Introduction

Cancer is a leading cause of death worldwide, resulting in nearly ten million deaths in 2020 according to WHO data [1]. In spite of this enormous burden of disease, late-stage presentation and lack of diagnosis and treatment remain common, leading to much higher mortality rates [2]. Each cancer type requires a different treatment regimen, so a correct diagnosis is essential to receiving the best treatment and reducing mortality [1, 3]. Good quality of care can also improve quality of life (e.g. through pain management), even when cure is no longer possible. Access to appropriate treatment is therefore of crucial importance, but inequalities in access have been observed for several groups, including PwD [4–10]. Over 1.3 billion people, or 16% of the world’s population, live with some form of disability, according to the 2022 World Report on Disability [11]. This figure is expected to grow further in the coming decades, as the population ages and chronic health conditions increase globally. On average, PwD are more likely to experience poor health, because of their underlying health condition/impairment and their socio-economically excluded position in society [12, 13]. They also face a range of barriers to accessing care, including long waiting times, high costs, ableist discrimination by health professionals, inaccessible buildings, inconvenient locations, and lack of communication among different parts of the healthcare team [12–14]. As a consequence, unmet healthcare needs are greater for PwD, contributing towards poorer health and higher mortality [11]. This general pattern of disability-related healthcare exclusion is reflected in known disparities in the use of cancer prevention services, as PwD have lower cancer screening rates than those without disabilities [13–18]. This gap may also exist with respect to cancer care, as several studies have recently reported that patients with disabilities might not be receiving state-of-the-art treatment standards for their cancers [19–23]. Furthermore, several studies suggest that cancer may be diagnosed at a later stage in patients with disabilities, and that they experience treatment disparities resulting in higher cancer-specific mortality rates [24, 25]. A recent meta-analysis from the USA showed that women with disabilities have 0.78 (95% CI: 0.72–0.84) lower odds of attending breast cancer screening and have 0.63 (95% CI: 0.45–0.88) lower odds of attending cervical cancer screening, compared to women without disabilities. A recent study from Taiwan reported that the probability of receiving colorectal cancer screening in people in the four categories of disability (intellectual and developmental disability, dementia, multiple disabilities, and moving functional limitation; OR = 0.53, 0.55, 0.62 and 0.81, respectively) was significantly lower than that in the general population [24, 26]. Two recent scoping reviews found that patients with intellectual disabilities may be at risk of experiencing inequities at various points during cancer clinical pathways, which as a consequence could have an impact on their overall and cancer-specific mortality and quality of life; it is thus of the outmost importance to identify and address these disparities [25, 27]. Consequently, the aim of this study is to conduct a systematic literature review to compare cancer outcomes and quality of cancer care between adults with and without disabilities.

Materials and methods

A systematic review of the literature was conducted describing differences in cancer-related care between patients with and without disabilities, according to the PRISMA reporting guidelines; the study was recorded on the NIHR Prospero register of systematic reviews with ID number CRD42022281506 [28, 29].

Data extraction and analysis

A table was created for data extraction (S1 Table in S1 File) listing authors, year of publishing, country where the study was undertaken, study design, type of cancer, type of disability, type of outcome, population size and overall risk of bias. One author (IT) extracted the data. A summary of study characteristics can be found in Table 1.

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Table 1. Summary of characteristics of included studies.

https://doi.org/10.1371/journal.pone.0285146.t001

We also created a summary of primary and secondary outcomes of each study); where possible, odds or prevalence ratios as a measure of association or p-values comparing measures in people with and without disabilities were extracted. Each study was also classified as “better”, “worse” or “null”, when outcomes respectively showed a better, worse or equal situation in quality of cancer care for PwD in comparison to people without disabilities.

A narrative synthesis was conducted according to the Cochrane SWiM guidelines.

Results

The search was conducted on July 13^th, 2022 resulting in 4140 titles identified (Fig 1).

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Fig 1. PRISMA flowchart.

https://doi.org/10.1371/journal.pone.0285146.g001

After removal of 408 duplicates, 3732 titles and abstracts were screened, and 3680 ineligible studies were excluded. Next, 52 full texts were retrieved and 21 were excluded because of ineligible study design, comparator, patient population, outcomes, intervention or setting. Finally, 31 studies were identified as eligible for the systematic review.

Risk of bias

Almost half of the 31 studies (45%, n = 14) had a medium risk of bias, while 12 studies had a low risk of bias (39%, n = 12). Finally, 5 papers were marked as having a high risk of bias. The ratings of risk of bias were summarized (Fig 2) with RobVis tool [36].

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Fig 2. Risk of bias.

D1 = Selection bias D2 = Information bias D3 = Misclassification bias; D4 = Confounding D5 = Missing data; Green = Low Yellow = Medium Red = High.

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Outcome results

Outcomes are summarized in Table 2.

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Table 2. Outcomes of studies and type of disability.

https://doi.org/10.1371/journal.pone.0285146.t002

Nineteen studies that included a measure of survival or mortality all showed, invariably, a direction of effect towards worse outcomes for PwD; this was often worsened by the degree of severity of disability [19, 22, 36, 44, 49, 54, 57, 66]. Only one study found no difference in overall survival or disease-free survival between patients with and without disabilities [38]. Among psychosocial disabilities, schizophrenia had generally the worst prognosis [36, 39, 42, 48, 60]. In studies that examined survival in cancer patients with all types of disability, there seemed to be far worse outcomes for those with severe disabilities and with intellectual impairment. In one study results showed that patients with schizophrenia had a cancer specific mortality rate 50% higher than patients without disabilities [39]. In another study about bladder cancer, the risk of cancer specific death was 35% higher for patients with severe mental illness compared to people without disabilities [19, 22, 42, 62].

In a large study about gastric cancer patients in South Korea, PwD were more likely not to receive proper staging tests to establish an appropriate treatment plan. Observing subgroups by disability type, the fact of not receiving treatment was more common for people with communication impairment (36.9% in severe and 31.4% in mild communication disability); the authors concluded that disability itself should not be a contraindication for receiving cancer treatment [22]. Another study about patients with leukaemia described how the treatment rate was lowest in those with major internal organ and communication disabilities; while for patients with major internal organ disabilities it is understandable to have a low treatment rate due to vital functions often lacking functional reserve, communication disabilities are not directly related to vital functions and the decision not to treat was hence not based solely on medical factors [63].

There were 16 studies showing lower chance in receiving state-of-the-art cancer treatment for PwD, and only one study with high risk of bias showed no difference, but data about gender and degree of disability was missing [59].

The studies showed that cancer treatment was suboptimal for PwD in many ways, and in particular that they had a lower likelihood of undergoing guideline-consistent surgery when indicated [22, 40, 42, 54, 58, 61, 63, 65]. Several studies showed that when PwD were correctly treated with guideline-consistent surgery, their mortality was similar or only slightly higher than controls [55, 60]. PwD were also more likely to face diagnosis and treatment delays—but not when access to screening was optimal, underlining the importance of good screening access [22, 45–47, 50, 67]. PwD were also less likely to receive curative-intent transplants for blood cancers, and more likely to receive inappropriate radical mastectomy instead of guideline-consistent minimally invasive procedures for breast cancer [19, 38, 57, 58, 62].

As for end-of-life and palliative care, 4 studies showed a direction of effect towards worse outcomes for PwD [36, 47, 48, 52]. One of these studies, with low risk of bias, showed an association between receiving outpatient treatment from a mental health professional and having less end-of-life ED visits, suggesting the importance of access to mental health services to improve end-of-life care [47]. One study showed an association between disability and worse access to prescriptions for pain treatment during cancer care, a situation likely to severely compromise quality of life [53]. Finally, a study reported that patients over age 55 with intellectual disability were more likely than controls to have worse access to specialist care in the last year of life [52].

Regarding other factors contributing to worse outcomes, one study showed an association between worse access to screening programs (for breast, colon and cervix cancers) and higher cancer specific mortality, underlining the inequality in screening practices [50]. Two other studies highlighted an association between barriers to screening and worse outcomes for gastric and breast cancer in PwD [22, 46]. Two studies detected even worse disparities in access to state-of-the-art treatment or end-of-life care related to ethnicity and age, with young disabled non-white men having the worst outcomes [47, 55]. One study of people with intellectual disabilities with any type of cancer suggested worse underdiagnosis for older females, while another focusing on breast cancer detected an association between physical disability and inappropriate invasiveness of treatment [49, 58]. In a study of non-small cell lung cancer patients, those with respiratory or nervous system disabilities had the lowest chance of receiving guideline-appropriate surgery, while another paper on lung cancer recorded the worst access to treatment among people with communication or neurologic disabilities [55, 63]. A study about stomach cancer and patients with all kinds of disabilities also found an association between worse outcomes and severe intellectual impairment [22].

Finally, three studies showed an association between worse outcomes of treatment access and poverty among people with cancer [19, 48, 63].

Discussion

In our review, compared to people without disabilities, PwD were found to have worse survival, higher overall and cancer-specific mortality, loss of chance for access to state-of-the-art care or curative-intent therapies, treatment delays, undertreatment or excessively invasive treatment, worse access to in-hospital services, less specialist healthcare utilization, more difficult access to pain medications and inadequate end-of-life quality of care. Only one eligible study found no difference in overall survival or disease-free survival between patients with and without disabilities; it was a small paper with a high risk of bias, with a cohort including only operable breast cancer in a small number of patients, and it still showed an association between disability and excessively invasive breast surgery without any clear cancer-related clinical reason. Furthermore, the incidence of disability in its retrospective cohort was inexplicably only half of the known national incidence, suggesting severe misclassification bias [38]. These finding suggest that differences in frequency of appropriate treatment appear to explain the higher cancer-specific mortality for this vulnerable population, with higher mortality likely due to loss of chance and unequal clinical care. Even if sometimes treatment decisions for PwD can be clinically complex, such as the above-mentioned case of cognitive impairment with legal consent or non-compliance issues, or when confronted with a disability-related shortened life expectancy or frailty for some syndromes, there is no plausible medical justification for such a wide disparity compared to patients without disabilities, and these results raise severe concerns about equality in cancer care [67, 68].

The results of this study are consistent with those of other recent literature reviews, showing that PwD experience inequities at several points throughout the cancer care pathway [12, 24, 68, 69]. Screening disparities have been known and documented for years: they can vary by disability type, severity, healthcare offer and social or demographic situations, with some differences across countries, but globally there is a largely similar trend of major barriers to screening for people with disability, showing a clear need to improve the inclusiveness of these early-diagnosis services [12, 24, 68].

Providing equitable cancer care has to start early in the cancer clinical pathway, because delays in receiving a diagnosis tend to lead to late access to treatment and worse outcomes [67]. A frequently observed issue is that new signs and symptoms tend to be attributed to often to the underlying disability, a clinical mistake called “diagnostic overshadowing” [70]. A recent scoping review about cancer outcomes in adults with intellectual and developmental disabilities has described disparities at every step of the way, from screening, to staging, to treatment and survival outcomes, recognizing how these experiences do not originate simply from a gap in early diagnosis, but from larger structural issues that ultimately hinders quality of the entire cancer care pathway [25]. Another review of cancer treatments for people with intellectual disabilities highlighted possible themes that might interfere with treatment, such as genetic syndrome frailty that might render certain drug treatments too dangerous, the issue of behavioral non-compliance in a subgroup of patients, and problems related to legal capacity and obtainment of informed consent. Still, these three factors should not represent an insurmountable barrier because with appropriate arrangements (e.g. pharmacology consults, procedural sedation, legal assistance) it should still be possible to offer guideline-consistent treatment to patients [68]. With physical disabilities clinical decisions can sometimes be objectively more difficult than in people without disabilities, because of concerns about baseline performance status or competing health risks due to invasive or toxic treatments that might result in further dramatic loss of function (e.g. possible loss of postoperative upper limb function after breast surgery in patients with previous spinal cord injury and lower limb paralysis); this has been described as a compelling reason to move towards better cooperation between cancer care clinicians and disability specialists who have been in charge of the patient well before their oncology episode, and also as one of the fundamental facts that make shared decision making with patients (or sometimes their families or caregivers) of the utmost importance [12].

This clear evidence of inequities emphasizes the very urgent need for better cancer care for PwD. Furthermore, disparity in healthcare for PwD is not unique to oncology, as research about the recent Covid-19 pandemic has clearly proven [71–76]. During the pandemic, PwD have died in disproportionate numbers–almost three times as much globally than people without disabilities—and have been excluded from the decision-making process, because their needs have been ignored; they have ended up facing an increasing amount of psychological distress, lack of social support, extreme isolation, food insecurity, disparities in health care access and even discrimination at work. In many cases, government response has compromised the human rights of disabled people, having exposed and magnified existing structural failings and inequalities [74, 75, 77, 78].

Recently, the second report of the Missing Billion Initiative has called for reimagining health systems with a vision of inclusive health informed by diverse perspectives of PwD, who are still facing worse health outcomes across SDG3 indicators (Sustainable Development Goal 3 by the WHO, i.e. ensure healthy lives and promote well-being for all at all ages), globally and with all sort of impairment types [78]. The first Missing Billion report had highlighted a substantial life expectancy gap of 10–20 years for PwD, with all-cause mortality rates approximately twice as high as those of people without disabilities [76]. Closing this gap is now a priority, but it requires long-term investments to design from the start health systems that expect, accept and connect PwD, with sufficient earmarked funds, dedicated leadership and clear governance based on data and evidence disaggregated by disability. Ideally service delivery should aim at affordability, autonomy of patients, accessibility, specific workforce skillsets and availability of rehabilitation services [78]. The multiple barriers experienced by PwD during their cancer care (Fig 3) are hence a reflection of a broader process of discrimination and disadvantage, mirrored in structural failings of current healthcare systems, within networks of intersecting factors that ultimately influence cancer outcomes [25, 79, 80].

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Fig 3. Barriers experienced by PwD during cancer care.

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Healthcare workers need to receive evidence-based and appropriate training about disabilities, directly involving PwD and using a monitoring system to measure cultural progress and outcome improvement. This could help foster a change to move away from the ableist attitudes that are too often still observed, contributing to wrong assumptions and subsequent mistakes of diagnostic overshadowing or failure to anticipate specific complications [12, 81]. In a very recent qualitative study from the USA, interviewed physicians, mostly middle-aged white males, felt inadequately reimbursed for accommodations required by the 1990 Americans with Disabilities Act; according to some of these doctors, these concerns simply led them to discharge patients with disabilities [82]. Many physicians openly spoke about the lack of accessibility in their clinics without any plans to improve it, and several demonstrated a complete lack of disability knowledge about how to manage very basic issues–even stating that they were regularly sending patients to a zoo, cattle processing plant or supermarket to obtain a weight if a patient was in a wheelchair and unable to stand; several doctors admitted that they rarely spoke to these patients, regardless of the patients’ ability to communicate, and that information was almost exclusively obtained from the caregiver. This confirms findings from previous qualitative research, that had described a lack of skills by healthcare workers to feel empathy for the embodied experience of living with a disability, with an obstinate resistance to adapting their habitual practice to these patients [10].

The importance of inclusive clinical trials to close the evidence gap about what works to improve cancer care for PwD cannot be overemphasized [79, 82–84]. There is still too little evidence about how to treat cancer in the population with disabilities, which is very diverse and can have widely different therapeutic needs (hence existing services must be offered in a flexible, respectful, inclusive and accessible way to be relevant for this patient population). Thus, it is of the utmost importance to include PwD in clinical trials in oncology—both for curative-intent interventions and for palliative treatments; yet, historically they have been left out of studies, due to many factors such as ableist prejudice, or multiple barriers such as accessibility of research facilities and access to transportation, or lack of caregivers’ engagement [83, 84]. Unfortunately, in clinical trials pre-existing conditions are often excluded, even if the conditions have little bearing on the treatment being tested or the outcome of the trial. Excluding disabled individuals from a study can result in a study population that does not even represent the general population, since disability often correlates with other inequalities (such as poverty and unemployment). The importance of targeting the recruitment of disabled individuals into clinical trials, as well as considering the unique barriers and motivations of this population, needs to be highlighted. A person with a disability may have difficulty traveling to a trial site; moreover, healthcare organizations should consider their audiences’ digital literacy and the accessibility of their communications. Funds should be allocated to improve healthcare communication, adapting multiple formats, using captions and alt-text or pictorial representations of concepts as appropriate for the specific context. In addition, disabled individuals appear to be underrepresented as investigators in scientific research [85]. Despite 19% of the UK’s general population identifying as disabled, only 4% of academic, research, and teaching staff do. Even if 25% of American adults live with a disability, in 2020 only 4% of US STEM PhDs were awarded to people with impaired hearing or vision, and just 1% to people with a mobility limitation. More disability-confident schemes and unconscious bias training could at least partially mitigate hiring discrimination, creating an academic workforce that better reflects the community in which it is based [86]. Recent evidence-based recommendations to promote inclusion in clinical trials include improving culture and sensitivity of staff through continuous education, receiving ongoing feedback from a community advisory panel during studies and increasing staff diversity to make sure underprivileged groups are represented [87].

Physicians and PwD should be able to collaborate along care pathways with shared-decision making, an approach based not only on clinical technical advice but on the life experience of patients, their caregivers and families, according to the principle of “Nothing About Us Without Us” [12]. In the clinical setting, barriers in physical access should be removed to avoid unacceptable delays in diagnosis and treatment [79, 80, 88]. Barriers in communication should be eliminated at several levels, from overcoming communication obstacles (not only for the hearing or visually impaired patients, but also with special-needs assistance for intellectual disability), to improving education of patients, clinicians and caregivers about cancer and the importance of screening, to training healthcare workers about the emotional and physical needs of PwD, enhancing cooperation with other specialists caring for them, in cross-functional teams, to anticipate and possibly reduce the impact of complications, with the goal of a patient-centred pathway [89]. Good communication is the foundation of achieving quality patient-centered care: assumptions about preferences can pose a risk like inaccurate information leading to medical errors and misdiagnoses. A recent qualitative study in the USA has shown that, in spite of healthcare workers trying their best, there are still many unsolved issues at this level and even many situations where physicians’ preferences go against patients’ wishes [87].

The strengths of this study include having followed PRISMA and ICM50 guidelines for systematic reviews; furthermore, the search strategy was based on a list of proven disability-specific terms and applied to the five largest medical databases analysing a twenty-year span of publications. This work has several limitations: firstly, the search strategy, limited to five databases and to English language only, might not be fully comprehensive; we did not include studies published in non-English languages because of resource challenges with respect to costs, time, and expertise in non-English languages, but their inclusion would have likely increased generalizability and reduced the overall risk of bias. Furthermore all the eligible papers were from high-income countries, limiting the generalizability of the results, even if there is no reason why the situation should be very different in low and middle-income countries., Qualitative papers and grey literature were not included in the search strategy, hence the views and opinions of PwD about their cancer care were not investigated. Study selection was performed by only one reviewer, which implies a lack of independent screening. We also did not perform tests to measure publication bias due to the high heterogeneity of the eligible studies; although methods exist for simultaneous assessment of heterogeneity and publication bias, and potential differential publication bias, they require very large meta-analysis to reliably disentangle their effects [35]. Moreover, only one reviewer evaluated papers for risk of bias. Finally, the findings were very diverse hence it was not possible to conduct a meta-analysis, and approximately 15% of the studies had a high risk of bias Almost half (45%) of the eligible studies had a medium risk of bias, mostly due to possible misclassification bias for inclusion of PwD based on disability records (that have a tendency to miss mild cases) or missing data like details about cancer treatment goals, behavioral factors or date of diagnosis [36, 37, 42, 43, 49, 54, 56, 64, 65]. Approximately 15% of the studies had a high risk of bias due to factors such as having a very small sample size, a short follow-up, low data quality, a biased cohort or using a self-reporting survey [38, 46, 51, 58, 59]. There are still gaps in knowledge about quality of cancer care for people with disability that remain unanswered based on our findings, such as whether certain subgroups of disabilities or cancer types experience more significant disparities, or how other social determinants of health might come into play (as many PwD are caught in a cycle of poverty and deprivation); more data is needed on these topics to allow disaggregated analyses. Further research is also needed to evaluate the effectiveness of specific training of healthcare workers on quality of care for these patients.

In conclusion, PwD often experience severe disparities in cancer care compared to people without disabilities; physical and cultural barriers at different levels must be eliminated to ensure they receive equitable care. There is an urgent need for a robust health policy effort by governments, reimagining health systems with a vision of inclusive health and a sustained commitment, building on decades of progress on disability rights and engaging the participation of PwD at all levels.

Supporting information

Acknowledgments

I.T. would like to thank Danae Rodriguez Gatta, for assistance with disability search terms, and Dr. Meena Cherian, for many fruitful discussions about health systems and development goals.