DOI:http://dx.doi.org/10.7314/APJCP.2015.16.18.

8567
Survival Analysis of Breast Cancer Cases in Iran using a Weibull Parametric Model

RESEARCH ARTICLE

Survival Analysis of Patients with Breast Cancer using Weibull

Parametric Model
Ahmad Reza Baghestani1, Sahar Saeedi Moghaddam1,2*, Hamid Alavi Majd1,
Mohammad Esmaeil Akbari2, Nahid Nafissi2, Kimiya Gohari1
Abstract
Background: The Cox model is known as one of the most frequently-used methods for analyzing survival
data. However, in some situations parametric methods may provide better estimates. In this study, a Weibull
parametric model was employed to assess possible prognostic factors that may affect the survival of patients with
breast cancer. Materials and Methods: We studied 438 patients with breast cancer who visited and were treated at
the Cancer Research Center in Shahid Beheshti University of Medical Sciences during 1992 to 2012; the patients
were followed up until October 2014. Patients or family members were contacted via telephone calls to confirm
whether they were still alive. Clinical, pathological, and biological variables as potential prognostic factors were
entered in univariate and multivariate analyses. The log-rank test and the Weibull parametric model with a
forward approach, respectively, were used for univariate and multivariate analyses. All analyses were performed
using STATA version 11. A P-value lower than 0.05 was defined as significant. Results: On univariate analysis, age
at diagnosis, level of education, type of surgery, lymph node status, tumor size, stage, histologic grade, estrogen
receptor, progesterone receptor, and lymphovascular invasion had a statistically significant effect on survival
time. On multivariate analysis, lymph node status, stage, histologic grade, and lymphovascular invasion were
statistically significant. The one-year overall survival rate was 98%. Conclusions: Based on these data and using
Weibull parametric model with a forward approach, we found out that patients with lymphovascular invasion
were at 2.13 times greater risk of death due to breast cancer.
Keywords: Breast cancer - survival analysis - Weibull parametric model - log-rank test

Asian Pac J Cancer Prev, 16 (18), 8567-8571

Introduction In 2012, the three most leading cancers in both sexes

worldwide were lung cancer (13% of the total), breast
Cancer is a general term used for a group of diseases cancer (11.9%) and colorectal cancer (9.7%); the most
that cause abnormal cells to divide without control and common types of cancer in men, respectively, are lung
overpass other tissues. In addition, if they expand out cancer (16.8%), prostate cancer (14.8%) and colorectal
of control, cancer can result in death (American Cancer cancer (10.1%) while in women they are ordered as breast
Society, 2014). Based on GLOBOCAN 2012, an estimated cancer (25.1%), colorectal cancer (9.2%) and lung cancer
14.1 million new cases of cancer and 8.2 million deaths (8.8%) (Ferlay et al., 2014). In spite of the reduction of
from cancer occurred in 2012 in both sexes. Estimation DALYs attributed to neoplasms, in patients with breast
of 5-year prevalent cases in 2012 showed that there were cancer DALYs increased from 167 (95% UI: 162-175)
32.5 million people (adult population) alive from both in 1990 to 174 (95% UI: 167-184) per 100,000 in 2010
sexes who had a cancer diagnosed during the previous (IHME, 2013). According to the most recent estimates for
five years (Ferlay et al., 2014). According to the Global breast cancer, there are 1.67 million new cases and 0.52
Burden of Disease (GBD) study, the estimated rate of million deaths globally (Ferlay et al., 2014). Similar to
Disability-Adjusted Life Years (DALY) attributed to all the global, breast cancer is the first common cancer and
neoplasms in both sexes worldwide was 2,793 (95% UI: the third leading cause of death among Iranian women
2,580-2,985) in 1990, which decreased over the time and (Sadjadi et al., 2005). Also, the age standardized mortality
finally reached 2,736 (95% UI: 2,532-2,889) in 2010 rate of breast cancer among Iranian women increased from
(IHME, 2013). Every one DALY demonstrates the loss 1.40 to 3.52 per 100,000 from 1995 to 2004 (Taghavi et
of one year of healthy life (May et al., 2015). In addition, al., 2012), which indicates the need for making further
7.6% of global DALYs are assigned to the neoplasms progress in care and services which are necessary for
(Murray et al., 2013). patients who suffer from cancer (Bray et al., 2013).

1
Department of Biostatistics, Faculty of Paramedical Sciences, 2Cancer Research Center, Shahid Beheshti University of Medical
Sciences, Tehran, Iran *For correspondence: [email protected]
Asian Pacific Journal of Cancer Prevention, Vol 16, 2015 8567
Ahmad Reza Baghestani et al
In order to evaluate the effectiveness of cares provided and Altman, 2004).
for patients with cancer, especially when the event of Weibull distribution in parametric survival model was
death is under the study, we can use survival analysis. used for multivariate analysis. In this step we used forward
Survival analysis is a set of methods used for analyzing approach. So we added the variable which had the lowest
a non-negative random variable which measures time to value of Akaike Information Criterion (AIC). The AIC,
occurrence of a specific event; the event can be death, which was developed by Hirotugu Akaike in 1974, is a
response to a particular treatment, occurrence, or relapse of measure of the goodness of fit of an estimated statistical
a specific disease, marriage, divorce, birth of children, and model (Akaike, 1974). When none of the remaining
so forth. These methods can describe the relation between
survival and covariates. There are three approaches for Table 1. Clinical, Pathological, and Biological
survival analysis; nonparametric, semi-parametric, and Characteristics in Patients with Breast Cancer
parametric. Cox semi-parametric method is the most Factors Categories No. of patients (%) P-value
common approach which is used by many researchers
because of its fewer assumptions. Among parametric Age at diagnosis
Under 40 yr. 88 20.1 0.005 *
approach, Weibull model is popular and more flexible
40 to 70 yr. 336 76.7
than Cox semi-parametric model.
Over 70 yr. 14 3.2
The Weibull, which was developed by Waloddi Education
Weibull in 1951, comes originally from engineering issues Illiterate 37 8.45 0.004 *
to analyze the survival data (Weibull, 1951); actually, it Elementary school 51 11.64
has been used to predict the proportion of future failures Secondary school 53 12.1
after it has observed a failed process in a given point Diploma 161 36.76
of time (Nelson, 2000). It has a hazard rate which is Academic 136 31.05
either increasing, decreasing, or constant (Klein and Marital
Single 24 5.48 0.2
Moeschberger, 2003). If the hazard rate is constant it will
Married 414 94.52
become exponential. Weibull is the only parametric model
Abortion
which has both proportional hazards and an accelerated Yes 153 34.93 0.72
failure-time representation (Klein and Moeschberger, No 285 65.07
2003). In addition, acceptance of Weibull model can be Breastfeeding
checked via graphical assessment (Kleinbaum and Klein, Yes 381 86.99 0.194
2011). No 57 13.01
Aim of the present study was to apply Weibull model Family history
to investigate the possible prognostic factors that may Yes 124 28.31 0.409
No 314 71.69
have an effect on survival of patients with breast cancer.
Type of surgery
Therefore, the only outcome considered here is survival.
BCS 274 62.56 <0.001 *
MRM 164 37.44
Materials and Methods Lymph node status
N0 198 45.21 <0.001 *
The present study incorporates data from patients who N1 121 27.63
were visited and treated at Cancer Research Center in N2 39 8.9
Shahid Beheshti University of Medical Sciences, Tehran, N3 80 18.26
Iran during 1992 to 2012; the patients were followed Tumor size
T1 111 25.34 <0.001 *
up until October 2014. The patients or patients’ family
T2 242 55.25
members were contacted via phone calls to confirm their
T3 85 19.41
health status (i.e. whether they are still alive or not) and to Stage
fill any gaps in their medical records. We had to exclude I 96 21.92 <0.001 *
some patients because of some reasons, first their medical II 193 44.06
records had incomplete information, second they were III 135 30.82
related to male and third, their cause of death was not IV 14 3.2
breast cancer. Eventually a total number of 438 women Histologic grade
with breast cancer were included in this analysis. Well differentiated 47 10.73 <0.001 *
Moderately differentiated 235 53.65
Univariate analysis was conducted using log-rank
Poorly differentiated 156 35.62
test in order to find the factors that had a significant
Estrogen Receptor
effect on survival time. The log-rank test is the most Positive 288 65.75 0.008 *
commonly-used statistical test in order to compare the Negative 150 34.25
survival distributions of two or more groups (ZAMAN Progesterone Receptor
and PFEIFFER, 2012). The null hypothesis in the log-rank Positive 172 39.27 0.007 *
test is that all survival curves are the same (Kleinbaum Negative 266 60.73
and Klein, 2011), more specifically for each time it Lymphovascular Invasion
calculates the observed number that faced to the event of Positive 312 71.23 <0.001 *
Negative 126 28.77
interest in each group and the number expected if there
were in reality no difference between the groups (Bland * Significant at the 5% level

8568 Asian Pacific Journal of Cancer Prevention, Vol 16, 2015

 DOI:http://dx.doi.org/10.7314/APJCP.2015.16.18.8567
Survival Analysis of Breast Cancer Cases in Iran using a Weibull Parametric Model
between date of cancer diagnosis and date of death due
to breast cancer (for those who died) and date of the last
follow-up (for those who were alive). The proposal of
the present study was approved by the ethical committee
of Shahid Beheshti University of Medical Sciences. The
privacy of participants upheld by the research organizer
and personal information were not included in this study.
The data were analyzed by STATA version 11. Quantitative
results were expressed as mean ± standard deviation. A
P-value lower than 0.05 was defined as significant.

Results

Figure 1. Negative Log of Negative Log Survivor A total number of 438 women with breast cancer were
Function Estimates included in this analysis. The mean of age at the time of
diagnosis was 48.37 ± 10.92 years and patients’ age ranged
from 22 to 84 years. Most of the patients were married
women (94.52 %) and they didn’t have history of breast
cancer in their family (71.69 %). The longest duration
of follow-up was 253 months. A total of 75 (17.12%)
deaths due to breast cancer were observed (non-censored
observations) up to October 2014. Using the life-table
method, the one-year overall survival (OS) rate of this
study population was 98% (95% CI: 97%-99%).
The graph of the -ln(-ln(S(t))) against log of failure
time followed a linear trend which indicated that
Weibull model is appropriate for this data (Figure 1).
The prognostic variables included in the model are age
at diagnosis, level of education, marital status, history of
abortion, history of breastfeeding, family history of breast
Figure 1. Hazard function against survival time cancer, type of surgery, number of metastatic lymph nodes,
tumor size, stage, histologic grade, estrogen receptor,
progesterone receptor, and lymphovascular invasion.
Table 2. Multivariate Analysis of Weibull Parametric In univariate analysis age at diagnosis (p=0.005),
Model with Prognostic Factors level of education (p=0.004), type of surgery (p<0.001),
lymph node status (p<0.001), tumor size (p<0.001),
Factors Categories HR (CI: 95%) P-value stage (p<0.001), histologic grade (p<0.001), estrogen
Lymph node status receptor (p=0.008), progesterone receptor (p=0.007), and
N0 0.18 (0.06 - 0.52) 0.002 * lymphovascular invasion (p<0.001) had a statistically
N1 0.44 (0.21 - 0.91) 0.027 * significant effect on survival time (Table 1).
N2 0.64 (0.33 - 1.25) 0.192 Multivariate analysis with forward approach was used
N3 ** 1
for total clinical, pathological, and biological variables,
Stage
I 0.42 (0.09 - 1.94) 0.268
regardless of whether the variable was found to be
II 0.33 (0.12 - 0.90) 0.030 * significant or not based on the results obtained from the
III 0.45 (0.21 - 0.93) 0.030 * univariate analysis. According to the results of multivariate
IV ** 1 analysis which are presented in Table 2, lymph node status,
Histologic grade stage, histologic grade, and lymphovascular invasion
Well differentiated 0.14 (0.02 - 1.11) 0.063 were statistically significant. Indeed, patients with
Moderately differentiated 0.51 (0.31 - 0.86) 0.011 * lymphovascular invasion positive were 2.13 times more
Poorly differentiated ** 1 at the risk of death due to breast cancer. Moreover, the
Lymphovascular invasion
slope of Weibull model is 1.54 (95% CI: 1.30-1.83) which
Positive 2.13 (1.26 - 3.58) 0.005 *
Negative ** 1
indicates the increasing hazard rate (Figure 2).
* Significant at the 5% level; ** Stands for a control group; HR, Hazard
Ratio; CI, Confidence Interval Discussion
To estimate the survival using multi-explanatory
variables had significant effect, adding variables was variables, researchers are largely interested in Cox
stopped. Univariate and multivariate analyses were carried proportional hazard model more than parametric models.
out based on the clinical, pathological and biological In a review of cancer journals for survival analyses
characteristics of patients. (Altman et al., 1995) it was found that only 5% of all
Survival time was calculated as the time interval studies had checked the underlying Cox’s assumptions.
Asian Pacific Journal of Cancer Prevention, Vol 16, 2015 8569
Ahmad Reza Baghestani et al
Furthermore, in many situations these assumptions do not collected from a single institution and therefore the
hold (Cox and Oakes, 1984) and will result in unreliable findings could not be generalized. Overall, about 80% of
outcomes. Therefore, it is recommended to use parametric our data were censored, therefore, for patients with breast
survival models. These models provide an interpretation cancer who did not experience death during the follow-up,
based on a particular distribution of the time to event cure rate models can be a good choice. Actually in the case
irrespective of proportional hazard assumptions. of long-term survival, cure rate models are better than
Several studies have been conducted on parametric Cox model (Rahimzadeh et al., 2014). So we suggest to
survival models (Sirott et al., 1993; Wilson, 1994; Nardi analyze these survival data using cure models.
and Schemper, 2003; Akram et al., 2007; Pourhoseingholi
et al., 2007; Moghimi-Dehkordi et al., 2008; HAYAT et Acknowledgements
al., 2010; Pourhoseingholi et al., 2011; Ravangard et al.,
2011; Zhu et al., 2011; Alizadeh et al., 2013; Binti Zulkifli It’s notable that the paper is extracted from MSc thesis
et al., 2013; Hashemian et al., 2013; Zare et al., 2013; of Sahar Saeedi Moghaddam in Biostatistics and has been
Vallinayagam et al., 2014). Also, Carroll’s study indicated financial supported by Cancer Research Center in Shahid
that in the analysis of survival data Weibull model can Beheshti University of Medical Sciences. In addition, it
provide a useful, parametric alternative to Cox’s regression deserves that we thank employees of Cancer Research
modeling (Carroll, 2003). Center and appreciate the collaboration of Dr. Maryam
Aim of this study was to assess the relationship Khayamzadeh for her kindly contribution.
between survival of patients with breast cancer and some
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