Cancer stage at presentation for incarcerated patients at a single urban tertiary care center.

Patients who are incarcerated are a vulnerable patient population and may suffer from less access to routine cancer screenings compared to their non-incarcerated counterparts. Therefore, a thorough evaluation of potential differences in cancer diagnosis staging is needed. We sought to examine whether there are differences in cancer stage at initial diagnosis between non-incarcerated and incarcerated patients by pursuing a retrospective chart review from 2010-2017 for all patients who were newly diagnosed with cancer at an urban safety net hospital. Incarceration status was determined by insurance status. Our primary outcome was incarceration status at time of initial cancer diagnosis. Overall, patients who were incarcerated presented at a later cancer stage for all cancer types compared to the non-incarcerated (+.14 T stage, p = .033; +.23 N stage, p < .001). Incarcerated patients were diagnosed at later stages for colorectal (+0.93 T stage, p < .001; +.48 N stage, p < .001), oropharyngeal (+0.37 N stage, p = .003), lung (+0.60 N stage, p = .018), skin (+0.59 N stage, p = 0.014), and screenable cancers (colorectal, prostate, lung) as a whole (+0.23 T stage, p = 0.002; +0.17 N stage, p = 0.008). Incarcerated patients may benefit from more structured screening protocols in order to improve the stage at presentation for certain malignancies.

Introduction

Persons who are incarcerated represent a unique and vulnerable, patient population. During the time they are incarcerated, these patients receive variable access to health care that is dependent upon the state in which they are incarcerated, the length of their incarceration, and the arrangements for health care providers made by their institution [1]. Incarcerated patients (IP) face both systemic barriers to care as well as vulnerability due to impediments to self-advocating due to their status as an inmate [2]. Both these issues may delay or limit their receipt of treatments that–outside the prison system–are more often given, such as direct-acting anti-viral agents for hepatitis C infection and opioid maintenance therapy for substance use disorders [3, 4]. Additionally, in the United States, IP are less likely to receive screenings for certain cancers in a timely fashion [5]. Overall mortality in persons with a history of incarceration is higher compared to people who have never been incarcerated [6, 7]. Additionally, IP carry a higher burden of chronic and acute health conditions, particularly infections including HIV, hepatitis C virus and other sexually transmitted infections [8-10]. Together, the barriers in access to care, in combination with increased chronic medical conditions and decreased screening tests, are likely associated with and may directly contribute to the increased overall mortality in people who are currently incarcerated or have a history of incarceration [11, 12].

Previous research has demonstrated that cancer is a leading cause of death for those who are currently or formerly incarcerated. A retrospective cohort study of 4,026 Texas state prisoners showed cancer and cardiovascular disease were the leading causes of death in prisoners age 55–84 [13]. Another similar study of 797 North Carolina prisoners showed cancer as the second leading cause of death. This study revealed that IP had higher liver cancer-related mortality compared to non-incarcerated population [14]. This difference does not necessarily end upon release from prison, as previously incarcerated patients have an excess mortality due to cancer compared to never-incarcerated patients [15]. These studies underscore the importance of recognizing cancer in IP, not just for their health while incarcerated, but also after release from prison.

The etiology of increased mortality from cancer in IP has not been subjected to rigorous study and is poorly understood. HCV and tobacco use, known cancer risk factors, are more prevalent amount IP populations. Taking these into account, it is not surprising that the incarcerated population has an increased incidence of both lung cancer and hepatocellular cancer compared to patients who are not incarcerated [16-18]. Current screening recommendations from the United States Preventive Services Task Force (USPSTF) for lung cancer include low dose Computerized Tomography (CT) scan for patients over 55 with more than 15 pack year smoking history [19]. Screening for hepatocellular carcinoma is indicated in patients with cirrhosis due to hepatitis C or alcohol and involves frequent abdominal imaging (either ultrasound or CT) according to society guidelines [20]. USPSTF recommends screening for colorectal cancer in all people age 50 and older [21]. Despite increased incidence of smoking, hepatitis C and alcoholism, appropriate screenings for hepatocellular carcinoma, lung cancer or colorectal cancer are not always performed according to national and international guidelines in the IP population [5]. Multiple reasons for decreased screenings among patients who are currently or previously incarcerated have been suggested, including poorer connection with primary care resources, lack of availability while incarcerated and following incarceration due to systemic barriers patients who were previously incarcerated also face [22, 23]. Regarding patients who are currently incarcerated, a recent study of the incarcerated population in Ontario, Canada showed these patients are more likely to be overdue for breast and colorectal cancer screening [11]. While not previously studied or documented, decreased availability of screening in prison is likely to also contribute to the lack of screening in this population.

Together these studies have highlighted that IP are less likely to receive the appropriate screenings compared to the general population. Therefore, this already vulnerable population is often not aware of that for which they must self-advocate nor are they in a position to do so. These situations, compounded, further decrease the likelihood of this at-risk population having their cancers detected at an early stage. In our study we assessed the association between incarceration and cancer stage upon initial diagnosis in all cancers as well as specific cancer sub-types, including those with robust screening guidelines.

Materials and methods

Data and population

This retrospective, observational study was carried out with a patient cohort at a large, urban, tertiary care safety-net hospital in New England from January 1, 2010 until December 31, 2017. Patients were identified through the hospital’s cancer registry database, with incarceration status determined through administrative billing data. After excluding non-malignant lesions, a total of 116 incarcerated and 2,860 non-incarcerated patients were included for analysis. After review of each case, additional cases were excluded due to either cancers not staged by American Joint Committee on Cancer (AJCC) 7th edition staging system or if the total number of cancer subtypes was too small for robust statistical analysis. A total of 74 incarcerated and 1,408 non-incarcerated patients were included in the final analysis (S1 Fig). Of these, 100% IP cases and 160 of non-incarcerated patients (NIP) cases (11.3% of total) were reviewed to ensure internal consistency of the cancer registry database. Patients were excluded if they carried a prior diagnosis of the primary cancer (i.e. previously treated and seeking second opinion) or had a recurrence of a prior cancer. Patients were marked as having a previous diagnosis of cancer if they were either diagnosed prior to January 1, 2010 and still receiving treatment throughout the study period or if they were diagnosed at an outside hospital and received treatment (surgery, radiation or chemotherapy) before transferring their care to our institution. Patients were excluded upon the basis of prior cancer recurrence if they had a relapse within 5 years of their last curative therapy. If there was a recurrence that occurred outside of the 5 years, the patient was included in the analysis as having a new, de novo cancer. These exclusion criteria allowed us to evaluate the staging of cancer upon initial diagnosis for non-incarcerated and incarcerated patients seen at our institution. This study was approved and monitored by the hospital’s Institutional Review Board. Given the study was retrospective, informed consent was waived by the IRB.

Study variables

Risk factors such as patients’ age at diagnosis, race and gender were extracted from the cancer registry database. Additional risk factor data for patients with lung or hepatocellular carcinoma were extracted manually via chart review. For lung cancer, extracted data included occupational exposures (radon, asbestos), TB status, smoking history and family history. The initial history and physical note at diagnosis of cancer was reviewed for each of these risk factors. Patient’s smoking history was documented in pack years. For patients who had quit, their year of quitting was also noted. TB status was noted as positive or negative based on either PPD, Quant-GOLD assay or three AFB negative sputum.

For hepatocellular carcinoma, history of hepatitis B and C viruses, cirrhosis, alcohol abuse and smoking history were extracted as important risk factors. Patients were noted to have a history of HCV if they had a recent serum antibody test positive for anti-HCV. HBV status was noted based upon routine hepatitis panel as follows: current infection with +HBsAg, resolved infection with -HBsAg, +anti-HBc, +anti-HBs and never infected with -HBsAg and -anti-HBc. Patients with cirrhosis or alcohol abuse were evaluated based upon ICD-9 or ICD-10 codes for each of the conditions.

The AJCC 7th edition staging system was used to stage each patient’s cancer at time of diagnosis [24]. We used the clinical tumor (T), nodal (N), metastatic (M) and full clinical AJCC stage as outcome variables indicative of prognosis [cite]. Additionally, we used binary indicators of tumor staging by grouping T1 and T2 as early stage and T3 and T4 as later stage. Similarly, for nodal stage N0 was grouped as early while N1, N2 and N3 were late. For clinical AJCC, stages I and II were marked as early stage and stages III and IV were marked as later stage.

Analytic approach

Our analysis proceeded in three steps. We first characterized the differences between the groups using two-tailed t-tests or chi-squared tests as appropriate. We then calculated mean cancer outcomes for IP and non-IP and compared them using two-sided t-tests, showing potential differences in cancer staging before adjustment for observed risk factors. Next, we employed inverse probability of treatment weighting (IPTW) to identify the effect of incarceration on initial cancer staging. This method is increasingly used in cancer studies, allowing investigators to reduce bias when assessing the effects of an intervention when treatment and control groups are nonequivalent [25].

For the IPTW, propensity scores were obtained using logistic regression with incarceration as the outcome and age, race, and gender as predictors. Each subject's weight was defined as the inverse of the probability of receiving the treatment (or non-treatment) that the subject received; incarceration vs. non-incarceration.

Weighted linear regression models were then used to identify the effect of incarceration on the cancer outcomes, after controlling for other risk factors. The results may be interpreted as average changes in cancer staging, or changes in predicted probability of late treatment for dichotomized outcomes. When the propensity score model is correctly specified, this technique consistently estimates the true treatment effect [26].

Results

Patient characteristics and cancer incidence

We identified a total of 74 patients who were diagnosed with cancer at our institution while incarcerated (IP) and 1408 patients who were not incarcerated (NIP) during the study period. The characteristics of our study sample are listed in Table 1. Demographic differences between the two groups were assessed using two-tailed t-tests or chi-squared tests as appropriate. Compared to NIP, IP were more likely to be male (94.6% vs. 68.8%, p < 0.001) and an older median age (62.4 vs. 57.2 years, p<0.001). In both IP and NIP, Caucasian (67.6% vs. 67.0%) was the most common race followed by African American (27.0% vs. 28.0%) and Hispanic (5.4% vs. 5.0%), revealing similar racial balance between groups (p = 0.978). The prevalence of specific cancers, however, varied between groups (p < .001), with hepatobiliary (31.1%), bronchopulmonary (20.3%) and oropharyngeal (14.9%) being most common in IP, while oropharyngeal (24.9%), bronchopulmonary (22.3%) and prostate (21.1%) were most common in NIP (Fig 1, S1 Table).

Table 1

Summary demographics for patients included in analysis.

Variable		Incarceration Status		P-value
		No	Yes
N		1,408	74	--
Age in years (Mean (SD))		57.2 (10.3)	62.4 (27.8)	< .001
Sex (N (%))				< .001
	Male	968 (68.9)	70 (94.6)
Race (N (%))				0.895
	African American	394 (28.0)	20 (27.0)
	Caucasian	943 (67.0)	50 (67.6)
	Hispanic	71 (5.0)	4 (5.4)
Tumor stage (%)				0.287
	0	14 (1.0)	1 (1.4)
	1	417 (30.5)	16 (21.9)
	2	391 (28.6)	25 (34.2)
	3	228 (16.7)	17 (23.3)
	4	317 (23.2)	14 (19.2)
Nodal stage (N (%))				0.254
	0	853 (62.1)	45 (62.5)
	1	195 (14.2)	8 (11.1)
	2	254 (18.5)	13 (18.1)
	3	72 (5.2)	6 (8.3)
Metastatic stage (N (%))				0.545
	0	1099 (79.5)	59 (80.8)
	1	283 (20.5)	14 (19.2)
AJCC stage (N (%))				0.507
	0	6 (0.4)	1 (1.4)
	1	300 (21.7)	12 (16.2)
	2	369 (26.7)	25 (33.8)
	3	217 (15.7)	11 (14.9)
	4	491 (35.5)	25 (33.8)

Differences were assessed using either two-tailed t-tests (for continuous variables) or chi-squared tests (for categorical variables). American Joint Committee on Cancer (AJCC).

Fig 1

Incidence of different cancer subtypes in incarcerated patients and non-incarcerated patients.

Bars represent the percentage of each cancer subtype in IP and NIP cases. Hepatobiliary (31.1%), Bronchopulmonary (20.3%) and oropharyngeal (14.9%) were most common in IP, while oropharyngeal (24.9%), bronchopulmonary (22.3%) and prostate (21.0%) were most common in NPI.

Unadjusted disparities in cancer staging

Evaluating AJCC staging for all cancers combined, IP were diagnosed at slightly later T (2.37 vs. 2.31, p = 0.618) and N stages (0.72 vs. 0.67, p = 0.670), however these differences did not reach significance (Table 2, S2 Table). IP and NIP were diagnosed at approximately the same M and overall AJCC stages.

Table 2

Descriptive statistics of cancer staging by incarceration status.

Cancer Type	Clinical Stage
	T			N			M			AJCC
	Incarcerated		Diff	Incarcerated		Diff	Incarcerated		Diff	Incarcerated		Diff
	Yes	No		Yes	No		Yes	No		Yes	No
Oropharyngeal	2.73	2.56	0.17	1.36	0.92	0.45	0.00	0.02	-0.02*	3.45	3.00	0.46
Lung	2.67	2.52	0.15	1.13	1.22	-0.08	0.47	0.46	0.00	2.87	2.96	-0.09
Liver	2.17	1.97	0.20	0.14	0.18	-0.05	0.09	0.19	-0.11	2.30	2.21	0.10
Esophageal	1.67	2.26	-0.60	0.83	0.72	0.11	0.33	0.31	0.02	2.50	2.73	-0.23
Colorectal	3.29	2.37	0.92*	1.14	0.57	0.57	0.29	0.31	-0.03	2.86	2.58	0.27
Prostate	1.75	1.94	-0.19	0.12	0.13	0.00	0.12	0.11	0.01	2.38	2.39	-0.01
Skin	2.00	2.02	-0.02	1.00	0.25	0.75	0.00	0.04	-0.04*	1.75	1.60	0.15
Screenable	2.46	2.30	0.16	0.69	0.67	0.02	0.19	0.21	-0.02	2.78	2.63	0.15
Overall	2.37	2.31	0.06	0.72	0.67	0.05	0.19	0.20	-0.01	2.64	2.64	-0.01

The table displays unadjusted averages and differences in tumor staging between prisoners and non-prisoners. Screenable cancers include liver, lung, colorectal, and prostate. Differences were assessed using two-sided t-tests.

*p<0.05

**p<0.01

***p<0.001.

As the cancer types differed significantly between the IP and NIP groups, we next sought to evaluate the staging within screening cancers and individually for each cancer type. While many individual cancer types did not show differences in overall staging or sub-staging, the IP group was diagnosed at a T stage that was 0.92 higher than the NIP group for colorectal cancers (95% CI, 0.22 to 1.62). Additionally, there were slight differences in M staging for oropharyngeal and skin cancers that were statistically significant but due to small numbers, were not considered clinically significant.

To further evaluate our patient population, we grouped each patient into early and late stage for tumor (T1, T2 vs. T3, T4), nodal (N0 vs. N1, N2, N3) and AJCC clinical stage (I, II vs. III, IV) groups to form binary indicators of early and late stage. There were no significant differences in early and late stage tumor, nodal or AJCC clinical staging between the IP and NIP groups, both overall or for specific cancers (S3 Table). IP were more likely to be diagnosed at a late stage for colorectal cancer (86% vs. 52%, p = 0.055), but this result was marginally significant.

Inverse probability of treatment weighting

The IPTW results for cancer staging are contained in Table 3. Overall, IP received cancer diagnoses that were at late T stages (+0.14, 95% CI 0.01 to 0.26) and N stages (+0.23, 95% CI 0.13 to 0.34) when compared to those who were not incarcerated (S4 Table). Similar results were found when focusing on screenable cancers only, where IP were diagnosed at later T stages (+0.23, 95% CI 0.09 to 0.38) and N stages (+0.17, 95% CI 0.04 to 0.29). For individual cancer types, the largest disparity for IP vs NIP occurred with T staging for colorectal cancer (+0.93, 95% CI 0.59 to 1.28). IP also received higher initial N staging for oropharyngeal (+0.37, 95% CI 0.12 to 0.61), lung (+0.60, 95% CI 0.11 to 1.10), colorectal (+0.48, 95% CI 0.22 to 0.73) and skin cancers (+0.59, 95% CI 0.12 to 1.05). On average, IP also received higher overall staging compared to NIP but these differences were only significant for oropharyngeal cancers (+0.36, 95% CI 0.05 to 0.67).

Table 3

Adjusted regression results for the effects of incarceration status on initial cancer staging, by cancer subtype.

Cancer Type	Incarcerated (#)		Clinical Stage
	No	Yes	T	N	M	AJCC
Oropharyngeal	351	11	0.16	0.37**	-0.01	0.36*
Lung	314	15	0.19	0.03	0.06	0.03
Liver	67	23	0.21	-0.03	-0.07	0.11
Esophageal	70	6	-0.39	0.25	0.05	0.07
Colorectal	198	7	0.93***	0.48***	-0.06	0.14
Prostate	296	8	-0.12	0.02	0.04	0.04
Skin	112	4	0.22	0.59*	-0.06	0.06
Screenable	875	53	0.23**	0.17**	-0.04	0.04
Overall	1408	74	0.14*	0.23***	-0.04	0.09

The table displays average differences in tumor staging between prisoners and non-prisoners after inverse probability of treatment weighting. Screenable cancers include liver, lung, colorectal, and prostate. p<0.05

**p<0.01

***p<0.001.

Fewer differences were observed in the IPTW analyses comparing absolute rates of early vs. late diagnoses (S5 Table). Compared to NIP, IP were more likely to receive a late T stage diagnosis for screenable cancers (+0.07, 95% CI 0.03 to 0.14) and colorectal cancer (+0.34, 95% CI 0.19 to 0.49). For N staging, IP were more likely to be diagnosed late for oropharyngeal (+0.22, 95% CI 0.10 to 0.34) and colorectal cancers (+0.16, 95% CI 0.01 to 0.31).

Since patients who are incarcerated are more likely to harbor risk factors for certain cancers (S6 and S7 Tables), we performed IPTW analyses which accounted for these risk factors for two cancer types where such data were available: hepatocellular carcinoma (HCC) and lung (S4 and S5 Tables). Incorporating the risk factors for HCC (viral status, smoking history, history of cirrhosis, history of alcoholism) had no impact on the results for stage of diagnosis. However, incorporating the risk factors for lung cancer (smoking history, asbestos exposure) showed a significant increase in nodal stage (+0.60, p = 0.05) in IP as compared to NIP (S4 Table).

Discussion

Patients who are incarcerated experience an increased mortality due to cancer, however the mechanism behind this has remained unclear. Our findings comport with previous research, which has suggested differential health literacy and screening rates by incarceration status as etiologies of increased mortality from cancer. We characterized differences in cancer stage at diagnosis between patients who are incarcerated and those who are not incarcerated. Our institutional setting is particularly suited for this analysis due to its treatment of a large portion of the state’s incarcerated patients, and its status as an urban safety net hospital with NIP demographics similar to the IP group.

Our initial analysis examined unadjusted cancer staging between the IP and NIP groups. While we found that colorectal cancers were diagnosed at a later T stage, the populations were generally similar with respect to cancer staging. However, the IP group was younger and more likely to be male compared to the NIP group. Therefore, we accounted for the demographic factors using IPTW models.

After adjusting for demographics, we found overarching disparities in T, N, and AJCC clinical stage between the IP and NIP groups. IP were diagnosed at later stages in our overall analysis as well as for several specific cancer types including colorectal, oropharyngeal, lung, skin. Screenable cancers (liver, lung, colorectal, prostate) showed a statistically significant increase in T and N staging for IP, suggesting these disparities in staging could be driven by lower screening rates and thus less early detection.

Our study suggests opportunities to improve screening and care processes for certain incarcerated patients. At a population level, the observed disparities in cancer staging between IP and NIP represent a potential human cost in terms of both quality of life and expected survival post-diagnosis. Later diagnoses may also limit the ability of IP to gain employment or assimilate back into their communities following release. The most striking difference is with the patients with colorectal cancer as our data indicates they are diagnosed at a significantly later stage. Guidelines and recommendations for colorectal cancer screening with colonoscopy have been established for decades and screening has an impressive effect on early detection of cancer as well as prevention with polypectomy. Understanding that IP are diagnosed at later stages should inform health care practices within the prison system and direct routine screening of all eligible patients. We recognize that cost is likely to represent a significant barrier and while colonoscopy is often preferred, additional screening through fecal occult blood tests are also viable options for this population and could aid in earlier detection. Current practices for screening in our state’s prison system are unknown, however it is notable that none of the patients diagnosed with colorectal cancer or lung cancer had documented appropriate screenings while incarcerated or were referred to our hospital following a positive result from screening.

While we detected differences in stage at diagnosis for multiple screenable cancers, it must also be recognized that many cancers do not have established screening tests, including oropharyngeal and skin cancers. The differences in stage at diagnosis in these cancers could be rooted in at least two possibilities: 1) decreased access to care overall while incarcerated or 2) life-long systemic injustice of patients who are of low socioeconomic status and make up the majority of the incarcerated persons in the United States. It must also be recognized that poor access health care is not only found in our prison system. It is perpetuated throughout each stage of life and leads to unstable households, adverse childhood events, unemployment, mental illness, substance use and acquisition of habits that increase risk for cancer (smoking, alcohol use, sexually transmitted infections, injection drug use and its associated infections). Therefore, we must promote screening of cancers in our incarcerated population but also recognize that prevention of patients becoming incarcerated starts with adequate access to health care early in life as well.

Our study has important strengths. Our institutional setting was particularly suited for this analysis due to its treatment of a large portion of the state’s incarcerated patients, and its status as an urban safety net hospital with NIP demographics similar to the IP group. However, our study also has several limitations. Due to the observational design, our findings should be interpreted as associations and we cannot make causal inferences between incarceration and later stage of cancer diagnosis. Certain demographic information was not available, including zip codes and income for the non-incarcerated group, which affected our ability to adjust for socioeconomic status. Our sample size limited our ability to conduct subgroup analyses for certain cancer types. Lastly, the continuity of care in the correctional system is fragmented and once patients are released they are often lost to follow up. Additionally, the length of incarceration for each patient is different. Taken both of these together we were thus unable to analyze the effect of incarceration (occurrence or length) on cancer survival and mortality. Further studies are needed to evaluate the impact of delayed detection in IP on future health outcomes, especially for colorectal cancers.

Conclusions

Compared to those who are not incarcerated, incarcerated persons may present at a later stage for several cancer types. This disparity is especially evident in screenable cancers such as colorectal cancer. Our results suggest a potential for improvement in the screening protocols for those who are incarcerated, particularly for colorectal cancers. Given the many barriers associated with routine screening for all who are incarcerated, initial reforms might be best focused on high-risk individuals.

Construction of the study sample.

(DOCX)

Click here for additional data file.

Frequency of cancer subtypes in incarcerated and non-incarcerated population.

(DOCX)

Click here for additional data file.

Descriptive statistics of cancer staging by incarceration status with confidence intervals.

(DOCX)

Click here for additional data file.

Descriptive statistics for early vs. late cancer staging, by cancer subtype.

(DOCX)

Click here for additional data file.

Adjusted regression results for the effects of incarceration status on initial cancer staging, by cancer subtype with confidence intervals.

(DOCX)

Click here for additional data file.

Adjusted regression results for the effects of incarceration status on early vs. late cancer staging, by cancer subtype.

(DOCX)

Click here for additional data file.

Lung cancer risk factors in IP and NIP groups.

(DOCX)

Click here for additional data file.

Hepatocellular carcinoma risk factors in IP and NIP groups.

(DOCX)

Click here for additional data file.

11 Jun 2020

PONE-D-19-34040

Stage at presentation for incarcerated patients at a single urban tertiary care center

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Reviewer #1: This analysis does not really have enough patients to make any reliable conclusions about this population. Also not having the insurance or income status is very problematic since this population of is often in the lower socioeconomic stratus which results in patients not doing screening and having later stage cancers.

Reviewer #2: This is an extremely welcome addition to the literature. I have several comments which, I believe, can make it a bit more accessible and therefore, important as the basis of advocacy for this population.

Page 3, line 71—“in some cases”? Please, this is as vulnerable population. Why are you mincing words on this?

Page 3, line 74—Please add something to the effect of the “health care provider arrangements with which the facility contracts”. The type of provider can make a huge difference, especially when contracts are with for-profit companies with incentives for minimal care.

Page 2, line 104—these recommendations need to be summarized—some are more and some much less available, or even recommended.

Page 4, line 108—why only blame the patient here? At least mention that one possible reasons for decreased screening is the lack of availability by the prison health facility!

Page 4, line 114—awkward sentence

Page 5, line 128-9—do you mean the number of specific type of cancer? Up to now, you have not mentioned that you are going to analyze types of cancer so this was confusing

Page 9, Table 1—spell out Tumor, Nodal, Metastatic; give a footnote for complete name of AJCC.

Page 14, line 302—this point needs much more emphasis

Overall Discussion—There needs to be more discussion about cancers that have and do not have reliable screening tests available, including tests that move beyond general screening (colorectal cancer) and look at people with, say HepC—how should their increased risk be addressed. I appreciate that this is not a medical paper but that does not mean that oropharyngeal cancer (for which there is no screening test as far as I am aware) should be equated with colorectal (which has a cheap, simple fecal-occult blood test).

Given the above, I don’t see how you can possible avoid at least some discussion about the health care available to this population. Is screening even available? Is any education provided? Don’t blame this on patient literacy—providers of this population (who have NO choices) have some responsibility for health education. How much does screening cost?

A follow-up study might be to determine if the prisons in the state have any cancer screening guidelines and how these are accessed.

**********

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Reviewer #2: Yes: Patricia J Kelly

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29 Jun 2020

Reviewer #1: This analysis does not really have enough patients to make any reliable conclusions about this population. Also not having the insurance or income status is very problematic since this population of is often in the lower socioeconomic stratus which results in patients not doing screening and having later stage cancers.

We thank Reviewer #1 for their input. Our data compare patients with a new diagnosis of malignancy who are incarcerated to those who are non-incarcerated at our institution, which is an urban, high volume, safety net hospital. The majority of our patient population is minority underserved and represents a similar demographic to those who are incarcerated. As the only major safety-net hospital in the Boston metropolitan area, all patients are able to receive care through the MassHealth program, which is able to provide insurance to 95% or more of the otherwise uninsured persons. Therefore, we believe that the absence of insurance and income status would not play a significant role in our analysis. Prior published analyses of our patient population have shown no difference in oncologic outcomes between patients based on insurance status, race or ethnicity or income level at our institution. (see: Morgan et al, JOGS; PMID# 30097966 and Sridhar et al, JACS; PMID# 31212101)

Reviewer #2: This is an extremely welcome addition to the literature. I have several comments which, I believe, can make it a bit more accessible and therefore, important as the basis of advocacy for this population.

Page 3, line 71 (42) — “in some cases”? Please, this is as vulnerable population. Why are you mincing words on this?

We thank Reviewer #2 for their input and we agree. This has been removed.

Page 3, line 74 (45) — Please add something to the effect of the “health care provider arrangements with which the facility contracts”. The type of provider can make a huge difference, especially when contracts are with for-profit companies with incentives for minimal care.

We thank Reviewer #2 for their input and we have revised the manuscript to state: During the time they are incarcerated, these patients receive variable access to health care that is dependent upon the state in which they are incarcerated, the length of their incarceration, and the arrangements for health care providers made by their institution.

Page 2, line 104 (74) —these recommendations need to be summarized—some are more and some much less available, or even recommended.

We thank Reviewer #2 for their input and we have revised the manuscript to state: Current screening recommendations from the United States Preventive Services Task Force (USPSTF) for lung cancer include low dose Computerized Tomography (CT) scan for patients over 55 with more than 15 pack year smoking history. Screening for hepatocellular carcinoma is indicated in patients with cirrhosis due to hepatitis C or alcohol and involves frequent abdominal imaging (either ultrasound or CT) according to society guidelines. USPSTF recommends screening for colorectal cancer in all people age 50 and older. Despite increased incidence of smoking, hepatitis C and alcoholism, appropriate screenings for hepatocellular carcinoma, lung cancer or colorectal cancer are not always performed according to national and international guidelines in the IP population [4].

Page 4, line 108 (84) — why only blame the patient here? At least mention that one possible reasons for decreased screening is the lack of availability by the prison health facility!

We thank Reviewer #2 for their input and we have revised the manuscript to state: “While not previously studied or documented, decreased availability of screening in prison is likely to also contribute to the lack of screening in this population.”

Page 4, line 114 (91) —awkward sentence

We thank Reviewer #2 for their input and we have revised the manuscript to state: “Together these studies have highlighted that IP have lower health literacy regarding screenings and they are unlikely to receive the appropriate screenings while incarcerated. Therefore, this already vulnerable population is often not aware of that for which they must self-advocate nor are they in a position to do so.

Page 5, line 128-9 (108) —do you mean the number of specific type of cancer? Up to now, you have not mentioned that you are going to analyze types of cancer so this was confusing

We thank Reviewer #2 for their input and we have revised the manuscript to state: “cancer subtypes”. We have also adjusted the last sentence of the Introduction (line 98) to state: “In our study we assessed the association between incarceration and cancer stage upon initial diagnosis in all cancers as well as specific cancer sub-types, including those with robust screening guidelines.”

Page 9, Table 1—spell out Tumor, Nodal, Metastatic; give a footnote for complete name of AJCC.

We thank Reviewer #2 for their input and we have revised the manuscript as recommended.

Page 14, line 302 (284) —this point needs much more emphasis.

We thank Reviewer #2 for their input and we have revised the manuscript to state: “The most striking difference is with the patients diagnosed with colorectal cancer as our data indicates they are diagnosed at a significantly later stage. Guidelines and recommendations for colorectal cancer screening with colonoscopy have been established for decades and screening has an impressive effect on early detection of cancer as well as prevention with polypectomy. Understanding that IP are diagnosed at later stages should inform health care practices within the prison system and encourage routine screening of all eligible patients. We recognize that cost is likely to represent a significant barrier and while colonoscopy is often preferred, additional screening through fecal occult blood tests are also viable options for this population and could aid in earlier detection.”

Overall Discussion—There needs to be more discussion about cancers that have and do not have reliable screening tests available, including tests that move beyond general screening (colorectal cancer) and look at people with, say HepC—how should their increased risk be addressed. I appreciate that this is not a medical paper but that does not mean that oropharyngeal cancer (for which there is no screening test as far as I am aware) should be equated with colorectal (which has a cheap, simple fecal-occult blood test).

We thank Reviewer #2 for their input and we have revised the manuscript to state: “While we detected differences in stage at diagnosis for multiple screenable cancers, it must also be recognized that many cancers do not have established screening tests, including oropharyngeal and skin cancers. The differences in stage at diagnosis in these cancers could be rooted in at least two possibilities: 1) decreased access to care overall while incarcerated or 2) life-long systemic injustice of patients who are of low socioeconomic status and make up the majority of the incarcerated persons in the United States. It must also be recognized that poor access health care is not only found in our prison system. It is perpetuated throughout each stage of life and leads to unstable households, adverse childhood events, unemployment, mental illness, substance use and acquisition of habits that increase risk for cancer (smoking, alcohol use, sexually transmitted infections, injection drug use and its associated infections). Therefore, we must promote screening of cancers in our incarcerated population but also recognize that prevention of patients becoming incarcerated starts with adequate access to health care early in life as well.”

Given the above, I don’t see how you can possible avoid at least some discussion about the health care available to this population. Is screening even available? Is any education provided? Don’t blame this on patient literacy—providers of this population (who have NO choices) have some responsibility for health education. How much does screening cost?

A follow-up study might be to determine if the prisons in the state have any cancer screening guidelines and how these are accessed.

We thank Reviewer #2 for their input and we have revised the manuscript to state: (line 294) – “Current practices for screening in our state’s prison system are unknown, however it is notable that none of the patients diagnosed with colorectal cancer or lung cancer had documented appropriate screenings while incarcerated or were referred to our hospital following a positive result from screening.”

Submitted filename: Response to Reviewers_PLOSone.docx

Click here for additional data file.

14 Jul 2020

PONE-D-19-34040R1

Cancer stage at presentation for incarcerated patients at a single urban tertiary care center

PLOS ONE

Dear Dr. Sunthankar,

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. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

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We look forward to receiving your revised manuscript.

Kind regards,

Sungwoo Lim, DrPH

Academic Editor

PLOS ONE

[Note: HTML markup is below. Please do not edit.]

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 #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 #2: Yes

**********

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

Reviewer #2: I Don't Know

**********

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 #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 #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 #2: Please see comments in attached PFD. I still feel that you lack appreciation for the lack of power that incarcerated people have in terms of accessing health care and for the great power that prison health care providers/system have for addressing providers.

**********

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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 #2: Yes: Patricia J Kelly

[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.]

While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step.

17 Jul 2020

1. Abstract - You are not examining potential delays, you are examining differences in stage at diagnosis. If you were examining potential delays, you would also be looking individual and system level reasons for delay.

We thank reviewer #2 for their input and our manuscript now refers to “differences” instead of “delays.”

2. Page 3, line 45 - At least put that they are not in a position to advocate for themselves first. Really, blaming poor health literacy on the part of prisoners for not getting screened is ridiculous. In almost every situation that I have seen--jails, prisons, county, state, federal, prisoners CANNOT advocate for themselves. I feel as if you are looking at this from only the perspective of a community provider or clinic. I am really trying to be non-judgmental about this but feel as if the whole writing team needs to spend a day shadowing a provider inside of a facility.

We thank reviewer #2 for their input and agree that these patients are unable to advocate for themselves while incarcerated and this is of great importance. We aimed to summarize the sparse research on etiologies of decreased screening, and did not intend to characterize differences in cancer staging as primarily a failure on the part of the incarcerated patient. The study team has extensive first-hand experience working with incarcerated populations. We agree that they are often limited by what they have available and often there are constrictions on practitioners ability to truly practice standard-of-care medicine with appropriate treatment of conditions (i.e. chemotherapy, hepatitis C treatment), let alone screening for these conditions and other preventative care. We have changed our introduction to now state: “Incarcerated patients (IP) face both systemic barriers to care as well as vulnerability due to impediments to self-advocating due to their status as an inmate. Both these issues may delay or limit their receipt of treatments that – outside the prison system – are more often given, such as direct-acting anti-viral agents for hepatitis C infection and opioid maintenance therapy for substance use disorders.”

We have also removed a reference to lower health literacy that was on lines 92-94.

We have updated the sentence (line 99-101) to say the following “Together these studies have highlighted that IP are less likely to receive the appropriate screenings compared to the general population.”

3. Page 4, line 84 - So many qualifiers. Decreased availability, likely, also contribute. Just say it. Lack of availability contributes to lack of screening.

We have streamlined our introduction to now state: “Multiple reasons for decreased screenings among patients who are currently or previously incarcerated have been suggested, including poorer connection with primary care resources and lack of availability while incarcerated and following incarceration due to systemic barriers patients who were previously incarcerated also face.”

4. Page 14, line 284 - Encourage? Direct routine screening

We agree and have changed “encourage” to “direct” as recommended.

Submitted filename: Response to Reviewers v2.docx

Click here for additional data file.

28 Jul 2020

Cancer stage at presentation for incarcerated patients at a single urban tertiary care center

PONE-D-19-34040R2

Dear Dr. Sunthankar,

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,

Sungwoo Lim, DrPH

Academic Editor

PLOS ONE

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 #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 #2: Yes

**********

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

Reviewer #2: I Don't Know

**********

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 #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 #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 #2: Thanks for your changes. I feel strongly that we cannot only serve as the health care providers for this population, but must also acknowledge the systemic factors that contribute to their poor health outcomes.

**********

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.

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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 #2: No