breast cancer care pathway case study

• Study protocol
• Open access
• Published: 12 May 2015

The patient-breast cancer care pathway: how could it be optimized?

• Sandrine Baffert 1 ,
• Huong Ly Hoang 1 ,
• Anne Brédart 2 ,
• Bernard Asselain 3 ,
• Séverine Alran 4 ,
• Hélène Berseneff 5 ,
• Cyrille Huchon 6 ,
• Caroline Trichot 7 ,
• Aline Combes 8 ,
• Karine Alves 9 ,
• Martin Koskas 10 ,
• Thuy Nguyen 11 ,
• Aurélie Roulot 12 ,
• Roman Rouzier 12 , 13 &
• Delphine Héquet 12 , 13  

BMC Cancer volume  15 , Article number:  394 ( 2015 ) Cite this article

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A care pathway is defined as patient-focused global care that addresses temporal (effective and coordinated management throughout the illness) and spatial issues (treatment is provided near the health territory in or around the patient’s home). Heterogeneity of the care pathways in breast cancer (BC) is presumed but not well evaluated. The OPTISOINS01 study aims to assess every aspect of the care pathway for early BC patients using a temporal and spatial scope.

Methods/Design

An observational, prospective, multicenter study in a regional health territory (Ile-de-France, France) in different types of structures: university or local hospitals and comprehensive cancer centers. We will include and follow during 1 year 1,000 patients. The study consists of 3 work-packages:

- Cost of pathway

The aim of this WP is to calculate the overall costs of the early BC pathway at 1 year from different perspectives (society, health insurance and patient) using a cost-of-illness analysis. Using a bottom-up method, we will assess direct costs, including medical direct costs and nonmedical direct costs (transportation, home modifications, home care services, and social services), and indirect costs (loss of production).

- Patient satisfaction and work reintegration

Three questionnaires will assess the patients’ satisfaction and possible return to work: the occupational questionnaire for employed women; the questionnaire on the need for supportive care, SCNS-SF34 (‘breast cancer’ module, SCNS-BR8); and the OUTPASSAT-35 questionnaire.

- Quality, coordination and access to innovation

Quality will be evaluated based on visits and treatment within a set period, whether the setting offers a multidisciplinary consultative framework, the management by nurse coordinators, the use of a personalized care plan, the provision of information via documents about treatments and the provision of supportive care.

The coordination between structures and caregivers will be evaluated at several levels. Day surgery, home hospitalization and one-stop breast clinic visits will be recorded to assess the patient’s access to innovation.

The assessment of care pathways encourages the implementation of new payment models. Our approach could help health care professionals and policymakers to establish other cost-of-illness studies and plan the allocation of resources on a patient basis rather than a visit basis.

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Health care systems have evolved into care pathway models in response to chronic diseases and the expenditures related to them. Disease management tends to be multidisciplinary and transversal, reducing the historic place of the hospital in favor of other long-term supports. The shortcomings of health care for chronic disease are shared issues for a number of countries. Cancer has become a chronic disease as a result of improved treatment. Breast cancer (BC) is a good example of a chronic cancer. Incidence, therapeutics, practices and costs of BC can vary substantially in a given area. There are 1.15 million incident cases of breast cancer per year worldwide [ 1 ]. The disease results in high costs in terms of care, out-of-pocket expenses and losses of productivity; the cost of breast cancer was 126 billion € in 2009 in Europe, corresponding to 12 % of all cancer-related costs [ 2 ]. Moreover, the heterogeneity of BC-related care pathways and structures at the regional level are presumed but not well evaluated.

Some international health policies aim to take a more global view of chronic disease. In France, a 2004 law named the referring physician as the organizer of the patient care pathway [ 3 ]. In 2009, the HPST law assigned a central role to the regional health agency (ARS) to improve the continuity of care in a given health territory in France [ 4 ]. A care pathway is defined by the ARS as patient-focused global care that takes a territorial approach. The concept includes education, prevention, diagnosis, treatment, rehabilitation, surveillance and social care. The care pathway addresses temporal (effective and coordinated management throughout the illness) and spatial issues treatment provided in or near the patient’s home health territory). The aim is to provide well-defined practices at well-defined times and places. Care pathways are also presumed to favor equity by facilitating access to care and to improve efficiency by reducing the inappropriate use of health resources.

National initiatives and incentives have enhanced planned care. The chronic care model [ 5 , 6 ], the use of patient-centered medical homes (PCMH) or the facilitation of practice in primary care are being actively promoted and tested in the United States along with bundled payment for some surgical treatments [ 7 ]. However, all of these processes focus on small portions of the care pathway. Multidimensional evaluations of the BC pathway have not yet been described.

Our study, OPTISOINS01, aims to assess every aspect of the care pathway for early BC patients from a chronological and spatial scope. It will describe the stages of the care pathway, including innovative organization. In this paper, we will describe the objectives and the design of the study.

OPTISOINS01 is an observational, prospective, multicenter study conducted with patients from a determined regional health territory. This study was approved by the French National ethics committee (CCTIRS Authorization n°14.602 and CNIL DR-2014-167) and covers research at all participating hospitals.

Setting and population

The three departments of interest in this study (Hauts-de-Seine, Yvelines, and Val d’Oise) cover 35 % of the population of the Ile-de-France region (total population: 11.9 million). With 2.17 million women living in this area, 61 % of whom are older than 45 years, the incidence and mortality of BC in this area are higher than the national rates. This territory was chosen for its heterogeneity in terms of the health care services provided and for its variation in professional densities and facilities, which is linked to the disparate urbanization and population incomes throughout the territory. Eight nonprofit hospitals participate in the study: three university hospitals (Antoine Béclère hospital, Clamart, France; Bichat-Beaujon hospital, Clichy and Paris, France; Louis Mourier hospital, Colombes, France), four local hospitals (André Mignot, Versailles, France; René Dubos, Pontoise, France; Poissy-St Germain hospital, Poissy, France; Victor Dupuy hospital, Argenteuil, France) and one comprehensive cancer center (Curie Institute, Paris and St Cloud, France). These are the hospitals that treat the most BC patients in the Yvelines, Hauts-de-Seine and Val d’Oise departments. Each hospital will include between 30 and 450 patients over 4–6-month period, depending on the yearly number of BC patients treated. A total of 1,000 patients will be included; approximately 150 will undergo outpatient surgery, and 200 will have home hospitalizations. The inclusion and exclusion criteria are presented in Table  1 .

Patients will be approached for the study during their surgery programming visit. The patients will be followed for 1 year, as described in Fig.  1 .

OPTISOIN study design

Objectives and endpoints

This study aims to identify the main care pathway after 1 year of early BC and to evaluate costs from different perspectives. The secondary objectives are to assess patient satisfaction, needs for supportive care, and work reintegration and to evaluate interactions between health care providers in and out of the hospital. In light of these objectives, the study consists of three work packages (WPs).

WP1: cost of pathway

The aim of this WP is to calculate the overall costs of the early BC pathway at 1 year from different perspectives (society, health insurance and patient) using a cost-of-illness analysis. Using a bottom-up method, we will assess direct costs, including medical direct costs and nonmedical direct costs (transportation, home modifications, home care services, and social services), and indirect costs (loss of productivity). Productivity losses will be measured in terms of lost wages using a human capital approach (HCA). From a societal perspective, the HCA estimates an individual’s contribution to society by applying labor force earnings as a measure of productivity. We will evaluate the out-of-pocket health expenses for BC. These include the costs associated with the use of health care services, alternative therapies, dietary supplements, specific cosmetic products, capillary prosthesis, clothes, domestic help and travel expenses. The protocol includes different data sources. Each patient will use a logbook to provide information about her socio-demographic status, her type of health insurance, her outpatient consumptions, her out-of-pocket expenses and her modes of work reintegration. The patient will update the logbook monthly from the post-surgical visit until the 1-year follow-up.

WP2: patient satisfaction and work reintegration

Three questionnaires will assess the patients’ satisfaction and possible return to work.

The occupational questionnaire for employed women includes the following items: dates of work and absence from work during treatments, work arrangements, on-shift status (e.g., the recognition of disability at work, applications for disability allowance, retirement, layoff) and the perceived quality of reintegration (e.g., relationships with colleagues and line management).

The supportive care need survey SCNS-SF34 [ 8 ] and its ‘breast cancer’ module, SCNS-BR8 [ 9 ] includes six care need subscales: “Physical and Daily Living”, “Psychological”, “Health System and Information”, “Patient Care and Support”, “Sexuality” and “Breast Cancer Specific Needs”. Response scores are standardized on a scale ranging from 0 to 100 with higher scores indicating higher needs. Adequate internal consistency (Cronbach’s α) estimates ranged from 0.80–0.93 in a French validation [ 10 ].

The OUTPASSAT-35 questionnaire [ 11 ] is adapted from the EORTC IN-PATSAT32 questionnaire [ 12 ] and has 35 items. The first two parts address physician and nurse care in terms of the professionals’ technical skills, relational quality, information provided and availability. The third part broaches service and organization in terms of information sharing among care providers, the identification of a referring physician, information provided by other staff members, wait times, and the physical environment of the hospital. Patients respond to the items using a 5-point scale. Summing the patient’s responses to the relevant items yields scores for each field and a total score that can be standardized on a scale from 0 to 100, with higher scores indicating higher patient satisfaction (Cronbach’s α ranging from 0.72 to 0.93).

WP3: quality, coordination and access to innovation

Quality will be evaluated based on the visits and treatment during a given period, whether the setting applies a multidisciplinary consultative framework, the management by nurse coordinators, the use of a personalized care plan, and the delivery of information documents related to treatments and supportive care.

Coordination and collaboration among structures and caregivers will be evaluated on several levels. The hospital care provider questionnaire addresses the practices of physicians who are in contact with the patient and the sharing of tools with outpatient caregivers. The referring physician questionnaire describes the role of the referring physician and his interaction with hospital caregivers. The center questionnaire addresses the hospital’s organization and activity and their labor and logistics expenses. An electronic case report form collects medical data and inpatient consumptions.

Several levels of collaboration will be assessed: the organization among different types of professionals within the same hospital, the collaboration among structures, and the individual collaborations among physicians within and outside the hospital.

Outpatient surgery, home hospitalization and one-stop breast clinic visits will be recorded to assess access to innovation.

Statistical analysis

The statistical analysis will be conducted in three steps. First, a descriptive analysis will be conducted on the population studied and on the care pathways.

Second, homogeneous groups of patients will be established based on the patients’ individual medical information, such as age, surgical management procedures, and adjuvant therapy (radiotherapy and chemotherapy). For a given homogeneous group of patients, care pathways and endpoints will be compared. The endpoints are the costs of care pathways, patient satisfaction, work reintegration, readmissions and time lapses between care stages. The variability of these endpoints will be studied in light of the patients’ socio-demographic characteristics and geographical situation and the structure of care. The third part of the analysis will consist of a descriptive approach, regardless of the group to which the patient belongs. A multiple correspondence analysis will be conducted with care resource use and socio-demographic and medical characteristics as active variables. The variables that constitute the endpoints will be projected onto a space defined by appropriate axes.

In the United States, the diversity of care pathways is limited by managed care plans. Coverage restrictions encourage patients to follow a certain care pathway within a network of health care providers that contract with insurers. Historically, the French health care system is characterized by the founding principle of liberty: liberty both for physicians to practice and for patients to use health care services. Currently, to control growing health care expenses, a number of questions and considerable debate has focused on the organization of care pathways. However, it appears that there is no general or unique scope for these pathways and no established monetary valuation of the cost pathways for any disease. The French National Cancer Institute has specifically called for proposals on economic assessments of care pathways since 2013. The OPTISOINS01 study was the only project that was positively perceived, and it was selected for a national grant in 2013.

The spatial and temporal scope of the care pathway still needs to be defined

To our knowledge, no term that describes the whole care process has been found in the literature. Authors often use the term “care pathway” without defining it specifically [ 13 ] or confuse the concept and the tool designed for its practical application (e.g., the European pathway association). The term “care pathway” is commonly used as a synonym for “clinical pathway”, “critical pathway”, “integrated care pathway” or “care map” to name the tool used to standardize care for a homogeneous group of patients. It lists in advance the acts to be performed by a single multidisciplinary team to meet established guidelines at a local level.

We chose to use the term “care pathway” to refer to the concept behind this quality improvement tool. As we use it, “care pathway” indicates the effective succession of care, structures and providers throughout the illness for each patient. The care pathways in our study are not planned but are observed as they happen. The succession of actors from several structures over a given period of time implies the temporal and spatial aspects of the care pathway. Because the notion of care pathway is global and includes the entire care process, the time frame and the spatial frame must be defined.

Several empirical studies have been published on the BC clinical pathway. Studies often compare patients’ situations before and after the clinical pathway implementation using selected indicators in the care process [ 14 ], and they sometimes compare costs [ 15 , 16 ].

Some studies evaluate the 1-year costs of BC but do not give details about the care services that compose the care pathway [ 17 ] or assess only hospital-specific cost items, excluding the social and ambulatory care sectors [ 17 , 18 ]. A model of the care pathway for new, non-metastatic BC has been proposed; it describes the temporal sequence of hospital care, but its costs were not assessed [ 19 ]. One published study evaluating BC pathways has been found in the literature. The authors assessed the 1-year care pathway of patients who underwent breast cancer surgery in 2009 in France. They proposed a method for grouping care pathways over a sequence of hospitalizations using claim data [ 18 ]. The pathway studied included only the hospital portion of the BC care at 1 year and did not refer to a specific health territory.

The assessment of care pathways encourages the implementation of new payment models

One major challenge associated with the optimization of a cancer care pathway is the implementation of new prospective payment methods, such as patient-based bundled payments.

Hospitals are usually funded by a prospective payment system based on diagnosis-related groups (DRGs). Patient assignments to DRGs are based on their primary diagnosis. This classification system was adapted from the US Healthcare Financing Group classification. The DRGs’ prices (tariffs) are established annually at a national level based on average costs. The financing of health care services implies the involvement of an individual producer, such as the hospital, the laboratory, the self-employed physician or the radiology center for example. The prospective payment system encourages the segmentation and multiplication of examinations or visits.

New payment models aim to encourage the efficiency of care pathway. In the United States, bundled payment, also known as episode-based payment, has been proposed as a strategy for reducing health care costs during health care reform debates, especially during the Obama administration. This type of payment is currently being implemented for surgery cases [ 7 ]. It replaces payments for each provider during a health care episode. This payment approach offers a single or package payment and implies that initial negotiation among providers and contract with the payers (health insurance) has occurred. Using an overall approach, the payers assess the resources consumed during each care episode and valorize them according to the average cost linked to best practices. This method takes into account the dispersion of patient outliers, introducing variability into the average management pathway and limiting losses through “stop loss” and other contracts that limit the financial losses for each professional. Our study will provide confidence intervals for bundled payments according to practice settings and regional parameters.

Bundled payment is expected to increase the efficiency and quality of health care because under that model, the financial risks are held by the health care providers. It aims to promote sharing and coordination among health professionals and to encourage a patient-focused care pathway approach in accordance with clinical practice recommendations. It can also provide transparency for consumers by fixing pricing and by publishing cost and outcomes data. Some European countries have introduced episode-based payment: Portugal did so in 2008 for dialysis, and the Netherlands did so in 2010 for type two diabetes, chronic obstructive pulmonary disease (COPD) and vascular risk management [ 20 , 21 ]. In France, several ongoing pilot studies are focusing on bundled payment for outpatient surgery [ 22 ], chronic renal insufficiency and radiation treatment for cancer.

The assessment of care pathways encourages the implementation of new payment models. Our approach could help health care professionals and policy makers establish other cost-of-illness studies and plan resource allocation on a patient basis rather than on a visit basis.

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Acknowledgments

This study was supported by a grant from the French National Cancer Institute dedicated to economic studies of innovative techniques.

Delphine Héquet benefit from a grant of “Fondation pour la Recherche Médicale” to conduct this study.

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Department of Health Economy, Institut Curie, 26 rue d’Ulm, 75005, Paris, France

Sandrine Baffert & Huong Ly Hoang

Department of Supportive Care, Institut Curie, 26 rue d’Ulm, 75005, Paris, France

Anne Brédart

Department of Biostatistics, Institut Curie, 26 rue d’Ulm, 75005, Paris, France

Bernard Asselain

Department of Surgical Oncology, Institut Curie, 26 rue d’Ulm, 75005, Paris, France

Séverine Alran

Department of Gynecology, René Dubos Hospital, 6, avenue de L’Ile de France, 95303, Pontoise, France

Hélène Berseneff

Department of Gynecology, Poissy-St Germain hospital, 10 Rue du Champ Gaillard, 78300, Poissy, France

Cyrille Huchon

Department of Gynecology, Antoine Béclère Hospital, 157 rue de la Porte de Trivaux, 92140, Clamart, France

Caroline Trichot

Department of Gynecology, André Mignot Hospital, 50 rue Berthier, 78000, Versailles, France

Aline Combes

Department of Gynecology, Argenteuil Hospital, 69 Rue Lt Colonel Prudhon, 95100, Argenteuil, France

Karine Alves

Department of Gynecology, Bichat Hospital, 46 rue Henri Huchard, 75018, Paris, France

Martin Koskas

Department of Gynecology, Louis Mourier Hospital, 178 rue des Renouillers, 92700, Colombes, France

Thuy Nguyen

Department of Surgical Oncology, Institut Curie-René Huguenin, 35 rue Dailly, 92210, St Cloud, France

Aurélie Roulot, Roman Rouzier & Delphine Héquet

Equipe d’Accueil 7285, Risk and safety in clinical medicine for women and perinatal health, University Versailles-Saint-Quentin, Montigny-le-Bretonneux, France

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Correspondence to Delphine Héquet .

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Competing interests.

The authors declare that they have no competing interests.

Authors’ contributions

SB and RR conceived the study. DH, SB, RR and HLH designed the study. AB conceived the part of the study concerning supportive care. BA conceived the part of the design concerning work reintegration. SA, HB, CH, CT, AC, KA, MK, TN, AR made substantial contributions to data acquisition. SB, HLH and DH were involved in drafting the manuscript. All of the authors gave final approval for this version of the manuscript.

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Baffert, S., Hoang, H.L., Brédart, A. et al. The patient-breast cancer care pathway: how could it be optimized?. BMC Cancer 15 , 394 (2015). https://doi.org/10.1186/s12885-015-1417-4

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DOI : https://doi.org/10.1186/s12885-015-1417-4

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• v.59; 2021 Oct

Quality indicators for breast cancer care: A systematic review

Marta maes-carballo.

a Department of General Surgery, Complexo Hospitalario de Ourense, Ourense, Spain

b Department of Preventive Medicine and Public Health, University of Granada, Granada, Spain

c Department of General Surgery, Hospital de Verín, Ourense, Spain

Yolanda Gómez-Fandiño

Ayla reinoso-hermida, carlos roberto estrada-lópez, manuel martín-díaz.

d Department of General Surgery, Hospital Santa Ana de Motril, Granada, Spain

Khalid Saeed Khan

e CIBER of Epidemiology and Public Health (CIBERESP), Madrid, Spain

Aurora Bueno-Cavanillas

f Instituto de Investigación Biosanitaria IBS, Granada, Spain

Associated Data

We evaluated breast cancer (BC) care quality indicators (QIs) in clinical pathways and integrated health care processes.

Following protocol registration (Prospero n o : CRD42021228867), relevant documents were identified, without language restrictions, through a systematic search of bibliographic databases (EMBASE, Scopus, Web of Science, MEDLINE), health care valuable representatives and the World Wide Web in April 2021. Data concerning QIs, measurement tools and compliance standards were extracted from European and North American sources in duplicate with 98% reviewer agreement.

There were 89 QIs found from 22 selected documents (QI per document mean 13.5 with standard deviation 11.9). The Belgian (38 QIs) and the EUSOMA (European Society of Breast Cancer Specialists) (34 QIs) documents were the ones that best reported the QIs. No identical QI was identified in all the documents analysed. There were 67/89 QIs covering processes (75.3%) and 11/89 (12.4%) for each structure and outcomes QIs. There were 21/89 QIs for diagnosis (30.3%), 43/89 for treatment (48.3%), and 19/89 for staging, counselling, follow-up and rehabilitation (21.4%). Of 67 process QIs and 11 outcome QIs, 20/78 (26%) did not report a minimum standard of care. Shared decision making was only included as a QI in the Italian document.

More than half of countries have not established a national clinical pathway or integrated breast cancer care process to achieve the excellence of BC care. There was heterogeneity in QIs for the evaluation of BC care quality. Over two-thirds of the clinical pathways and integrated health care processes did not provide a minimum auditable standard of care for compliance, leaving open the definition of best practice. There is a need for harmonisation of BC care QIs.

• • The quality of breast cancer care has become a preference for health systems.
• • There was no established set of quality indicators to harmonise BC quality management’s evaluation. A consensus is needed.
• • Most of the integrated breast cancer care processes or clinical pathways did not indicate any standard for care compliance.
• • No quality indicators specifically related to patient satisfaction or Primary care were found in our study.
• • Shared decision making was only included as a QI in the Italian document.
• • There is a vast space for improvement, and future studies should pay attention to this issue.

1.  Introduction

Breast cancer (BC), the most common cancer in women with more than 2 million new cases per year, is one of the prime reasons for female cancer death [ 1 ]. Its survival rate varies depending on the country, with a 90% estimated 5-years survival for women with non-metastatic invasive breast cancer in developed countries [ 2 ]. Its treatment is becoming more complex. The greater therapeutic complexity requires an improvement in care quality management.

Clinical pathways, i.e. methodologies for the mutual decision making and organisation of care for a well-defined group of patients during a well-defined period of time [ 3 ], or integrated breast cancer assistance processes, i.e. “preventive, diagnostic, therapeutic, follow-up and care activities, aimed at the comprehensive management of people with BC and those with increased risk of BC” [ 4 ] have been deployed to manage and standardise care [ 5 ]. The aim of these quality documents is to increase the quality of care, reduce risks, enhance efficiency and improve patient satisfaction. They include a series of QIs for continuous improvement, aiming to guarantee the effectiveness of a clinical care pathway and enhance the quality of care, patient satisfaction and outcome [ 6 , 7 ]. Three types of QIs are considered essential for capturing care quality [ 8 ]. They cover structure (includes all the resources involved in the provision of services), process (evaluates the activities carried out during patient care; describes the care that the patient receives) and outcomes (evaluates the final product of care) [ [9] , [10] ].

Our primary research has shown that no systematic reviews were comparing QIs for BC care. Although several QIs have been proposed to harmonise BC care quality management, there is still no consensus among different Professional Societies or Health Administrations [ 11 ]. Many studies have used their own QIs, so the comparison between findings of different clinical audits is difficult [ [12] , [13] , [14] , [15] , [16] , [17] , [18] ]. Thus, they remain disparities in the quality of BC care across areas and hospitals to the detriment of women's health. This review aimed to evaluate systematically the QIs, their measurement tools and their compliance standards of care in clinical pathways and integrated health care processes documents.

2.  Methods

A protocol-driven systematic review was performed following prospective registration (Prospero n o : CRD42021228867), and it was reported in line with the PRISMA statement (Preferred Reporting Items for Systematic Review and Meta-Analysis Protocols) [ [19] , [20] ].

2.1. Data sources and searches

A systematic search for relevant published literature was performed without language restrictions associating MeSH terms “breast cancer”, “breast neoplasms”, “quality indicators”, “quality care”, and including word alternatives, covering all the documents published until February 2021. We looked for online databases (MEDLINE, Web of Science, EMBASE and Scopus). Appendix A shows the search strategy. Most of the proposals that measure cancer care quality were usually not formally published in scientific journals and were not indexed in databases. This involved an extensive manual search of grey literature in retrieving recommendations made by European institutions active in this field (QIs of BC care management) on the World Wide Web. We have also contacted more than 200 breast cancer experts from European and American countries to help us in the process. The European Breast Centres Network, Europa Donna (The European Breast Cancer Coalition) representatives from each country, the main hospitals, universities and the specifically Governments, and Ministries of Health of each country have been contacted three or more times waiting for at least one week between emails. More additional initiatives were searched in the identified publications’ bibliographies to include other essential studies in our review.

2.2. Study selection and data extraction

Initiatives encouraging quality measures (clinical pathways and integrated breast cancer integrated processes) in BC care produced by European professional institutions and societies or governmental agencies were included. We have also added remarkable institutional position papers based on breast quality indicators specifically as the EUSOMA working group's [ 7 ]. All these selected documents were compared to EUSOMA's. We included clinical pathways and integrated health care program documents with at least one section dedicated to BC. Those that deal with QIs in general cancer have not been included. Only those that specifically mention BC in a sub-section or even within the text were selected. Randomised controlled trials (RCTs) and observational studies, narrative reviews, scientific reports, discussion papers, conference abstracts and posters, and clinical practice guidelines and consensus were excluded.

We have only included European and North American documents because both areas have the biggest global R&D (research and development) investments and the highest number of publications worldwide [ 21 ].

Three reviewers (MMC, CREL and ARH), breast cancer specialists, analysed the potential eligibility of each of the titles from the citations independently. The full-text versions were requested and assessed, working separately to ratify eligibility. A fourth reviewer (YGF) helped to solve disagreements by consensus or arbitration. Duplicate proposals were removed. Where multiple versions were found, the most updated version of the guidelines was included. Data were collected from the selected BC QIs initiatives in duplicate, independently.

2.3. Quality indicators

Four reviewers (MMC, YGF, CREL and ARH) extracted data in a piloted proforma to assess the reporting of BC QIs from the integrated breast cancer assistance processes based on EUSOMA's [ 7 ]. A summary table of EUSOMA QIs in BC care and their characteristics (the definition for each indicator, the type of QI (17 mandatory for a EUSOMA breast unit certification), the minimum and target standard of care (ST), and the level of evidence) is shown in Appendix B . Other QIs extracted from the analysis of the different integrated breast cancer health care processes, clinical pathways documents and other remarkable position papers studied were collected when no similar QI was found in the EUSOMA's. Our team considered that two QIs were the same when measuring the same process, even when there were slight differences between population targets and minimum standards of care (ST). We have stated a ST as the level at which the average, prudent provider in a given community would practice. We have studied the QI ST range as the area of variation between upper and lower limits on a particular scale. All these differences were reported individually in the Results section of this manuscript. These analysed QIs were classified according to Donabedian's framework type (structural, process and outcome indicators) [ 8 ] and according to the EUSOMA classification [ 7 ] concerning the intervention they were measuring (diagnosis, treatment, staging, counselling, follow-up and rehabilitation and others).

2.4. Data analysis and synthesis

Reviewers consistency in data extraction was initially studied by the intraclass correlation coefficient (ICC), and the reliability level “>0.90” was considered excellent [ 22 ]. However, when disagreements appeared, an arbitrator would help to reach a consensus. If disagreement persisted, this arbitrator would take the final decision. A descriptive statistical analysis was conducted for analysing and classifying the selected QIs. An overarching qualitative synthesis was done to describe the findings. All the analyses were performed with the Stata 15.0 statistical package (StataCorp LLC, College Station, TX, USA).

3.1. Study selection

A total of 1615 potentially relevant documents were found; 1397 were from online databases (EMBASE, Web of Science, MEDLINE and Scopus), and 218 were from additional sources (websites of relevant European institutions, health care relevant representatives and the World Wide Web). The selection criteria were not met by 1462 documents, and 131 were found duplicated. Finally, only 22 documents met the eligibility criterion for the full evaluation. Only one document was finally added from online databases for assessing eligibility. The rest of the 21 documents were found in the grey literature after looking for them in the proper European institutions’ websites, contacted breast cancer experts from each country to help us in the process, and reviewed the identified documents’ bibliography. The study selection process is shown in the flow diagram in Fig. 1 . The characteristics of the selected documents (year of publication, institution, continent/country/Autonomous Community, evidence analysis used for QIs assessment, type of document (if it is a specific BC document or not, presence of a specific subsection on BC, the appearance of QIs in the document analysed) are synthesised in Table 1 . Based on our selection method, Table 1 also shows 37/59 (63%) countries with no clinical pathway or integrated health care process found. Most of the quality documents analysed were from Western countries (81%, 17/21).

Flow diagram detailing the study selection.

Table 1

Integrated BC health care processes and clinical pathways analysed and their characteristics. Countries with no quality care documents retrieved.

3.2. General quality indicators assessment

A set of 89 QIs were found from the 22 selected documents [ [7] , [23] , [24] , [25] , [26] , [27] , [28] , [29] , [30] , [31] , [32] , [33] , [34] , [35] , [36] , [37] , [38] , [39] , [40] , [41] , [42] , [43] ]. Thirty-four belonged to the EUSOMA statement [ 7 ] (see Appendix B ), and the remaining 55 were other indicators derived from the rest of the documents studied that did not appear in EUSOMA. ICC for reviewer agreement was 0.98. Appendix C showed the different indicators selected and the quality document where they have appeared. The vast majority of the indicators were of the process (75.3%; 67/89), 11/89 (12.4%) were structural indicators, and finally, 11/89 (12.4%) were indicators of outcomes. These indicators cover all steps of BC care management from diagnosis (21/89; 30.3%), treatment (43/89; 48.3%), and staging, counselling, follow-up and rehabilitation (19/89; 21.4%). No QIs specifically related to Primary Care were found in our study.

3.3. Most common used quality indicators

The BC QIs reporting was heterogeneous ( Appendix C ). The mean number of QIs in each document was 13.5 (Standard deviation 11.9). The Belgian (38 QIs) [ 26 ], the EUSOMA (34 QIs) [ 7 ], and the Spanish (28 QIs) [ 40 ] documents were those that registered more indicators. Albania [ 25 ], Denmark [ 27 ], Romania [ 36 ], Slovenia [ 37 ], Sweden [ 38 ] and one of the Irish documents [ 31 ] did not present any QIs in their clinical pathways or integrated breast cancer assistance processes.

Only 14 (63.6%) documents collected any BC QI. No indicator was present in all these quality documents analysed. The indicators that appeared more frequently in the analysed documents were “proportion of BC cases who preoperatively underwent breast and axilla radiology and physical examination” (78.6%; 11/14) with a ST range from 85 to 95% [ [7] , [23] , [26] , [29] , [30] , [33] , [35] , [39] , [40] , [41] , [42] ], “proportion of patients with BC who had a preoperative histologically or cytologically confirmed malignant diagnosis (B5 or C5)” (71.4%; 10/14; ST range 85–90%) [ [7] , [23] , [26] , [29] , [30] , [34] , [35] , [40] , [42] ], “proportion of BC cases for which prognostic and predictive parameters have been recorded” (57.1%; 8/14; ST = 95%) [ [7] , [26] , [29] , [30] , [33] , [35] , [39] , [40] , [41] ], “proportion of patients with invasive cancer who underwent image-guided axillary staging” (64.3%; 9/14; ST range 85–100%) [ [7] , [23] , [26] , [29] , [30] , [34] , [35] , [40] ], “proportion of BC patients to be discussed pre and postoperatively by a multidisciplinary team (MDT)” (71.4%; 10/14; ST range 85–100%) [ [7] , [23] , [26] , [30] , [32] , [33] , [35] , [39] , [40] , [41] , [42] ], “proportion of BC patients (DCIS only) who received just one operation (excluding reconstruction)” (57.1%; 8/14; ST range 80–90%) [ [7] , [26] , [29] , [32] , [33] , [40] , [41] ], “proportion of BC patients receiving immediate reconstruction” (64.3%; 9/14; ST range 40–85%) [ [7] , [23] , [30] , [32] , [33] , [34] , [40] , [41] , [42] ], “proportion of invasive cancer and clinically negative axilla cases who underwent sentinel lymph node biopsy (SLNB) only, excluding primary systemic treatment (PST) cases” (78.6%; 11/14; ST range 90–100%) [ [7] , [23] , [26] , [28] , [29] , [30] , [32] , [35] , [40] , [41] , [42] ], and “proportion of HER2+ infiltrating carcinoma (T > 1 cm or N+) treated with chemotherapy who received adjuvant trastuzumab” with an appearance of 57.1% (8/14) (ST range 85–95%) [ [7] , [23] , [26] , [29] , [33] , [35] , [40] , [41] ]. Moreover, other four QIs, “proportion of BC cases examined preoperatively by MRI (excluding PST's patients)” (ST range <10 or <20%) [ [7] , [23] , [30] , [32] , [34] , [35] , [39] ], “proportion of BC patients with less than X days/weeks of delay from the RT indication to its initiation” (6–48 weeks; ST range 90%) [ [23] , [24] , [28] , [29] , [30] , [32] , [33] ], and “proportion of BC with axillary lymph nodes (>=pN2a) who received post-mastectomy RT to the chest wall and all (non-resected) regional lymph-nodes” (ST range 90–95%) with an appearance all of them in 50% of the quality documents (7/14) [ [7] , [23] , [26] , [29] , [33] , [35] , [42] ].

3.4. Quality indicators minimum standard

We have compared variations in the same QI in the different documents analysed in which it appeared. Appendix C synthetase these differences for the same indicator obtained in the analysis of all the documents. Regarding process and outcome QIs ( Appendix C ), 26% of these did not state a ST (20.9%, 14/67, QIs of the process and 54.5%, 6/11, QIs of outcomes). The QI for which a ST value was given more frequently was “proportion of patients with BC who had a preoperative histologically or cytologically confirmed malignant diagnosis (B5 or C5)” with values ranging between 85% (for EUSOMA and one of the Spanish documents) [ [7] , [42] ], 90% (for Irish and two Spanish) [ [30] , [40] , [41] ] or 95% (for French) [ 28 ]. This was also the QI for which minimum variability was observed for the ST values of the indicators. “Proportion of BC cases for which prognostic and predictive parameters have been recorded”, and “proportion of BC patients who undergo surgery within less than 30 days after the MDT decision”, all of them QIs of the process, showed no range variability for the ST values recommended ( Appendix C ). The QIs of structure, which are yes or no statements, did not establish any ST value.

Concerning QIs of results ( Appendix C ), BC detection, invasive cancer and in situ cancer incidences, recurrence and mortality rates, “proportion of BC patients with follow-up (data on life status and recurrence rate) for at least 5 years, and patients’ satisfaction” did not state any ST. On the other hand, 40% of patients should receive immediate reconstruction according to EUSOMA [ 7 ] and 70% according to the Italian program [ 32 ]. The percentage of axillar lymphadenectomies that resect more than ten nodes should reach 100% [ 40 ]. More than 90% of BC cases with lymphedema or without recovery of shoulder mobility should be referred to rehabilitation [ 32 ]. Finally, the BC survival rate should be more than 50% in patients who have completed treatment [ 23 ].

3.5. Quality indicators about timing processes

Appendix C highlights in grey all the QIs related to timing in the BC care management. Half of the QIs (52.9%, 9/17) did not set a ST despite indicating the time required between processes for compliance.

3.6. Shared decision making as a quality indicator

The presence of shared decision making (SDM) in the Clinical Pathways and integrated breast cancer assistance processes documents was analysed. Only the integrated breast cancer assistance process manuscripts from the USA [ 23 ] and Italy [ 32 ] recognized its importance (See Appendix C ). American integrated breast cancer process indirectly insisted on developing a QI for measuring the quality of the doctor-patient relationship. An indicator of SDM use by the health professionals measure was only proposed by the Italian document (ST = 100%) [ 32 ].

4. Discussion

4.1. main findings.

More than half of the European and American countries have not had any clinical pathway or integrated breast cancer care process to reach the excellence of BC care. QIs description was heterogeneous, with not a single identical indicator appearing in all the documents analysed. Secondly, there were only four comparable QIs that appeared more frequently in the analysed documents: “proportion of BC cases who preoperatively underwent breast and axilla radiology and physical examination”, “proportion of patients with BC who had a preoperative histologically or cytologically confirmed malignant diagnosis (B5 or C5)”, “proportion of BC patients to be discussed pre and postoperatively by a multidisciplinary team (MDT)”, and “proportion of patients with IC who underwent image-guided axillary staging”, all of them related to the process. One-quarter of the QIs of the process and outcome did not state a ST. We observed a minimum variability for “proportion of patients with BC who had a preoperative histologically or cytologically confirmed malignant diagnosis (B5 or C5)” ST; there was consensus in a quarter of the studied manuals. Despite indicating the time required between compliance processes with the indicator, half of the documents did not set a ST of accomplishment. Two documents recognized SDM importance, but only Italian collected a QI about measuring SDM use. There were not found QIs related to Primary Care.

The vast majority of QIs identified were process QIs (over three-quarters), and these were also found in more documents. They covered all the phases of BC care management from suspicion, diagnosis, treatment, and staging, counselling, follow-up and rehabilitation.

4.2. Strengths and weaknesses

To our knowledge, an evaluation comparing QIs for BC care management suggested by different Professional Societies or Health Administrations has not been reported previously. Our review gave a comprehensive perspective with a reasonable number of clinical pathways or integrated breast cancer assistance processes documents included using a wide search without language restrictions. This gave a strong global vision on the QIs situation for the whole BC diagnostic-therapeutic-follow-up process.

One possible limitation of this review could be that only European and North American documents were appraised. We have chosen these two continents because both regions have the biggest global R&D (research and development) investments, so they would have the highest number of publications worldwide [ 21 ]. More than three-quarters of the documents came from Western countries. Most of the quality care documents analysed were not formally published in scientific journals or were not indexed in databases. This involved an extensive manual search of grey literature in retrieving recommendations made by European and American institutions active in this field (QIs of BC care management) on the World Wide Web. Although our systematic review had no language restrictions, most of the documents studied have not been published in medical journals and were published in the local language of the country, which have made the searching difficult. We have tried to combat this problem by choosing reviewers experts in many languages (English, Spanish, Portuguese, Italian, French and German). To provide an accurate vision of the existing recommendations from European and American countries, we have contacted more than 200 prestigious experts on BC and quality management care by email (at least 3 times with a time lapse of one week per message): European Breast Centres Network and Europa Donna representatives from each country, the main hospitals, universities and the specific Governments, and Ministries of Health. Most of the contacted representatives have admitted that their countries have not had a national clinical pathway or integrated care process and a standard set of QIs and have stated that every region, county, or even hospital has developed their own indicators. ESMO handbooks and NCCN guidelines have been established as some of the most used guidances for a big part of the countries. More additional initiatives were searched in the identified publications’ bibliographies to include other essential studies in our review. Therefore, some of these manuals may not have been found due to the difficult search.

Furthermore, comparing the EUSOMA position paper [ 7 ], and the clinical pathways or integrated breast cancer assistance processes studied was limited. EUSOMA's was only focused on BC care management in specialised Units, while the rest of the quality documents included all the care management process from the practitioner's referral to follow-up. In addition to the indicators collected in EUSOMA, the other QIs referred to care before and after admission to BC Units and included all the levels as aspects of care in quality assessment. So, incorporating these other documents presents advantages since they allow us to coordinate better communication with other levels and healthcare services, helping to improve compliance by including their singularities and requirements in the QIs measurements.

The level of evidence available on the QIs identified in the scientific literature was variable, and we had to deal with the subjective nature of the data extraction. We minimised the effect of these potential limitations by three experienced BC specialist clinician's analysis. A consensus meeting to unify criteria was done before duplicate data extraction assessment. An independent arbitrator (fourth reviewer) was concerned about the significant deviation that arose and helped reach consensus. It was reassuring to note that the reviewer agreement was excellent, with the ICC >98%.

4.3. Implications

The use of QIs could be extended to all BC care management stages, allowing monitoring processes' evolution over time and could be compared with other centres [ [12] , [13] , [14] , [15] , [16] , [17] , [18] ]. Although several QIs have been proposed to harmonise BC care quality management's evaluation, there is still no consensus between countries [ 11 ]. So, the comparison between studies is difficult, reducing the possibility of establishing conclusions that could be extrapolated to other health care areas or hospitals [ [12] , [13] , [14] , [15] , [16] , [17] , [18] ].

The development of QIs in general oncology is complex [ 44 ]. The concept of quality is broad and requires several indicators to explore different dimensions of the same issue. This could be problematic because similar QIs could not measure the same element. Furthermore, technological advances and the appearance of new treatments are happening fast, so it is a field in constant expansion, and frequent updates are required.

A considerable proportion of the indicators proposed were related to hospital settings because most of the clinical activity for cancer might occur at this level of care. In the QIs set analysed, we did not find any QI explicitly related to Primary Care. However, future reviews should pay more attention to ambulatory care processes if we want to have a comprehensive quality assessment. Most poverty-stricken countries present resource constraints that penalise and result in more poor BC care management [ 45 ]. Further studies should be done to investigate the differences between the indicators according to the country's wealth.

With an emphasis on patient-centred care, the use of shared decision making (SDM), i.e. “an approach in which the doctor and the patient share the best available evidence and where the patient is supported to consider options and reach decisions about the process according to their preferences and values” [ 46 ] should be considered a key indicator in care quality management [ [47] , [48] , [49] ].

There is still a long way before the achievement of consensus. Current efforts must be required to reach an agreement between institutions [ 50 ]. Although the European Commission is currently carrying out an initiative to develop by consensus, indicators for Breast Units that guarantee good practice and excellent patient care, their results are not available yet [ 51 ]. Consensus-based quality indicators are needed to allow analysis in a clear, precise and straightforward way. This will allow data to be extrapolated and to be able to evaluate and compare different populations with different requirements. In our review, there were included specific documents about BC QIs such as EUSOMA [ 7 ], L'Institut National Du Cancer in France [ 28 ], the Belgian Cancer Registry [ 26 ], the NICE quality standard [ 39 ], the National Health System [ 41 ] and the Spanish Foundation of Senology and Breast Disease program [ 42 ], which have emphasised the importance of establishing a universal set of QIs. The majority of the countries did not have had any national clinical pathway or integrated breast cancer care process, which is extremely worrying, taking into account that these documents are essential to achieve an excellent quality of care.

The establishment of minimum and optimal quality STs is useful to assess the degree of compliance and the need for improvement of a QI. Currently, there is no ST for more than one-quarter of the QIs. As it has been remarked in EUSOMA, new researches should be developed, and new manuals would add them in the future [ 7 ].

Our analysis has identified a gap that offers an essential contribution to further research and debate, including assessing BC quality indicators. There is a broad space for improvement. Future studies and a reach of consensus in this vital matter would be highly recommended and merit urgent consideration.

5. Conclusions

More than half of the countries have not had a national clinical pathway or integrated breast cancer care process to achieve the excellence of BC care. There is no established set of QIs to harmonise BC care quality assessment, and their descriptions are heterogeneous. The comparison between studies has been difficult, reducing the possibility of establishing conclusions that could be extrapolated. Most of the integrated breast cancer assistance processes or clinical pathways did not indicate STs for compliance. Only one document collected the importance of the measurement of the use of SDM in BC, an already demonstrated QI for management care. No QIs specifically related to Primary Care were found in our study. A consensus set of BC care QIs is needed, something that future studies should pay attention to.

Contributors

All the authors certify a relevant contribution to the conception and design of the review, development of the search strategy, establishment of the inclusion and exclusion criteria, extraction, analysis, and interpretation of the data. MMC was involved in the conception and design of the review, literature search, data collection and analysis, quality appraisal, and writing. CREL, ARH and YGF were involved in data collection. ABC was involved in the design of this review, conducted the quality appraisal, in the writing, and provided critical revision of the paper. KSK helped with the writing and provided critical revision of the paper. MMD provided critical revision of the paper. All authors read and provided the final approval of the version to be published.

Financial support and sponsorship

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

Data sharing statement

All the supplementary materials can be accessed upon request via email to the corresponding authors of this study.

Declaration of competing interest

The study was conducted in the University of Granada, Spain. There are no conflicts of interest.

Acknowledgments

KSK is a Distinguished Investigator funded by the Beatriz Galindo (senor modality) Program grant given to the University of Granada by the Ministry of Science, Innovation, and Universities of the Spanish Government. We are thankful for the collaboration of the Europa Donna (The European Breast Cancer Coalition) representatives from Belgium Dr Hirsch and Carly, Dr Aleksandrova from Bulgaria, Dr Moldovanova from Russia, Dr Skjoldborg Hansen from Denmark, Dr Egypt from Estonia, Dr Niemi from Finland, Dr Debiais from France, Dr Sartataviciene from Lithuania, Dr Fischbach from Luxembourg, Dr Barilaro from Monaco, Dr Mellem from Norway, Dr Brankovic-Magica from Serbia, Dr Spanić from Slovenia, Dr Bergsten from Sweden, Dr Corbat from Switzerland, Dr Sprengers from the Netherlands, Dr Spittle from the UK, Dr Maistruck from Ukraine and Europa Donna from Portugal. And we would also like to thank Dr Isabel Rubio (EUSOMA and ESSO President) in Spain, Dr Verhoeven at the Breast Centre Voorkempen in Belgium, Dr Ejlertsen, Dr Bohl and Dr Valvere from the Estonian Cancer Society, Dr Espie from the Hôpital Saint-Louis in France, Dr Winkler from the Hungarian League against cancer, Dr Zsuzsanna from the University of Szeged in Hungary, Dr Arnardóttir from the Landspitali University Hospital in Iceland, Dr. Dillenbourg from the Université de Liège in Luxembourg, Dr Daly from the University Hospital Waterford in Ireland, Ms Drochon and Dr Goncharenko from the Institute Nacional du Cancer in France, Dr Jenset from the Swedish Breast Cancer Association, Dr Fredriksson from the Karolinska Institutet in Sweden, Dr Ana Andrijević from the Institute for pulmonary diseases of Vojvodina, Prof Vrancken Peeters from the Dutch Breast Cancer Audit, Dr Verloop and Dr Siesling from IKNL, Prof Ozmen from the Istanbul Florence Nightingale Hospital, Prof Ozaydin from the Turkish Breast Health Society, Dr Lorez from the Swiss Federal Office of Health, the Swiss Cancer League, Dr Mousavi from the Cancer Registry of eastern Switzerland, and Dr Dagmar from the Swiss Office Q-Label. Finally, we are also grateful for the help provided by the Irish Cancer Society, the Norwegian Breast Cancer Association, the MD Anderson Cancer Center in Spain, the Canadian Breast Cancer Network and the Institute of Breast Disease FUCAM in Mexico, the Ministries of Health from Ireland, Georgia, Iceland, Lithuania and Luxembourg.

Appendix C Supplementary data to this article can be found online at https://doi.org/10.1016/j.breast.2021.06.013 .

Appendix 0. PRISMA 2009 Checklist

From: Moher D, Liberati A, Tetzlaff J, Altman DG, The PRISMA Group (2009). Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement. PLoS Med 6(7): e1000097. https://doi.org/10.1371/journal.pmed1000097 .

For more information, visit: www.prisma-statement.org . Page 2 of 2.

Appendix A. Data sources and search strategy

AA.1 Sample search strategy for MEDLINE.

We conducted a systematic search on April 30th, 2021 in MEDLINE (via PubMed) using the following combination of free-text terms:

• #1 breast cancer [all]
• #2 breast neoplasms [all]
• #3 quality indicators [all]
• #4 quality care [all]
• #5 2010 [pdta]: 3000[pdta]
• # #6 AND #10 AND #11 AND #12

Results: 8 articles.

AA.2 Online databases.

• 3. Web of Science

AA.3 Websites of European institutions.

• 1. EUSOMA, Europe
• 2. Professional institutions and societies or governmental agencies from each European country

AA.4 Health care representatives.

• 1. EUSOMA (European Society of Breast Cancer Specialists), Europe
• 2. Europa Donna (European Breast Cancer Coalition), Europe
• 3. ESSO (European Society of Surgical Oncology), Europe
• 4. EUBREAST (European Breast cancer Research Association of Surgical Trialists), Europe
• 5. Breast Cancer Care Network
• 6. National governments and Ministries of Health
• 7. Main hospitals from each country

Appendix B. Summary table of EUSOMA Quality Indicators in breast cancer care!

The level of evidence was graded according to the short version of the United States Agency for Healthcare Research and Quality (AHRQ).

Appendix C. Supplementary data

The following is the Supplementary data to this article: