impact the individual country’s response to the COVID-19 pandemic. Understanding these differences is important for developing targeted, effective interventions adapted to the specific patient population to ultimately improve the management of head and neck cancer patients.

Several strategies have been proposed to address the age-related fear of COVID-19 in cancer care. First, telemedicine approaches can ensure early detection and regular follow-up of head and neck cancer patients while being accepted by a broad range of patient populations 23. This approach allows individuals with high levels of COVID-19 anxiety to stay away from hospitals. Furthermore, implementing contingency plans can instill a sense of security and ensure the continuity of patient care during a pandemic 24.

Finally, this was the first study on the effects of the pandemic on the treatment of head and neck cancer patients in B&H. Interestingly, B&H was the country with the fourth highest mortality due to COVID-19 globally in January of 2021 8. The country faced political and bureaucratic obstacles that hindered its ability to effectively response to the pandemic 8. Additionally, the relatively low level of public awareness and compliance with public health guidelines, such as wearing masks and social distancing, may have contributed to the rapid spread of the virus within communities 8. Accordingly, the present study’s results are reassuring and show that our reference center was able to maintain a stable level of head and neck cancer patient care during the pandemic, despite several pandemic-related restraints.

Several limitations counter the findings of the present study. First, the retrospective design is associated with an inherent bias regarding data availability due to the use of historical data, which did not allow us to retrieve time intervals between diagnosis and treatment initiation. Moreover, it should be further elucidated if the pandemic hindered timely therapy starting after a diagnosis of cancer. Additionally, the generalisability of our results may be limited since our study is a single-institution experience. Future studies should implement a multicentric assessment of hospitals in B&H or from adjacent regions to create a more comprehensive picture and point out the specific needs of this patient population.

Conclusions

This study provides insights into the effects of the COVID-19 pandemic on managing head and neck cancer patients in the middle-income country of B&H. The pandemic cohort presented with a significantly older population, emphasising the potential impact of disease-related anxiety on younger individuals, which may result in delayed diagnosis and treatment of cancer. Future efforts should prioritise this population’s specific informational and psychological needs to ensure timely and appropriate cancer care, especially in the event of future pandemics. Furthermore, this study can serve as a foundation for future research on the impact of COVID-19 on cancer patients within different healthcare systems.

Conflict of interest statement

The authors declare no conflict of interest.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Author contributions

AL: design, acquisition of data, analysis, and writing of the manuscript; FB: design, analysis, and supervision; DTL: design, acquisition of data, analysis, and critical revision of the manuscript; MH: design, analysis, and critical revision of the manuscript; AS: design, acquisition of data, analysis, and critical revision of the manuscript; AI: acquisition of data, and critical revision of the manuscript; TT: analysis, and critical revision of the manuscript; SU: acquisition of data, and critical revision of the manuscript; AH: acquisition of data, and critical revision of the manuscript; FFB: design, acquisition of data, analysis, writing of the manuscript, and supervision.

Ethical consideration

The current study was approved by the Ethics Committee of the University Clinical Center Tuzla (Nr. 02-09/2-29/22) and was conducted following the principles of the Declaration of Helsinki. Patient consent was waived due to the retrospective nature of the study.

Figures and tables

Variables/categories Total (n = 228) pre-COVID-19 (n = 87) COVID-19 (n = 141) Difference between pre-COVID-19 and COVID-19 p value
Age
   < 65 116 53 (60.9%) 63 (44.7%) -16.2%
   ≥ 65 112 34 (39.1%) 78 (55.3%) 16.2% 0.017
Gender
   Male 161 65 (74.7%) 96 (68.1%) -6.6%
   Female 67 22 (25.3%) 45 (31.9%) 6.6% 0.286
Table I.Age and gender distribution. Significant results (p ≤ 0.05) are highlighted in bold. Distributional differences between the pre-COVID-19 and the COVID-19 groups were analyzed using Pearson’s chi-square test.
Variables/categories Total (n = 228) pre-COVID-19 (n = 87) COVID-19 (n = 141) Difference between pre-COVID-19 and COVID-19 p value
Histology
   Squamous cell 161 60 (69%) 101 (71.6%) 2.7%
   Papillary thyroid 37 16 (18.4%) 21 (14.9%) -3.5%
   Follicular thyroid 6 3 (3.4%) 3 (2.1%) -1.3%
   Medullary thyroid 2 1 (1.1%) 1 (0.7%) -0.4%
   Basal cell 7 1 (1.1%) 6 (4.3%) 3.1%
   Malignant melanoma 3 2 (2.3%) 1 (0.7%) -1.6%
   Myoepithelial 4 1 (1.1%) 3 (2.1%) 1%
   Adenoid cystic 2 0 (0%) 2 (1.4%) 1.4%
   Invasive ductal 1 0 (0%) 1 (0.7%) 0.7%
   Other§ 5 3 (3.4%) 2 (1.4%) -2% 0.712
Primary site
   Head and neck 155 59 (67.8%) 96 (68.1%) 0.3%
   Thyroid 47 19 (21.8%) 28 (19.9%) -2%
   Skin 26 9 (10.3%) 17 (12.1%) 1.7% 0.886
Head and neck subsite
   Larynx 103 42 (71.2%) 61 (63.5%) -7.6%
   Oropharynx 26 11 (18.6%) 15 (15.6%) -3%
   Hypopharynx 6 1 (1.7%) 5 (5.2%) 3.5%
   Nasopharynx 1 1 (1.7%) 0 (0%) -1.7%
   Sinonasal 5 1 (1.7%) 4 (4.2%) 2.5%
   Salivary gland 5 1 (1.7%) 4 (4.2%) 2.5%
   CUP 9 2 (3.4%) 7 (7.3%) 3.9% 0.565
T category
   Tis 11 3 (3.4%) 8 (5.7%) 2.2%
   T1 69 23 (26.4%) 46 (32.6%) 6.2%
   T2 65 24 (27.6%) 41 (29.1%) 1.5%
   T3 57 24 (27.6%) 33 (23.4%) -4.2%
   T4 18 10 (11.5%) 8 (5.7%) -5.8%
   Tx 8 3 (3.4%) 5 (3.5%) 0.1% 0.566
N category
   N0 129 43 (49.4%) 86 (61%) 11.6%
   N1 27 17 (19.5%) 10 (7.1%) -12.4%
   N2 33 11 (12.6%) 22 (15.6%) 3%
   N3 15 6 (6.9%) 9 (6.4%) -0.5%
   Nx 24 10 (11.5%) 14 (9.9%) -1.6% 0.067
M category
   M0 227 87 (100%) 140 (99.3%) -0.7%
   M1 1 0 (0%) 1 (0.7%) 0.7% 1.000
Stage
   0 11 3 (3.4%) 8 (5.7%) 2.2%
   I 76 27 (31%) 49 (34.8%) 3.7%
   II 50 20 (23%) 30 (21.3%) -1.7%
   III 35 16 (18.4%) 19 (13.5%) -4.9%
   IV 51 19 (21.8%) 32 (22.7%) 0.9% 0.806
   Unknown 5 2 (2.3%) 3 (2.1%) -0.2%
Grading
   G1 10 5 (5.7%) 5 (3.5%) -2.2%
   G2 84 29 (33.3%) 55 (39%) 5.7%
   G3 44 15 (17.2%) 29 (20.6%) 3.3% 0.609
   Unknown 88 36 (41.4%) 52 (36.9%) -4.5%
CUP: cancer of unknown primary; §: sarcoma (n = 4); chordoma (n = 1).
Table II.Tumour characteristics. Distributional differences between the pre-COVID-19 and the COVID-19 groups were analysed using Fisher’s exact or Pearson’s chi-square test.
Variables/categories Total (n = 228) pre-COVID-19 (n = 87) COVID-19 (n = 141) Difference between pre-COVID-19 and COVID-19 p value
Primary treatment
   Primary surgery 186 71 (81.6%) 115 (81.6%) 0%
   RT 8 4 (4.6%) 4 (2.8%) -1.8%
   CHT 1 0 (0%) 1 (0.7%) 0.7%
   RCHT 4 1 (1.1%) 3 (2.1%) 1%
   Palliative care 17 6 (6.9%) 11 (7.8%) 0.9%
   Unknown 12 5 (5.7%) 7 (5%) -0.8% 0.975
RT: radiotherapy; CHT: chemotherapy; RCHT: radio-chemotherapy.
Table III.Treatment modalities of cancer patients. Distributional differences between the pre-COVID-19 and the COVID-19 groups were analysed using Fisher’s exact test.

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Affiliations

Alexander Lein

Department of Otorhinolaryngology, Head and Neck Surgery, Medical University of Vienna, Vienna, Austria

Fuad Brkic

Department of Otorhinolaryngology, University Clinical Center Tuzla, Tuzla, Bosnia and Herzegovina

David T. Liu

Department of Otorhinolaryngology, Head and Neck Surgery, Medical University of Vienna, Vienna, Austria

Markus Haas

Department of Otorhinolaryngology, Head and Neck Surgery, Medical University of Vienna, Vienna, Austria

Almir Salkic

Department of Otorhinolaryngology, University Clinical Center Tuzla, Tuzla, Bosnia and Herzegovina

Azra Ibrisevic

Department of Otorhinolaryngology, University Clinical Center Tuzla, Tuzla, Bosnia and Herzegovina

Sabrina Uscuplic

Department of Otorhinolaryngology, University Clinical Center Tuzla, Tuzla, Bosnia and Herzegovina

Alen Harcinovic

Department of Otorhinolaryngology, University Clinical Center Tuzla, Tuzla, Bosnia and Herzegovina

Thomas Thurner

Department of Otorhinolaryngology, Head and Neck Surgery, Medical University of Vienna, Vienna, Austria

Faris F. Brkic

Department of Otorhinolaryngology, Head and Neck Surgery, Medical University of Vienna, Vienna, Austria

Copyright

© Società Italiana di Otorinolaringoiatria e chirurgia cervico facciale , 2024

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