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Keywords:

  • diagnosis;
  • prostate cancer;
  • socioeconomic status;
  • survival treatment

Abstract

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgements
  7. Conflict of Interest Disclosures
  8. References

BACKGROUND:

The objective of the current study was to evaluate the impact of socioeconomic disparities on prostate cancer presentation, treatment, and prognosis in Geneva, Switzerland, in which healthcare costs, medical coverage, and life expectancy are considered to be among the highest in the world.

METHODS:

This population-based study included all patients diagnosed with invasive prostate cancer among the resident population between 1995 and 2005. Patients were divided into 3 socioeconomic groups according to their last known occupation. Compared were patient and tumor characteristics and treatment patterns between socioeconomic groups. Cox multivariate regression analysis was used to assess and explain socioeconomic inequalities in prostate cancer-specific mortality.

RESULTS:

Compared with patients of high socioeconomic class, those of low socioeconomic class were more often foreigners, were found less frequently to have screen-detected cancer, were found to have a more advanced stage of disease at diagnosis, and less often had information regarding disease characteristics and staging. These patients underwent prostatectomy less frequently and were more often managed with watchful waiting. The risk of dying as a result of prostate cancer (hazards ratio [HR]) in patients of a low versus high socioeconomic status was increased 2-fold (95% confidence interval [95% CI], 1.5-2.6). After adjustment for patient and tumor characteristics and treatment, the mortality risk was no longer found to be significantly increased (HR, 1.2; 95% CI, 0.8-1.6).

CONCLUSIONS:

In the current study, patients of low socioeconomic class were found to be at increased risk of dying as a result of their prostate cancer. This increased mortality is largely attributable to delayed diagnosis, poor diagnostic workup, and less invasive treatments in these individuals. Cancer 2009. © 2009 American Cancer Society.

Cancer patients with low socioeconomic status (SES) have an increased risk of dying as a result of their disease compared with the risk in patients of higher SES.1, 2 This association has been established for several other cancer sites, such as the breast, cervix, colon, etc.3-6

SES plays an important role in prostate cancer. Higher SES has been associated with more frequent PSA screening,7, 8 a lower stage of disease at diagnosis, and better tumor differentiation.9, 10 With regard to prostate cancer survival, results are not always consistent. Previous studies have reported both positive association10, 11 and no association between SES and prostate cancer-specific survival.12-14

Access inequalities to appropriate care and therapy as well as differences in tumor biology are possible explanations for survival differences between SES classes.

Inconsistent or inadequately measuring of socioeconomic factors may affect conclusions regarding the relation between SES and health outcomes, and this appears to be particularly true when other strong determinants of survival, such as race/ethnicity, complicate establishing the true association.15 Many previous studies regarding SES and prostate cancer mortality are from North America, particularly from the United States, in which the area code generally is used as surrogate of individual level of SES.8, 9, 12, 13, 16, 17 In addition, SES measures may have different meanings in different populations.15 Furthermore, to our knowledge, few studies to date have evaluated factors impacting social disparities in prostate cancer mortality, such as differences in screening, disease stage at diagnosis, tumor characteristics, and treatment.1, 13, 18

To the best of our knowledge, no studies are currently available regarding disparities and prostate cancer mortality in Switzerland, a country with an extremely well-developed healthcare system19, 20 Medical insurance is compulsory for all residents. The cost for this compulsory insurance package amounts to approximately 350 euros per month per person. The Swiss government covers the complete medical insurance fees for indigent individuals (approximately 10%of the population) and covers between 5% and 25% of the insurance fees for people with low income (approximately 17% of the population). The basic insurance package covers universal access to preventive and therapeutic care as well as pharmaceuticals. It has been estimated that <3% of the population is not insured.21 The main supplementary health insurance policies, known as private and semi-private, cover additional benefits not covered by compulsory health insurance (ie, free choice of hospital physician and superior levels of hospital accommodation). Approximately 25% of the population has 1 of the main forms of supplementary health insurance.

In the current study, we evaluated the effect of SES on presentation, screening, tumor characteristics, treatment, and survival in prostate cancer patients in a population-based cohort of men diagnosed in Geneva, Switzerland.

MATERIALS AND METHODS

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgements
  7. Conflict of Interest Disclosures
  8. References

We used data from the Geneva Cancer Registry (Geneva, Switzerland), which records all incident cancers occurring in the population of the canton (approximately 465,000 inhabitants in 2007). All hospitals, pathology laboratories, and practitioners are requested to report all cancer cases. Trained registrars systematically abstract data from medical and laboratory records. Physicians regularly receive questionnaires to obtain missing data. Recorded data include sociodemographic variables, method of detection, prostate-specific antigen (PSA) level at the time of diagnosis, tumor characteristics (including histology, differentiation based on tumor grade, and Gleason score), stage at diagnosis according to the TNM classification, lymph node status, treatment, survival status, and cause of death. The registry regularly assesses survival data. The index date was the date of confirmation of diagnosis or the date of hospitalization if it preceded the diagnosis and pertained to the disease. Active follow-up is performed yearly using the files of the Cantonal Population Office, which is in charge of registration of the resident population. Trained registrars establish cause of death by systematically consulting clinical records, interpreting questionnaires completed by the patient's physician, or both.

Between January 1, 1995, and December 31, 2005, a total of 2865 men were diagnosed with prostate cancer in the resident population. We excluded 76 men with prostate cancer diagnosed at the time of death and 51 men for whom information regarding SES was missing. The final cohort included 2738 patients.

The Geneva Cancer Registry systematically retrieves the patient's most recent occupation from the files of the Cantonal Population Office. We used the classification of vital statistics, which includes 12 major groups subdivided into 40 submajor groups and 130 minor groups.22 Occupational subgroups were classified into SES indicators on 7 levels based on the Social Classes of the British Registrar General.23 For the purpose of the current study, we regrouped SES into 3 levels only: low (manual employees and skilled and unskilled workers, including farmers), middle (nonmanual employees and clerks), and high (professionals, executives, administrators, and entrepreneurs).24

For this study, variables of interest were age, nationality (Swiss vs other), period of diagnosis (1995-1999 vs 2000-2005), and sector of care (public vs private). We classified the method of detection as screening (by PSA with or without digital rectal examination) and other (including fortuitous discovery during treatment for other diseases and after symptoms). Tumor stage was based on the TNM classification system. We used pathologic stage, or when absent, clinical stage. Tumors were classified as T1 (clinically unapparent tumor not palpable or visible by imaging), T2 (tumor confined within the prostate), T3 (tumor extends through the prostate capsule with or without invasion of the seminal vesicles), T4 (tumor is fixed or invades adjacent structures), and TX (unknown). Lymph node invasion was classified as N0 (no regional lymph node metastasis), N1 (regional lymph node metastasis), and NX (unknown) and distant metastasis as M0 (absent), M1 (present), or MX (unknown). Differentiation was classified as grade 1 (well-differentiated: Gleason score of 2-4), Grade 2 (moderately differentiated: Gleason score of 5-6), Grade 3 to 4 (poorly differentiated, undifferentiated: Gleason score of 7-10), and unknown.25

Stage was classified in 5 groups: stage I (T1a and N0 and Gleason score 1), stage II (T1a and N0 and Gleason score 2-4; or T1a or T1b, or T1 or T2 and N0 and any Gleason score), stage III (T3 and N0 and any Gleason score), stage IV (T4 and N0 and any Gleason score, or any T and N1 and any Gleason score, or any T and any N and M1 and any Gleason score), and unknown.26

Treatments given during the first 6 months after a diagnosis of prostate cancer included prostatectomy (radical, retropubic, or perineal), hormonal treatment (surgical or hormonal castration), and external radiotherapy (with or without hormonal therapy). Brachytherapy was not used during the study period. Watchful waiting was comprised of active follow-up of the patient and treatment only in the case of disease progression. We did not consider transurethral prostate resection as surgical treatment for prostate cancer.

Differences between SES levels were tested with the chi-square test. Follow-up of patients was completed on December 31, 2006. We calculated cumulative disease-specific survival rates by Kaplan-Meier analysis and tested survival differences with the log-rank test. We evaluated the impact of SES on disease-specific survival by multivariate Cox proportional hazards analysis, adjusting for age (in continuous), period of diagnosis (in continuous), method of detection, lymph node status, tumor stage, differentiation, sector of care, and treatment. To evaluate to what extent patient and tumor characteristics, method of detection, treatment, and sector of care explained the socioeconomic differences in prostate cancer survival, we gradually entered the factors in the Cox model. Analyses were performed using SPSS statistical software (version 15; SPSS Inc, Chicago, Ill). All P values <.05 were considered statistically significant.

RESULTS

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgements
  7. Conflict of Interest Disclosures
  8. References

Table 1 shows the demographic and tumor characteristics of the study population. There were 839 men of low SES (30.6%), 1173 of middle SES (42.8%), and 726 of high SES (26.5%). Men of low SES were older at the time of diagnosis, more likely to be foreigners, were less frequently diagnosed by screening, and underwent treatment more often in the public sector. They presented with a higher tumor grade and more advanced stage of disease at the time of diagnosis than men of middle or high SES. They had also less information regarding tumor characteristics and stage of the disease. However, the proportion of patients with an unknown Gleason score/grade was high: approximately 10%, for all the SES levels. Men of low SES underwent prostatectomy less often and were more frequently managed by watchful waiting. The treatment differences by SES also remained significant when stratifying by stage of disease at diagnosis. In particular, in the group of patients with early stage disease, the proportion of men who underwent surgery was 56% in the high SES group, 52% in the middle SES group, and 47% in the low SES group (P value for Pearson chi-square = .023).

Table 1. Patient and Tumor Characteristics, Method of Detection, Sector of Care, and Treatments According to Socioeconomic Status Among Men With Prostate Cancer (Geneva 1995–2005)
CharacteristicsSocioeconomic StatusP
Low No. (%)Middle No. (%)High No. (%)
All patients839 (30.6)1173 (42.8)726 (26.5) 
Mean age at diagnosis, y71.369.368.9.000
Nationality   .019
 Swiss448 (61.7)795 (67.8)535 (63.8) 
 Other278 (38.3)378 (32.2)304 (36.2) 
Period of diagnosis   .268
 1995-1999290 (39.9)425 (36.2)316 (37.7) 
 2000-2005436 (60.1)748 (63.8)523 (62.3) 
Method of detection   .000
 Screening351 (48.3)724 (61.7)529 (63.1) 
 Symptoms207 (28.5)265 (22.6)177 (21.1) 
 Other168 (23.1)184 (15.7)133 (15.9) 
Sector of care   .000
 Private368 (50.7)801 (68.3)635 (75.7) 
 Public358 (49.3)372 (31.7)204 (24.3) 
Stage of disease   .006
 I-II322 (44.4)613 (52.3)435 (51.8) 
 III177 (24.4)282 (24.0201 (24.0) 
 IV146 (20.1)176 (15.0)125 (14.9) 
 Unknown81 (11.2)102 (8.7)78 (9.3) 
Lymph node invasion    
 No360 (49.6)689 (58.7)512 (61.0).000
 Yes44 (6.1)71 (6.1)56 (6.7) 
 Unknown322 (36.7)413 (35.2)271 (32.3) 
Gleason grade   .040
 Well-differentiated (Gleason 2-4)51 (7.0)887 (7.4)68 (8.1) 
 Moderately differentiated (Gleason 5-6)290 (39.9)549 (46.8)395 (47.1) 
 Poorly or undifferentiated (Gleason 7-10)306 (42.1)428 (36.5)302 (36.0) 
 Unknown79 (10.9)109 (9.3)74 (8.8) 
Type of treatment   .001
 Prostatectomy253 (34.8)474 (40.4)382 (45.5) 
 Radiotherapy141 (19.4)246 (21.0)141 (16.8) 
 Hormonal therapy100 (13.8)116 (9.9)79 (9.4) 
 Watchful waiting164 (22.6)245 (20.9)180 (21.5) 
 Other68 (9.4)92 (7.8)57 (6.8) 

After a median follow-up of 3.9 years (range, 4 days-12 years), 1730 patients (63%) were still alive, 840 (31%) had died (385 of prostate cancer), and 168 (6.1%) were lost to follow-up. The 5-year cumulative survival rate for prostate cancer was 88% (95% confidence interval [95% CI], 84-92%) among men of high SES, 84% (95% CI, 82-86%) among men of middle SES, and 77% (95% CI, 73-81%) among men of low SES (P value for log-rank test <.001). Subgroup analysis by stage indicated that SES differences in prostate cancer mortality were present only among patients with advanced stage disease; among those patients diagnosed at stage III to stage IV, the 5-year survival rates of men in the high, middle, and low SES groups were 53% (95% CI, 41-65%), 39% (95% CI, 29-49%), and 27% (95% CI, 17-37%), respectively (P value for log-rank test = .019). No differences were observed for patients with stage I to II disease (P value for log-rank test = .124) (Fig. 1).

thumbnail image

Figure 1. The 5-year overall prostate cancer-specific cumulative survival according to socioeconomic level is shown (Geneva, 1995-2005) in (a) the overall cohort, (b) patients with stage I through stage II prostate cancer, and (c) patients with stage III through stage IV prostate cancer.

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Unadjusted Cox analysis demonstrated that patients in the low SES group had a significantly higher risk of death from prostate cancer than patients in the high SES group (crude hazards ratio [HR], 2.0; 95% CI, 1.5-2.6 [P < .001]) (Table 2).

Table 2. Unadjusted and Adjusted Prostate Cancer-Specific Mortality Risk According to Patient Characteristics, Period, Sector of Care, and Tumor Characteristics (Geneva 1995–2005)
 Unadjusted HR95% CIMultiadjusted HR*95% CI
  • HR indicates hazards ratio; 95% CI, 95% confidence interval.

  • *

    Multivariate analysis adjusted for age, socioeconomic status, nationality, period of diagnosis, method of detection, sector of care, clinical stage of disease, grade, and type of treatment.

  • P < .001.

  • Reference value.

  • §

    P < .01.

  • P < .05.

  • With or without hormonal therapy.

Age at diagnosis (continuous)1.111.10-1.121.031.0-1.1
Socioeconomic status    
 High1.0 1.0 
 Middle1.31.0-1.71.10.8-1.6
 Low2.01.5-2.61.20.9-1.7
Nationality    
 Swiss1.0 1.0 
 Other1.81.4-2.41.20.9-1.6
Period of diagnosis (continuous)0.910.87-0.941.00.94-1.02
Method of detection    
 Screening1.0 1.0 
 Symptoms8.86.5-123.12.2-4.4
 Other5.33.7-7.52.31.5-3.5
Sector of care    
 Private1.0 1.0 
 Public2.72.1-3.31.5§1.1-2.0
Stage of disease    
 I-II1.0 1.0 
 III1.9§1.2-3-11.30.8-2.2
 IV2618-377.04.6-11
Gleason grade    
 Well-differentiated (Gleason 2-4)1.0 1.0 
 Moderately differentiated (Gleason 5-6)1.90.7-5.33.41.0-11
 Poorly or undifferentiated (Gleason 7-10)114.1-298.12.5-26
 Unknown2911-79123.6-38
Type of treatment    
 Prostatectomy1.0 1.0 
 Radiotherapy1.71.0-2.81.60.9-2.7
 Hormonal therapy4.73.1-7.12.61.6-4.1
 Watchful waiting1711-252.61.7-4.2
 Other117.1-171.71.1-2.8

After adjustment for age, sector of care, method of detection, stage of disease, tumor grade, and treatment (all independent and significant determinants of prostate cancer-specific mortality), low SES was no longer found to be significantly associated with prostate cancer-specific mortality (adjusted HR, 1.2; 95% CI, 0.8-1.6) (Table 2).

Table 3 shows the modification of prostate cancer-specific mortality risk after stepwise adjustment for other prognostic factors. The excess mortality risk associated with a low SES diminished but remained statistically significant after adjustment for sociodemographic patient characteristics such as age, period of diagnosis, and nationality, and for tumor characteristics such as stage and grade. Compared with men of high SES, the multiadjusted HR was 1.3 for men of middle SES (95% CI, 0.9-1.7) and 1.4 for men of low SES (95% CI, 1.0-2.0) (P = .031). After further adjustment for method of detection, the risk of death from prostate cancer for patients of low SES was still higher than for patients of high SES, although the difference was not significant (HR, 1.4; 95% CI, 1.0-1.9 [P = .054]). Adjustment for type of treatment and sector of care further reduced the excess risk of mortality among patients of low SES (Table 3). Subgroup analysis by stage confirmed that the excess mortality was limited to patients with stage III through IV disease, with a crude HR of 1.8 (95% CI, 1.3-2.5; P = .001) for the low SES group. Then again, adjustment for tumor and patient characteristics, screening, sector of care, and treatment lowered the risk, which then became not statistically significant (HR, 1.2; 95% CI, 0.8-1.7 [P = .401]).

Table 3. Risk (HR) of Dying as a Result of Prostate Cancer According to Socioeconomic Status After Progressive Adjustment on Other Putative Explanatory Factors (Geneva Cancer Registry, 1995–2005)
Socioeconomic LevelNo.DeathsUnadjusted HRHR Adjusted for Age, Period of Diagnosis, and NationalityHR Additionally Adjusted for Stage and Grade of DiseaseHR Additionally Adjusted for Method of DetectionHR Additionally Adjusted for Sector of Care and Treatment
  • HR indicates hazards ratio.

  • *

    Reference value.

  • P < .001.

  • P < .05.

High*8397111111
Middle11731261.3 (1.0-1.7)1.2 (0.9-1.6)1.3 (0.9-1.8)1.3 (0.9-1.8)1.1 (0.8-1.5)
Low7261122.0 (1.5-2.6)1.5 (1.1-2.0)1.4 (1.0-2.0)1.4 (1.0-1.9)1.2 (0.8-1.6)
P value for Wald test .000.043.094.141.667

DISCUSSION

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgements
  7. Conflict of Interest Disclosures
  8. References

Despite the high quality of and widespread access to medical care in Geneva, Switzerland, the results of the current study demonstrate that prostate cancer patients of low SES have a 2-fold increased risk of death from their disease compared with prostate cancer patients of high SES. Socioeconomic discrepancies in prostate cancer mortality were limited to patients with an advanced stage of disease at the time of diagnosis. However, differences in PSA screening, tumor characteristics, treatment, and sector of care almost completely explain the increased mortality observed among patients of low SES.

In Geneva, prostate cancer patients of low SES were older, and presented with a higher tumor grade and more advanced stage of disease at the time of diagnosis than patients of high SES. This might be the consequence of a lower awareness regarding PSA screening and prostate cancer warning signs among patients of low SES. However, less health conscious behavior, in terms of the underutilization of preventive services, may have played a role as well. Prostate tumors can be detected early through PSA screening, and it has been well documented that SES affects access and utilization of PSA screening.7, 8, 16 Indeed, in our study, approximately 63% of prostate cancers diagnosed among men of high SES are detected through screening compared with 48% for men of low SES. The results of the current study are consistent with previous studies reporting that men from higher social classes are more likely to be diagnosed with localized disease8, 10, 13, 27 and that lower SES is associated with a lower likelihood of undergoing PSA testing.7 Although evidence that prostate cancer deaths are reduced by PSA screening is insufficient, its use may still serve as a marker of delivery of care.

We also observed a high proportion of patients with unknown Gleason score/grade, who had an extremely higher risk of dying from prostate cancer. These patients were older (>52% were aged ≥80 years at the time of diagnosis) and tended not to receive surgery as treatment for their prostate cancer (only 6.5% underwent surgery, whereas 49% were managed by watchful waiting and 33% by hormonal therapy only). This finding reveals a tendency not to perform a biopsy or initiate an aggressive treatment because of the older age of the patient and possible presence of comorbidities, which in turn may explain the extremely high risk of dying from prostate cancer noted in this population. The majority of these cases were relative to the period 1995 through 2000 (63.3%) and, with time, we observed a trend toward a decrease in the proportion of patients without available tumor grade.

In the current study, men of low SES tended to receive treatment with curative intent, such as surgery or radiotherapy, less often and were more often managed by watchful waiting. The differences in treatment were not explained by differences in the stage of disease at the time of diagnosis, because they persisted when considering only patients with early stage prostate cancer. This result confirms the findings of other studies reporting that men with lower SES were less likely to be treated at all, and that men with a lower educational level were less likely to undergo prostatectomy and more likely to receive radiotherapy.17, 28, 29

With regard to prostate cancer-specific survival and SES, we found an 11% unadjusted survival difference between men of low versus high SES. The excess mortality risk associated with low SES remained significant, even after adjusting for tumor characteristics at diagnosis. The excess mortality risk disappeared when we introduced method of detection, sector of care, and treatment into the Cox model, suggesting that SES differences in prostate cancer-specific mortality are largely attributable to socioeconomic differences in diagnosis and treatment. Although the evidence base for the benefits of screening and treatment options is not yet fully developed for prostate cancer, PSA screening with or without digital rectal examination and curative treatments such as prostatectomy and radiotherapy have been shown to be major determinants of outcome.13, 30-33 Lead time and length time biases linked to early detection through PSA screening may partially explain the survival advantage observed among patients with a high SES. However, we found that the differences based on SES in prostate cancer mortality were limited to patients with advanced disease, for whom the impact of such biases is definitively less strong; on the contrary, the choice of treatment most likely plays a more important role. One likely reason why the effect of social inequalities in treatment is more important in patients with later stage disease than in those with early stage disease is because of the much higher mortality burden of stage III through IV prostate cancers.

The association between SES and prostate cancer survival has been demonstrated in previous studies.10-14 In the majority of them, SES remained an independent determinant of mortality even after adjustment for clinical and treatment factors, indicating a residual effect not explained by differences in the healthcare received.3, 30, 33, 34 However, a great heterogeneity exists among the SES indicators used and the variables chosen to adjust for confounding and that may explain the divergence with the results of the current study. Furthermore, in studies in which access to healthcare was considered to be equivalent among men of different SES, no association has been observed.12, 14

The results of the current study are derived from population-based cancer registry data covering all incident cases of prostate cancer in the canton of Geneva. No inclusion restrictions were made. The follow-up was prospectively determined and complete for 94% of the study population, and cause of death was ascertained for 94% of the persons who died. SES was assessed at the individual level. Furthermore, we had complete information regarding therapy. In addition, the study population was relatively uniform in terms of ethnicity, leaving little room for confounding by ethnicity.

We realize that, despite detailed information regarding patient and tumor characteristics and treatment, there is still room for residual confounding associated with unrecorded prognostic factors, such as surgical margin status, type and dose of radiotherapy, and the patient's compliance with treatment. Evidence also indicates that a single measure of SES is of limited information and that other unmeasured socioeconomic factors may affect conclusions regarding the particular health outcome and population of interest.15 The patient's most recent occupation as registered at the Cantonal Population Office was the only measure of SES available for the current study and, although collected at an individual level, it may not be sufficient to capture the multidimensional nature of SES. However, studies conducted in Europe have repeatedly found strong correlations between occupational status using a similar classification as ours and diverse health indicators, even after controlling for other commonly used socioeconomic measures such as education and income.15 In addition, we had no information available regarding comorbidities, which could influence not only general but also prostate cancer-specific mortality, because comorbidities may influence choice of treatment, compliance, or host response to tumor. However, adjustment for comorbidities in previous large, population-based studies resulted in nearly no differences in HR estimates of overall mortality.13

In conclusion, we observed strong disparities with regard to access to care and treatment of prostate cancer between socioeconomic groups in a country that has 1 of the best equipped healthcare systems in Europe19 and compulsory basic insurance for the entire population. These differences may explain the higher prostate cancer-specific mortality risk associated with low SES. Policies ensuring a more equitable access to screening and treatment are needed to eliminate these disparities.

Acknowledgements

  1. Top of page
  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgements
  7. Conflict of Interest Disclosures
  8. References

We thank Stina Blagojevic for her technical and editorial help and Hyma Schubert and the registry team for their assistance during the investigation.

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  2. Abstract
  3. MATERIALS AND METHODS
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgements
  7. Conflict of Interest Disclosures
  8. References
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