Impact of the COVID-19 Pandemic on Cervical Cancer Screening in Brazil: A Nationwide Population-Based Study

Abstract

Cervical cancer is a leading cause of morbidity and mortality among women, particularly in low- and middle-income countries. Early detection through routine Pap smear screening is essential to prevent disease progression. The COVID-19 pandemic severely disrupted healthcare services worldwide, including cancer screening programs. This study aimed to evaluate the impact of the COVID-19 pandemic on cervical cancer screening in Brazil. A nationwide retrospective population-based study was conducted using data from the Cancer Information System (SISCAN) of Brazil’s public health system (SUS). Data from 2018–2019 (pre-pandemic) were compared to 2020–2021 (pandemic period) regarding the number of Pap smear tests performed, regional distribution, and diagnostic outcomes. Furthermore, data from 2022–2023 were incorporated to evaluate the volume of cytopathological exams performed in the post-pandemic context. Statistical analyses included paired t-tests, Wilcoxon signed-rank tests, and repeated measures ANOVA with Bonferroni correction. A significant reduction in Pap smear testing was observed nationwide during the pandemic (p < 0.01), with variations across regions. Despite fewer screenings, there was an increase in unsatisfactory exams and a rise in adenocarcinoma and atypical findings in some regions. In contrast, the post-pandemic period showed a significant recovery in the number of exams, reaching volumes comparable to those observed before the pandemic (p < 0.05). The COVID-19 pandemic substantially reduced cervical cancer screening coverage in Brazil, highlighting structural vulnerabilities in the healthcare system. Strengthening organized screening programs is essential to mitigate the long-term impact of these disruptions.

1. Introduction

Cervical cancer remains a leading cause of morbidity and mortality among women worldwide, with early detection through Pap smear screening being the most effective method for preventing the disease [1,2]. In Brazil, the public health system plays a crucial role in providing access to cervical cancer screening, aiming to detect precursor lesions early and reduce cancer-related deaths [3]. Organized and timely screening strategies are essential, especially in settings with high incidence rates and significant regional disparities in access to healthcare services.

However, on 11 March 2020, the World Health Organization declared the global outbreak of coronavirus disease 2019 (COVID-19) a pandemic. The primary focus for most countries then shifted to the care and treatment of COVID-19 patients, significantly disrupting global healthcare systems, including those in Brazil. To mitigate the transmission of COVID-19 and maintain health system capacity, the government implemented numerous public health measures, such as social distancing and lockdowns. These measures led to the postponement of non-essential medical services [4,5].

This interruption severely impacted the continuity of routine screenings, including Pap smears, which are crucial for the early detection of cervical cancer [6]. Consequently, delays in diagnosis and treatment allowed the progression of neoplasms to advanced stages, resulting in higher mortality rates [7]. The incidence of cervical cancer increased from 43.3% before the pandemic to 56.8% during the pandemic [8], and delays in treatment were associated with an increased mortality rate [9], underscoring the serious implications of screening interruptions on patient outcomes.

Beyond the clinical impact, the pandemic also exposed long-standing structural challenges within the Brazilian healthcare system, including regional inequalities, insufficient workforce distribution, and fragmented data infrastructure [10]. These issues disproportionately affect socioeconomically disadvantaged populations, particularly in the North and Northeast regions, where healthcare resources are often limited and reliance on the public health system is high [11]. The pandemic amplified these disparities, further hindering access to routine preventive care for vulnerable women [12].

Although the impact of the COVID-19 pandemic on cervical cancer screening has been explored in previous studies [13,14,15], there is still a need for nationally representative analyses that incorporate detailed geographic, demographic, and temporal perspectives. This study addresses this gap by evaluating the effects of the pandemic on cervical cancer screening in Brazil using official, population-based data, with stratification by region and age group. In addition to comparing pre-pandemic (2018–2019) and pandemic (2020–2021) periods, the study includes data from 2022–2023 to assess the recovery of screening coverage in the post-pandemic context.

By identifying trends in Pap smear testing and diagnostic outcomes across different phases, this research offers valuable evidence to inform the reorganization of early detection programs, promoting resilience, equity, and continuity of care within the Brazilian public health system.

2. Materials and Methods

2.1. Study Design and Population

The study used a retrospective, population-based design. Data were collected from the DATASUS platform, specifically the Cancer Information System (SISCAN), which is a nationwide public health database managed by the Ministry of Health. This database includes information on the number of cervical cancer screening tests conducted in the public health system network, categorized by region, age group, and cytological diagnosis. The study population consisted of women who were eligible for cervical cancer screening through the SUS, aged from 25 to 64 years, during the years 2018–2021. Data were extracted for the following periods: pre-pandemic (2018–2019) and pandemic (2020–2021).

2.2. Data Collection and Variables

Data on the number of Pap smears performed were collected by region (North, Northeast, Central-West, Southeast, and South) and age group (25–49, 50–64). Cytological diagnoses were also recorded, including negative for intraepithelial lesion or malignancy (NILM), atypical squamous cells of undetermined significance (ASC), low-grade squamous intraepithelial lesions (LSIL), high-grade squamous intraepithelial lesions (HSIL), and cases of adenocarcinoma. The main outcome was the number of Pap smear tests performed during each period, and secondary outcomes included changes in the diagnostic categories over time. To assess the impact of the pandemic on screening, the number of tests performed during the pandemic (2020–2021) was compared to the pre-pandemic period (2018–2019).

2.3. Statistical Analyses

Descriptive statistics were used to summarize the data. Categorical variables were analyzed using absolute and relative frequencies. To assess the impact of the COVID-19 pandemic on the number of Pap smears performed, the monthly volumes across three periods—pre-pandemic (2018–2019), pandemic (2020–2021), and post-pandemic (2022–2023)—were compared. For this purpose, a repeated measures analysis of variance (ANOVA) was applied, followed by Bonferroni-adjusted post hoc pairwise comparisons to identify specific differences between periods. To compare the number of Pap smears performed before and during the pandemic, the relative change between the periods was calculated using the following formula:

$$\mathrm{R}\mathrm{e}\mathrm{l}\mathrm{a}\mathrm{t}\mathrm{i}\mathrm{v}\mathrm{e}\mathrm{ }\mathrm{C}\mathrm{h}\mathrm{a}\mathrm{n}\mathrm{g}\mathrm{e}(\%)=\left({\displaystyle \frac{{{Exams}_{2020-2021}-Exams}_{2018-2019}}{{Exams}_{2018-2019}}}\right)\times 100$$

The Shapiro–Wilk test was applied to verify the normality of the distribution of continuous variables. For normally distributed data, the t-test for paired samples was used to compare the monthly number of tests between the two periods at the national level and by region. For non-normally distributed data, the Wilcoxon test was applied. All statistical analyses were conducted using R software (version 4.5.1), JASP software (version 0.14.1) and Microsoft Excel (version 2016), with a significance level set at 5%.

2.4. Ethical Considerations

Given that this study used publicly available secondary data without personal identification, it did not require approval from an ethics committee. However, the data were collected and analyzed following the ethical standards outlined by the Ministry of Health for public health research.

3. Results

During the pandemic period, there was a significant reduction in the total number of Pap smears performed across Brazil compared to the pre-pandemic period (p < 0.01). When comparing the monthly volume of cytopathological exams across the three periods (2018–2019, 2020–2021, and 2022–2023), a statistically significant difference was observed for Brazil as a whole (p < 0.01), as well as when considering the five macro-regions separately (p = 0.013) (

Table 1. Cytopathological exams performed in the periods 2018–2019, 2020–2021, and 2022–2023, in Brazil and by region (n = 38,985,844).

Variables	Period			p-Value *
	2018–2019	2020–2021	2022–2023
Monthly volume of cytopathological exams in Brazil	1,161,819 ± 114,720	834,783 ± 228,871	1,252,218 ± 226,578	<0.01
Volume of cytopathological exams by Region	2,788,366 ± 1,718,076	2,003,480 ± 1,216,074	3,005,323 ± 1,741,790	0.013

Data are expressed as mean and standard deviation (mean ± standard deviation). * The significance of the difference in monthly means between periods was assessed using repeated measures ANOVA, followed by pairwise comparisons with Bonferroni adjustment.

).

Post hoc pairwise comparisons using Bonferroni-adjusted t-tests revealed significant reductions in the national monthly average between 2018–2019 and 2020–2021 (p = 0.001), and a subsequent significant increase between 2020–2021 and 2022–2023 (p = 0.001). No statistically significant difference was found between 2018–2019 and 2022–2023 (p = 0.390), suggesting a recovery to pre-pandemic levels. Regionally, the only significant post hoc difference was observed between 2020–2021 and 2022–2023 (p = 0.043), reinforcing the evidence of recovery in cytopathological screening after the critical pandemic period.

Figure 1 presents the number of cytopathological exams conducted in Brazil by region during the pre-pandemic and pandemic periods. Figure 2 shows the relative variation in the number of cytopathological exams between 2018–2019 and 2020–2021 by age group in Brazil and by region.

Although there was a reduction in the number of Pap smears performed across the five macro-regions of Brazil, a notable shift in the profile of cytopathological reports captured by the TABNET system was observed. Despite the decrease in the number of exams performed during the pandemic period (2020–2021) compared to the pre-pandemic period (2018–2019), there was an increase in the number of unsatisfactory reports. Additionally, an increase in adenocarcinoma reports was observed in the South region and atypical squamous cells of undetermined significance (ASC-US) in the North region during 2020–2021 (Figure 3).

Student’s t-test for paired samples or the Wilcoxon test were applied to determine if there were differences between periods in the following factors: (1) monthly volume of cytopathological exams; (2) volume of cytopathological exams by region; and (3) volume of cytopathological exams by type of report, both in Brazil and by region. The results are presented in

Table 2. Evaluation of differences in exam quantities between periods: 2018–2019 and 2020–2021, in Brazil and its regions.

Variables	Test Statistic	p-Value *
Monthly volume of cytopathological exams in Brazil	5.121	<0.01
Cytopathological exams by region	3.467	0.026
Cytopathological exams by report type in the North Region	−0.405	0.686
Cytopathological exams by report type in the Northeast Region	−1.214	0.225
Cytopathological exams by report type in the Southeast Region	−1.483	0.138
Cytopathological exams by report type in the South Region	−1.214	0.225
Cytopathological exams by report type in the Central-West Region	−1.483	0.138
Cytopathological exams by report type in Brazil	−1.214	0.225

* Significance of the difference in monthly means between periods was assessed using Student’s t-test for related samples or the Wilcoxon test. Bold values indicate significance at p < 0.05.

. In the analysis of exams conducted per month, significant differences were found in the quantity performed in the two periods (p < 0.01). However, in the analysis by type of report, the changes did not show significant differences between periods (p > 0.05) (Table 2).

4. Discussion

This study evaluated the impact of the COVID-19 pandemic on cervical cancer screening in Brazil. The findings indicate a significant reduction in Pap smear tests conducted during the pandemic period, posing a challenge to the early detection of precursor lesions for cervical cancer. Despite being a simple and cost-effective screening tool, systemic limitations and the strain caused by COVID-19 hindered the continuity of preventive healthcare services [16].

The disruption to normal healthcare services caused by the pandemic is likely to lead to increased numbers of cervical cancers being diagnosed during the recovery period [13,17]. The redirection of Brazil’s public healthcare system resources to COVID-19 care, including the suspension of elective and outpatient services, contributed to the reduced availability of Pap smear testing [4,16]. This aligns with other studies reporting similar declines in screening rates globally during the pandemic [4,18,19].

Clinically, the reduction in screening volumes may result in delayed diagnosis of cervical intraepithelial neoplasia, increasing the risk of progression to invasive cancer, which can worsen prognosis, increase treatment complexity, and raise cancer-related mortality, particularly among underserved populations [20,21]. Economically, the treatment of advanced cervical cancer is significantly more expensive than early-stage interventions, potentially increasing the financial burden on the Brazilian public health system and widening health inequities.

Similar patterns have been reported in other low- and middle-income countries where disruptions in screening during the pandemic led to substantial decreases in early detection and increased diagnosis of advanced cases [18,22,23,24]. In contrast, high-income countries with organized screening systems demonstrated a faster recovery in screening coverage post-lockdown, maintaining more equitable access across different population groups [25,26]. This contrast highlights the importance of structured, population-based screening programs in ensuring resilience during health emergencies. Notably, our study demonstrated an increase in unsatisfactory cytological test results, likely due to high turnover and reduced training of healthcare personnel during this period [13].

The pandemic exposed structural vulnerabilities within Brazil’s healthcare system, particularly affecting populations in socioeconomically disadvantaged regions [18,27], as shown by results from studies [28,29,30,31,32]. To reduce regional disparities, especially in the North and Northeast, policies must prioritize equitable distribution of human and technological resources. Strengthening the training of cytology professionals and expanding community-based outreach strategies, such as mobile clinics and culturally tailored education campaigns, would further enhance access and improve early detection outcomes.

In addition to the overall reduction in Pap smear volume, changes in the diagnostic profile of cytological reports deserve attention. Despite fewer exams during the pandemic, we reported an increase in the absolute number of unsatisfactory results, suggesting a decline in sample quality likely due to staff shortages, insufficient training, or operational strain in primary care. Studies reported similar findings at the national level, highlighting growing concerns about sample adequacy during this period [33,34]. Regionally, the South showed more adenocarcinoma diagnoses, and the North had increased ASC-US findings. Though not statistically significant, they suggest potential shifts in lesion detection patterns, possibly due to delayed follow-up, underdiagnosis in earlier stages, or changes in case severity resulting from disruptions in screening services.

Several individual- and community-level barriers likely contributed to the decline in screening rates. Fear of contracting COVID-19 at healthcare facilities discouraged many women from seeking preventive care, particularly those with underlying health conditions or those responsible for caregiving roles [33]. Limitations in public transportation during lockdowns further reduced access to screening services, especially in rural or peripheral urban areas [34].

Moreover, many primary care units were repurposed for COVID-19 care or operated at reduced capacity, compromising the availability of routine gynecological services. These challenges were particularly acute for women of lower socioeconomic status, who often rely exclusively on the public health system. Geographic disparities in infrastructure and workforce may have further amplified these inequalities, especially in the North and Northeast regions compared to the more developed South and Southeast [34,35].

This study has limitations. As an ecological study using secondary aggregated data, we cannot infer individual-level associations or control for potential confounders such as health-seeking behaviors, comorbidities, or access to private services. Therefore, caution is warranted when interpreting regional variations, as aggregated data may lead to ecological fallacies, where group-level associations do not necessarily reflect individual-level realities. In addition, coverage bias may exist, especially in remote or underserved regions where underreporting is more likely.

The data also do not account for variations in regional public health policies, the availability of trained personnel, or temporary administrative barriers that could have influenced screening rates independently of the pandemic. Finally, the absence of demographic and socioeconomic indicators (such as education, race/ethnicity, and income) limits our ability to assess disparities and equity in access to screening services.

Therefore, our study highlights the need for a robust public health framework capable of sustaining preventive programs during emergencies. Policymakers must prioritize reorganizing cancer screening and care services, ensuring they remain accessible and effective even in challenging scenarios. These steps are crucial to reducing the long-term impacts of delayed cancer diagnosis and treatment.

To strengthen the resilience and equity of cervical cancer screening in Brazil, key policy actions should include transitioning to an organized, population-based program integrated with digital health systems for real-time tracking and follow-up. A centralized call-and-recall infrastructure with predefined screening intervals is essential to ensure regular participation. Expanding mobile health units and outreach initiatives can help overcome geographic and logistical barriers. Equitable allocation of financial and human resources, including the training and distribution of cytology professionals, must be prioritized. Finally, integrating screening continuity into national emergency preparedness protocols is crucial to safeguard preventive services during future crises.

5. Conclusions

COVID-19 disrupted cervical cancer screening in the public health system network, worsening healthcare disparities. The study highlights the need for resilient health systems that ensure continuous services during crises. Transitioning to organized screening models and strengthening healthcare worker training are essential to address these challenges. Further research is needed to assess the long-term impact of screening delays and guide policies to minimize future disruptions in cancer care.