(2024) 22:327
Ortiz et al. BMC Medicine
https://doi.org/10.1186/s12916-024-03535-4

BMC Medicine

RESEARCH

Open Access

Recent cervical cancer incidence, stage
at diagnosis, and mortality trends in Puerto
Rico, 2001–2019
Ana P. Ortiz1,2*, Carlos R. Torres‑Cintrón3, Eduardo J. Santiago‑Rodríguez1, Jeslie M. Ramos‑Cartagena1,
Tonatiuh Suárez‑Ramos3, Haluk Damgacioglu4,5, Vivian Colón‑López1, Karen J. Ortiz‑Ortiz1,2,3 andAshish A. Deshmukh4,5

Abstract
Background Cervical cancer incidence is rising in Puerto Rico (PR). Whether the increase is real or reflectiveof increased diagnostic scrutiny remains unclear.
Methods Using data from the PR Central Cancer Registry for 2001–2019, we estimated trends of hysterectomy-corrected cervical cancer incidence and mortality rates, overall, and by stage at diagnosis and age.
Results Overall, cervical cancer incidence (per 100,000) increased 1.6%/year (95% CI, -0.5% to 3.8%) from 12.5 to 15.3,
with a prominent increase in distant-stage disease (4.5%/year [95% CI, 1.6% to 8.0%]), particularly among screening
age eligible (25–64-year-old) women (5.8%/year [95% CI, 2.1% to 10.6%]). Mortality rates in this age-group remained
stable during the study period.
Conclusions Increased occurrence of distant-stage disease among screening-eligible women is troubling and may
reflect a real increase. Future research is needed to elucidate the factors underlying these trends. Improved prevention
is also an urgent priority to reverse the rising cervical cancer incidence in PR.
Keywords Cervical cancer, Incidence, Mortality, Epidemiology, Puerto Rico*Correspondence:
Ana P. Ortiz
ana.ortiz7@upr.edu
1
University of Puerto Rico Comprehensive Cancer Center, P.O.
Box 363027, 00936‑3027 San Juan, Puerto Rico
2
Graduate School of Public Health, Medical Sciences Campus, Universityof Puerto Rico, San Juan, Puerto Rico
3
Comprehensive Cancer Center, Puerto Rico Central Cancer Registry,
Cancer Control and Population Sciences Division, University of Puerto
Rico, San Juan, Puerto Rico
4
Department of Public Health Sciences, Medical University of South
Carolina, Charleston, SC, USA
5Hollings Cancer Center, Medical University of South Carolina, Charleston,SC, USA

Background
Cervical cancer continues to be a major public healthissue among the Hispanic population living in the
United States (US) [1]. Unfortunately, in recent years,
cervical cancer incidence has not decreased in themainland US [2]. On the other hand, Puerto Rico (PR),a US territory that is home to nearly 2 million Hispanic
or Latino population, is seeing a continued rise in cervical cancer incidence [3]. Timely follow-up care andtreatment after an abnormal Pap result have been hampered due to repetated disaster events and the decreasing number of gynecologists on the island, where
healthcare infrastructure is already inadequate [4]. As
a result, cervical cancer incidence patterns, particularly stage at diagnosis, and mortality may have been

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Ortiz et al. BMC Medicine(2024) 22:327

influenced in recent years. In this study, we sought toevaluate trends of hysterectomy-corrected cervicalcancer incidence and mortality rates in PR, overall andstratified by stage at diagnosis and age.

Methods
Incidence and mortality data were obtained from the
PR Central Cancer Registry for 2001–2019, which collects sociodemographic and clinical information on all
cancers diagnosed. We also used data from the 17-registries Surveillance, Epidemiology, and End Results(SEER) Program for 2001–2019, and evaluated incidence trends among Hispanic women in the mainland
US. Cervical cancer cases were identified using theInternational Classification of Diseases for Oncology
Third Edition site codes C53.0 to C53.9, and histology
codes 8010 to 8671 and 8940 to 8941were used in orderto focus on HPV-associated cases only. Hysterectomy
information was obtained from the Behavioral Risk
Factor Surveillance System (BRFSS) during the study
period. Hysterectomy-corrected incidence and mortality rates were estimated following methods employedin similar studies [5, 6].
BRFSS is a nationally representative survey conductedby phone in the US and three territories (includingPR) and collects information about health-related risk
behaviors, health conditions, and the use of preventive
services [7]. Logistic regression was used to calculatesmoothed hysterectomy prevalence estimates considering age groups (18–24, 25–29, 30–34, 35–39, 40–44,
45–49, 50–54, 55–59, 60–64, 65–69, 70–74, 75–79, and80 + years), survey years, and an interaction term forage group and survey year. Age and year specific hysterectomy prevalence rates were used to estimate thecorresponding population at-risk, by excluding the proportion of women with a history of hysterectomy fromthe denominators. After the corrections for hysterectomy
prevalence were completed, incidence and mortality
rates were standardized based on the age distribution of
the 2000 US population.
Joinpoint Regression Program software (version
5.0.2) was used to estimate annual percent changes(APC) and average annual percent changes (AAPC)of trends, with their corresponding 95% confidence
intervals (95% CI), which were calculated using theempirical quantile method. Incidence analysis was
stratified by stage (localized, regional, and distant)and age (< 25 years, 25–64 years and ≥ 65 years), andmortality analysis was stratified by age (< 25 years,
25–64 years and ≥ 65 years). Since all the information
evaluated in this study was de-identified, the University of Puerto Rico Comprehensive Cancer Center

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Institutional Review Board considered this study
exempt.

Results
A total of 3,916 cervical cancer cases were diagnosedin PR during the study period. Trends of hysterectomycorrected cervical cancer incidence rates are presented inTable 1. During 2001–2019, hysterectomy-corrected cervical cancer incidence in PR (per 100,000 person-years)
increased from 12.5 to 15.3 (AAPC, 1.6% [95% CI, -0.5%
to 3.8%]), largely driven by a marked rise during 2001–2010 (APC, 3.5% [95% CI, 1.3% to 26.6%]). In recent years(2010–2019), incidence moderated (APC, -0.3% [ 95% CI,-17.8% to 1.9%]).
Trends in incidence according to stage at diagnosis arealso presented in Table 1. Notably, distant stage cervicalcancer incidence increased 4.5%/year (95% CI, 1.6% to8.0%) during 2001–2019. Localized stage cervical cancer
incidence increased, although not significantly, during
2001–2009 (APC, 4.5% [95% CI, -4.8% to 11.9%]), followed by a non-significant decrease during 2009–2013(APC, -9.8% [95% CI, -18.6% to 10.9%]) and a recent nonsignificant increase during 2013–2019 (APC, 3.5% [95%CI, -3.3% to 22.4%]). Regional stage cervical cancer incidence increased during 2001–2017 (APC, 2.6% [95% CI,
1.7% to 4.8%]), followed by a decline in 2017–2019 (APC,-16.3% [95% CI, -25.3% to -0.3%]).
Trends of cervical cancer incidence comparing Puerto
Rican and Hispanic women in the US are presented inFig. 1. Contrary to PR, cervical cancer incidence among
Hispanic women in the US is decreasing overall, andfor localized and regional stages. For distant stage, we
observed that US Hispanic women have a higher incidence. Despite of this, late-stage diagnoses among US
Hispanic women have stabilized, while we observed anincrease in PR.
In the analysis stratified by age, overall, non-significant
changes in incidence rates were observed among theyoungest (< 25 years) (APC, 1.2% [95% CI, -7.0% to 9.5%])and oldest (≥ 65 years) (AAPC, -1.1% [95% CI, -3.3% to1.2%]) age groups. Among 25–64-year-old group, incidence fluctuated during the study period, with a nonsignificant decrease during 2001–2005 (APC, -2.9% [95%CI, -12.9% to 3.4%]), followed by a significant increaseduring 2005–2009 (APC, 9.7% [95% CI, 2.6% to 17.0%]),and a recent stabilization during 2009–2019 (APC, 0.1%
[95% CI, -2.3% to 1.7%]).
Trends of cervical cancer incidence rates by age andstage at diagnosis, reveal that in the 25–64-year-old
group, localized tumors did not change during 2001–
2019 (APC, 0.3% [95% CI, -1.5% to 2.0%]). Regional stage
tumors had a significant increase during 2001–2017(APC, 4.0% [95% CI, 9.0% to 38.8%]), followed by a recentOrtiz et al. BMC Medicine(2024) 22:327

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Table 1 Trends of hysterectomy-corrected cervical cancer incidence rates in Puerto Rico, by stage at diagnosis and age, 2001–2019
2001–2019

Overall

Calendar trends

Cases

Ratea

3,916

14.46

Periodb

APC, % (95% CI)

AAPC, % (95% CI)

2001–2010

3.5 (1.3 to 26.6)*

1.6 (-0.5 to 3.8)

2010–2019-0.3 (-17.8 to 1.9)

Stage
Localized

Regional

1,910

1,098

7.05

4.05

2001–2009

4.5 (-4.8 to 11.9)

2009–2013-9.8 (-18.6 to 10.9)

2013–2019

3.5 (-3.3 to 22.4)

2001–2017

2.6 (1.7 to 4.8)*

2017–2019-16.3 (-25.3 to -0.3)*

0.8 (-1.0 to 2.5)

0.3 (-0.9 to 2.0)

Distant291

1.07

2001–2019

4.5 (1.6 to 8.0)*

4.5 (1.6 to 8.0)*

Unknown

617

2.29

2001–2007-12.1 (-41.4, -0.1)*

2.7 (-0.6 to 5.8)

2007–201141.4 (15.4, 84.2)*

2011–2019-1.7 (-12.0, 3.6)

Age group, y< 25Overall46

0.36

Localized

NA

0.19

2001–2019

1.2 (-7.0 to 9.5)

1.2 (-7.0 to 9.5)––

Regional

NA

–

–

–

Distant

NA

–

–

–

Unknown

NA

–

–

–

3,007

21.53

2001–2005-2.9 (-12.9 to 3.4)

1.5 (0.6 to 2.5)*

2005–2009

9.7 (2.6 to 17.0)*

25–64
Overall

2009–2019

0.1 (-2.3 to 1.7)

Localized

NA

11.11

2001–2019

0.3 (-1.5 to 2.0)

0.3 (-1.5 to 2.0)

RegionalNA

6.01

2001–2017

4.0 (9.0 to 38.8)*

1.6 (-1.0 to 6.2)

2017–2019-16.2 (-35.5 to 4.6)

Distant

NA

1.53

2001–2019

5.8 (2.1 to 10.6)*

5.8 (2.1 to 10.6)*

UnknownNA

2.88

1.2 (-2.1 to 4.5)

2001–2006-18.1 (-48.3, -2.1)*

2006–201424.1 (15.8, 59.3)*

2014–2019-9.7 (-25.2, 0.0)

≥ 65
Overall

863

24.81

2001–2019-1.1 (-3.3 to 1.2)

-1.1 (-3.3 to 1.2)

Localized

NA

9.52

2001–2006

14.0 (1.4 to 74.8)*-2.6 (-6.2 to 1.3)

2006–2019-8.3 (-15.2 to -5.5)*

Regional

NA

7.07

DistantNA

2.16

UnknownNA

6.06

2001–20192001–2019-2.8 (-5.8 to 0.1)

-2.8 (-5.8 to 0.1)––

4.6 (0.9, 9.5)*

4.6 (0.9, 9.5)*

APC Annual percent change
AAPC Average annual percent changeaRates were calculated as the number of cases per 100,000 person-years, and age-adjusted using the 2000 US populationb

The period of each segment was determined based on the identification of calendar years when a statistically significant change in the APC, or joinpoint, occurred*

Significantly different from 0

NA Number suppressed due to a small value (n < 16) in one of the categories– Could not be calculated

non-significant decrease during 2017–2019 (APC, -16.2%[95% CI, -35.5% to 4.6%]). A significant increase of 5.8%/
year (95% CI, 2.1% to 10.6%) occurred for distant stage

cervical cancer. Among ≥ 65 years group, significant
changes were observed during the study period, with anintial increase during 2001–2006 (APC, 14.0% [95% CI,

Ortiz et al. BMC Medicine(2024) 22:327

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Fig. 1 Trends of hysterectomy-corrected cervical cancer incidence rates in Puerto Rico and US Hispanic women, 2001–2019. Data points represent
observed incidence rates (cases per 100 000 person-years). Rates are age-adjusted to the 2000 US population

1.4% to 74.8%]), followed by a recent decrease in 2006–2019 (APC, -8.3% [95% CI, -15.2% to -5.5%]). A non-significant decrease was observed for regional stage tumors
in the oldest group (APC, -2.8% [95% CI, -5.8% to 0.1%]).
Although hysterectomy-corrected mortality rates(per 100,000 person-years) increased from 2.5 in 2001
to 4.0 in 2019, no significant changes were observed
overall (APC, -0.4% [95% CI, -2.3% to 1.6%]) nor in the
25–64-years age group (APC, 0.4% [95% CI, -1.8% to2.7%]). Among the ≥ 65 years group, a non-significant
initial increase in mortality rate was documented in
2001–2003 (APC, 48.9% [95% CI, -1.2% to 120.1%]),
followed by a significant decrease during 2003–2019(APC, -3.1% [95% CI, -15.1% to -0.9%]) (Table 2).

Discussion
In this population-based analysis of cervical cancer incidence and mortality patterns during 2001–2019 in PR,
we observed that incidence rates increased among thescreening age-eligible (25–64 years) group, while mortality rates remained stable. Increased occurrence of latestage disease and no reductions in mortality suggest thatthe rising of cervical cancer incidence in PR may be realand not reflective of increased screening.
Similar to our findings, a recent US-based study also
demonstrated that distant-stage cervical cancer incidence increased significantly at a similar rate (4.4%/year) among non-Hispanic White women living in lowincome counties and a positive 1.5%/year change was also

Table 2 Trends of hysterectomy-corrected cervical cancer mortality rates in Puerto Rico, by age, 2001–2019
2001–2019

Overall

Calendar trends

Deaths

Rate

948

3.40

a

Periodb

APC, % (95% CI)

AAPC, % (95% CI)

2001–2019-0.4 (-2.3 to 1.6)

-0.4 (-2.3 to 1.6)––

2001–2019

0.4 (-1.8 to 2.7)

0.4 (-1.8 to 2.7)

2001–2003

48.9 (-1.2 to 120.1)

1.6 (-3.4 to 5.9)

2003–2019-3.1 (-15.1 to -0.9)*

Age group, y
< 25

NA

–

25–64

NA

3.97

   ≥ 65

NA

10.37

APC Annual percent change
AAPC Average annual percent changeaRates were calculated as the number of deaths per 100,000 person-years, and age-adjusted using the 2000 US populationb

The period of each segment was determined based on the identification of calendar years when a statistically significant change in the APC, or joinpoint, occurred*

Significantly different from 0

NA Number suppressed due to a small value (n < 16) in one of the categories– Could not be calculated

Ortiz et al. BMC Medicine(2024) 22:327

observed among Hispanic women [8]. Moreover, a study
using data from the Texas Cancer Registry reported that
non-Hispanic Black and Hispanic women had higher
odds of late-stage cervical cancer diagnosis, primarily
attributed to a higher neighborhood socioeconomic disadvantage among these populations [9]. While the reason
for these patterns remains unclear, one may speculatethat suboptimal screening behaviors and disruptions infollow-up care in low-resourced settings may be contributors. Future research is needed to explain these patterns
among low-resourced US settings.
Barriers to cervical cancer screening in PR include low
educational attainment, low income, and lack of healthinsurance, smoking, morbid obesity, and high-risk sexual
behaviors [10–12]. In addition, our research team documented that hurricanes Irma and Maria in 2017 and the
COVID-19 pandemic in 2020 had an impact on cervical cancer screening uptake in the island [13]. Thus, ourstudy findings together with documented barriers toscreening in PR highlight the need for continued efforts
to reduce these barriers and promote the prevention andearly detection of cervical cancer in this population.
More research focused on assessing and addressing
barriers to cervical cancer screening and timely followup and treatment is needed in this population. This willbe essential to achieve the goal of cervical cancer elimination established by the World Health Organization (< 4cases per 100,000 population) [14]. For cervical cancer
screening, our research team documented that 70% ofcervical cancer patients in PR diagnosed from 2011–2014
were screened within 3 years prior their diagnosis [15].
Among these, only 22% were also tested for HPV, showing lower utilization of HPV testing in this populationin comparison to cervical Papanicolau. While future
research should evaluate the impact of HPV testing
uptake on disease trends in PR, our findings evidence significant increases in late stage and not early stage disease.
Unfortunately, similar to the US, strategies to enhance
screening delivery (patient reminder, navigation) are notwidely implemented in PR in the absence of evidence
on their effectiveness and cost-effectiveness. A recently
funded study (Grant: 1R01CA282424) will evaluate theseinterventions and HPV self-sampling approach with thegoal to provide foundational data to ensure the wide
implementation of these interventions.
Strengths of this study include the use of the PR Central Cancer Registry database, which allowed us to have
population-based data from PR to describe the incidence
and mortality rates in our analysis. Among limitations,
we could not include individual information such as history of cervical cancer screening uptake and HPV infection and other information related to barriers to cervicalcancer screening, follow-up, and access to treatment.

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Conclusions
In summary, cervical cancer incidence in PR is increasing, especially distant-stage disease among screening eligible persons. Future research must elucidate the factors
underlying these trends and the potential impact of the
COVID-19 pandemic on future disease trends. Continued improvement in prevention is needed to mitigate therising cervical cancer burden in PR.
Abbreviations
AAPC	Average annual percent change
APC	Annual percent change
BRFSS	Behavioral Risk Factor Surveillance System
PR	Puerto Rico
US	United States
Acknowledgements
Not applicable.
Authors’ contributions
The authors confirm contribution to this paper as follows: study conception
and design: APO, CRT, EJS, JMR, HD, VC, KJO, AAD; data preparation and analysis: CRT, EJS, TSR; interpretation, and writing: APO, EJS, JMR, HD, AAD; supervision: APO, AAD; critical review and editing: all authors. All authors reviewed
the results and approved the submitted manuscript.
Authors’ Twitter handles@AnaPatriOrtiz (APO); @edusan218 (EJS); @ashish_deshmukh (AAD); @GroupHpv (HPV Interest Group led by research team).
Funding
This study was partially funded by the University of Puerto Rico and the
University of Texas MD Anderson Cancer Center Partnership for Excellencein Cancer Research (NCI Grant 2U54CA096297 and Grant 2U54CA096300),
by The effectiveness, cost-effectiveness, and budget impact of interventions
to improve the delivery of cervical cancer screening in Puerto Rico study(NCI Grant 1R01CA282424) and by the National Program of Cancer Registries (NPCR) of the Centers for Disease Control and Prevention (CDC) (Grant
NU58DP006318) to the Puerto Rico Central Cancer Registry (PRCCR). The
funders did not play a role in the design of the study; the collection, analysis,
and interpretation of the data; the writing of the manuscript; and the decision
to submit the manuscript for publication.
Availability of data and materials
The data that supports the findings of this study came from the Puerto RicoCentral Cancer Registry (PRCCR) database. Thus, data from this study is not
publicly available because of the confidentiality agreement between PRCCR
and the authors. Nevertheless, investigators could obtain the data through
PRCCR following the confidentiality procedures. PRCCR data can be requested
through the following site: https://​rcpr.​org/​Datos-​de-C%​C3%​A1ncer/​
Acceso-​a-​Datos.

Declarations
Ethics approval and consent to participate
The University of Puerto Rico Comprehensive Cancer Center Institutional
Review Board considered this study exempt (number: 2019–09-11).
Consent for publication
Not applicable.
Competing interests
Dr. Deshmukh reported receiving consulting fees from Merck Inc and Value
Analytics Lab outside the submitted work. Dr. Ortiz has been a consultant
for Merck Inc and participates in an institutional grant funded by Merck Inc
outside the submitted work. No additional competing interests were reportedby the rest of the authors.

Ortiz et al. BMC Medicine(2024) 22:327

Received: 21 March 2024 Accepted: 18 July 2024

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