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Patient delay and related influencing factors in Chinese women under 35 years diagnosed with cervical cancer: A cross-sectional study

Open AccessPublished:November 14, 2022DOI:https://doi.org/10.1016/j.apjon.2022.100165

      Abstract

      Purpose

      Patient delay was defined as an interval between the discovery of the initial symptoms and diagnosis, which was longer than 90 days. This study aimed to determine the patient delay rate and related factors in women with cervical cancer in Hunan Province, South-Central China.

      Methods

      A cross-sectional study was conducted among 140 women with cervical cancer aged < 35 years from October, 2019 to March, 2021. Assumptions in Andersen Behavioral Model of Health Services Utilization were used to measure the factors influencing patient delay. Logistic regression models were used to identify factors associated with patient delay. A p-value of < 5% was considered significant.

      Results

      A total of 57 (40.71%) young women with cervical cancer had patient delay, with an average delay time of 178.70 (307.90) days. Predisposing factors, such as religion, unemployment, health beliefs related to cancer screening, and a history of cervical cancer screening within 2 years or more (p<0.05), were associated with patient delay. Enabling factors, such as distance to the nearest medical facility and type of the nearest medical facility, were associated with a reduced likelihood of patient delay. With the need-for-care factor, young women who experienced vaginal pain after or during intercourse had a higher risk (adjusted odds ratio, 33.48; 95% confidence interval, 3.22–348.68, p=.003) of patient delay.

      Conclusions

      These findings reinforce the need for programs to enhance knowledge and awareness about cervical cancer screening and the importance of early diagnosis in women to help eliminate cervical cancer in China by 2050.

      Keywords

      Introduction

      1.1 Background

      Cervical cancer is the fourth most common cancer in women
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      Estimates of incidence and mortality of cervical cancer in 2018: a worldwide analysis.
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      • Bruni L.
      • et al.
      Estimates of incidence and mortality of cervical cancer in 2018: a worldwide analysis.
      . China contributes to more than 18% of the global cervical cancer burden, with 106,000 cases and 48,000 deaths
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      • Bruni L.
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      Estimates of incidence and mortality of cervical cancer in 2018: a worldwide analysis.
      . Human suffering, societal burden, and high economic costs associated with cancer have been reported in many countries
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      • Yu C.
      Comparison of Secular Trends in Cervical Cancer Mortality in China and the United States: An Age-Period-Cohort Analysis.
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      Cervical cancer mortality among young women in Latin America and the Caribbean: trend analysis from 1997 to 2030.
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      Socio-economic and cultural vulnerabilities to cervical cancer and challenges faced by patients attending care at Tikur Anbessa Hospital: a cross sectional and qualitative study.
      , including China
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      Comparison of Secular Trends in Cervical Cancer Mortality in China and the United States: An Age-Period-Cohort Analysis.
      . Although the maximum incidence rate is recorded around the age of 40 years, the number of cervical cancer cases is increasing at an alarming rate among younger women in China
      • Zhou P.
      • Chen D.
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      Cervical Cancer Mortality in Younger Women. Journal of General Internal Medicine.
      , that is, approximately 11 cases per 100,000, with an annual increase of 3.05% (p<0.001)
      • Zhang Z.
      • Liu C.
      • Ren H.
      • Liang S.
      Trends in the incidence and mortality of cervical cancer among Chinese women from 2003 to 2018.
      . High frequencies of cervical adenocarcinoma
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      • Huang Y.
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      Trends in Cervical Cancer in Young Women in Hubei, China.
      and lymphatic metastasis
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      Cervical cancer mortality among young women in Latin America and the Caribbean: trend analysis from 1997 to 2030.
      have been identified in young women, especially in those who are ≤35 years old; those with aggressive tumors have a poor prognosis
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      Clinicopathological Features and Survival of Adolescent and Young Adults with Cervical Cancer.
      ,
      • Li K.
      • Li Q.
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      • Yin R.
      The distribution and prevalence of human papillomavirus in women in mainland China.
      . These factors make early diagnosis of cervical cancer in women an important societal target worldwide
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      • Bruni L.
      • et al.
      Estimates of incidence and mortality of cervical cancer in 2018: a worldwide analysis.
      .
      The World Health Organization recently announced a global strategy toward the elimination of cervical cancer and set the goal of reducing the global annual age-standardized incidence to 4 per 100,000 women
      • Petts R.A.
      • McClain M.B.
      • Azad G.
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      System navigation models to facilitate engagement in pediatric behavioral health services: A systematic review.
      . The concept of “delayed diagnosis” appears in the literature as an obstacle in cancer prevention and treatment
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      • Patnick J.
      • Forbes L.J.
      Delays in diagnosis of young females with symptomatic cervical cancer in England: an interview-based study.
      . Delayed diagnosis can lead to enlargement of the tumor, increased distant metastasis rate and TNM staging, a higher risk of relapse and death, and poor clinical outcomes
      • Hanna T.P.
      • King W.D.
      • Thibodeau S.
      • et al.
      Mortality due to cancer treatment delay: systematic review and meta-analysis.
      ,
      • Matsuo K.
      • Huang Y.
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      • Ragab O.M.
      • Roman L.D.
      • Wright J.D.
      Association between definitive chemoradiotherapy wait-time and survival in locally-advanced cervical cancer: Implications during the coronavirus pandemic.
      . Delayed diagnosis is categorized into four components: patient delay, healthcare provider delay, referral delay, and system delay
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      • Hanchi Z.
      • Haddou Rahou B.
      • Bekkali R.
      • Ahid S.
      • Mesfioui A.
      Determinants of Patient Delay in Seeking Diagnosis and Treatment among Moroccan Women with Cervical Cancer.
      . These different types of delays play an important role in the prevention, diagnosis, and management of cancer
      • Ouasmani F.
      • Hanchi Z.
      • Haddou Rahou B.
      • Bekkali R.
      • Ahid S.
      • Mesfioui A.
      Determinants of Patient Delay in Seeking Diagnosis and Treatment among Moroccan Women with Cervical Cancer.
      . Patient delay is an important obstacle in effective cancer prevention
      • Lim A.W.
      • Ramirez A.J.
      • Hamilton W.
      • Sasieni P.
      • Patnick J.
      • Forbes L.J.
      Delays in diagnosis of young females with symptomatic cervical cancer in England: an interview-based study.
      ,
      • Ouasmani F.
      • Hanchi Z.
      • Haddou Rahou B.
      • Bekkali R.
      • Ahid S.
      • Mesfioui A.
      Determinants of Patient Delay in Seeking Diagnosis and Treatment among Moroccan Women with Cervical Cancer.
      . In the literature, patient delay is defined as an interval longer than 90 days between the discovery of the initial symptoms and diagnosis
      • Lim A.W.
      • Ramirez A.J.
      • Hamilton W.
      • Sasieni P.
      • Patnick J.
      • Forbes L.J.
      Delays in diagnosis of young females with symptomatic cervical cancer in England: an interview-based study.
      ,
      • Ouasmani F.
      • Hanchi Z.
      • Haddou Rahou B.
      • Bekkali R.
      • Ahid S.
      • Mesfioui A.
      Determinants of Patient Delay in Seeking Diagnosis and Treatment among Moroccan Women with Cervical Cancer.
      ,
      • Dereje N.
      • Addissie A.
      • Worku A.
      • et al.
      Extent and Predictors of Delays in Diagnosis of Cervical Cancer in Addis Ababa, Ethiopia: A Population-Based Prospective Study.
      . Studies conducted in Africa reported that the median patient delay in patients with cervical cancer ranged from 97 to 133 days
      • Dereje N.
      • Addissie A.
      • Worku A.
      • et al.
      Extent and Predictors of Delays in Diagnosis of Cervical Cancer in Addis Ababa, Ethiopia: A Population-Based Prospective Study.
      • Mimouni H.
      • Hassouni K.
      • El Marnissi B.
      • et al.
      The Care Pathway Delays of Cervical Cancer Patient in Morocco.
      • Rudd P.
      • Gorman D.
      • Meja S.
      • et al.
      Cervical cancer in southern Malawi: A prospective analysis of presentation, management, and outcomes.
      . One study that focused on women under 35 years of age showed that the median patient delay was 270 days (range, 90–720 days), which was significantly longer than that in the older group (270 vs. 60 days, p=0.0009)
      • Robinson K.M.
      • Christensen K.B.
      • Ottesen B.
      • Krasnik A.
      Socio-demographic factors, comorbidity and diagnostic delay among women diagnosed with cervical, endometrial or ovarian cancer.
      . Therefore, further deterioration of cancer caused by long-term patient delay makes young women bear more treatment burden and face a more severe survival dilemma
      • Hanna T.P.
      • King W.D.
      • Thibodeau S.
      • et al.
      Mortality due to cancer treatment delay: systematic review and meta-analysis.
      ,
      • Matsuo K.
      • Huang Y.
      • Matsuzaki S.
      • Ragab O.M.
      • Roman L.D.
      • Wright J.D.
      Association between definitive chemoradiotherapy wait-time and survival in locally-advanced cervical cancer: Implications during the coronavirus pandemic.
      .
      Evidence in China is particularly limited, with only one study showing that the rate of patient delay in women with cervical cancer in the whole age group was 45% in China
      • Ma J.
      • Zhu Q.
      • Han S.
      • et al.
      Effect of socio-economic factors on delayed access to health care among Chinese cervical cancer patients with late rectal complications after radiotherapy.
      . However, government-led cervical cancer screening has only been available for women aged 35–60 years in China
      • Zhou P.
      • Chen D.
      • Shi L.
      Cervical Cancer Mortality in Younger Women. Journal of General Internal Medicine.
      , which allows women older than 35 years to receive immediate diagnosis and treatment after early screening for cervical cancer. Therefore, it is uncertain whether the rate of patient delay in women under 35 years of age is underestimated. Thus, further research is needed to investigate patient delays in young women in China.

      1.2 Theoretical background

      The Behavioral Model of Health Services Utilization
      • Andersen R.M.
      Revisiting the behavioral model and access to medical care: does it matter?.
      provides a specific path for understanding the personal and external resource factors of patient delays. The model was developed to understand the determinants of health service utilization and to consider societal and individual determinants from the perspective of systematic analysis. This model has three key elements: predisposing, enabling, and requiring variances
      • Andersen R.M.
      Revisiting the behavioral model and access to medical care: does it matter?.
      . These elements can either expedite or hinder individuals’ utilization of services
      • O'Donovan M.A.
      • McCallion P.
      • McCarron M.
      • Lynch L.
      • Mannan H.
      • Byrne E.
      A narrative synthesis scoping review of life course domains within health service utilisation frameworks.
      .
      Predisposing factors include social demographic characteristics, such as age, religion, sex, basic beliefs, and attitudes pertaining to health services, which create conditions to increase the probability of health service utilization
      • O'Donovan M.A.
      • McCallion P.
      • McCarron M.
      • Lynch L.
      • Mannan H.
      • Byrne E.
      A narrative synthesis scoping review of life course domains within health service utilisation frameworks.
      . Enabling factors are those that hinder or facilitate health service utilization; these factors include the availability, affordability, and accessibility of drugs and healthcare services
      • Wang H.
      • Hua X.
      • Yao N.
      • et al.
      The Urban-Rural Disparities and Associated Factors of Health Care Utilization Among Cancer Patients in China.
      . Furthermore, the need-for-care factors are variables concerning the perception of individuals’ health status
      • SoleimanvandiAzar N.
      • Kamal S.H.M.
      • Sajjadi H.
      • et al.
      Determinants of Outpatient Health Service Utilization according to Andersen's Behavioral Model: A Systematic Scoping Review.
      . The model has been applied to health-seeking behavior and its determinants
      • Agrawal P.
      • Chen T.A.
      • McNeill L.H.
      • et al.
      Factors Associated with Breast Cancer Screening Adherence among Church-Going African American Women.
      ,
      • Ahmad A.
      Health-Seeking Behavior and Its Determinants among Mine Workers in the Karauli District of Rajasthan in India.
      . It has also been found to be effective in predicting care delays
      • Liabsuetrakul T.
      • Oumudee N.
      Effect of health insurance on delivery care utilization and perceived delays and barriers among southern Thai women.
      ,
      • Vang S.S.
      • Dunn A.
      • Margolies L.R.
      • Jandorf L.
      Delays in Follow-up Care for Abnormal Mammograms in Mobile Mammography Versus Fixed-Clinic Patients.
      . For example, predisposing factors, such as high illiteracy level, low socioeconomic status, comorbidities
      • Robinson K.M.
      • Christensen K.B.
      • Ottesen B.
      • Krasnik A.
      Socio-demographic factors, comorbidity and diagnostic delay among women diagnosed with cervical, endometrial or ovarian cancer.
      , lack of awareness, and lack of knowledge of early symptoms and causes
      • Ouasmani F.
      • Hanchi Z.
      • Haddou Rahou B.
      • Bekkali R.
      • Ahid S.
      • Mesfioui A.
      Determinants of Patient Delay in Seeking Diagnosis and Treatment among Moroccan Women with Cervical Cancer.
      , are accountable for patient delay among patients with cervical cancer. Studies have also found that the lack of a routine screening program could lead to patient delay
      • Zeleke S.
      • Anley M.
      • Kefale D.
      • Wassihun B.
      Factors Associated with Delayed Diagnosis of Cervical Cancer in Tikur Anbesa Specialized Hospital, Ethiopia, 2019: Cross-Sectional Study.
      . However, population-wide cervical cancer screening is only available for women aged 35–60 years in China
      • Zhou P.
      • Chen D.
      • Shi L.
      Cervical Cancer Mortality in Younger Women. Journal of General Internal Medicine.
      , and we cannot determine whether patient delay in young women is associated with inadequate cancer screening. Moreover, no study has comprehensively analyzed factors that may be associated with a delay in the diagnosis of cancer in young women.
      Therefore, the present study aimed to investigate the patient delay rate in young women with cervical cancer under 35 years of age in China, and to explore factors associated with patient delay among this population. We used the Behavioral Model of Health Services Utilization
      • Andersen R.M.
      Revisiting the behavioral model and access to medical care: does it matter?.
      , which provides a specific path to understand personal and external resource factors of patient delay for the diagnosis of cancer. The predisposing, enabling, and need factors associated with patient delay were also investigated among young women with cervical cancer. These results provide support for early prevention and control of cervical cancer in the young population
      • Petts R.A.
      • McClain M.B.
      • Azad G.
      • Shahidullah J.D.
      System navigation models to facilitate engagement in pediatric behavioral health services: A systematic review.
      .

      1.3 Objectives

      The specific objectives of this survey were to (1) investigate the patient delay rate and (2) analyze its main influencing factors among young women with cervical cancer in Hunan province.

      Methods

      This article was written according to the Strengthening the Reporting of Observational Studies in Epidemiology 2007 (STROBE 2007)
      • von Elm E.
      • Altman D.G.
      • Egger M.
      • Pocock S.J.
      • Gøtzsche P.C.
      • Vandenbroucke J.P.
      The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies.
      . The STROBE checklist is available in Additional File 1.

      2.1 Study design

      A cross-sectional study was conducted to examine the rate of patient delay and the potential determinants among young women with cervical cancer between October 27, 2019 and March 18, 2021 in Hunan province, China.

      2.2 Study setting and participants

      This study was conducted in a tumor hospital in Hunan province, China. The incidence of cervical cancer was 43.6 per 100,000 in 2017 in Hunan province, ranking among the top three in China
      • Zhang Z.
      • Liu C.
      • Ren H.
      • Liang S.
      Trends in the incidence and mortality of cervical cancer among Chinese women from 2003 to 2018.
      , and it was higher than the global average rate (13.1/100,000)
      • Arbyn M.
      • Weiderpass E.
      • Bruni L.
      • et al.
      Estimates of incidence and mortality of cervical cancer in 2018: a worldwide analysis.
      . The hospital, as a single tumor hospital in Hunan province, accepts patients from the entire province. The recruitment of research subjects from the hospital could make the samples sufficiently representative.
      The participants were women who were admitted to the study hospital during the data collection period. The inclusion criteria were as follows: (1) age < 35 years and (2) new diagnosis of cervical cancer or cervical intraepithelial neoplasia (CIN). The exclusion criteria were as follows: (1) participating in or having participated in similar studies in the past and (2) severe physical or mental illness and inability to cooperate with the investigation.

      2.3 Data collection

      The medical records of women who were admitted to the study hospital and diagnosed with cervical cancer were screened by trained hospital staff who acted as research assistants (RA) at the hospital. Potential participants who met the inclusion criteria received a phone call from an RA who explained the purpose of the study and asked about their preliminary interest in joining the study. If the participant was willing, the RA would confirm their eligibility and set a time and place to obtain written informed consent and provide the questionnaire.
      A self-report questionnaire was developed based on two paths: first, conclusions from previous studies that reported factors associated with patient delay in women with cervical cancer
      • Tadesse S.K.
      Socio-economic and cultural vulnerabilities to cervical cancer and challenges faced by patients attending care at Tikur Anbessa Hospital: a cross sectional and qualitative study.
      ,
      • Lim A.W.
      • Ramirez A.J.
      • Hamilton W.
      • Sasieni P.
      • Patnick J.
      • Forbes L.J.
      Delays in diagnosis of young females with symptomatic cervical cancer in England: an interview-based study.
      ,
      • Ouasmani F.
      • Hanchi Z.
      • Haddou Rahou B.
      • Bekkali R.
      • Ahid S.
      • Mesfioui A.
      Determinants of Patient Delay in Seeking Diagnosis and Treatment among Moroccan Women with Cervical Cancer.
      ,
      • Robinson K.M.
      • Christensen K.B.
      • Ottesen B.
      • Krasnik A.
      Socio-demographic factors, comorbidity and diagnostic delay among women diagnosed with cervical, endometrial or ovarian cancer.
      ,
      • Marlow L.A.
      • McGregor L.M.
      • Nazroo J.Y.
      • Wardle J.
      Facilitators and barriers to help-seeking for breast and cervical cancer symptoms: a qualitative study with an ethnically diverse sample in London.
      • Yu C.K.
      • Chiu C.
      • McCormack M.
      • Olaitan A.
      Delayed diagnosis of cervical cancer in young women.
      • Kaku M.
      • Mathew A.
      • Rajan B.
      Impact of socio-economic factors in delayed reporting and late-stage presentation among patients with cervix cancer in a major cancer hospital in South India.
      • Gyenwali D.
      • Pariyar J.
      • Onta S.R.
      Factors associated with late diagnosis of cervical cancer in Nepal.
      ; second, the conceptual framework by Andersen
      • Andersen R.M.
      Revisiting the behavioral model and access to medical care: does it matter?.
      (Figure 1), the model provides a framework to complement more factors that affect health service utilization, such as access to health services and perceived health status.
      The final comprehensive questionnaire in Chinese version with 31 items consisted of two parts: (1) The outcome measure was the rate of patient delay (which was classified as to whether there was a delay in symptom presentation) in young women with cervical cancer. The exact time and length of delay were recorded. (2) Independent variables were grouped into three dimensions: 1) predisposing factors included sociodemographic characteristics (age, nationality, religion, marital status, educational status, occupation, habitual residence, and income), family history, history of gestation, menstruation, sexual life, and health beliefs related to cancer screening. 2) enabling factors included medical insurance, type and distance from the nearest medical facility, services available in the nearest medical facility, serviceable time, and available professional nurses in the nearest medical facility. 3) the need-for-care factor was captured as self-perceived symptoms associated with cervical disease (vaginal bleeding after sexual intercourse, no cause of vaginal bleeding, regular lower abdominal pain unrelated to menstruation, vaginal pain after or during intercourse, vaginal discharge with unusual odor or color, and other symptoms).
      A pretest was conducted on seven young women with cervical cancer to ensure that the questionnaire was appropriately structured and consistent. A 2-day training was given to data collection assistants to improve the data collection process. The principal investigator performed close supervision to ensure the completeness of the questionnaires at the time of data collection. Data editing and clearance were performed to ensure proper data management.
      Ethical approval was obtained from the Nursing and Behavioral Medicine Research Ethics Review Committee, Xiangya School of Nursing, Central South University (E2019080).

      2.4 Data analysis

      The required sample size was determined using a single-population proportion formula based on the following assumptions: about 45% of patient delay data were taken from the results of a study conducted by Ma et al.
      • Ma J.
      • Zhu Q.
      • Han S.
      • et al.
      Effect of socio-economic factors on delayed access to health care among Chinese cervical cancer patients with late rectal complications after radiotherapy.
      in women with cervical cancer in China, with 95% CI (confidence interval) and a margin of error of 9%. The minimum sample size was calculated using the following formula:
      N=(Zα/2)2P(1P)σ2


      where N is the sample size, Z α /2 is the normal distribution value at 95% CI (Z = 1.96), P is the proportion of patient delay (45%)
      • Ma J.
      • Zhu Q.
      • Han S.
      • et al.
      Effect of socio-economic factors on delayed access to health care among Chinese cervical cancer patients with late rectal complications after radiotherapy.
      , and σ is the margin of error (9%), which is generally 0.1–0.2 times of the estimated total ratio (45%). Therefore, the final sample size after adding a 15% nonresponse rate was 139 young women with cervical cancer.
      Data were imported into IBM SPSS version 26.0 statistical software (Armonk, NY, USA) for analysis. Only the complete data for the included variables were used. Summary descriptive statistics were calculated using appropriate measures of central tendency (mean) and dispersion (standard deviation [SD]) for continuous data and number and percentage for categorical data.
      Independent sample t-tests and one-way ANOVA were performed to explore the associations between patient delay and categorical independent variables. Variables with significant associations with patient delay (P-value < 0.05) in bivariate analysis were qualified for binary logistic analysis. Binary logistic analysis models were used to identify the independent factors associated with patient delay in young women with newly diagnosed cervical cancer. The “enter” regression technique was used to run the analysis. Statistical significance was set at p < 0.05.

      Results

      3.1 Characteristics of the study population

      A total of 1,559 newly diagnosed patients with cervical cancer were tracked throughout the study, among whom 432 (27.71 %) were 35 years old and below. A total of 147 participants were eligible and willing to participate in the study, and thus, 147 questionnaires were issued. After removing the incomplete data (n = 7), the final sample size was 140. The summary descriptive statistics for the 140 patients are presented in Tables 1 and 2. The minimum age of the study participants was 21 years, and the maximum age was 35 years, with a mean (SD) age of 30.94 (2.83) years. Among 140 young women with cervical cancer, 124 were hospitalized because of the self-discovery of symptoms. The most common symptom was “vaginal bleeding after sexual intercourse” (40/140, 28.6%) and “no cause of vaginal bleeding” (26/140, 18.6%), while the remaining 16 patients were referred for screening or other diseases (Figure 2).
      Table 1Predisposing Factors of young women with cervical cancer.
      VariablesCategoriesMean or FrequencySD or Percent (%)
      Age, mean (SD)30.942.83
      Ethnicity, n (%)Han11783.6
      Ethnic minorities2316.4
      Region, n (%)No religion7553.6
      Buddhism3525.0
      Taoism32.1
      Christianity85.7
      Else1913.6
      Marital status, n (%)Married11985.0
      Divorced or widowed139.3
      Spinsterhood75.0
      Education status, n (%)Primary school or below1812.9
      Junior high school7855.7
      High school or technical school3122.1
      College or above139.3
      Habitual residence, n (%)Countryside10877.1
      City3222.9
      Occupation, n (%)Unemployed5136.5
      Farmer4532.1
      Worker2014.3
      Merchant1611.4
      civil servant85.7
      Monthly income, n (%), yuanIndetermination2618.6
      ≤30005841.4
      3000-60004330.7
      6000-9000128.6
      >90001.7
      Family history of cervical cancer, n (%)Yes53.6
      No13596.4
      Family history of other cervical diseases, n (%)Yes1712.1
      No12387.9
      The number of pregnancy, mean (SD), times2.311.11
      The number of abortion, mean (SD), times.56.83
      The number of children, mean (SD), times1.76.75
      Age of menarche, mean (SD)13.471.57
      Menstrual cycle, mean (SD), day29.813.63
      Age of first intercourse, mean (SD)20.102.67
      Sexual frequency, mean (SD), times a week3.092.38
      History of Cervical cancer screening, n (%)Within half year3424.3
      Within a year3424.3
      Within 2 years1410.0
      Within 3 years139.3
      Never4532.1
      Health Belief, n (%)Attach importance to disease treatment4028.6
      Attach importance to disease prevention6747.9
      Neglect the two aspects3323.6
      Whether know cervical cancer screening policies, n (%)Yes6848.6
      No7251.4
      Table 2Enabling Factors of young women with cervical cancer.
      VariablesCategoriesMean or FrequencySD or Percent (%)
      Medical insurance, n (%)No insurance32.1
      New-type Rural Cooperative Medical Insurance11682.9
      Basic medical insurance system for urban residents2115.0
      Reimbursement rate of medical insurance, n (%)≤30%3323.6
      31%-50%5942.1
      51%-70%2417.1
      ≥71%2417.1
      Nearest medical facility, n (%)Pharmacy2316.4
      Clinic139.3
      Township health center6546.4
      County-level hospital or above3927.9
      Distance of nearest medical facility, n (%), km≤12618.6
      ≤55942.1
      ≤103021.4
      ≤201410.0
      ≤5075.0
      >5042.9
      Serviceable time of nearest medical facility, n (%)Only weekday daytime128.6
      Only daytime3726.4
      Only weekday0
      24-hour service9165.0
      Services available in nearest medical facility, n (%)
      Over-The-Counter Medications purchaseYes8359.3
      No5740.7
      Outpatient or emergencyYes9567.9
      No4532.1
      InpatientYes8862.9
      No5237.1
      Professional nurses in nearest medical facility, n (%)Yes9064.3
      No5035.7
      Figure 2
      Figure 2Need-For-Care factors (self-perceived symptoms) of young women with cervical cancer.

      3.2 Patient delay in young women with cervical cancer

      Patient delay was defined as an interval longer than 90 days between the discovery of initial symptoms and diagnosis
      • Lim A.W.
      • Ramirez A.J.
      • Hamilton W.
      • Sasieni P.
      • Patnick J.
      • Forbes L.J.
      Delays in diagnosis of young females with symptomatic cervical cancer in England: an interview-based study.
      • Hanna T.P.
      • King W.D.
      • Thibodeau S.
      • et al.
      Mortality due to cancer treatment delay: systematic review and meta-analysis.
      • Matsuo K.
      • Huang Y.
      • Matsuzaki S.
      • Ragab O.M.
      • Roman L.D.
      • Wright J.D.
      Association between definitive chemoradiotherapy wait-time and survival in locally-advanced cervical cancer: Implications during the coronavirus pandemic.
      . For patients who were referred, we counted the duration from the time when the referral was recommended for diagnosis. Among the 140 respondents, 57 (40.71 %) had patient delays. The minimum delay time of this population was 90 days, and the maximum was 375 days, with the mean (±SD) delay time of 178.70 (307.90) days.

      3.3 Determinants of patient delay among young women with cervical cancer

      Twenty-nine variables were tested for potential association with patient delay in young women with cervical cancer. Sixteen patients had a significant association with patient delay (Table 3).
      Table 3Univariable and Multivariable Analyses of Factors Associated with Patient Delay.
      FactorsUnivariableMultivariable
      OR (95% CI)P ValueOR (95% CI)P Value
      Predisposing Factors
      Religion
      No region1.001.00
      Buddhism2.89(1.18-7.05).0203.21(1.02-10.11).047
      Taoism1.26(.11-14.76).8522.68(.10-73.28).560
      Christianity3.79(.59-24.50).1623.97(.50-31.23).191
      Else3.47(1.21-9.97).0213.96(1.10-14.20).035
      Marital status
      Married1.001.00
      Divorced or widowed4.40(1.10-17.56).0364.40(.70-27.59).114
      Spinsterhood.66(.12-3.56).6291.33.17-10.16).782
      Education status
      College or above1.001.00
      Primary school or below10.00(1.44-69.26).0208.23(.77-87.53).081
      Junior high school4.32(.88-21.21).0712.85(.42-19.60).286
      High school or technical school1.74(.31-9.69).528.77(.10-6.14).801
      Occupation
      civil servant1.001.00
      Unemployed10.50(1.11-98.91).04016.93(1.09-262.47).043
      Farmer4.20(.47-37.56).1995.32(.37-75.77).217
      Worker.82(.06-10.62).882.77(.04-14.39).859
      Merchant4.67(.45-48.26).1967.92(.47-134.18).152
      History of Cervical cancer screening
      Never1.001.00
      Within half year.25(.09-.71).009.25(.07-.87).030
      Within a year.12(.04-.36).000.11(.03-.43).001
      Within 2 years.13(.03-.56).006.13(.02-.76).023
      Within 3 years.41(.11-1.49).177.38(.08—1.78).219
      Health Belief
      Neglect the two aspects1.001.00
      Attach importance to disease treatment.39(.16-.94).036.23(.07-.73).013
      Attach importance to disease prevention.29(.10-.79).016.23(.06-.82).023
      Enabling Factors
      Reimbursement rate of medical insurance
      ≥71%1.001.00
      ≤30%3.78(1.14-12.47).0294.65(.92-23.59).063
      31%-50%1.89(.64-5.61).2522.99(.60-14.95).182
      51%-70%1.51(.43-5.36).5232.54(.41-15.63).316
      Distance of nearest medical facility
      ≤1 KM1.001.00
      ≤5 KM1.30(.40-4.19).6601.40(.37-5.33).624
      ≤10 KM3.33(.86-12.98).0833.79(.586-24.50).162
      ≤20 KM7.60(1.07-54.09).0438.88(.87-153.80).065
      ≤50 KM4.43(1.27-15.49).0206.02(1.44-25.26).014
      >50 KM13.93(2.78-69.88).00122.54(3.30-153.80).001
      Nearest medical facility
      Pharmacy1.001.00
      Clinic1.11(.35-3.50).8571.01(.25-4.04).985
      Township health center1.42(.39-5.24).5971.23(.20-7.59).827
      County-level hospital or above.28(.11-.68).005.17(.05-.67).011
      Services available in nearest medical facility- Over-The-Counter Medications purchase
      No1.001.00
      Yes.48(.23-1.00).050.42(.16-1.08).073
      Need-For-Care factors
      Self-perceived Symptoms
      Vaginal bleeding after sexual intercourse1.001.00
      No cause of vaginal bleeding.71(.19-2.60).600.40(.08-1.85).239
      Regular lower abdominal pain unrelated to menstruation2.25(.43-11.82).3381.19(.18-8.04).857
      Vaginal pain after or during intercourse33.00(3.77-288.62).00233.48(3.22-348.68).003
      Vaginal discharge with unusual odor or color3.50(1.22-10.02).0202.78(.82-9.48).101
      Else2.40(.74-7.76).1442.35(.56-9.80).240
      After adjusting for all other predictors through multivariable analysis, predisposing factors, such as religion, occupation, health beliefs related to cancer screening, and history of cervical cancer screening, were found to be significantly associated with patient delay. Buddhism (adjusted OR [aOR], 3.21; 95% CI, 1.02–10.11, p=0.047) or other religions (aOR, 3.96; 95% CI, 1.10–14.20, p=0.035), and unemployment (aOR, 16.93; 95% CI, 1.09–262.47, p=0.043) were associated with an increased likelihood of patient delay. Attaching importance to disease treatment (aOR, 0.23; 95% CI, 0.07–0.73, p=0.013) or prevention (aOR, 0.23; 95% CI, 0.06–0.82, p=0.023) and a history of cervical cancer screening within 2 years or more (aOR<1, p<0.05) were associated with a reduced likelihood of patient delay.
      The enabling factors that were significantly associated with patient delay in young women with cervical cancer were the distance to the nearest medical facility and type of the nearest medical facility. A distance of 20 to 50 km from the nearest medical facility (aOR, 6.02; 95% CI, 1.44–25.26, p=0.014) or >50 km (aOR, 22.54; 95% CI, 3.30–153.80, p=0.001) was associated with an increased likelihood of patient delay. Regarding the nearest medical facility, county-level hospitals or above (aOR, 0.17; 95% CI, 0.05–0.67, p=0.011) were associated with a reduced likelihood of patient delay compared with pharmacies.
      With the need-for-care factor, young women who experienced vaginal pain after or during intercourse had a higher risk (aOR, 33.48; 95% CI, 3.22–348.68, p=0.003) of patient delay than those who experienced vaginal bleeding after sexual intercourse.

      Discussion

      4.1 Main findings

      This study showed that 40.71% of the respondents had patient delay, which is lower than the patient delay rate (45%) of all ages reported by Ma et al.
      • Ma J.
      • Zhu Q.
      • Han S.
      • et al.
      Effect of socio-economic factors on delayed access to health care among Chinese cervical cancer patients with late rectal complications after radiotherapy.
      in China and that in another study in Brazil (92.6%)34; however, it was significantly higher than that of young women in the United Kingdom (28%)
      • Lim A.W.
      • Ramirez A.J.
      • Hamilton W.
      • Sasieni P.
      • Patnick J.
      • Forbes L.J.
      Delays in diagnosis of young females with symptomatic cervical cancer in England: an interview-based study.
      . Although the patient delay rate in young women is lower than that in some developing countries, this group has a longer delay time, with an average delay time of 178.10 days, which is significantly longer than 110 days in Brazil
      • Ferreira da Silva I.
      • Ferreira da Silva I.
      • Koifman R.J.
      Cervical Cancer Treatment Delays and Associated Factors in a Cohort of Women From a Developing Country.
      , 162 days in Malawi
      • Rudd P.
      • Gorman D.
      • Meja S.
      • et al.
      Cervical cancer in southern Malawi: A prospective analysis of presentation, management, and outcomes.
      , 91 days in Denmark
      • Robinson K.M.
      • Ottesen B.
      • Christensen K.B.
      • Krasnik A.
      Diagnostic delay experienced among gynecological cancer patients: a nationwide survey in Denmark.
      , and 97 days in Ethiopia
      • Dereje N.
      • Addissie A.
      • Worku A.
      • et al.
      Extent and Predictors of Delays in Diagnosis of Cervical Cancer in Addis Ababa, Ethiopia: A Population-Based Prospective Study.
      . In the last 5 years, no study has specifically reported patient delays in young women. The present results showed that the status quo of timely health seeking is not optimistic in this population; diagnosis delay and disease progression caused by patient delay might be important reasons for the poor prognosis in this population
      • Torres-Roman J.S.
      • Ronceros-Cardenas L.
      • Valcarcel B.
      • et al.
      Cervical cancer mortality among young women in Latin America and the Caribbean: trend analysis from 1997 to 2030.
      ,
      • Pan S.
      • Jiang W.
      • Xie S.
      • Zhu H.
      • Zhu X.
      Clinicopathological Features and Survival of Adolescent and Young Adults with Cervical Cancer.
      . The overall trend demonstrated a decline in cervical cancer mortality, while cervical cancer deaths tended to occur in younger age groups
      • Wang J.
      • Bai Z.
      • Wang Z.
      • Yu C.
      Comparison of Secular Trends in Cervical Cancer Mortality in China and the United States: An Age-Period-Cohort Analysis.
      ,
      • Wei M.
      • Zhou W.
      • Bi Y.
      • Wang H.
      • Liu Y.
      • Zhang Z.-J.
      Rising Mortality Rate of Cervical Cancer in Younger Women in Urban China. Journal of General Internal Medicine.
      (up to 5.5% annually)
      • Zhou P.
      • Chen D.
      • Shi L.
      Cervical Cancer Mortality in Younger Women. Journal of General Internal Medicine.
      .

      4.2 Determinants of patient delay among young women with cervical cancer

      In this study, we explored the determinants of patient delay from three aspects: predisposing, enabling, and need-for-care factors.
      First, the need factor, namely, self-perceived symptoms, was the most dominant predictor of patient delay in young women with cervical cancer, even after adjusting for predisposing and enabling variables. Young women with self-perceived vaginal pain after or during intercourse (aOR, 33.48; 95% CI, 3.22–348.68, p=0.003) had a higher likelihood of patient delay than those who experienced vaginal bleeding after sexual intercourse. People with various symptoms of certain health conditions may put up behaviors to get rid of such conditions
      • Shao S.
      • Zhang H.
      • Chen X.
      • et al.
      Health education services utilization and its determinants among migrants: a cross-sectional study in urban-rural fringe areas of Beijing, China.
      . Therefore, other factors may account for these differences. First, young women aged less than 35 years might have limited knowledge and cognition of cervical cancer; they might even think that the mild symptoms (vaginal pain after or during intercourse) they experienced were normal
      • Fontham E.T.H.
      • Wolf A.M.D.
      • Church T.R.
      • et al.
      Cervical cancer screening for individuals at average risk: 2020 guideline update from the American Cancer Society.
      . Second, considering high health-related expenses along with deficiencies in free screening for cervical cancer, young women might be more likely to neglect symptoms or take self-purchased nonprescription drugs instead of seeking healthcare services in medical institutions when they only have a minor illness
      • Tadesse S.K.
      Socio-economic and cultural vulnerabilities to cervical cancer and challenges faced by patients attending care at Tikur Anbessa Hospital: a cross sectional and qualitative study.
      . These findings reinforce the need for programs to enhance knowledge and awareness of cervical cancer-related symptoms and the importance of early diagnosis in young women
      • Dereje N.
      • Addissie A.
      • Worku A.
      • et al.
      Extent and Predictors of Delays in Diagnosis of Cervical Cancer in Addis Ababa, Ethiopia: A Population-Based Prospective Study.
      .
      Second, we observed that one predisposing variable, namely religion, significantly contributed to patient delay in young women with cervical cancer. Women who were Buddhist or belonged to other religions were more likely to have delayed diagnosis. Special religious beliefs may affect people’s health service-seeking behavior. Hunan is a multiethnic region influenced by Buddhism and other traditional religions, such as polytheism. As such, young women in this area are more likely to endorse fatalistic beliefs
      • Nelson K.
      • Geiger A.M.
      • Mangione C.M.
      Effect of health beliefs on delays in care for abnormal cervical cytology in a multi-ethnic population.
      and hold the view that the etiology of cervical cancer is due to breaching social taboos or undertaking unacceptable behavior. Moreover, fear of stigmatization could make them reluctant to seek timely care
      • Mesafint Z.
      • Berhane Y.
      • Desalegn D.
      Health Seeking Behavior of Patients Diagnosed with Cervical Cancer in Addis Ababa, Ethiopia.
      .
      In addition, negative health beliefs and awareness of cervical cancer screening seem to be important factors in increasing patient delay, indicating their synergistic effects with unstable career factors. The possible explanations could be divided into two aspects. First, population-wide cervical cancer screening has only been available for women aged 35–60 years in China
      • Zhou P.
      • Chen D.
      • Shi L.
      Cervical Cancer Mortality in Younger Women. Journal of General Internal Medicine.
      , and young women aged less than 35 years may be overlooked by the government. Health education related to cervical cancer has no effect on this population compared with that in developed countries
      • Fontham E.T.H.
      • Wolf A.M.D.
      • Church T.R.
      • et al.
      Cervical cancer screening for individuals at average risk: 2020 guideline update from the American Cancer Society.
      . On the other hand, young women have more economic and caregiving responsibilities for their families
      • Zeleke S.
      • Anley M.
      • Kefale D.
      • Wassihun B.
      Factors Associated with Delayed Diagnosis of Cervical Cancer in Tikur Anbesa Specialized Hospital, Ethiopia, 2019: Cross-Sectional Study.
      , and they are reluctant to spend excessive time and money on some symptoms that are not serious in their awareness
      • Tadesse S.K.
      Socio-economic and cultural vulnerabilities to cervical cancer and challenges faced by patients attending care at Tikur Anbessa Hospital: a cross sectional and qualitative study.
      , especially when income is not steady. Consistent with the need factor, these findings reinforce the need for education programs to enhance knowledge and awareness of cervical cancer screening and the importance of early diagnosis in young women
      • Dereje N.
      • Addissie A.
      • Worku A.
      • et al.
      Extent and Predictors of Delays in Diagnosis of Cervical Cancer in Addis Ababa, Ethiopia: A Population-Based Prospective Study.
      . Increasing the budget for vaccination against human papillomavirus and cervical cancer screening in young women in the low economic levels will also be important to eliminate cervical cancer in China by 2050
      • Xia C.
      • Hu S.
      • Xu X.
      • et al.
      Projections up to 2100 and a budget optimisation strategy towards cervical cancer elimination in China: a modelling study.
      .
      Marital and educational statuses were not significant predictors of patient delay in the multivariable model. Univariable analysis indicated that young women with low education levels or who were widowed or divorced had strongly increased odds of patient delay. This finding was unexpected, given that marital and educational status is often shown to be an influential predictor of health-seeking behavior among women
      • Burrowes S.
      • Holcombe S.J.
      • Leshargie C.T.
      • et al.
      Perceptions of cervical cancer care among Ethiopian women and their providers: a qualitative study.
      ,
      • Morhason-Bello I.O.
      • Kareem Y.O.
      • Adewole I.F.
      Modeling for Predictors of Knowledge Score on Etiology and Prevention Strategies for Cervical Cancer Among Women of Reproductive Age in Ibadan.
      . Considering the small sample size of this study, future studies should focus on young women with cervical cancer as a unique group for the investigation of patient delay and influencing factors.
      Despite the importance of promoting early diagnosis and reducing the incidence of care delay, few studies have investigated the accessibility factors of health services that may influence the health-seeking behavior of young women with cervical cancer
      • Ashing-Giwa K.
      • Rosales M.
      Evaluation of therapeutic care delay among Latina- and European-American cervical cancer survivors.
      . Our study indicated that some enabling factors, such as the distance to the nearest medical facility, were predictors of patient delay in young women with cervical cancer. The greater the distance from the medical facility, the higher the likelihood of patient delay, which might be due to the reduced availability of medical treatment due to the long distance
      • Liu G.
      • Xue Y.
      • Qian Z.
      • et al.
      Healthcare-seeking behavior among pregnant women in the Chinese hierarchical medical system: a cross-sectional study.
      . Although hierarchical diagnosis and treatment have been implemented for many years, people still prioritize senior general hospitals in medical treatment selection in China
      • Peng X.
      • Tang X.
      • Chen Y.
      • Zhang J.H.
      Ranking the Healthcare Resource Factors for Public Satisfaction with Health System in China-Based on the Grey Relational Analysis Models.
      , indicating low subjective trust in primary medical services among young women with cervical cancer.
      A possible explanation could be the inconsistency between the objective quality of healthcare provided and the subjective quality perceived by patients
      • Rao S.
      • Xue H.
      • Teuwen D.E.
      • Shi H.
      • Yi H.
      Measurements of quality of village-level care and patients' healthcare-seeking behaviors in rural China.
      ; therefore, to improve service quality, patients should identify the actual quality of primary health care precisely and then improve their satisfaction, thereby promoting the more efficient use of primary-level health resources.

      4.3 Strengths and limitations

      In general, research on patient delays in young women with cervical cancer is lacking. In addition to the demographic data and pregnancy history mentioned in previous studies, the present study comprehensively included a series of factors related to medical behavior. The findings provide a basis for policy decision-makers and healthcare professionals to determine multilevel factors of barriers to health service utilization in young women with cervical cancer. This study ultimately contributed to the development of more effective interventions and increased access to medical welfare among vulnerable populations.
      This study had several limitations. First, it was limited to Hunan province due to constraints of time and funds, and the sample size was small due to the particularity of the population. Second, all the items in the questionnaire were self-reported, which could be a source of bias. Although the questionnaire was pretested before surveying, it was not fully validated. Third, we started the data collection process before coronavirus disease 2019 (COVID-19) occurred, and we could not explore the likely impact of COVID-19 on the results using the available data. Finally, the inability to infer causality from observational research was acknowledged. Further research is required to address these deficiencies.

      Conclusion

      Limited research has explored factors associated with patient delay in young women with cervical cancer. Evidence indicates that early diagnosis and treatment are the most cost-effective measures for eliminating cervical cancer among young women. Our study found that the rate of patient delay in young women with cervical cancer reached 40%, and was positively associated with predisposing, enabling, and need-for-care factors. These findings reinforce the need for programs to enhance knowledge and awareness of cervical cancer screening and the importance of early diagnosis in young women to help eliminate cervical cancer in China by 2050.

      Funding

      This work was supported by Hunan Women's Federation [grant numbers 19WTB03].

      Author contributions

      Jun MA: Conceptualization; Data curation; Formal analysis; Investigation; Methodology; Roles/Writing - original draft. Yang LUO: Conceptualization; Funding acquisition; Methodology; Project administration; Supervision; Writing - review & editing. Shengbo YANG: Conceptualization; Formal analysis; Writing - review & editing. Xiangyu LIU: Investigation; Methodology. Yueyang PENG: Investigation; Roles/Writing - original draft. Honghong WANG: Formal analysis; Writing - review & editing. Maritta Valimaki: Writing - review & editing. Can Gu: Conceptualization; Data curation; Funding acquisition; Methodology; Project administration; Supervision; Roles/Writing - original draft; Writing - review & editing.

      Declaration of Competing Interest

      The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

      Acknowledgements

      The authors would like to thank Editage (www.editage.cn) for English language editing.

      Appendix A. Supplementary data

      The following is the supplementary data to this article:

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