Skip to main content
Advertisement
Browse Subject Areas
?

Click through the PLOS taxonomy to find articles in your field.

For more information about PLOS Subject Areas, click here.

  • Loading metrics

Interventions to increase cervical screening uptake among immigrant women: A systematic review and meta-analysis

  • Zufishan Alam,

    Roles Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Software, Visualization, Writing – original draft, Writing – review & editing

    Affiliation Centre for Health Services Research, Faculty of Medicine, The University of Queensland, Brisbane, Queensland, Australia

  • Joanne Marie Cairns ,

    Roles Data curation, Investigation, Writing – review & editing

    joanne.cairns@hyms.ac.uk

    Affiliation Hull York Medical School, University of Hull, Hull, United Kingdom

  • Marissa Scott,

    Roles Data curation, Investigation

    Affiliation School of Medicine, The University of Queensland, Brisbane, Queensland, Australia

  • Judith Ann Dean,

    Roles Conceptualization, Supervision, Writing – review & editing

    Affiliation School of Public Health, Faculty of Medicine, The University of Queensland, Brisbane, Queensland, Australia

  • Monika Janda

    Roles Conceptualization, Formal analysis, Methodology, Supervision, Writing – review & editing

    Affiliation Centre for Health Services Research, Faculty of Medicine, The University of Queensland, Brisbane, Queensland, Australia

Abstract

Numerous intervention studies have attempted to increase cervical screening uptake among immigrant women, nonetheless their screening participation remains low. This systematic review and meta-analysis aimed to summarise the evidence on interventions to improve cervical screening among immigrant women globally and identify their effectiveness. Databases PubMed, EMBASE, Scopus, PsycINFO, ERIC, CINAHL and CENTRAL were systematically searched from inception to October 12, 2021, for intervention studies, including randomised and clinical controlled trials (RCT, CCT) and one and two group pre-post studies. Peer-reviewed studies involving immigrant and refugee women, in community and clinical settings, were eligible. Comparator interventions were usual or minimal care or attention control. Data extraction, quality appraisal and risk of bias were assessed by two authors independently using COVIDENCE software. Narrative synthesis of findings was carried out, with the main outcome measure defined as the cervical screening uptake rate difference pre- and post-intervention followed by random effects meta-analysis of trials and two group pre-post studies, using Comprehensive Meta-Analysis software, to calculate pooled rate ratios and adjustment for publication bias, where found. The protocol followed PRISMA guidelines and was registered prospectively with PROSPERO (CRD42020192341). 1,900 studies were identified, of which 42 (21 RCTS, 4 CCTs, and 16 pre-post studies) with 44,224 participants, were included in the systematic review, and 28 with 35,495 participants in the meta-analysis. Overall, the uptake difference rate for interventions ranged from -6.7 to 96%. Meta-analysis demonstrated a pooled rate ratio of 1.15 (95% CI 1.03–1.29), with high heterogeneity. Culturally sensitive, multicomponent interventions, using different modes of information delivery and self-sampling modality were most promising. Interventions led to at least 15% increase in cervical screening participation among immigrant women. Interventions designed to overcome logistical barriers and use multiple channels to communicate culturally appropriate health promotion messages are most effective at achieving cervical screening uptake among immigrant women.

Introduction

Cervical cancer, despite being preventable, is a leading cause of cancer diagnosis and death among women worldwide, with 342,000 women dying in 2020 [1] Women in low and lower-middle income countries are most affected [2, 3]. Advances in biomedical research has led to the introduction of novel surgical, radiotherapeutic and systemic options for the treatment of cervical cancer [4]. Research evidence clearly shows that secondary prevention in terms of screening can effectively reduce cervical cancer mortality [5]. Screening options now being employed worldwide include Pap and HPV test [6]. Although many high-income countries have successful screening programs, disparities remain among certain population subgroups [7]. Immigrants have been identified as a subgroup with lower cervical screening uptake [8]. Therefore, multiple studies have delivered interventions to bring about better screening uptake among immigrant women globally.

Three systematic reviews have summarised studies involving health promotion interventions to increase cervical screening uptake among at-risk population subgroups. Of those, two focused on specific migrant groups i.e., Asian and Hispanic immigrant populations and indicated the role of sociocultural factors and population characteristics in intervention effectiveness [9, 10]. Whereas the third review on studies conducted between 2006–16 focused on activities for increasing cervical screening uptake among low socioeconomic groups, indicating effectiveness of HPV self-sampling [9]. Reviews have been carried out to summarise the evidence on interventions that used specific strategies such as education provision, Human Papilloma Virus (HPV) self-sampling or health care provider (HCP) counselling among the Indigenous/native women [1114]. However, none of these previous reviews addressed the overall diverse immigrant populations in different parts of the world, nor summarised various intervention strategies for increasing cervical screening in immigrants. Given the recent launch of global initiative to eliminate cervical cancer as a public health problem by WHO [15], it is critical to systematically review the evidence on effectiveness of interventions, among under reached groups such as immigrants.

Thus, the objective of this study was to obtain the systematic evidence, expanding on immigrant population subgroups from various backgrounds, not limited to intervention strategies of specific type, as opposed to previous reviews and to compare the effect of intervention between intervention and control groups through meta-analysis. This review aimed to systematically summarise the global and up to date evidence on interventions aiming to increase cervical screening uptake among immigrant and refugee women, and quantify their effectiveness via providing a pooled estimate of the effect, through a meta-analysis. A further aim was to extract the characteristics of interventions most effective for increasing cervical screening uptake, in order to inform researchers and policy makers of the most promising intervention components to include in future interventions and to identify find any remaining knowledge gaps.

Methods

This systematic review followed PRISMA 2020 guidelines [16] (checklist included in S1 Table). The protocol was registered with International Prospective Register of Systematic reviews (PROSPERO) Registration number: CRD42020192341. Refer to S1 File for published protocol.

Study search

Pubmed, Scopus, EMBASE, CINAHL, PsycINFO, CENTRAL and ERIC were searched from inception to 12th October 2021. The search strategy was developed with guidance by a professional librarian and combined the most appropriate keywords, MESH terms and Boolean operators, such as ((cervical cancer OR cancer of the cervix OR cervical neoplasm)) OR cervical cancer, uterine)) AND (((screening OR detection OR Pap test OR Pap smear)) OR cervical smear))) AND (((immigrant* OR migrant* OR refugee* OR emigrant*)) OR (emigrants and immigrants)))). S2 Table (a-h) provide the full electronic search strategy for each database. Additionally, bibliographies of included articles were hand-searched to identify other potentially relevant studies (S2 Table (i)). Titles and abstracts of studies were screened to identify interventions or health promotion activities aimed to increase cervical screening uptake among immigrant or refugee women. The database search was repeated in June 2022 to include any recently published studies.

Study eligibility and selection

Original, peer-reviewed studies of any design ((randomised controlled trials (RCT), clinical controlled trials (CCT), cohort analytic pre-post (Quasi experimental) studies), with both simple and complex interventions were included, without restriction of language. Studies with interventions focusing only on increasing cervical cancer and screening knowledge, but not behaviour, and descriptive studies exploring patterns of cervical screening uptake among immigrant groups were excluded. Studies without complete outcome data were also excluded, after attempting to contact the authors for details. Studies involving immigrant and refugee women from any background were included. Conference proceedings and theses were excluded. Studies were independently retrieved and screened against inclusion criteria by at least two reviewers (ZA, JC, MS) via COVIDENCE, with resolution of any difference through mutual discussion.

Data extraction

Fields predesignated by the authors were used to extract study data, including publication details (author, year), population characteristics (sample size, age, ethnicity, baseline screening status), study setting and location, recruitment method, intervention characteristics (type of intervention, control and intervention group, follow up period), and outcome measure(s). The outcome measure of primary interest for the systematic review was difference in cervical screening uptake from pre- to post-intervention in the intervention group, expressed as percentage. When the study reported more than one outcome measure, or calculations for different time intervals, the one with higher value was used. According to PRISMA guidelines, data were also extracted independently by at least two authors (ZA, MS, JC).

Synthesis of extracted data and meta-analysis

Extracted data were then synthesised and reported narratively, arranging studies based on intervention type (simple/multifaceted), study setting (urban, rural community/clinical), source of outcome data measurement (self-reported/record based), screening method offered (self-sampling/pap test/ combined), mode of delivery (in person/via use of mail/telephone/media), intervention format (brochures/video/combined), guidance by a theoretical or behaviour change model (theoretically guided) and involvement of personnel (HCPs/Promotoras). Outcome data was reported with ranges across studies with similar characteristics.

The review was followed by meta-analysis of RCTs, CCTs and two-group pre-post studies. Meta-analysis was performed using Comprehensive Meta-Analysis (CMA) software Version 3 [17]. Due to wide variety of interventions used and populations addressed, random effects model was selected. The pooled effect size (ES) was calculated from the proportion of women screened post intervention in the intervention and control groups, respectively, and was reported with 95% confidence intervals along with p values (p<0.05 considered as threshold for statistical significance). Q statistics and I2 values were reported to inform about heterogeneity. A statistically significant Q value is indicative of heterogenous distribution of ES, whereas the I2 statistic describes ES heterogeneity contributed by non-sampling error. Additionally, a prediction interval with 95% confidence interval was calculated, which is an accurate measurement of heterogeneity and variance of the ES, and gives more information on the distribution of effect than I2 analysis alone [18]. To explore heterogeneity further, studies were then stratified into subgroups based on explanatory variables such as study type. Analysis was only performed when there were three or more studies available in a stratification group.

Publication bias was assessed by visual funnel plots inspection, assessment of symmetry via Egger’s test and Begg–Mazumdar Kendall’s Tau test. When bias was found, it was adjusted using trim and fill method introduced by Duval and Tweedie [19]. Sensitivity analysis was also conducted by removing studies with low quality (that scored weak on EPHPP scale), as well as an evident outlier with the highest effect size.

Critical synthesis and quality appraisal of the studies

The quality of included studies was appraised using the Effective Public Health Care Practice Project (EPHPP) quantitative study quality assessment tool. This tool was first published in 1998 and effectively measures quality of intervention studies, especially in public health [20, 21]. It assesses six criteria: selection bias (representation by target population), study design and randomisation, confounders and their adjustment, blinding of participants and assessors, validity and reliability of data collection methods, and withdrawals and dropouts. The scores were determined by two independent reviewers (ZA, JC) and inter-rater reliability using Cohen’s kappa calculated.

Results

In total, 1,900 articles were retrieved from databases including Pubmed (392), Scopus (459), EMBASE (480), CINAHL (356), PsycINFO (140), CENTRAL (53) and ERIC (3) and bibliographies of the included articles (17) (Fig 1). After removal of 1,151 duplicates, 749 studies remained. Their titles and abstracts were searched to include relevant interventions, yielding 103 studies. Of these, 42 articles were chosen after a full text review, with 28/42 included in the meta-analysis. Remaining studies (61) were excluded as they lacked full text (10), had irrelevant outcomes/inadequate information on outcome measures (23), focused on increasing knowledge only (3), focused on intervention design (9) or included generalised information summary (7) only, addressed irrelevant populations (8), or consisted of review (1).

thumbnail
Fig 1. PRISMA flowchart for the systematic review and meta-analysis process.

https://doi.org/10.1371/journal.pone.0281976.g001

Characteristics of the included studies

Of the 42 studies in total, 21 were RCTs, four CCTs, 12 (single group pre-post) and four (two group pre-post) cohort analytic studies. Table 1 provides the characteristics of overall studies included in the systematic review. The majority of studies (23) were conducted between 2011–2021. The number of participants ranged from 42–10,810, age ranged from 18–72 years, with similar participant characteristics in the controlled trials as in overall studies, while the cohort analytic studies had a smaller maximal number of participants (65–1,732).

thumbnail
Table 1. Number of studies grouped by characteristics in the systematic review.

https://doi.org/10.1371/journal.pone.0281976.t001

Baseline screening status of participants in most of the studies (34/42) was under- or never- screened, however nine studies included participants who were up to date with screening as well. The majority of studies (36/42) were conducted in community settings (residences, churches, community centres, consulates); 31 in metropolitan and five in rural areas, whereas the rest (5/42) were conducted in healthcare settings (refugee/immigrant clinics). The majority of studies were conducted in the US (31), with relatively few in other countries: Canada (3), Hong Kong (3), UK (2), and Norway (2). Nearly one third (14) of the studies targeted multiethnic participants, whereas the rest involved immigrants from specific backgrounds only, including Latinas (4), Vietnamese (5), Hispanic (5), South Asian (4), Filipino (1), Chinese (2), Mexican (2), Korean (2), Cambodian (1), Somali (1) and Pacific Islander (1).

Most of the studies involved immigrant women from the community not belonging to any specific profession, while six studies focused on specific subgroups i.e., nail salon workers, farmworkers, and female sex workers (Table 2). The follow-up time after intervention ranged between two months to four years, with the majority having six months follow-up. Based on the EPHPP tool, most studies were weak in quality (21), followed by moderate (15) and strong (5).

thumbnail
Table 2. Characteristics of the individual studies in the systematic review, with reported outcome measures.

https://doi.org/10.1371/journal.pone.0281976.t002

Intervention characteristics

Difference in cervical screening uptake ranged from 20–96% in the pre-post studies and -6.7 to 81% in controlled studies, for an overall range difference of -6.7 to 96% (Table 2). Almost all intervention studies focused on increasing cervical screening uptake through education, with eight using brochures or flip charts, 13 using audio-visual tools, and 10 using a combination of both. The screening uptake difference ranged from 16.7–81% for interventions using brochures, 2.4–87% for those using videos and -6.7 to 70% using a combination of both. The majority of the interventions (34/42) were delivered in person via Promotoras or health care workers, with three combining these with mailed materials [20, 28, 50], and one with media delivered education [31], whereas three solely used telephone, mail and media each [24, 29, 34]. Of the reviewed studies, 15 used behavioural intervention techniques beyond education such as motivation, persuasion and role modelling via survivors, celebrities, and narrative videos (screening uptake difference -6.7 to 77%). Three studies used specialised immigrant clinics to reach the target population (screening uptake difference 51−96%) [32, 55, 56].

Although most interventions promoted Pap test only, three focused on increasing HPV self-sampling in combination with Pap test, and resulted in increased cervical screening by 66−77%, compared to 11−48% increase in Pap test arms [42, 43, 47]. Another RCT offered self-sampling option only in person or by mail resulting increasing cervical screening by 81 and 72%, respectively [50]. Relatively few studies (3) involved health care practitioners in intervention delivery, of which one RCT, conducted in family doctor practices, yielded screening uptake increase by 2.6% [58] and two single group pre-post studies by 52−87% [40, 55]. Moreover, navigation, reminders and financial incentives as additional components of intervention were used in 26 studies, reporting screening uptake increases by 8−96%. Most studies (25) assessed screening uptake through self-reported uptake of -6.7 to81%, whereas 17 used objective measures such as medical record extraction reporting an increase of 2.6−96%. Not all controlled trials used completely unexposed control arms, seven studies used minimal intervention groups [33, 36, 41, 45, 47, 54, 61], three used intensive intervention groups as control arms [44, 52, 59], whereas four used attention control interventions such as physical activity or diabetes education [30, 41, 46, 48]. When grouped based on type of control group, participants in the intervention group had a change in cervical screening of -6.6 to 24.8% in studies with non-exposed control groups, 8−77% with a minimally exposed control groups, 38−81% in intensive interventions control groups, and 3−19% in control groups offered attention control interventions.

Results from meta-analysis

The 28 studies included in the meta-analysis had 35 intervention arms. They included 35,495 participants overall, 20,685 in the control arms and 14,810 in the intervention arms, respectively. Pooled ES of cervical screening yielded a rate ratio of 1.49 (95% confidence interval (CI): 1.36–1.65), (Fig 2) with a Q value of 402.2 and I2 value of 93%, indicating high heterogeneity. Prediction interval calculation indicated that the true ES in 95% of the comparable populations would fall between 0.95–2.34, thus concluding that cervical screening intervention would likely, but not always, be effective in immigrant populations. However, funnel plot inspection (Fig 3), Begg–Mazumdar Kendall’s Tau (–0.43, p = 0.001) and Egger tests (intercept = 3.66, p = 0.0001) indicated publication bias. Therefore, the ES was recalculated using Duval and Tweedie’s trim and fill method, with 10 studies being adjusted, resulting in an ES of 1.15 (95% CI 1.03−1.29, p < 0.001) (Table 3). Substantial heterogeneity remained in almost all subgroups that were formed based on explanatory variables, indicating differences in intervention design, methodology and populations. Publication bias was also evident for most subgroups and adjusted accordingly (Table 3).

thumbnail
Fig 2. Forest plot for effect size (rate ratio) for getting screened post-intervention in overall 28 studies included in the meta-analysis.

https://doi.org/10.1371/journal.pone.0281976.g002

thumbnail
Fig 3. Publication bias evident from the funnel plot for the overall studies included in the meta-analysis.

https://doi.org/10.1371/journal.pone.0281976.g003

thumbnail
Table 3. Results for effect sizes among studies grouped by common variables, with observed heterogeneity and adjusted effect size for publication bias.

https://doi.org/10.1371/journal.pone.0281976.t003

Subgroup meta-analysis indicated that when information and education was delivered using multiple modalities such as brochures and visual media strategies, ES (1.29 (95% CI: 0.83–2.00)) were higher, compared to using each modality alone (Refer to S1 Fig (a-k) for the subgroup forest plots). Results also suggested that multifaceted interventions had higher likelihood of increasing screening (ES 1.19 95% CI: (1.04–1.36)) compared to provision of education alone (ES 1.10 (95% CI: 0.97–1.24)). Studies with interventions delivered in person had a higher ES of 1.18 (95% CI: 1.04–1.35) compared to the ones that were not (ES 1.13 (95% CI 0.98–1.30)). It was observed that interventions with attention control arms such as exercise and diabetes education had lower effect (ES 1.04 (95% CI: 1.00–1.09)), compared to those with non-exposed control groups (ES 1.23 (95% CI: 1.04–1.44)) or minimal intervention groups (ES 1.15 (95% CI: 0.88–1.51)).

Interventions with under- or never-screened participants had considerably higher ES of 1.34 (95% CI: 1.00–1.81)), compared to those that also included participants up to date (ES 1.10 (95% CI: 1.06–1.14). Theoretically guided intervention studies had higher ES as did the ones involving community health workers and those conducted at broader level involving multiple locations within the country. No statistically significant difference in ES was seen in groups based on length of follow up, outcome source or study quality. When sensitivity analysis was conducted by removing studies with low quality [28, 63], or those evident as outliers in the funnel plot [47], heterogeneity indices remained the same and no effect was observed on the effect size.

Quality appraisal and risk of bias

Quality appraisal results suggested that the majority of the cohort pre-post studies were weak (13) due to lack of randomisation and participant blinding, contributing towards low overall quality scores. Common reasons for the controlled trials to be weak included selection bias due to lack of representative population when participants were conveniently sampled, or lack of details on confounder adjustment. Refer to S3 Table for description of individual quality criteria for all studies included in meta-analysis. Inter-rater reliability testing between the two quality raters (ZA, JC) yielded Cohen’s Kappa of 0.4. The reason for low kappa score was differences in perception of rating criteria (selection bias, confounding) between the reviewers.

Discussion

This study critically reviewed and meta-analysed interventions to increase cervical screening uptake among immigrant women globally. The review found that culturally appropriate interventions such as those providing HPV self-sampling methodology and targeted clinics for immigrants are most effective. Meta-analysis found that multicomponent interventions were more beneficial than single component ones, as were those theoretically guided, delivered in-person and using multiple formats of information delivery. Participant characteristics, such as baseline screening status also influenced the success of the interventions, as did the type of intervention selected for the control group.

To our knowledge this is the first systematic review and meta-analysis to comprehensively map the global evidence on the effectiveness of interventions to increase cervical screening in immigrant women. It compared the intervention effect sizes based on characteristics such as delivery format, involvement of HCPs, modes of educative material, screening status of participants and type of control group. The strengths of this study include following a prospectively registered protocol, clearly and transparently outlining our search strategy and methods of analysis, having multiple reviewers independently working on each review stage, and investigating novel methods of encouraging screening i.e., self-sampling, not included in previous intervention reviews on immigrants. However, this review also has certain limitations. First, although we conducted a comprehensive search of multiple databases, some studies might not have been located. We tried to overcome this through hand citation searches. Second, we found the EPHPP tool was more favorable towards experimental studies compared to non-controlled studies resulting in most studies being scored of weak quality. We also found significant heterogeneity in the studies limiting the number we could include in the sub-group meta-analyses.

The meta-analysis results suggested a low overall ES of 1.15 (95% CI 1.03–1.29) across all intervention studies after adjustment for publication bias. Although the results suggest a positive effect of interventions for cervical screening uptake, the results need to be interpreted with caution, in light of high heterogeneity (I2 = 93%, Q = 402.2). However, heterogeneity often cannot be prevented in behaviour change studies, especially when dealing with diverse populations that require interventions adapted to their special needs. Similar heterogeneity has been observed in studies reporting meta-analysis of intervention studies for screening for other cancers [64]. Publication bias encountered in this review suggests that studies with less positive outcomes may exist but are difficult to trace [65]. Despite our efforts to find these unpublished studies, none could be discovered. Additionally, low Kappa score as evaluated in our study indicates weak interrater reliability on the quality appraisal of the studies. However, the literature suggests that the Kappa index may amplify disagreement estimate among the raters [66]. A low Kappa index is more of a concern when dealing with diagnostic tests in clinical studies [67] compared to quality appraisal, as in the current study.

The interventions included in the systematic review ranged from simple approaches such as mere provision of information, to those incorporating multiple components such as support of women using behaviour change techniques, patient navigation and practical help (provision of clinics for immigrants, childcare and transport). It was evident that the complex multifaceted interventional options, addressing broad areas of behavioural change and helping overcome the logistic constraints, were more effective at improving cervical screening uptake. It is similar to what has been reported for screening uptake for other cancers [64, 68], and for cervical screening among women generally [9]. In contrast to the systematic review findings, meta-analysis suggested that combined modes of information provision such as brochures, visual media as well as written information are more effective than using each of these strategies alone, similar to previous findings [69]. The difference between systematic review and meta-analysis findings could reflect that the meta-analysis mainly included higher quality studies and trials. Interventions that were guided by theoretical behaviour change models also had statistically significant stronger ES compared to the studies which were not. The advantages offered by interventional designs based on theoretical models have been summarised previously [70].

Interventions in broad populations, including both under- and well-screened women, compared to those including under- or never-screened women only, were less effective. Previous research also reported better effectiveness of risk-targeted rather than population-based interventions [71]. Thus, choosing the population on which to intervene is important, although it might be less convenient to reach a specific proportion rather than an entire immigrant population subgroup.

One of the intervention methods that recently became available and seems promising is HPV self-sampling. Although meta-analysis could not be performed due to the limited number of self-sampling studies available, the systematic review reported it resulted in higher screening compared to other interventions. A previous systematic review and meta-analysis reported self-sampling is more effective in increasing screening participation than traditional Pap testing in women generally [14]. Various barriers to screening common among immigrant women, such as modesty, religious reasons, and female HCP preference favour usage of HPV self-sampling in this population [72]. Similarly, HCP involvement significantly improved screening uptake, although few studies of interventions targeting HCP behaviours have been carried out. Interventions aimed at HCPs alongside the women could be important in enhancing screening uptake as suggested for other cancers [73]. The systematic review also reported the advantage of use of specialised clinics to reach immigrant women and enhance their screening uptake. Although meta-analysis could not be performed due to lack of eligible studies, a previous meta-analysis indicated specialised clinics to be strongly effective in increasing immunisation and cancer screening uptake among adults [74]. Likewise, cultural appropriateness is important when dealing with individuals of immigrant background, with availability of materials in the women’s native language being critical. All studies in this review used the same languages as that of the participants and often involved lay community health workers, such as Promotoras; this personalised approach was effective in the meta-analysis. Therefore, policies designed to address cervical screening services and interventions for migrants should take into consideration relevance of cultural responsiveness when including components such as information provision, navigation as well as financial incentives.

Another interesting finding from the systematic review was higher screening uptake rates when outcomes were assessed objectively rather than through self-report, although meta-analysis did not report statistically significant difference among the two groups, A possible explanation could be greater reliability of clinical records which can be obtained without the need of follow-up of each individual participant, reducing the non-response bias.

None of the included study reported cost-effectiveness of the intervention used, it is recommended to include this outcome in future studies. This would be of high practical value, allowing the policymakers to understand the choice of intervention, including of HPV self-sampling method. A recent systematic review of studies assessing cost of HPV self-sampling compared to standard screening strategies, reported it to be highly cost-effective for under screened women in high income countries, either when offered alone or in combination with other strategies [75]. Furthermore, effect of certain variable of interest, age and such as length of stay of participants in the country, could be explored through meta-regression in future studies.

In conclusion, this review identified a large number of studies, that have evaluated interventions to increase uptake of cervical screening amongst immigrant women. The findings suggest that interventions with multifaceted, culturally sensitive components, addressing practical challenges and including HPV self-sampling modality, could lead to significant increase in cervical screening participation among immigrant women. Review findings also suggest that using multiple channels to communicate with the target audience is the next most important feature of a likely successful intervention strategy. However, due to substantial heterogeneity observed in the meta-analysis results, intervention effects need to be interpreted cautiously. There is opportunity to study interventions that involve trusted HCPs [76, 77]. We recommend future research on this topic adopts robust study designs to improve the quality of the studies and avoid potential contamination. Theoretically guided interventions, targeted in their approach to ensure recruitment of women who could benefit most from an intervention, are recommended.

Supporting information

S1 File. Published PROSPERO protocol for the systematic review and meta-analysis.

https://doi.org/10.1371/journal.pone.0281976.s001

(PDF)

S1 Fig. Forest plots showing sub-group analysis for cervical screening intervention studies included in the meta-analysis.

https://doi.org/10.1371/journal.pone.0281976.s002

(DOCX)

S1 Table. PRISMA 2020 checklist as used in the review process.

https://doi.org/10.1371/journal.pone.0281976.s003

(DOCX)

S2 Table. Search strategy as used in different databases.

https://doi.org/10.1371/journal.pone.0281976.s004

(DOCX)

S3 Table. Quality appraisal of studies included in the systematic review.

https://doi.org/10.1371/journal.pone.0281976.s005

(DOCX)

References

  1. 1. Sung H, Ferlay J, Siegel RL, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021; 71: 209–249. pmid:33538338
  2. 2. Serrano B, Brotons M, Bosch FX, Bruni L. Epidemiology and burden of HPV-related disease. Best Pract Res Clin Obstet Gynaecol. 2018;47:14–26. pmid:29037457
  3. 3. Shrestha AD, Neupane D, Vedsted P, Kallestrup P. Cervical Cancer Prevalence, Incidence and Mortality in Low and Middle Income Countries: A Systematic Review. Asian Pac J Cancer Prev. 2018;19(2):319–24. pmid:29479954
  4. 4. D’Oria O, Corrado G, Laganà AS, Chiantera V, Vizza E, Giannini A. New Advances in Cervical Cancer: From Bench to Bedside. International Journal of Environmental Research and Public Health. 2022 Jun 9;19(12):7094. pmid:35742340
  5. 5. Landy R, Pesola F, Castañón A, Sasieni P. Impact of cervical screening on cervical cancer mortality: estimation using stage-specific results from a nested case–control study. Br J Cancer. 2016;115(9):1140–6. pmid:27632376
  6. 6. Giannini A, Bogani G, Vizza E, Chiantera V, Laganà AS, Muzii L, et al. Advances on Prevention and Screening of Gynecologic Tumors: Are We Stepping Forward?. InHealthcare 2022 Aug 24 (Vol. 10, No. 9, p. 1605). MDPI. pmid:36141217
  7. 7. Davies-Oliveira J, Smith M, Grover S, Canfell K, Crosbie E. Eliminating cervical cancer: progress and challenges for high-income countries. Clin Oncol. 2021;33(9):550–9. pmid:34315640
  8. 8. Machado S, Wiedmeyer M-l, Watt S, Servin AE, Goldenberg S. Determinants and Inequities in Sexual and Reproductive Health (SRH) Care Access Among Immigrant Women in Canada: Findings of a Comprehensive Review (2008–2018). J Immigr Minor Health. 2022;24(1):256–99. pmid:33811583
  9. 9. Lu M, Moritz S, Lorenzetti D, Sykes L, Straus S, Quan H. A systematic review of interventions to increase breast and cervical cancer screening uptake among Asian women. BMC Public Health. 2012;12(1):413. pmid:22676147
  10. 10. Mann L, Foley KL, Tanner AE, Sun CJ, Rhodes SD. Increasing cervical cancer screening among US Hispanics/Latinas: a qualitative systematic review. J Cancer Educ. 2015;30(2):374–87. pmid:25154515
  11. 11. Rees I, Jones D, Chen H, Macleod U. Interventions to improve the uptake of cervical cancer screening among lower socioeconomic groups: a systematic review. Prev Med. 2018;111:323–35 pmid:29203349
  12. 12. Musa J, Achenbach CJ, O’Dwyer LC, Evans CT, McHugh M, Hou L, et al. Effect of cervical cancer education and provider recommendation for screening on screening rates: A systematic review and meta-analysis. PLoS One. 2017;12(9):e0183924. pmid:28873092
  13. 13. Naz MSG, Kariman N, Ebadi A, Ozgoli G, Ghasemi V, Fakari FR. Educational interventions for cervical cancer screening behavior of women: a systematic review. Asian Pac J Cancer Prev. 2018;19(4):875. pmid:29693331
  14. 14. Racey CS, Withrow DR, Gesink D. Self-collected HPV testing improves participation in cervical cancer screening: a systematic review and meta-analysis. Can J Public Health. 2013;104(2):e159–e66. pmid:23618210
  15. 15. Gultekin M, Ramirez PT, Broutet N, Hutubessy R. World Health Organization call for action to eliminate cervical cancer globally. Int J Gynecol Cancer. 2020 Apr 1;30(4):426–7. pmid:32122950
  16. 16. Page MJ, Moher D, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. PRISMA 2020 explanation and elaboration: updated guidance and exemplars for reporting systematic reviews. BMJ. 2021;372. pmid:33781993
  17. 17. Borenstein M, Hedges L., Higgins J., & Rothstein H. Comprehensive Meta-Analysis Version 3. Biostat, Englewood, NJ: Borenstein M, Hedges L, Higgins J, Rothstein H; 2013.
  18. 18. IntHout J, Ioannidis JP, Rovers MM, Goeman JJ. Plea for routinely presenting prediction intervals in meta-analysis. BMJ Open. 2016;6(7):e010247. pmid:27406637
  19. 19. Duval S, Tweedie R. Trim and fill: a simple funnel‐plot–based method of testing and adjusting for publication bias in meta‐analysis. Biometrics. 2000;56(2):455–63. pmid:10877304
  20. 20. Thomas B, Ciliska D, Dobbins M, Micucci S. A process for systematically reviewing the literature: providing the research evidence for public health nursing interventions. Worldviews Evid Based Nurs. 2004;1(3):176–84. pmid:17163895
  21. 21. Armijo‐Olivo S, Stiles CR, Hagen NA, Biondo PD, Cummings GG. Assessment of study quality for systematic reviews: a comparison of the Cochrane Collaboration Risk of Bias Tool and the Effective Public Health Practice Project Quality Assessment Tool: methodological research. J Eval Clin Pract. 2012;18(1):12–8. pmid:20698919
  22. 22. Bird J. A., McPhee S. J., Ha N. T., Le B., Davis T., & Jenkins C. N. Opening pathways to cancer screening for Vietnamese-American women: lay health workers hold a key. Preventive medicine, 1998; 27(6), 821–829. pmid:9922064
  23. 23. McAvoy BR, Raza R. Can health education increase uptake of cervical smear testing among Asian women? Br J Med. 1991;302(6780):833–6. pmid:1958248
  24. 24. Kernohan E. Evaluation of a pilot study for breast and cervical cancer screening with Bradford’s minority ethnic women; a community development approach, 1991–93. Br J Cancer Suppl. 1996;29:S42. pmid:8782798
  25. 25. Goldsmith DF, Sisneros GC. Cancer prevention strategies among California farmworkers: preliminary findings. J Rural Health. 1996;12:343–8. pmid:10162865
  26. 26. Jenkins CN, McPhee SJ, Bird JA, Pham GQ, Nguyen BH, Nguyen T, et al. Effect of a media-led education campaign on breast and cervical cancer screening among Vietnamese-American women. Prev Med. 1999;28(4):395–406. pmid:10090869
  27. 27. Byrd TL, Wilson KM, Smith JL, Coronado G, Vernon SW, Fernandez‐Esquer ME, et al. AMIGAS: a multicity, multicomponent cervical cancer prevention trial among Mexican American women. Cancer. 2013;119(7):1365–72. pmid:23280399
  28. 28. Jackson JC, Do H, Chitnarong K, Tu S-P, Marchand A, Hislop G, et al. Development of cervical cancer control interventions for Chinese immigrants. J Immigr Health. 2002;4(3):147–57. pmid:16228758
  29. 29. Meade CD, Calvo A, Cuthbertson D. Impact of culturally, linguistically, and literacy relevant cancer information among Hispanic farmworker women. J Cancer Educ. 2002;17(1):50–4. pmid:12000108
  30. 30. Taylor VM, Hislop TG, Jackson JC, Tu S-P, Yasui Y, Schwartz SM, et al. A randomized controlled trial of interventions to promote cervical cancer screening among Chinese women in North America. J Natl Cancer Inst. 2002;94(9):670–7. pmid:11983755
  31. 31. Jibaja-Weiss ML, Volk RJ, Kingery P, Smith QW, Holcomb JD. Tailored messages for breast and cervical cancer screening of low-income and minority women using medical records data. Patient Educ Couns. 2003;50(2):123–32. pmid:12781927
  32. 32. Maxwell AE, Bastani R, Vida P, Warda US. Results of a randomized trial to increase breast and cervical cancer screening among Filipino American women. Prev Med. 2003;37(2):102‐9. pmid:12855209
  33. 33. Lam TK, McPhee SJ, Mock J, Wong C, Doan HT, Nguyen T, et al. Encouraging Vietnamese-American women to obtain pap tests through lay health worker outreach and media education. J Gen Intern Med. 2003;18(7):516–24. pmid:12848834
  34. 34. Grewal S, Bottorff JL, Balneaves LG. A Pap test screening clinic in a South Asian community of Vancouver, British Columbia: challenges to maintaining utilization. Public Health Nurs. 2004;21(5):412–8. pmid:15363021
  35. 35. Black MEA, Frisina A, Hack T, Carpio B. Improving early detection of breast and cervical cancer in Chinese and vietnamese immigrant women. Oncol Nurs Forum. 2006;33(5):873–6. pmid:16986222
  36. 36. Dietrich AJ, Tobin JN, Cassells A, Robinson CM, Greene MA, Sox CH, et al. Telephone care management to improve cancer screening among low-income women: A randomized, controlled trial. Ann Intern Med. 2006;144(8):563–71. pmid:16618953
  37. 37. Wong WCW, Wun YT, Chan KW, Liu Y. Silent killer of the night: A feasibility study of an outreach well-women clinic for cervical cancer screening in female sex workers in Hong Kong. Int J Gynecol Cancer. 2008;18(1):110–5.
  38. 38. Fernandez ME, Lin J, Leong-Wu C, Aday L. Pap smear screening among Asian Pacific Islander women in a multisite community-based cancer screening program. Health Promot Pract. 2009;10(2):210–21. pmid:19372282
  39. 39. O’Brien MJ, Halbert CH, Bixby R, Pimentel S, Shea JA. Community health worker intervention to decrease cervical cancer disparities in Hispanic women. J Gen Intern Med. 2010;25(11):1186–92. pmid:20607434
  40. 40. Wang X, Fang C, Tan Y, Liu A, Ma GX. Evidence-based intervention to reduce access barriers to cervical cancer screening among underserved Chinese American women. J Womens Health. 2010;19(3):463–9. pmid:20156089
  41. 41. Nuño T, Martinez ME, Harris R, García F. A promotora-administered group education intervention to promote breast and cervical cancer screening in a rural community along the US–Mexico border: a randomized controlled trial. Cancer Causes Control. 2011;22(3):367–74.
  42. 42. White K, Garces IC, Bandura L, McGuire AA, Scarinci IC. Design and evaluation of a theory-based, culturally relevant outreach model for breast and cervical cancer screening for latina immigrants. Ethn Dis. 2012;22(3):274–80. pmid:22870569
  43. 43. Jandorf L, Ellison J, Shelton R, Thélémaque L, Castillo A, Mendez EI, et al. Esperanza y vida: A culturally and linguistically customized breast and cervical education program for diverse latinas at three different United States Sites. J Health Commun. 2012;17(2):160–76. pmid:22059729
  44. 44. Sewali B, Okuyemi KS, Askhir A, Belinson J, Vogel RI, Joseph A, et al. Cervical cancer screening with clinic-based Pap test versus home HPV test among Somali immigrant women in Minnesota: A pilot randomized controlled trial. Cancer Med. 2015;4(4):620–31. pmid:25653188
  45. 45. Carrasquillo O, Kobetz- Kerman EN, Alonzo Y. A randomized trial of self-sampling for human papilloma virus among minority immigrant women in need of cervical cancer screening: findings from the South Florida center for reducing cancer disparities. J Gen Intern Med. 2015;30:S90.
  46. 46. Han H-R, Song Y, Kim M, Hedlin HK, Kim K, Ben Lee H, et al. Breast and cervical cancer screening literacy among Korean American women: A community health worker–led intervention. Am J Public Health. 2017;107(1):159–65. pmid:27854539
  47. 47. Ma GX, Fang C, Tan Y, Feng Z, Ge S, Nguyen C. Increasing cervical cancer screening among Vietnamese Americans: A community-based intervention trial. J Health Care Poor Underserved. 2015;26(2 Suppl):36. pmid:25981087
  48. 48. Elder JP, Arredondo EM, Haughton J, Perez LG, Martinez ME. Fe en Acción/Faith in Action: promotion of cancer screening among churchgoing Latinas. Cancer Epidemiol Biomarkers Prev. 2016;25(3).
  49. 49. Ilangovan K, Kobetz E, Koru-Sengul T, Marcus EN, Rodriguez B, Alonzo Y, et al. Acceptability and feasibility of human papilloma virus self-sampling for cervical cancer screening. J Womens Health. 2016;25(9):944–51. pmid:26890012
  50. 50. Luque JS, Tarasenko YN, Reyes-Garcia C, Alfonso ML, Suazo N, Rebing L, et al. Salud es Vida: a Cervical Cancer Screening Intervention for Rural Latina Immigrant Women. J Cancer Educ. 2017;32(4):690–9. pmid:26757902
  51. 51. Dunn SF, Lofters AK, Ginsburg OM, Meaney CA, Ahmad F, Moravac MC, et al. Cervical and Breast Cancer Screening After CARES: A Community Program for Immigrant and Marginalized Women. Am J Prev Med. 2017;52(5):589–97. pmid:28094134
  52. 52. Kobetz E, Seay J, Koru-Sengul T, Bispo JB, Trevil D, Gonzalez M, et al. A randomized trial of mailed HPV self-sampling for cervical cancer screening among ethnic minority women in South Florida. Cancer Causes Control. 2018;29(9):793–801. pmid:29995217
  53. 53. Brown LD, Vasquez D, Salinas JJ, Tang X, Balcázar H. Evaluation of Healthy Fit: A community health worker model to address Hispanic health disparities. Prev Chronic Dis. 2018;15(4).
  54. 54. Savas LS, Heredia NI, Coan SP, Fernandez ME. Effectiveness of a community health worker-delivered intervention to increase breast and cervical cancer screening among medically underserved hispanics. J Glob Oncol. 2018;4:19.
  55. 55. Wong CL, Choi KC, Law BM, Chan DN, So WK. Effects of a community health worker-led multimedia intervention on the uptake of cervical cancer screening among South Asian women: a pilot randomized controlled trial. Int J Environ Res Public Health. 2019;16(17):3072. pmid:31450853
  56. 56. Chan D, So W. The impact of community-based multimedia intervention on the new and repeated cervical cancer screening participation among South Asian women. Public Health. 2020;178:1–4. pmid:31593783
  57. 57. Kiser LH, Butler J. Improving Equitable Access to Cervical Cancer Screening and Management. Am J Nurs. 2020;120(11):58–67. pmid:33105224
  58. 58. Fernández-Esquer ME, Nguyen FM, Atkinson JS, Le YC, Chen S, Huynh TN, et al. Sức Khỏe là Hạnh Phúc (Health is Happiness): promoting mammography and pap test adherence among Vietnamese nail salon workers. Women Health. 2020;60(10):1206–17.
  59. 59. Ochoa CY, Murphy ST, Frank LB, Baezconde-Garbanati LA. Using a Culturally Tailored Narrative to Increase Cervical Cancer Detection Among Spanish-Speaking Mexican-American Women. J Cancer Educ. 2020;35(4):736–42. pmid:31020621
  60. 60. Møen KA, Kumar B, Igland J, Diaz E. Effect of an Intervention in General Practice to Increase the Participation of Immigrants in Cervical Cancer Screening: a Cluster Randomized Clinical Trial. JAMA Netw Open. 2020;3(4):e201903. pmid:32236530
  61. 61. Wong CL, Choi KC, Chen J, Law BM, Chan DN, So WK. A Community Health Worker–Led Multicomponent Program to Promote Cervical Cancer Screening in South Asian Women: A Cluster RCT. Am J Prev Med. 2021. pmid:33781617
  62. 62. Choi SY. Development of an educational program to prevent cervical cancer among immigrants in Korea. Asian Pac J Cancer Prev. 2013;14(9):5345–9. pmid:24175823
  63. 63. Qureshi SA, Gele A, Kour P, Møen KA, Kumar B, Diaz E. A community-based intervention to increase participation in cervical cancer screening among immigrants in Norway. BMC Med Res Methodol. 2019;19(1):1–8.
  64. 64. Dougherty MK, Brenner AT, Crockett SD, Gupta S, Wheeler SB, Coker-Schwimmer M, et al. Evaluation of Interventions Intended to Increase Colorectal Cancer Screening Rates in the United States: A Systematic Review and Meta-analysis. JAMA Inten Med. 2018;178(12):1645–58. pmid:30326005
  65. 65. Sun J, Freeman BD, Natanson C. Chapter 22—Meta-analysis of Clinical Trials. In: Gallin JI, Ognibene FP, Johnson LL, editors. Principles and Practice of Clinical Research (Fourth Edition). Boston: Academic Press; 2018. p. 317–27.
  66. 66. Feinstein AR, Cicchetti DV. High agreement but low kappa: I. The problems of two paradoxes. Journal of clinical epidemiology. 1990 Jan 1;43(6):543–9. pmid:2348207
  67. 67. McHugh ML. Interrater reliability: the kappa statistic. Biochemia medica. 2012 Oct 15;22(3):276–82 pmid:23092060
  68. 68. Pasick RJ, Hiatt RA, Paskett ED. Lessons learned from community‐based cancer screening intervention research. Cancer: Interdisciplinary International Journal of the American Cancer Society. 2004;101(S5):1146–64. pmid:15316912
  69. 69. Marcus AC, Crane LA. A Review of Cervical Cancer Screening Intervention Research: Implications for Public Health Programs and Future Research. Prev Med. 1998;27(1):13–31. pmid:9465350
  70. 70. Eccles M. The Improved Clinical Effectiveness Through Behavioral Research Group (ICEBERG). Designing theoretically-informed implementation interventions. Implement Sci. 2006;23;1(1):4.
  71. 71. Zulman DM, Vijan S, Omenn GS, Hayward RA. The relative merits of population‐based and targeted prevention strategies. Milbank Quarterly. 2008;86(4):557–80. pmid:19120980
  72. 72. Marlow LA, Waller J, Wardle J. Barriers to cervical cancer screening among ethnic minority women: a qualitative study. J Fam Plann Reprod Health Care. 2015;41(4):248–54. pmid:25583124
  73. 73. Aragones A, Schwartz MD, Shah NR, Gany FM. A randomized controlled trial of a multilevel intervention to increase colorectal cancer screening among Latino immigrants in a primary care facility. J Gen Intern Med. 2010;25(6):564–7. pmid:20213208
  74. 74. Stone EG, Morton SC, Hulscher ME, Maglione MA, Roth EA, Grimshaw JM, et al. Interventions that increase use of adult immunization and cancer screening services: a meta-analysis. Ann Intern Med. 2002;136(9):641–51. pmid:11992299
  75. 75. Malone C, Barnabas RV, Buist DS, Tiro JA, Winer RL. Cost-effectiveness studies of HPV self-sampling: A systematic review. Prev Med. 2020 Mar 1;132:105953. pmid:31911163
  76. 76. Aubin‐Auger I, Laouénan C, Le Bel J, Mercier A, Baruch D, Lebeau JP, et al. Efficacy of communication skills training on colorectal cancer screening by GP s: a cluster randomised controlled trial. Eur J Cancer Care. 2016;25(1):18–26.
  77. 77. Brouwers MC, De Vito C, Bahirathan L, Carol A, Carroll JC, Cotterchio M, et al. Effective interventions to facilitate the uptake of breast, cervical and colorectal cancer screening: an implementation guideline. Implement Sci. 2011;6(1):1–8.