Clinical Characteristics and Survival of Patients With De Novo Metastatic Prostate Cancer Treated With Androgen Deprivation Therapy and Taxane-based Chemotherapy in Uganda: a Retrospective Cohort Study

doi:10.21203/rs.3.rs-5036307/v1

Background: Prostate cancer is the second most common cancer among men worldwide. Mortality is highest among patients in resource-limited settings, in part due to late-stage disease. Among patients with metastatic prostate cancer (mPCa), studies have shown significant improvement in overall survival with the use of androgen deprivation therapy (ADT) and taxane-based chemotherapy. However, outcome data among patients treated with chemo-endocrine therapy are scarce in many resource-limited settings (RLSs). The aim of this study was to determine the clinical characteristics and 5-year overall survival (OS) of patients with de novo mPCa treated at the Uganda Cancer Institute (UCI).

Methods: A retrospective cohort study was conducted between 2015 and 2019, and the data of patients with histologically confirmed prostate cancer and radiological evidence of metastasis were reviewed. Data on clinical and laboratory characteristics, overall survival, and predictors of survival were extracted. P<0.05 was considered to indicate statistical significance.

Results: A total of 300 patients were enrolled over the 5-year study period. The median age was 68 (IQR 61.5-74) years. At presentation, lower urinary tract symptoms were reported in nearly all patients (96.7%, n=290), and 40% (n=120) of patients had grade 5 histological scores. In addition to receiving ADT, the majority of patients (70.3%, n=211) received at least 6 cycles of chemotherapy. Overall survival at one year was 92.4% (95% CI: 88.6%-94.9%), but it declined to 45.2% (95% CI: 36.8%-53.2%) at 5 years. A high Gleason score, the presence of visceral metastasis and receiving <6 cycles of chemotherapy were predictors of poor outcomes.

Conclusion: Patients with de novo mPCa in Uganda present with high histologic grades and high baseline PSA levels but have improved 5-year overall survival with a combination of chemotherapy and ADT as a first-line treatment. We recommend interventions to reduce late presentation and prospective studies to evaluate treatment efficacy in this population.

prostate cancer

metastasis

androgen deprivation therapy

chemotherapy

Prostate cancer is the second most commonly diagnosed cancer among men globally and the most common cancer among men in Africa¹. Although the current burden of cancer is enormous worldwide, the number of cases of prostate cancer are further predicted to more than triple by 2040², in part due to an aging population and economic growth³. In Uganda, the incidence of prostate cancer is estimated to increase by 5.2% annually, the highest rate recorded for any cancer in the country^4,5. Although prostate cancer is a seemingly similar disease, the age-standardized incidence rate of prostate cancer is highest in Europe, but the age-standardized mortality rate is highest in Africa, suggesting that men of African descent have more aggressive disease and worse prognoses than their Caucasian counterparts, although the underlying mechanisms are poorly understood.

A number of studies in Uganda have shown that approximately 90% of patients who require appropriate treatment present with advanced disease^6,7, but few studies have investigated the outcomes of this group of patients. The standard of care for metastatic castrate-naïve prostate cancer patients is continuous ADT plus taxane-based chemotherapy. This was evidenced by a meta-analysis of a number of trials^8–10 that showed a statistically significant reduction in the risk of death among patients with metastatic prostate cancer who were treated with ADT combined with docetaxel. According to these studies, many international guidelines recommend chemohormonal therapy for metastatic hormone-sensitive prostate cancer. The purpose of our study was to evaluate the survival of patients with de novo metastatic prostate cancer in Uganda who received treatment in the era of combination taxane-based chemotherapy and ADT as first-line treatment and to determine the predictors of their survival.

Study design and setting

This was a retrospective cohort study. This study was conducted at the Uganda Cancer Institute (UCI). The UCI is a comprehensive national cancer referral center, and the East Africa Center of Excellence in Oncology receives approximately 4,000 new cancer patients annually and approximately 20 new prostate cancer patients per month. The Cancer Institute has a records department where patient charts are stored according to histological diagnosis, and each patient is assigned a unique identifier.

Inclusion criteria and sampling procedure

Patients who were admitted to the UCI from January 2015 to December 2019 with a documented histological diagnosis of prostate cancer, radiological evidence of metastasis and receiving a combination of taxane-based chemotherapy and ADT were included in the study.

Purposive sampling: All patients who fulfilled the inclusion criteria were purposively included in the study.

Sample size estimation

The sample size was estimated using Stata/IC 16.0, power analysis for the Cox proportional hazards model, a one-sided test, adjusting for censoring; power=80%, significance level=0.05, hazard ratio=1.2, standard deviation=0.842, N=263

The estimated sample size for Cox PH regression was 263 participants.

Study variables

For each chart, we extracted data on demographics, comorbidities, baseline laboratory parameters, treatments received and vital status (alive, dead and lost to follow-up). The demographic variables included age at diagnosis with cancer and region of residence in Uganda. Clinical characteristics included patient comorbidities, ECOG status, symptoms at presentation and Gleason score grouping. The laboratory characteristics included histology grade, baseline PSA levels, white blood cell (WBC) counts, and hemoglobin levels.

Data collection

The patient register at the UCI records office was used to identify all patients with prostate cancer during the study period. The following data were extracted using a pretested data abstraction form: patient demographics, clinical symptoms at presentation, comorbidities, physical exam findings, diagnostic tests, treatments received and overall outcomes. PSA levels (ng/ml) at diagnosis were grouped into <100 and ≥100. The Gleason score was grouped into low grade, intermediate grade and high grade. Low/intermediate scores were categorized as a total score of 6, 7 or 8. A high Gleason score was categorized as a total score of 9 or 10. We determined the vital status of patients by follow-up phone calls and by recording the date of death for those in whom death was documented in their charts or through death certificates. The date of last contact (e.g., hospital visit or follow-up phone calls) for patients who were alive during the follow-up period (i.e., censoring) was recorded. Patients who could not be reached by phone calls or who did not have records of vital status in their charts were defined as lost to follow-up.

Data Analysis

The data were analyzed using Stata/IC 16.0. Numerical data were summarized using frequencies, percentages, means (± standard deviations) for normally distributed continuous data or medians (interquartile ranges) for continuous but skewed variables. The biochemical response (TPSA) of patients with mPCa treated with ADT and docetaxel was calculated as the proportion of patients with a PSA concentration ≤4.0 ng/mL according to the 95% confidence interval. The Kaplan‒Meier method was used to estimate overall survival with 95% confidence intervals (95% CIs) at 1, 3 and 5 years. Survival time was defined as the time from the diagnosis of mPCa to death. Cox proportional hazards regression was applied to estimate mortality hazard ratios (HRs) with 95% confidence intervals (CIs). Variables with P <0.2 in univariable models were selected for multivariable models. All tests were two-sided. The multivariate Cox regression model was tested for proportionality using the Schoenfeld residuals. For models that violated the proportionality assumption, we used stratified Cox model analysis. The threshold for statistical significance was set to a two-tailed α < 0.05.

Ethical considerations

This study was conducted in accordance with the ethical principles of the Declaration of Helsinki. The Uganda Cancer Institute Research and Ethics Committee approved the study protocol and provided waiver of consent (approval number UCI-2021-15).

A total of 340 charts were retrieved, 40 of which were excluded. Of the excluded patients, 25 did not have a documented histological diagnosis of prostate cancer, 11 did not have documented radiological evidence of metastasis, and 4 had recurrent disease.

A total of 300 records of adult patients with a confirmed diagnosis of de novo mPCa were included in the study. The median age was 68 years (IQR 61.5-74), and the majority (47.3%, n=142) of patients who self-reported being from the central region of Uganda (26.7%, n=80) were from the western region. Lower urinary tract symptoms were present in nearly all patients (96.7%, n= 290), bone pain was reported in 56.7% (n=170), fracture in 5.7% (n=17) and erectile dysfunction in 5.0% (n=15). Among the documented comorbidities, hypertension was the most common (36.7%, n=110), whereas only 6.7% (n=20) of patients had HIV disease. In this study, half of the patients were symptomatic but fully ambulatory, with an ECOG score of 1 (50.7%, n=152).

According to the analysis, the majority of patients had high histological grades of disease: 40.0% (n= 120) had grade five disease, and 24.0% (n=72) had grade four disease. Lymphovascular invasion and perineural invasion were present in 17.3% (n=52) and 42% (n=126) of patients, respectively. The median TPSA was 414.75 ng/ml (IQR: 100-1273 ng/ml). Bone was the most common site of metastasis, present in 85.3% of patients (n=256). Nonregional pelvic lymph nodes (48.0%, n=144) and visceral metastases were documented in 75 patients (25.0%), and the sites of these metastases included the liver (10.3%, n=31), lung (16.3%, n=49), brain (1.7%, n=5. At initial presentation, 24.3% (n=73) of the patients had anemia, with a hemoglobin level less than 10 g/dl. The median alkaline phosphatase concentration was 210 U/L (normal range 135-150 U/L). Regarding treatment received, 81.3% (n=244) of patients received medical castration with a luteinizing hormone-releasing hormone (LHRH) agonist, whereas 80 (26.7%) received bilateral subcapsular orchiectomy. Seventy percent of the patients (n=211) received 6 or more cycles of docetaxel. Seventy-four patients (21.3%) received radiotherapy to the spine, and 271 (90.3%) patients received bisphosphonates (Supplementary Table 1).

At 5 years following the diagnosis of mPCa, 35 participants were alive, 107 had died, and 158 were censored prior to 5 years of follow-up (median 29.3 months of follow-up). Overall survival was 92.4% (95% CI: 88.6%-94.9%) at one year, 65.9% (95% CI: 59.3%-71.6%) at three years and 45.2% (95% CI: 36.8%-53.2%) at five years. These are shown in Figure 1. According to the multivariate analysis, a high Gleason score (Figure 2), the presence of visceral metastasis (Figure 3) and an elevated WBC count were predictors of poor outcomes among the studied patients (Table 2). Receipt of ≥ 6 cycles of chemotherapy (p≤0.001) with no dose adjustment (p=0.21) was associated with survival benefit (Figures 4 and 5).

Table 1: Baseline demographic characteristics of patients with metastatic prostate cancer during the 5-year study period.

Patient characteristics	Total N=300	Percentage (100%)
Age in Years	Median: 68	IQR 61.5-74.0
43-60 years	66	22.0%
61+	234	78.0%
Region of Origin
Central	142	47.3%
Other	158	52.7%
Comorbidities
Diabetes Mellitus	27	9.0%
Hypertension	110	36.7%
HIV	20	6.7%
Heart Disease	7	2.3%
Deep venous thrombosis	19	6.3%
ECOG
0	23	7.7%
1	152	50.7%
2	83	27.7%
3	42	14.0%
Symptoms at presentation
Bone pain	170	56.7%
Spinal cord compression	47	15.7%
Lower Urinary Tract Symptoms	290	96.7%
Blood in the Urine	52	17.3%
Failure to pass urine	149	49.7%
Lower limb swelling	104	34.7%
Paraplegia/Paraparesis	63	21.0%
Nocturia	277	92.3%
Increased frequency of urination	280	93.3%
Fracture	17	5.7%
Erectile Dysfunction	15	5.0%
Histological Grade
Grade 1	24	8.0%
Grade 2	30	10.0%
Grade 3	31	10.3%
Grade 4	72	24.0%
Grade 5	120	40.0%
Missing	23	7.7%
Treatments received
Luteinizing Hormone Releasing_ Agonist	244	81.3%

Treatment of Bisphosphonates	271	90.3%
Radiotherapy for spine metastasis	64	21.3%
Baseline PSA Category
PSA (≥100 ng/mL)	236	78.7%
PSA (<100 ng/mL)	60	20.0%
≥ 50% Increase of PSA following a reduction	185	61.7%
Laboratory parameters
WBC Normal (4 to 12)	263	87.7%
WBC Reduced (<4)	29	9.7%
WBC Elevated (≥12)	8	2.7%
Hemoglobin ≤ 8 g/dl	28	9.3%
Hemoglobin >8 & ≤10 g/dl	49	16.3%
hemoglobin>10 g/dl	223	74.3%

Table 2. Predictors of overall survival according to univariate and multivariate analyses

	UNIVARIABLE				MULTIVARIABLE
Variable	Haz. Ratio	95% CI		P>\|Z\|	Haz. Ratio	95% CI		P>\|Z\|
ECOG Status
(0-1)	1.0				1.0
(2-3)	1.5	1.05	2.25	0.027	1.2	0.81	1.91	0.309
Signs & Symptoms
Bone pain
No	1.0				1.0
Yes	2.0	1.29	2.96	0.001	1.6	0.93	2.62	0.092
Laboratory parameters at baseline
WBC
Normal (4 to 12)	1.0				1.0
Reduced (<4)	0.3	0.11	0.81	0.018	0.4	0.14	1.11	0.078
Elevated (≥12)	5.1	2.78	9.43	0.000	5.3	2.55	10.97	0.000
Gleason score

Low/Intermediate (6,7 & 8)	1.0				1.0
High (9 & 10)	1.6	1.09	2.40	0.016	1.7	1.13	2.67	0.012
Presence of bone metastasis
No	1.0				1.0
Yes	2.7	1.27	5.76	0.010	2.3	0.97	5.69	0.060
Visceral metastasis
No	1.0				1.0
Yes	2.1	1.38	3.18	0.000	2.5	1.61	3.96	0.000
Presence of Pelvic lymph nodes metastasis
No	1.0				1.0
Yes	0.6	0.42	0.91	0.014	1.0	0.67	1.63	0.842
Number of cycles received
1-5 Cycles	1.0				1.0
≥ 6 Cycles	0.3	0.19	0.43	0.000	0.3	0.21	0.55	0.000
Dose Adjustment
Yes	1.0				1.0
No	1.6	1.08	2.48	0.021	1.3	0.81	2.20	0.259
Baseline PSA
PSA (≥100 ng/mL)	1.0
PSA (<100 ng/mL)	0.9	0.56	1.35	0.546

Reducing cancer-related morbidity and mortality is a global concern. Our study is the first on treatment outcomes among patients with mPCa treated with a combination of ADT and taxane-based chemotherapy as a first-line treatment in Uganda. In this study, we highlight the commendatory benefit of the above combination in patients with metastatic disease at the Uganda Cancer Institute (UCI) and present a high Gleason score, the presence of visceral metastasis and receiving a few doses of chemotherapy as predictors of worse outcomes.

In Uganda, only 20% of cancer patients are reported to reach the UCI, which is located in the central region of the country for care¹¹. In our study, more than half of the patients were from outside the central region, which may have contributed to their late presentation. The baseline PSA level is an independent predictor of death from prostate cancer¹². However, there is controversy regarding the role of PSA screening for prostate cancer; on the one hand, it may lead to overdiagnosis and excess treatment of indolent disease¹³^, but on the other hand, it may delay the presentation of mPCa at onset^14,15. In our study, the median PSA was >400 ng/ml, which is several times greater than that in many RRSs^15,16 but consistent with the high baseline PSA in other sub-Saharan African (SSA) countries^17,18. We found that distant metastasis predicted poor outcomes, which is in agreement with other studies that established that patients with prostate cancer and visceral metastasis have a worse prognosis¹⁹ than those with bone-only metastasis. Therefore, increased access to prostate cancer screening, early diagnosis and treatment in the different regions of the country through the operation of regional cancer centers is recommended.

The use of ADT plus taxane-based chemotherapy in our study showed a significant survival benefit, comparable to the median OS of 57.6 months among patients who received a similar combination in the RRS²⁰. However, recent treatment outcomes for patients with mPCa are lacking for many RLS patients. Prior to 2016, a population-based analysis of 10 sub-Saharan studies showed a 5-year overall survival of only 16% for patients with stage IV prostate cancer²¹. This low survival could have been due to the limited use of ADT and taxane-based chemotherapy among these patients, as this study was carried out before the adoption of such combination treatment as a first-line treatment in many countries. Interestingly, a study in Central Sudan revealed a 37% 5-year OS for patients with distant mPCa despite the lack of use of chemotherapy as a treatment modality in this population²². Notably, one-third of patients in this study were also treated with abiraterone, a factor that might account for the improved survival. We found that patients who received 6 or more cycles of chemotherapy and dose adjustment of chemotherapy were associated with better survival, which was probably attributed to better performance status and reduced treatment toxicity, respectively. In our study, the number of metastatic lesions was not studied; therefore, the disease was not adequately subcategorized as low- or high-volume disease. Additionally, in this study, testosterone level testing was scarce, yet assessment of testosterone levels during ADT is critical for ensuring appropriate treatment of prostate cancer. It is therefore possible that several patients progressed to castrate resistance while on treatment, therefore affecting survival.

The literature suggests that patients of African ancestry have a higher incidence of prostate cancer, transformation rate and mortality from prostate cancer^23–25. This finding is in agreement with many studies in sub-Saharan Africa showing that the majority of patients present to care for or even for screening for advanced or metastatic prostate cancer^17,18,26. Treatment of mPCa is expensive and not widely available in many resource-limited settings; the availability of these medicines at the UCI is therefore highly commendable. Nonetheless, prevention of prostate cancer or a cure for metastatic disease has yet to be identified. As such, prospective local studies to define prostate cancer in this population are of utmost importance in a bid to curb the growing cancer burden, which is highest in LMICs.

In conclusion, among patients with de novo mPCa in Uganda who are treated with taxane-based chemotherapy and ADT, 5-year overall survival is favorable, and the presence of visceral metastasis predicts a worse outcome. We recommend the operation of regional cancer centers in Uganda and prospective treatment studies in prostate cancer patients.

Strengths and limitations

Our study provides useful local cancer epidemiological data that may add to the limited knowledge required for an effective national cancer control program. These findings also inform prospective studies on prostate cancer in resource-limited settings where the majority of patients present with advanced disease. Limitations encountered in our study included its retrospective design, limited subcategorization of disease, and specific factors such as the precise dosage of chemotherapy, compliance with treatment and circumstances at death, among others, which could not be assessed through this chart review study.

UCI: Uganda Cancer Institute

SSA: sub-Saharan Africa

LMICs: Low- and middle-income countries

mPCa: metastatic prostate cancer

OS: Overall survival

PSA: Prostate Specific Antigen

ADT- Androgen Deprivation Therapy

HR- Hazard Ratio

RLS- Resource Limited Setting

LHRH- Luteinizing Hormone Releasing Hormone

ECOG- Eastern Cooperative Oncology Group

CI- Confidence Intervals

IQR- Interquartile Range

WBC- White Blood Cell

Ethical approval and consent to participate

This study was conducted in accordance with the ethical principles of the Declaration of Helsinki. The Uganda Cancer Institute Research and Ethics Committee approved the study protocol and provided waiver of consent (approval number UCI-2021-15).

Consent for publication

Not applicable.

Availability of data and materials

The data sets used and/or analyzed during the current study are available from the corresponding author upon reasonable request.

Funding

This study was supported by the Uganda Cancer Institute and African Development Bank.

Funding.

Competing interests

The authors declare no competing interests.

Author Contributions

AB, FO, BN, EK and OJ contributed towards conception and design of the study. AB and FO contributed towards the provision of study materials or patients. All authors contributed to the collection and assembly of data. KRM contributed to the data analysis, and all authors contributed to the data interpretation. All authors contributed towards manuscript writing. All authors read and approved the final manuscript. All aspects of the work are accountable by all authors

Acknowledgement

The authors acknowledge the Uganda Cancer Institute and Health Professional Education Partnership Initiative for their financial and administrative support.

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No competing interests reported.

Clinical Characteristics and Survival of Patients With De Novo Metastatic Prostate Cancer Treated With Androgen Deprivation Therapy and Taxane-based Chemotherapy in Uganda: a Retrospective Cohort Study

Status:

Journal Publication

Version 1

Abstract

Figures

BACKGROUND

METHODS

Inclusion criteria and sampling procedure

Data Analysis

Ethical considerations

RESULTS

DISCUSSION

Conclusion

Abbreviations

Declarations