Advancing health equity in cancer care: The lived experiences of poverty and access to lung cancer screening.

BACKGROUND: Individuals living with low income are more likely to smoke, have a higher risk of lung cancer, and are less likely to participate in preventative healthcare (i.e., low-dose computed tomography (LDCT) for lung cancer screening), leading to equity concerns. To inform the delivery of an organized pilot lung cancer screening program in Ontario, we sought to contextualize the lived experiences of poverty and the choice to participate in lung cancer screening.
METHODS: At three Toronto academic primary-care clinics, high-risk screen-eligible patients who chose or declined LDCT screening were consented; sociodemographic data was collected. Qualitative interviews were conducted. Theoretical thematic analysis was used to organize, describe and interpret the data using the morphogenetic approach as a guiding theoretical lens.
RESULTS: Eight participants chose to undergo screening; ten did not. From interviews, we identified three themes: Pathways of disadvantage (social trajectories of events that influence lung-cancer risk and health-seeking behaviour), lung-cancer risk and early detection (upstream factors that shape smoking behaviour and lung-cancer screening choices), and safe spaces of care (care that is free of bias, conflict, criticism, or potentially threatening actions, ideas or conversations). We illuminate how 'choice' is contextual to the availability of material resources such as income and housing, and how 'choice' is influenced by having access to spaces of care that are free of judgement and personal bias.
CONCLUSION: Underserved populations will require multiprong interventions that work at the individual, system and structural level to reduce inequities in lung-cancer risk and access to healthcare services such as cancer screening.

Introduction

Lung cancer is one of the most commonly diagnosed cancers in Canada, and is responsible for a quarter of all cancer-related deaths [1]. Screening using low-dose computed tomography (LDCT) has the potential to diagnose lung cancer at an earlier stage thereby increasing the likelihood of curative therapy [2]. Effective screening interventions must reach populations at high-risk. Thus, engagement with individuals between the ages of 55–74 years, who have smoked cigarettes daily for a minimum of 20 years is critical for success [3].

Historically, individuals with lower levels of income and/or education, or recent immigrants are least likely to undertake preventative health practices such as cancer screening [4]. For lung cancer screening this is particularly problematic since the greatest lung cancer incidence is found in populations disadvantaged by a variety of social determinants such as income and education [5]. Lung cancer screening therefore presents two very specific challenges: (i) a disease distribution that is proportionate to the degree of social disadvantage; and (ii) an opportunity to screen for the disease in the target population, but with a potentially low uptake.

Quantitative and mixed methods studies document that individuals at high-risk of developing lung cancer who decline lung cancer screening are more likely to be active smokers, report personal blame or stigma, perceive lower benefit from undertaking the test, or have fatalistic beliefs about their own well-being [6-8]. Current recommendations to target this group therefore are aimed at enhancing invitation strategies [8], developing interventions to support decision-making and decreasing knowledge conflicts about screening between physicians and patients [7]. In this context, a major knowledge gap is an understanding of the lived experiences of individuals who are socially disadvantaged and the factors that influence their choice to access preventative health services, such as LDCT lung cancer screening. Thus, to address this knowledge gap, we conducted a qualitative study in Ontario where the implementation of lung cancer screening is currently being piloted.

Methods

Study design

Theoretical thematic analysis (TTA) is a qualitative research methodology that provides a systematic way to organize, describe and interpret data using a guiding theoretical lens [9]. TTA can be used to socially contextualize data [9] and inform the development of evidence-based policies applicable to the real-world setting of patients, providers and policy makers [10]. TTA is useful in analyzing participant perspectives, particularly if the perspectives are different, by highlighting similarities and differences across datasets to generate unanticipated insights [9, 11]. We therefore used TTA to answer the following research question: What are the perspectives of individuals living with low income towards lung cancer screening and the choice to access or not access screening?

Theoretical framework

The morphogenetic approach is a critical realist theory which posits that three primary causal powers determine individual behaviour; namely, structural relationships in society, sociocultural interactions between individuals, and individual agency [12, 13]. The term “morpho” takes its roots from the word shape, and “genesis” from the word shaping [12]. To be morphogenetic therefore implies taking action for change and the processes that elaborate or change system and/or structure. On the contrary, to be morphostatic implies to resist change and to maintain the status quo [12].

The morphogenetic approach has been described as the preferential framework with which to understand agency in higher education [14, 15] and individual transformation in criminology [16]. In this study we introduce the morphogenetic approach to health services research and describe how it can be used to critically contextualize the enablers of health seeking behaviour in health promotion practice.

The core assumptions of the morphogenetic approach (Fig 1) are: (i) that structural relationships pre-exist in society (T1); (ii) that these social structures influence social interaction (T2); (iii) that causal relationships exist between individuals and groups that influence social interaction (T3); and (iv) that social interaction can influence individual agency and social structure (T4) [12]. Subsequently, we applied these core assumptions to theorize the ‘choice’ to access lung cancer screening for individuals living with low income in the following way (Fig 1) [17]:

Fig 1

Theorizing choice in health promotion though the morphogenetic approach.

T1: Social, political, cultural and economic contexts influence current lung cancer risk;

T2: Socially-disadvantaged patients interact with the health system through various contexts;

T3: These interactions condition patients to respond in a certain way;

T4: The choice to seek preventative health care is based on these interactions and can lead to:

T4a: Morphostasis or structural reproduction, by negative perspectives towards health and health seeking choices, that subsequently maintains the status quo and perpetuates lung cancer risk; or

T4b: Morphogenesis or structural elaboration, by positive perspectives towards health and health seeking choices that subsequently transforms behaviour and potentially lowers lung cancer risk.

Participant recruitment

Participants were recruited from three primary care sites in downtown Toronto that serve a wide demographic of patients, including those experiencing low income, homelessness and addictions. Eligible patients met the provincial referral criteria for individuals at high-risk for developing lung cancer: i) were between 55 to 74 years of age, ii) had smoked daily for at least 20 years, and iii) did not have any active cancers. We followed provincial exclusion criteria: prior lung cancer, under surveillance for lung nodules, or history of hemoptysis, unexplained weight loss or a life-threatening condition. No prior association existed between the principal researcher and participants prior to the commencement of the study.

Participants were recruited from March 2019 to January 2020 and were categorised as screeners or non-screeners in the following way:

Screeners

Screeners were study-eligible participants, referred by their healthcare provider, who chose to screen with LDCT. Upon receiving a referral, the patient navigator at the provincial lung cancer pilot screening site called patients to determine eligibility by conducting a risk assessment using PLCOM2012 criteria [18]. Patients were study-eligible if their calculated risk score was >2% in the next six years [19], had recently received a LDCT, and consented to be contacted for a research interview. The 2% threshold is the current screening eligibility criterion being used in the province of Ontario for lung cancer screening [20].

Non-screeners

Non-screeners were patients who chose not to undergo LDCT lung cancer screening. Recruitment of non-screeners through the clinical sites was challenging as eligible participants who were not interested in screening were also not interested in participating in the research study. We therefore used a technique called derived rapport [21] in order to recruit non-screeners by leveraging one health provider’s established relationship with a low-income patient community. Thus, patients were assessed for lung cancer screening eligibility by that health provider. When participants were not interested in screening they were informed about the study, and introduced to the first author (AS) who was on-site to conduct interviews immediately thereafter.

Data collection

Interview guides were developed using the guiding theoretical lens. Separate interview guides were developed for screeners (S1 File) and non-screeners (S2 File) in order to explore different choices in health seeking behaviour. The interview guides included questions on smoking history, smoking cessation, living conditions, and perspectives on health and preventative health care such as lung cancer screening. Semi-structured interviews were conducted with open-ended questions to encourage a participant-led dialogue.

All interviews were conducted by the first author (AS). The Research Ethics Board at Unity Health Toronto provided ethics approval for the study. This included the board’s approval to obtain verbal consent from all participants before beginning the research interview. Therefore, prior to the interview all participants were given information about the purpose of the research study and expectations from the interview including interview duration and usage of data. The first author (AS) discussed the ways in which results from the research study would be disseminated and sought approval to record participants verbal consent. After participants agreed to proceed, audio recording was initiated, verbal consent taken, and included in transcribed files as part of data collection. This process was approved by the REB at Unity Health Toronto.

Non-screeners were interviewed face-to-face in the clinic space of the healthcare provider who had facilitated their recruitment immediately after they had provided consent. Screeners were interviewed four to six weeks after they underwent LDCT lung cancer screening. Interviews with screeners were performed via telephone in order to reduce attrition as face-to-face interview appointments in low-income populations can be hindered by competing priorities and constrained resources that detract from research participation [21]. Interviews lasted approximately 40 to 60 minutes.

All interviews were audio-recorded then transcribed by a professional transcriptionist. Audio files were sent to the transcriptionist on the day of the interviews and transcripts were reread (by AS) for accuracy within two days. Personal identification was removed from the audio and transcribed files, and pseudonyms were given to all participants. Field notes taken during the interviews were added to the study files. Interviewing continued till the point of conceptual saturation.

Participants provided sociodemographic data using a pre-existing health equity survey [22] to capture data including information on the participants’ housing status, ethnicity, language, sexual orientation, disability status, and household income.

Data analysis

We used TTA to organize, describe and interpret the data [9]. The first (AS) and last author (AL) read through the data multiple times to search for repeated patterns of meaning [9] and to develop a coding framework. NVivo 12 software was used to organize the data manually and to code units with similar meaning, even if they did not sync with the theoretical inquiry. This was important to ensure that patterns in text were not missed or disregarded [23]. Line-by-line coding was applied to the textual data (AS), and codes were developed iteratively during weekly consultations between two authors (AS, AL). AS is a medical doctor and critical qualitative researcher. AL is a family physician and clinical epidemiologist. Both AS and AL research health inequities. The larger interdisciplinary research team (all authors) met regularly during all research phases to discuss challenges and emerging themes, and provided an opportunity to regularly peer debrief until we reached conceptual saturation [24] and our final themes. The extended research team comprised of clinical oncologists (GL, LE), radiation oncologists (MG), clinician scientists in addiction and mental health (PS) and homelessness (SH) as well a federal level policy maker that is involved in the implementation of lung cancer screening in Canada (EN). As a team we were concerned with themes occurring at the latent level (Braun & Clarke, 2006). Latent themes seek to explain or understand why participants said or acted in a certain way, and as such differ from semantic themes which are limited to a description of data rather than its interpretation [25].

Results

Characteristics of study sample

We interviewed 18 screen-eligible individuals (eight screeners, ten non-screeners), who were primarily male, white and Canadian-born (Table 1). At the time of interview, seven participants were living in a homeless shelter in downtown Toronto. Eight participants lived in subsidized apartments through Toronto Community Housing, and the remaining three were renting their accommodations. Most participants reported annual incomes below $30,000 a year, while two reported income levels between $30,000 and $59,000. Participants who declined to undergo lung cancer screening were more likely to be living in the homeless shelter (seven participants) and report incomes below $30,000 (nine participants).

Table 1

Participant sociodemographic information.

	Screeners	Non-Screeners
Total	8	10
Age categories
50–59	1	2
60–69	3	7
70+ years	4	1
Sex
Male	7	10
Female	1	0
Immigrant status
Foreign-born	2	4
Canadian-born	6	6
Ethnicity
White–(North American, European)	6	7
Asian—East (e.g., Chinese, Japanese, Korean)/ South (e.g., Indian, Pakistani, Sri Lankan)	1	1
Other (including Indigenous, Indian and Latin American	1	2
Self reported income (in Canadian dollars)
0–29,999	6	9
30,000–59,000	2	0
60,000–89,000	0	0
90,000–119,000	0	0
120,000 plus	0	0
Missing	0	1
Sexual orientation
Heterosexual	7	10
Gay/Bisexual/Lesbian/Queer/Two-Spirit/Other	1	0
Housing
Own Home	0	0
Renting Home	3	0
Community housing	5	3
Homeless shelter	0	7

Themes

Fig 2, shows a thematic map connecting our three main themes: Pathways of disadvantage, upstream determinants of lung cancer risk and early detection, and safe spaces of care.

Fig 2

Thematic map.

Understanding the perspectives on choice for access to lung cancer screening for individuals living with low income.

An overview of the themes is discussed below. The complete set of themes, subthemes and illustrative quotes that were derived from the transcripts is shown in Table 2.

Table 2

Themes, subthemes, and illustrative quotes from interview transcripts.

THEME—SUBTHEME	ILLUSTRATIVE QUOTES
Pathways of disadvantage: a social trajectory over the life course that significantly influences health risk and health promotion practices
1. WORKING CONDITIONS2. COMORBIDITIES3. LIVING CONDITIONS4. LIFE OUTLOOK	“I’m always worried about tomorrow. It’s like okay, I have some (money) this week okay, let’s see if I can get some more for next week” (Jack).“When you drive a taxi especially……. your income is very fluid. You can do well one day and just barely cover your costs the next. So, yeah, there are times when it has been difficult to make ends meet” (Caitlyn).“I was working with like a subcontractor… I was paid by the job, yeah. I was paid by the job and not by hour, not by hour… I used to work and then I got sick and when I get in and out from the hospital, I lost my job and yeah I lost my job, I don’t have no income” (Rocco.)“My body. It’s like the problems with my back and everything just didn’t instantly happen. It’s, it was going on with me for like years you know and even when I was 40 years old, 45 years old like my back just pounded like crazy like I was always in a lot of pain and I ran you know dozers and scrapers for years” (Philip).“You know it does not immediately appear, like appearance, like just stress. But after a while you feel like tired, headache, irritate, you know the mood is sometimes just uncontrollable something like that. You want to escape. You want to be alone. These kind of things (Walter)”.“Well I pretty much wound up in shelters because like when you run heavy equipment it’s not like I was working all year round. I would only work maybe eight months out of each year you know and it was all union work so sometimes the jobs the union would send me to would be six months, some would be a year, some would be longer so I was in and out of shelters you know “(Philip).“Oh, the housing I mean it’s $2,000.00 a month for an apartment and you got to have first and last. Where is a guy who’s working, or in a hostel, (or) you know even if he gets a decent job that’s paying $20.00 an hour, he’s going to have to stay there for three months to make up enough money and that’s if everything goes perfect for him at $20.00 an hour. I mean you’ll have enough to, because he might get a place for $1,700.00 you never know but I mean then you might have to travel right across town to get to his job too, so that’s another $150.00 that he’s going to have to spend a month” (Barry).“I just turned 60, yeah. Monday, I turned 60. Well I’m over the hill. Yeah, I haven’t got, and what I got, a couple of years, a couple of years left? I think so. Something like that” (Jarod).“For me it was because I had housing and I wanted to look into my health. But for guys on the street and in hostels man, they have other priorities. They need housing first before they can do anything. And that’s going to be their problem and like yeah, I’ll do that, sure but right now I’m doing this, I need housing you know; you’re way down at the bottom of their priority list right now because for me anyway, you would be too because I need housing. I got to get myself quiet and healthy first and a sane mind at least to be able to make an appointment but I mean you’re not going to do that when you’re fighting with residents and staff at a shelter or on the streets” (Barry).
Upstream determinants of Lung cancer risk and early detection: the social and economic factors which shape smoking behaviour and lung cancer screening choices
1. SMOKING CONTEXT2. SMOKING CESSATION3. SCREENING PERSPECTIVES	“We used to smoke behind the yard you know in the school during school break you know” (Harold).“I guess like 14, 15; 15 years of age and I guess I was starting. Other people were starting to smoke so I thought yeah, I’ll go along with it, with the crew or something like that… Cigarettes in those days were $0.45 cents I think for a package of cigarettes so even with my measly earnings delivering newspapers I was able to purchase cigarettes so the price was right and then they were available and there was no advertisements about harm to your health on at that time. There was very little said about cigarette smoking, and it was heavily propagandized in Hollywood films and that, so you know (it was) just a thing of the time” (Patrick).“Things were very cheap (where I was) … I paid $0.25 for a large pack of cigarettes so it was easy to be …a heavy chain smoker” (Barry).“I quit smoking for over a year but then I moved into the building where I am now at Sherbourne and Dundas and the stress of all the stuff going on in the building and all the crackheads and drug dealers on the corner I started smoking again” (Jaden).“Probably seeing other people smoke, smelling it, you know like the smoke in the air” (Kane).“Yeah, I tried before but like the stress doesn’t help much but right now my stress level is pretty good. Like some days I don’t even smoke a cigarette. Some days I smoke one, two like for the last three months and it’s like okay, if I have no stress and I’m happy and walking around and I can go like two, three days without having a cigarette” (Jack).“Everybody has priorities. You have priorities in life. You have choices to make every day. You have a priority whether you want to do something next week or not or whether you want to make a plan … Sometimes you just put it aside until you need to use it and so people that are homeless okay, they’re not looking to get help at that end. They’re looking to get help to find a home … Well (smoking cessation for me) was planned because when I was smoking a pack and a half a day and then I cut it down to a package and a quarter a day, then I cut it down to a pack a day, then down to ¾ of a pack a day, then I cut it down to a half a pack a day and then I cut it down to six cigarettes a day. At that point I went to my health provider and got on a plan to get the patch for I think it was two weeks on my arm and to cut out smoking completely” (Hank).“When you’re worried about issues of making ends meet, there are several things that could happen. When you’re unemployed you can very easily seep into apathy and when you’re apathetic you don’t get up off your butt and go and have a test to see if you’ve got lung cancer. I think that’s probably, you know that’s my wisest words on it. I think you know when you’re, when everything is okay and especially if you’re retired it’s much easier for people to go to a clinic and have a test which only takes what ten minutes? But when you’re unemployed and you know you’ve got economic problems then you might think to yourself well you know I’m worried about getting a job and keeping my house and so forth and you think well I’ll put that off. I’ve got other things to worry about right now you know’ (Harold).
Safe spaces of care: a place of clinical care which is free of bias, judgement, conflict, criticism, or potentially threatening actions, ideas or conversations
1. POWER2. INFLUENCE	“The most important impact is not having less money to spend, it is that you have to face the government workers. They are not very sympathetic to that thing. They treat you like you are a beggar or pest or something like that. It’s that kind of feeling. It makes you feel that you don’t want to come to them to ask for help” (Walter).“They helped me with 60% of the cost of my prescription. One day she said to me that I am taking advantage of the system and I don’t know how? How with all my gratitude and the love that I have for her? It made me feel like shit. It made me feel like when I was a little kid and my mother put me on the street to beg for a piece of bread, looking for something to eat in the garbage cans, and a few tomatoes” (Rocco).“I got treated really bad from doctors and I didn’t want to go into another office and get treated like a piece of garbage because you come out and you feel twice as bad” (Damien).“Well she has a street-like attitude about things … she doesn’t have to talk with fancy words, and you know. We get along well like our rapport is quite good. She knows where I’m from and you know a lot more than most people know about me so, yeah, she’s somebody I feel I can trust you know. You can tell her things and it’s; she understands what you’re talking about and stuff like that … You’re not actually on a visit there, you’re just talking to her and its straight talk, like she doesn’t treat you like you’re below her or anything like that” (Jaden).“The more you trust, the more you trust that person, the more you’re going to be willing when they do suggest things” (Caitlyn).

Pathways of disadvantage

Clustering of disadvantage is a phenomenon whereby people who are disadvantaged in one area, such as income, are also disadvantaged in other areas, such as housing, food security, and educational opportunities [26]. Graham et al [27] have described the clustering of disadvantage from a life course perspective in relation to smoking behaviour to illuminate how poor circumstances in childhood influence future educational achievement and economic prospects contributing to a pathway of disadvantage that is deeply entwined with adult smoking behaviour. Given that it was neither the purpose nor scope of this study to identify the links between childhood circumstance and adult lung cancer risk and health seeking choices we bracketed our analysis of the life course to begin with working conditions and to end with current risk for lung cancer. The theme pathways of disadvantage, therefore, describes a social trajectory of events over the life course that influence lung cancer risk and health seeking behaviour.

In our study, all participants described precarious working conditions leading to economic instability and fluidity of material resources such as income. Participants also recounted physical or mental disabilities related to their working conditions or life circumstance. Specifically, half of the participants reported severely restricted current mobility due to spinal/joint injuries and arthritis that were associated with prior employment in manual labour. All participants had experience of being de-housed. Participants recounted the reasons for experiencing housing insecurity as income precarity and associated comorbidities. For participants who chose to undergo lung cancer screening, housing was described as a key determinant that influenced positive life outlook and perspectives towards preventative health care in general.

Upstream determinants of lung cancer risk and early detection

Smoking is the single largest risk factor for lung cancer and an individual’s smoking history is a key enrolment criterion for the lung cancer screening pilot in Ontario. Accordingly, we define the theme upstream determinants of lung cancer risk and early detection as the social and economic factors which shape smoking behaviour and lung cancer screening choices.

All participants described the context in which they initiated smoking at an early age, recounting in detail the social acceptability of smoking, availability of cigarettes at an affordable price point, a lack of awareness of the associated harms, and mass media advertising which promoted its use. All participants recounted in detail how they had attempted smoking cessation. At the time of interviews however, only three participants had successfully been able to quit smoking and an additional four were actively enrolled in a smoking cessation program. Of the three participants able to quit smoking, one was living in subsidized housing and the other two were renting their homes (reporting incomes between $30–59,000 a year). These participants described how having access to material resources (such as income and housing) directly influenced their ability to choose and benefit from smoking cessation.

The three participants who had successfully quit smoking chose to be screened for lung cancer. Access to material resources had a direct influence on lung cancer screening perspectives. All eight participants who had undergone screening had their own place to stay (subsidized housing or rent). Five of eight reported having participated in other preventative health checks such as colon cancer screening. Participants who chose not to screen had competing priorities such as making ends meet, unemployment and housing security that were more pressing needs than screening for an illness which could possibly occur several years later.

Safe spaces of care

A safe space of care is a place that is free of bias, judgment, conflict, criticism, or potentially threatening actions, ideas or conversations. For our study, we limited this theme to the lived experiences of participants’ encounters with front line health workers and the impact of these experiences on their subsequent health promoting choices. We build on the definitions of power (the ability of an agent to act), ‘power over’ (a social relation in which one person/group dominates to shape the available ‘choices’ of a subjugated person/group) [28] and influence (the power to have a direct effect on someone so as to change their actions in an important way) to contextualise the health seeking choices of participants ~ i.e. morphogenesis (accessing lung cancer screening) or morphostasis (declining lung cancer screening).

An important observation in our study was that all three participants who were renting their home chose to be screened for lung cancer, whilst all seven participants in the homeless shelter declined. Of eight participants who were living in subsidized housing at the time of the interviews, five chose to be screened for lung cancer, and three declined. All five who chose to be screened reported having a collaborative/supportive/non-judgemental relationship with their providers that promoted their personal health and wellbeing. These participants shared experiences of care that were sensitive to their life circumstances. Subsequently, participants recounted their clinical encounters as pleasant and comfortable. In contrast to these experiences, the three participants living in subsidized housing who declined lung cancer screening described encounters that were judgmental and insensitive to the sociohistorical realities that constituted their lives. Participants used words such as, “worthlessness”, “garbage”, “beggar” and “pest”, as they recounted these experiences.

Discussion

Despite a publicly funded health system in Canada, participation in population-wide screening programs has not been universal. Differences in screening uptake are associated with income, education and immigrant status [4]. Individuals who live with greater degrees of social disadvantage have a higher risk of some cancers and poorer overall survival; this is directly correlated with the social determinants of health and how they intersect across the cancer care continuum [29]. Therefore, new interventions such as lung cancer screening must take into consideration differences in utilization and needs, which are based on social location. This is key to preventing an inadvertent widening of the health equity gap that already exists between population groups. Our study sought to fill this knowledge gap in the context of lung cancer screening which is currently being pilot tested in the province of Ontario. Specifically, we wanted to understand the perspectives on choice for lung cancer screening in patients living with low income in order to inform the design and delivery of lung cancer screening as an organized program.

Through semi-structured interviews with individuals living with low income who chose to undergo or not undergo lung cancer screening, we found that participants’ interest in screening depended on the availability of adequate housing, which subsequently empowered participants to seek care to advance their health and wellbeing. Further, clinical encounters created a space that needed to be navigated without personal bias and with sociohistorical sensitivity. Participants who recounted their clinical encounters as places of judgment-free care had meaningful relationships with their physicians, and they subsequently trusted their physicians’ judgement and recommendations.

All participants in our study initiated smoking at a very early age, recounting cigarettes as being available, accessible and, “the thing to do”. Much of this context is related to the mass-marketing campaigns that ran across media stations and sensationalized smoking in the 1950’s and 1960’s [30]. Since then, policies enacted to limit the marketing and use of tobacco products in public spaces have led to decreases in smoking rates across Canada. However, this distribution is skewed such that individuals living with socioeconomic disadvantage are more likely to smoke and less likely to cease smoking [31].

Recent studies have highlighted that willingness to quit smoking is equal across social classes; however, socially-disadvantaged smokers are more likely to: (i) live in an environment where they socialize and work with other socially-disadvantaged people for whom smoking is considered acceptable [32]; (ii) use smoking as a way to relax and cope with high daily stress levels [33]; and (iii) report experiences of disadvantaged childhood, educational and employment trajectories that shape the pattern and frequency of cigarette consumption [27]. These findings are closely reflected in the lived experiences of our study participants all of whom had attempted smoking cessation at least once, yet only three had quit successfully.

In our study, the three participants who had successfully quit smoking reportedly quit because they became more proactive towards their own health once they had found housing and all three took part in lung cancer screening. Participants identified living conditions (housing) to be a key determinant of health and wellbeing, particularly in the context of a preventative health check such as lung cancer screening. Significantly, only those participants who had their own place to call home felt empowered enough to seek opportunities to advance their health and then take action to utilize the service of screening. Participants who chose not to undergo screening lived in diverse housing situations that were generally less secure (subsidized housing; homeless shelter). For these participants, lack of adequate housing was one barrier to care.

Another barrier was the attitude and influence of treating physicians, which determined participants’ willingness to continue to engage with the health system. In Canada, physicians are gatekeepers to and proponents of lung cancer screening and therefore have a critical role in ensuring equitable healthcare delivery. We have described physician perspectives on access to lung cancer screening for individuals living with low income elsewhere; a key finding was that an equity-oriented approach and attention to the upstream determinants of lung cancer by physicians will be needed in order to improve equitable access to lung cancer screening [34]. Our findings suggest that physicians and other healthcare practitioners must learn how to deliver care that is free of personal biases to prevent the perpetuation of oppression and the systemic reproduction of health inequities.

According to the “inverse equity hypothesis” [35] population-based health interventions are more rapidly adopted by the wealthy, a term described as “top inequality” [36]. This is in contrast to “bottom inequality” which refers to the lag in adoption experienced by the poorest when the intervention has reached high coverage across the remainder of the population (Victora et al., 2005). Thus, individuals developing health interventions must recognize patterns of health inequality and adapt policies and processes to mitigate these effects [37] and prevent a widening of the health equity gap between socially advantaged and disadvantaged population groups [38].

Midstream interventions [39, 40] geared at reducing cigarette consumption in the socially-disadvantaged are only likely to be truly successful if incorporated into a broader program that addresses the social context of smoking behaviour. As a standalone intervention, nicotine replacement therapy is unlikely to be highly effective in influencing smoking behaviour and reducing lung cancer risk for those who are socially-disadvantaged. Similarly, lung cancer screening as a midstream public health program may inadvertently increase health inequities unless proactive and multipronged strategies are in place to increase uptake. Screening programs may also neglect the underlying social context of smoking behaviour, such that even if individuals are screened for lung cancer, they may continue to face increased lung cancer risk due to the daily stressors that influence their choice to continue smoking. This approach to care is ignorant of the lived realities of those at high-risk of developing lung cancer, the target population of the lung cancer screening program. An equity-focused approach to screening programs therefore, would demand attention to the social context of cancer risk and utilization rates based on social location.

Health systems can determine how to respond best to inequitable health intervention uptake by engaging with patients to identify strategies that enhance intervention effectiveness [41]. Conducting future patient-oriented research that incorporates the lived experience of those at high-risk for lung cancer to guide the development of a multipronged approach (such as education, resources, and tools) can maximize the availability and accessibility of the intervention to the target population [42]. This approach, called targeting within universalism implies that a universally available intervention must be accompanied by specific uptake strategies that positively discriminate towards those at highest risk [43].

Strengths and limitations

The focus of our study was on perspectives towards preventative healthcare, particularly lung cancer screening for individuals living with low income. As such, we have offered an analysis of the lived experiences of choice in relation to income and social class, using a critical realist lens termed the morphogenetic approach. We realize that using a different analytical lens to frame our research, such as intersectionality, would have offered alternative themes and policy recommendations; this can be a future research area as interventions are evaluated for their population effectiveness based on differences in social identity. In particular, we recommend future research with racial and ethnic minority groups in order to understand how stigma and/or racism may create further barriers to healthcare. The homogenous nature of our non-screening participant sample reflects how we recruited through the established practice of one health provider. However, by using this approach, our study is able to demonstrate how derived rapport [21] can be used to reach research participants who are both high-risk (in terms of health risk for lung cancer) and hard-to-reach (in terms of difficulty to access for research) for a variety of reasons such as geographic location, economic deprivation, or vulnerability due to stigma and disenfranchisement [44, 45]. As a qualitative research study, we have described our study setting, recruitment strategy and participant population in order to promote transferability of our research findings.

Conclusion

Inherently, any health promotion program that focuses only on individual uptake, such as choosing to undergo cancer screening, runs the risk of masking the fundamental causes of health conditions and may inadvertently widen health inequities that already exist. Program oversight by a governance structure that is focused on monitoring, tracking and advancing progress towards health equity will be needed. Ultimately, the health system must actively resist increasing the health equity divide by targeting both upstream social policies (that will ultimately reduce cancer risk), as well as midstream interventions that can enhance health seeking choices. To do this would require an emphasis on the social policies that facilitate stable work, adequate income, and secure housing. One of the ways in which this can be achieved is through the integration of patient-identified priorities. Future research into the lived experiences of patients can continue to provide meaningful insights into what works, and what is needed to enhance health promoting opportunities.

Interview guide for screeners.

(PDF)

Click here for additional data file.

Interview guide for non-screeners.

(PDF)

Click here for additional data file.

Consolidated criteria for reporting qualitative studies (COREQ) checklist.

(PDF)

Click here for additional data file.

9 Mar 2021

PONE-D-21-01483

Advancing Health Equity in Cancer Care: The Lived Experiences of Poverty and Access to Lung Cancer Screening.

PLOS ONE

Dear Dr. Sayani,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Specifically, the paper is way too long (~5000 words) and needs to be shorted by half.  The topic is of interest, but one of the reviewers was unclear about the heavy focus on affordable housing as a proxy for SES.  This needs to be explained more clearly.  The limitations of the qualitative approach needs to be mentioned in the discussion and what specific next steps would the author recommend to address obvious disparities in lung cancer screening. However, because the paper addresses a topic of important that has not received much attention in the published literature we invite you to submit a substantial revised and shortened version  of the manuscript that addresses the points raised during the review process.

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Michael Cummings, PhD

Academic Editor

PLOS ONE

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'AS is supported by a Postdoctoral Fellowship Award from the Canadian Institutes for Health Research. AL is supported by a New Investigator Award from the Canadian Institutes for Health Research, as Clinician Scientist by the Department of Family Medicine at the University of Toronto and as Chair of Implementation Science at the Peter Gilgan Centre for Women’s Cancers at Women’s College Hospital in partnership with the Canadian Cancer Society. AL is the Provincial Primary Care Lead for Cancer Screening at Ontario Health (Cancer Care Ontario). GL is supported by the Lusi Wong Early Detection of Lung Cancer Program and the Alan B. Brown Chair. GL has received funding from an unrestricted Boehringer Ingerheim grant to develop and implement electronic methods of identifying patients suitable for lung cancer screening in family physician offices. PS is a Clinician Scientist funded by Centre of Addiction and Mental Health, Department of Family and Community Medicine and the Ministry of Health and Long Term Care to direct the STOP program- An Ontario wide smoking cessation program focused on reducing inequities of access for discriminated and underrepresented populations. He also receives support from the Medical Psychiatry Alliance. He has independent grants from the GRAND program, created as an arms-length peer reviewed program for smoking cessation. He is an advisor to both Cancer Care Ontario and Canadian Partnership Against Cancer (CPAC) on tobacco cessation in patients with Cancer. EN is an employee of the CPAC, a pan-Canadian health organization, funded by Health Canada.'

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Reviewer #1: Yes

Reviewer #2: Partly

Reviewer #3: Yes

**********

2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: N/A

Reviewer #2: N/A

Reviewer #3: N/A

**********

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Reviewer #1: Yes

Reviewer #2: No

Reviewer #3: Yes

**********

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Reviewer #3: Yes

**********

5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: Sayani and colleagues present the results of a qualitative research study aimed at describing barriers and facilitators to lung cancer screening in low income individuals in Toronto. The methodology and theoretical framework are sound, and the findings are important as countries consider how to target those at the highest risk for lung cancer and are also the most disadvantaged due to socioeconomic status. I have the following comments:

1) Overall, the manuscript is quite lengthy of a read at over 5000 words. I understand that PlosOne does not have a limit on words but would encourage the authors to summarize methodology and limitations and strengths sections further.

2) Similarly, the authors chose to embed representative quotes into the body of the text which extends the length of the manuscript. I would suggest considering instead constructing a table that pulls from the themes, subthemes and key findings presented in Figure 2 and putting in representative quotes into the table. If the authors chose to leave the quotes embedded, I would suggest reducing the length of the quotes. For example, participant Philip’s quotes could be shortened considerably. In addition, including quotes from the other 18 participants rather than utilizing the same participants might better support the themes and conclusions identified.

3) In the discussion section, the paragraph that discusses gender-based differences in smoking is not particularly relevant to the focus of the manuscript especially given the low number of female participants and distracts. I would suggest removing.

Reviewer #2: This interesting manuscript aims to address gaps in understanding factors that influence individual choices in preventative health care particularly lung cancer screening. While providing an interesting insight into experiences for the study cohort, the sample size is relatively small and the findings do not appear specific to lung cancer screening, even though the interview questions focussed on screening. The most important finding of this study appears to be the impact of housing instability. However the data presented do not link this tightly to choice in lung cancer screening. Rather this appears (quite logically) to affect health and attitudes more globally. This study describes of the impact of housing instability and income (as markers of SEC disadvantage) on general attitudes towards health and smoking cessation but is limited in its ability to "unpack" detailed reasons to avoid screening. The profound effect of housing instability appears to override other considerations. As a result more detailed reasons may be hard to elicit.

Other comments:

- the screen selection threshold for PLCOm2012 at 2% is higher than some published data and this is worth acknowledging in the discussion

- not clear whether the "derived rapport" technique was used across all three sites or not - could this introduce bias?

- description of sites would be of value for distribution of demographics in the denominator groups

- there are likely to be factors that influence screening uptake that can't be detected in this small sample (noting the very low levels of uptake detected in the USA - Pham Clin Lung Cancer. 2020 May;21(3):e206-e211. )

- the "judgmental and insensitive" clinical encounters warrant further discussion esp. for future research

While the comments from interviewees were very interesting, the sample is small and the findings - dominated by housing status - are not clearly shown to be linked to rejection of LC screening over and above other preventative health interventions.

Reviewer #3: I found the paper very compelling and thorough - and, distressing. As a strong advocate for both LDCT screening and tobacco cessation, it is housing (and associated economic issues) that is a critical factor - which is yet for another discipline to address.

Two typos: one is the difference between the $30 - 50,000 (line 248) or line 173: $30 - 59,000.

Line 323 should be 'groups' rather than 'group'.

**********

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Reviewer #1: No

Reviewer #2: No

Reviewer #3: Yes: Carolyn Dresler, MD, MPA

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1 Apr 2021

Dear Dr. Cummings,

Thank you for your comments and feedback on the manuscript PONE-D-21-01483 Advancing Health Equity in Cancer Care: The Lived Experiences of Poverty and Access to Lung Cancer Screening.

Kindly find attached to this letter revised versions of the manuscript (with tracked changes and an unmarked copy) based on your feedback. Our point-by-point changes/ comments are detailed below:

1. Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming.

Thank you we have edited the file to match the formatting requirements of PLOS ONE.

2. In your Methods section, please provide additional information about the participant recruitment method and the demographic details of your participants. Please ensure you have provided sufficient details to replicate the analyses such as:

a) the recruitment date range (month and year),

b) a description of how participants were recruited, and

c) descriptions of where participants were recruited and where the research took place (e.g. name of clincial site).

We have now included more details in the methods section about the recruitment date and specified how we used derived rapport to recruit non-screeners. We have also included a description of the primary care sites through which participants were recruited. To protect the identity of participants we are not disclosing the names of the clinical sites.

3. Please state in the manuscript Methods:

- Why written consent could not be obtained

- Whether the Institutional Review Board (IRB) approved use of oral consent

- How oral consent was documented

Thank you, we have now included in detail the process of verbal consent and the approval of this process from our IRB.

4. Thank you for stating the following in the Competing Interests section:

'AS is supported by a Postdoctoral Fellowship Award from the Canadian Institutes for Health Research. AL is supported by a New Investigator Award from the Canadian Institutes for Health Research, as Clinician Scientist by the Department of Family Medicine at the University of Toronto and as Chair of Implementation Science at the Peter Gilgan Centre for Women’s Cancers at Women’s College Hospital in partnership with the Canadian Cancer Society. AL is the Provincial Primary Care Lead for Cancer Screening at Ontario Health (Cancer Care Ontario). GL is supported by the Lusi Wong Early Detection of Lung Cancer Program and the Alan B. Brown Chair. GL has received funding from an unrestricted Boehringer Ingerheim grant to develop and implement electronic methods of identifying patients suitable for lung cancer screening in family physician offices. PS is a Clinician Scientist funded by Centre of Addiction and Mental Health, Department of Family and Community Medicine and the Ministry of Health and Long Term Care to direct the STOP program- An Ontario wide smoking cessation program focused on reducing inequities of access for discriminated and underrepresented populations. He also receives support from the Medical Psychiatry Alliance. He has independent grants from the GRAND program, created as an arms-length peer reviewed program for smoking cessation. He is an advisor to both Cancer Care Ontario and Canadian Partnership Against Cancer (CPAC) on tobacco cessation in patients with Cancer. EN is an employee of the CPAC, a pan-Canadian health organization, funded by Health Canada.'

a. Please confirm that this does not alter your adherence to all PLOS ONE policies on sharing data and materials, by including the following statement: "This does not alter our adherence to PLOS ONE policies on sharing data and materials.” (as detailed online in our guide for authors http://journals.plos.org/plosone/s/competing-interests). If there are restrictions on sharing of data and/or materials, please state these.

Please note that we cannot proceed with consideration of your article until this information has been declared.

Thank you for this information. We have now included the statement as recommended in our competing interests.

b. Please include your updated Competing Interests statement in your cover letter; we will change the online submission form on your behalf.

Thank you. We have now included this information in our cover letter and appreciate your assistance with the online submission.

5. Please ensure that you refer to Figure 2 in your text as, if accepted, production will need this reference to link the reader to the figure.

This has been corrected, thank you.

6. Please include your table as part of your main manuscript and remove the individual file. Please note that supplementary tables should remain as separate "supporting information" files.

Thank you, all tables have now been included in the main manuscript file.

7. Please include captions for your Supporting Information files at the end of your manuscript, and update any in-text citations to match accordingly. Please see our Supporting Information guidelines for more information: http://journals.plos.org/plosone/s/supporting-information

Thank you, we have formatted the supporting files with PLOS ONE criteria.

8. Your ethics statement should only appear in the Methods section of your manuscript. If your ethics statement is written in any section besides the Methods, please delete it from any other section.

Thank you we have placed ethics in the methods section.

Reviewer #1: Sayani and colleagues present the results of a qualitative research study aimed at describing barriers and facilitators to lung cancer screening in low income individuals in Toronto. The methodology and theoretical framework are sound, and the findings are important as countries consider how to target those at the highest risk for lung cancer and are also the most disadvantaged due to socioeconomic status. I have the following comments:

We thank the reviewer for this comment and for highlighting the knowledge gap which our work seeks to address.

1) Overall, the manuscript is quite lengthy of a read at over 5000 words. I understand that PlosOne does not have a limit on words but would encourage the authors to summarize methodology and limitations and strengths sections further.

Thank you for this comment. We have revisited the manuscript and shortened certain areas – in particular the methodology and limitations/ strengths section as suggested. As a qualitative study it is important for us provide thick description, and we have eliminated as much text as possible without drawing away from the process and outcomes of our work. To the best of our knowledge, our manuscript is the first to describe the use of the morphogenetic approach in health services research. Therefore, it is important to fully describe the theory and its applicability to understanding health seeking choices, which we demonstrate through our study for lung cancer screening participation.

2) Similarly, the authors chose to embed representative quotes into the body of the text which extends the length of the manuscript. I would suggest considering instead constructing a table that pulls from the themes, subthemes and key findings presented in Figure 2 and putting in representative quotes into the table. If the authors chose to leave the quotes embedded, I would suggest reducing the length of the quotes. For example, participant Philip’s quotes could be shortened considerably. In addition, including quotes from the other 18 participants rather than utilizing the same participants might better support the themes and conclusions identified.

Thank you, we have removed all quotations from the paper and added a table instead.

3) In the discussion section, the paragraph that discusses gender-based differences in smoking is not particularly relevant to the focus of the manuscript especially given the low number of female participants and distracts. I would suggest removing.

Thank you for this comment. We have removed this paragraph.

Reviewer #2: This interesting manuscript aims to address gaps in understanding factors that influence individual choices in preventative health care particularly lung cancer screening. While providing an interesting insight into experiences for the study cohort, the sample size is relatively small and the findings do not appear specific to lung cancer screening, even though the interview questions focussed on screening. The most important finding of this study appears to be the impact of housing instability. However the data presented do not link this tightly to choice in lung cancer screening. Rather this appears (quite logically) to affect health and attitudes more globally. This study describes of the impact of housing instability and income (as markers of SEC disadvantage) on general attitudes towards health and smoking cessation but is limited in its ability to "unpack" detailed reasons to avoid screening. The profound effect of housing instability appears to override other considerations. As a result more detailed reasons may be hard to elicit.

We thank the reviewer for this comment. We have now included a more robust description on the clustering of disadvantage (including low income, housing status and employment etc) in the Results section and how this ties into a trajectory over the life course which is entwined with a higher likelihood of smoking. We have also included a more detailed thematic map (Fig. 2) which ties each of the themes together – specifically housing and screening. Housing is an important determinant of health, however, in the context of smoking behaviour needs special attention as a contributor to smoking patterns as well as barrier to screening. We hope to have addressed this satisfactorily in the manuscript.

Other comments:

- the screen selection threshold for PLCOm2012 at 2% is higher than some published data and this is worth acknowledging in the discussion

The screen selection threshold of >2% is the screening eligibility criterion being used in the province of Ontario for lung cancer screening. This has now been added to the Methods section.

- not clear whether the "derived rapport" technique was used across all three sites or not - could this introduce bias?

We have described how derived rapport was used with one health provider – the resulting homogenous nature of participants is described in the limitations of the study.

- description of sites would be of value for distribution of demographics in the denominator groups

Thank you we have now included a brief description of the clinical sites where participants were recruited from.

- there are likely to be factors that influence screening uptake that can't be detected in this small sample (noting the very low levels of uptake detected in the USA - Pham Clin Lung Cancer. 2020 May;21(3):e206-e211. )

Thank you for this comment. As a critical qualitative study we sought to contextualise the lived experiences of participants who were eligible for lung cancer screening and their choice to access screening or not. Using this approach we are able to illuminate some policy and training gaps that are specific to increasing the equitable delivery of lung cancer screening.

- the "judgmental and insensitive" clinical encounters warrant further discussion esp. for future research

We appreciate this comment. We have published qualitative interviews with physicians to understand their perspectives on access to lung cancer screening for individuals living with low income. We have now cited this work in the discussion section.

While the comments from interviewees were very interesting, the sample is small and the findings - dominated by housing status - are not clearly shown to be linked to rejection of LC screening over and above other preventative health interventions.

Thank you for this feedback. We reached conceptual saturation with our data through iterative interviewing and peer-debriefing (described in methods). We have tied housing more deeply to the issue of smoking and lung cancer screening in the themes: pathways of disadvantage and the upstream determinants of lung cancer risk and early detection.

Reviewer #3: I found the paper very compelling and thorough - and, distressing. As a strong advocate for both LDCT screening and tobacco cessation, it is housing (and associated economic issues) that is a critical factor - which is yet for another discipline to address.

Thank you so much for your feedback. We appreciate your comment and hope to move towards a policy discourse which will promote equity in lung cancer screening.

Two typos: one is the difference between the $30 - 50,000 (line 248) or line 173: $30 - 59,000.

Line 323 should be 'groups' rather than 'group'.

Thank you, these corrections have been made.

We thank the reviewers for their insightful feedback and hope to have addressed the reviewers comments appropriately.

We look forward to your positive consideration,

Yours sincerely,

Ambreen Sayani, MD MSc PhD

Submitted filename: ResponseLetter_SayaniA_31March2021.docx

Click here for additional data file.

23 Apr 2021

Advancing Health Equity in Cancer Care: The Lived Experiences of Poverty and Access to Lung Cancer Screening.

PONE-D-21-01483R1

Dear Dr. Sayani,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication.

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If your institution or institutions have a press office, please notify them about your upcoming paper to help maximize its impact. If they’ll be preparing press materials, please inform our press team as soon as possible -- no later than 48 hours after receiving the formal acceptance. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org.

Kind regards,

Michael Cummings, PhD

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: All comments have been addressed

Reviewer #2: All comments have been addressed

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

Reviewer #2: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: N/A

Reviewer #2: N/A

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: Yes

**********

6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: Thank you, all of my comments have been addressed. The work presented here is important and the authors should be complemented.

Reviewer #2: Thank you to the authors for this comprehensive revision.  The paper has improved in response to reviews and my comments have been satisfactorily addressed.  The inclusion of quotes from study subjects in Table 2 works well.  The limitations of the study and areas for further research are presented well in the discussion.

**********

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: No

Reviewer #2: No

27 Apr 2021

PONE-D-21-01483R1

Advancing health equity in cancer care: the lived experiences of poverty and access to lung cancer screening.

Dear Dr. Sayani:

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

If your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org.

If we can help with anything else, please email us at plosone@plos.org.

Thank you for submitting your work to PLOS ONE and supporting open access.

Kind regards,

PLOS ONE Editorial Office Staff

on behalf of

Dr. Michael Cummings

Academic Editor

PLOS ONE