OrIGINaL PaPerS - Advances in Clinical and Experimental Medicine

original papers
Adv Clin Exp Med 2013, 22, 3, 369–375
ISSN 1899–5276
© Copyright by Wroclaw Medical University
Barbara Śliwaa–c, Piotr Szelachowskia, c, d, Marta Strutyńska-Karpińskae, f
An Analysis of the Impact of Clinico-Pathological
Features on Long-Term Results Following
Esophagectomy Due to Squamous Cell Carcinoma
of the Thoracic Esophagus
Analiza wpływu wybranych cech kliniczno-patologicznych na wynik
odległy w grupie chorych poddanych resekcji przełyku piersiowego
z powodu płaskonabłonkowego raka
Department and Clinic of Gastrointestinal and General Surgery of Wroclaw Medical University, Poland
A – research concept and design; B – collection and/or assembly of data; C – data analysis and interpretation;
D – writing the article; E – critical revision of the article; F – final approval of article; G – other
Abstract
Background. Squamous cell carcinoma of the esophagus is one of the neoplasms characterized by an exceptionally
latent course, dynamic development and poor prognosis. The stage of the disease at the time of treatment is started
the greatest impact on the long term results.
Objectives. The aim of this study was to evaluate selected clinical-pathological features as prognostic factors for
long term survival among patients who have undergone esophagectomies due to squamous cell carcinoma. The
features analyzed were age, gender, the stage of the disease and the type of tumor. Long-term survival rates (2, 5
and 10 years) were analyzed in relation to the particular features.
Material and Methods. The study group consisted of 65 patients diagnosed with squamous cell carcinoma of the
thoracic esophagus who underwent esophagectomies between 1997 and 2008. The statistical analysis was performed with Statistca 8.0 software. Gehan-Wilcoxon, chi and Kaplan-Meier tests were carried out.
Results. The research did not find any statistically significant correlation between the patients’ gender and survival
time (Gehan-Wilcoxon p = 0.83; log-rank p = 0.86). The results showed no statistically significant correlation
between the patients’ age and survival time (Gehan-Wilcoxon p = 0.75; log-rank p = 0.47). The only statistically
significant impact of the stage of the disease on the survival time was a correlation between the longer survival time
and the stage I and II of the disease (Chi p = 0.15). The log-rank test revealed that survival time is significantly
shorter in cases of involved nodes (Gehan-Wilcoxon p = 0.054; log-rank p = 0.014).
Conclusions. Among the clinical-pathological features investigated, only metastases in regional lymph nodes had
any significant impact on long-term survival (Adv Clin Exp Med 2013, 22, 3, 369–375).
Key words: squamous cell carcinoma of the esophagus, esophagectomy, prognostic factor of long-term survival.
Streszczenie
Wprowadzenie. Płaskonabłonkowy rak przełyku jest zaliczany do nowotworów o wyjątkowo skrytym przebiegu,
dużej dynamice rozwoju i skrajnie niekorzystnym rokowaniu. Faktem jest, że stopień zaawansowania raka przełyku
w chwili podjęcia leczenia operacyjnego ma decydujący wpływ na wynik odległy.
Cel pracy. Ocena wybranych cech kliniczno-patologicznych jako czynnika prognostycznego przeżyć odległych
w grupie chorych po resekcji przełyku z powodu raka płaskonabłonkowego. Analizie poddano takie cechy jak:
wiek i płeć, stopień zaawansowania i zróżnicowania raka oraz prześledzono współzależność przeżyć odległych (2-,
5- i 10-letnich) w odniesieniu do poszczególnych cech.
Materiał i metody. Badana grupa obejmowała 65 pacjentów z rozpoznanym płaskonabłonkowym rakiem piersiowego odcinka przełyku, którzy w latach 1997–2008 byli poddani operacji resekcyjnej. Wykorzystano następujące
testy statystyczne: Statistica 8.0, Gehan-Wilcoxon, Chi, Kaplan-Meier.
370
B. Śliwa, P. Szelachowski, M. Strutyńska-Karpińska
Wyniki. Wykazano brak istotnej statystycznie korelacji między płcią a czasem przeżycia (Gehan-Wilcoxon p = 0,83;
log-rank p = 0,86). Wykazano brak istotnej statystycznie korelacji między wiekiem pacjenta a czasem przeżycia.
(Gehan-Wilcoxon p = 0,75; log-rank p = 0,47). Nie wykazano istotnego statystycznie wpływu stopnia zaawansowania na długość przeżycia, niemniej jednak wyraźnie wykazano korelację między wydłużonym czasem przeżycia
a stopniem zaawansowania 1 i 2 (Chi p = 0,15). Za pomocą testu log-rank wykazano istotną statystycznie zależność
– zajęcie przez komórki nowotworowe węzłów chłonnych skraca czas przeżycia (Gehan-Wilcoxon p = 0,054; logrank p = 0,014).
Wnioski. Biorąc pod uwagę cechy kliniczno-patologiczne wykazano, że jedynie cecha N miała istotny wpływ na
wynik odległy (Adv Clin Exp Med 2013, 22, 3, 369–375).
Słowa kluczowe: płaskonabłonkowy rak przełyku, resekcja przełyku, czynnik prognostyczny przeżyć odległych.
Squamous cell carcinoma of the esophagus
(ESCC) is characterized by an exceptionally latent
course, dynamic development and a particularly
poor prognosis [1–3]. Similar to pancreatic, lung
and liver carcinomas, it has an aggressive course
and unfavorable long term results. In most patients with esophageal cancer, treatment is started
after dysphagia has already been diagnosed, which
implies considerable advancement of the disease.
The basic treatment for esophageal carcinoma is
a radical resection of the esophagus with a twoor three-field lymphadenectomy [4–6]; however,
no proof has been presented so far that two- field
lymphadenectomy is sufficient. It also hasn’t been
proven that three-field lymphadenectomy is the
treatment of choice, i.e., absolutely necessary in
every case [5, 7, 8].
Research by Lee et al. indicates that postoperative chemotherapy applied in squamous cell
carcinoma patients with lymph node metastases
increases the rate of five-year survival after an
esophagectomy [9]. They stated that neo-adjuvant
therapy in patients in advanced stages of the disease allows more radical resections and contributes to longer survival times [6, 10–12].
Lengthy research seeking specific markers that
would allow an early stage of carcinoma to be diagnosed has not been successful.
Due to the increasing number of patients with
carcinoma of the digestive tract and of the esophagus, researchers are investigating the reasons for
unsatisfactory long term survival rates among patients after surgical procedures. The current study
looks at multiple clinico-pathological features,
tissue markers and circulating markers, surgical
methods and multimodal therapy and their impact
on long term survival rates.
The aim of this article is to analyze selected
clinical-pathological features in a group of patients
who underwent surgical resection of thoracic
esophagus because of squamous cell carcinoma,
and to assess the long-term results in relation to
particular features. The features analyzed were
age, gender, the stage of the disease, the depth of
the tumor infiltrate (T) and metastases in regional
lymph nodes (N).
Material and Methods
The research group consisted of 65 patients,
both women and men, diagnosed with histopathologically confirmed thoracic squamous cell
carcinoma, who underwent esophagectomy in the
Clinic of Gastrointestinal and General Surgery at
Wroclaw Medical University (Wrocław, Poland)
between 1997 and 2001. Detailed information
about the research group was obtained from the
clinic’s medical records.
The stage of the disease was assessed according to the TNM Classification of Malignant Tumors, and histopathological data from the resected
esophagus and nodes were taken from the archives
of the Department of Pathological Anatomy at
Wroclaw Medical University. Further information
about the patients was obtained by telephone from
the patients or their relatives in 47 cases (72.3%),
and from in the Lower Silesian regional authorities
in 18 cases (27.7%).
The statistical data were analyzed using Statistica 8.0 software. Log-rank, Gehan-Wilcoxon, chi
and Kaplan-Meier tests were used for the analysis
of the cumulated ratio of survivors, and the Cox
test was used for multivariate analysis. Statistical
significance was set at p < 0.005.
Results
The analysis of age and gender revealed that in
the research group of 65 patients, in which 76.9%
were males, the average age at the time of the resection was 56 years ± 18 years (Table 1).
The patients were divided into two groups:
those under 56 years of age at the time of the resection, and those 56 years of age and older. The
Kaplan-Meier statistical analysis did not reveal any
significant correlation between age of the patient
at the time of the resection and survival time. According to the Gehan-Wilcoxon test, p = 0.75, and
according to the log rank test, p = 0.47. The results
are presented in Figure 1. There were 30 patients
in the group under 56 years of age; 20 died of them
371
Long-Term Results Following Esophagectomy Due to ESCC
Fig. 1. Analysis of survival time relative to age
Ryc. 1. Analiza przeżywalności zależnie od
wieku
Cumulative survival rates
Cumulative survival times according to Kaplan
Complete
Cut
Age:
< 56 years old
≥ 56 years old
Time
Cumulative survival times according to Kaplan
Complete
Cut
Fig. 2. Analysis of survival time relative to
gender
Cumulative survival rates
Fig. 2. Analiza przeżywalności zależnie od płci
females
males
Time
died during the five-year study period and 10 survived. In the group aged 56 and over, there were
35 patients; 26 died and 9 survived.
The Kaplan-Meier statistical analysis did not
reveal any statistically significant correlation between gender and survival time after resection.
This was confirmed by the Gehan-Wilcoxon test
(p = 0.83) and log-rank test (p = 0.86), presented
in Figure 2.
The research group consisted of 50 men, out
of whom 50% survived and 15 women, among
whom 39% survived the five-year study period.
The values are not statistically significant, so gender cannot be considered a useful prognostic factor in ESCC.
The analysis of the stage of the disease stage
revealed that in the group of 65 patients, 42 were
in stage I to IIA of the disease. The 23 patients with
diagnosed metastases in the regional lymph nodes
were already in stage IIB or III (Table 2).
For the statistical analyses, the research group
was divided into subgroups according to the
TNM. Theoretical groups were created: Group 1
– T1N0M), Group 2 – T2N0M0, Group 3 T3N0M0,
Group 4 – T4N0M0, Group 5 – T1N1M0, Group 6
– T2N1M0, Group 7 – T3N1M0, Group 8
– T4N1M0, Group 9 – T3N1M1. Considering the T and N features in the examined material, no one in the research group qualified for
Group 5 (T1N1M0) (Table 2). The survival curves
in Groups 1, 2, 3 and 4 were analyzed separately
from Groups 6, 7, 8 and 9. Significant differences
in the survival times between two group sequences
would relate to the N feature – the involvement of
lymph nodes – which in the case of Groups 1–4
was N0, while in Groups 6–9 it was N1.
Analyzing the T feature – the depth to which
the tumor has infiltrated the esophageal wall – by
the Kaplan-Meier and chi tests revealed no statistically significant correlation between survival time
and the infiltrate depth in the esophageal wall
(p = 0.15).
Despite a lack of statistical significance, there
was a marked tendency for longer survival times
in patients in the early stages of the disease (Figure 3).
372
B. Śliwa, P. Szelachowski, M. Strutyńska-Karpińska
Table 1. Gender and age classification of the study group (n = 65)
Table 1. Płeć i przedziały wiekowe w badanej grupie chorych (n = 65)
Age – years (Wiek – lata)
30–39
40–49
50–59
60–69
70–79
total (%)
Males (Mężczyźni)
(n)
1
7
25
12
5
50
(76.9%)
Females (Kobiety)
(n)
0
3
7
1
4
15 (23.1%)
Total (Suma)
(%)
1
(1.5%)
10
(15.4%)
32
(49.3%)
13
(20%)
9
(13.8%)
65
(100%)
Table 2. The study group classified by the stage of the disease according to the TNM scale
Table 2. Rozkład stopni zawansowania raka w skali TNM
w badanej grupie chorych
Stage of the disease (TNM)
(Stopień zaawansowania
choroby)
The number
of patients
(Liczba pacjentów)
I – (T1N0M0)
3
IIB – (T1N1M0)
0
IIA – (T2N0M0)
18
IIB – (T2N1M0)
9
IIA – (T3N0M0)
20
III – (T3N1M0)
9
III – (T4N0M0)
1
III – (T4N1M0)
4
IV – (T3N1M1)*
1
* This refers to one patient with thoracic esophagus
cancer, in which histopathological examination proved
metastases in the subphrenic lymph nodes.
* IV T3N1M1 dotyczy jednego chorego z rakiem piersiowego odcinka przełyku, gdzie za pomocą badania histopatologicznego preparatu stwierdzono przerzuty w węzłach
chłonnych podprzeponowych (cecha M1).
Feature N was evaluated in two groups: Group
N0 (n = 42) was node negative, and Group N1
(n = 23) was node positive The Kaplan-Meier
analysis in the log-rank test based on cumulative
survival rates showed a statistically significant correlation (p = 0.014) between the presence of metastases in regional lymph nodes and lower survival time, as well as a higher survival time in patients
with node negative carcinoma (Figure 4). The Gehan-Wilcoxon test results were on the threshold of
significance (p = 0.054) confirming the tendency
described above despite the small number patients
in the group. In the N0 group (n = 42), 17 patients
survived; in N1 (n = 23) only 2 patients survived.
The impact of the patients’ gender and age of
patients and the condition of the regional lymph
nodes on the survival times was also analyzed in
the Cox test. The results were similar to the Kaplan-Meier analysis presented above.
In the multivariate analysis considering the
impact of being male (p = 0.99), age under 56 years
(p = 0.52) and the involvement of lymph nodes
(p = 0.012), only node involvement was statistically significant for shortening survival time.
Discussion
The subject of this study was an analysis of the
impact of gender, age, the depth of the tumor infiltration in the esophageal wall (T) and the condition
of the lymph nodes (N) on survival time after a resection. A Kaplan-Meier analysis of survival curves,
log-rank test, Gehan-Wilcoxon test, chi test and
multivariate analysis based on the Cox test showed
that the condition of the lymph nodes has a statistically significant impact on survival time, and that
none of the other variables are significant.
The results obtained regarding the impact of
metastases in the nodes on survival time are the
same as the results reported in the literature on the
subject. A Japanese study from 2008 showed that
node involvement is an independent predictive
factor of relapse after esophagectomy: The authors
found a correlation between shortened survival
time and the presence of metastases in the lymph
nodes [13]. In 2010 Japanese researchers proved
that the number of regional lymph nodes involved
is the most significant prognostic factor in cases
of ESCC, and stated that the depth of infiltration
of the primary tumor is an important factor responsible for the development of metastases in the
nodes [14].
373
Long-Term Results Following Esophagectomy Due to ESCC
Fig. 3. Analysis of survival time
relative to the stage of the disease
Cumulative survival times according to Kaplan
Complete
Cut
Cumulative survival rates
Ryc. 3. Analiza przeżywalności
zależnie od stopnia zaawansowania
group
group
group
group
group
group
group
1
2
3
6
7
8
9
Time
Accumulated proportion of survival time according to Kaplan-Meier
Complete
Cut
Fig. 4. Analysis of survival time
relative to N
Cumulative survival proportion
Ryc. 4. Analiza przeżywalności
zależnie od cechy N
advanced stage 0
advanced stage 1
Time
The recommended treatment in such cases is
the excision of as many lymph nodes as possible at
the time of resection. There are guidelines as to the
exact number of nodes to be removed in relation
to the depth of infiltration of the tumor.
The importance of the oncological condition
of the lymph nodes was also emphasized by Zhang
et al., who indicated that the critical factor in survival time is the involvement of a second lymph
node [15]. This research, however, does not include an evaluation of the impact of the number of
nodes involved because of scarce clinical data and
the retrospective character of the study. An earlier
study by Tachibana et al. indicated that the ratio of
the involved nodes to the number of all examined
nodes is significant only in cases of locoregionalstage esophageal cancer and in cases of diagnosed
metastases in the cervical and ventral nodes [16].
A 2005 study by Kunisaki et al. also indicated that
in ESCC the number of lymph nodes with metastases and the ratio of involved nodes to the number of all examined nodes is a far better prognostic
factor than the anatomical approach used in the
TNM classification system [17]. Many authors
stress the significantly higher prognostic value of
the condition of the lymph nodes as compared to
the stage of involvement according to the TNM
scale [18]. These findings are similar to the current
research, which showed no statistically significant
correlation between local advancement of the tumor and long-term survival. There are also studies
that show the prognostic relevance of the size of
the nodes with metastases, as well as the diameter
of the focus of the metastases [19, 20].
The presence of metastases in the lymph
nodes has recently aroused keen interest among
clinicians. Micrometastases may develop into neoplastic tumors, causing relapse and non-response
to treatment [21, 22].
In addition to the impact of the condition of
the lymph nodes (N) on survival time, the current research investigated the impact of the depth
of the tumor’s infiltration in the esophageal wall
(T). No statistically significant correlation between
374
B. Śliwa, P. Szelachowski, M. Strutyńska-Karpińska
T and survival time. In the literature, opinions as
to the relevance of T in the prognosis of ESCC patients following a resection vary greatly. Japanese
researchers compared the impact of T and N on
survival time and concluded that T, unlike N, does
not contribute to the prognosis in this group of
patients [23, 24]. Contradictory results have been
presented by Chinese researchers: Wang et al. stated that extent of the long axis of the tumor has an
impact on survival time after resection. The longer
the tumor was, the shorter the survival time was. It
should be noted, however, that the results of that
study referred exclusively to patients with metastases in the nodes. In cases of no metastases in the
nodes, the length of the tumor had no statistically
significant impact on the prognosis [25].
The tendencies described above have also
been confirmed by British and American authors [26, 27]. According to Australian research
from 2011, shallower infiltration (T), a lack of metastases in the nodes (N) and radical esophagectomy are considered oncologically favorable prognostic factors for a five-year survival period [28].
Recent Chinese studies have confirmed those results [29, 30].
The current study also evaluated the impact of
the patients’ age and gender on survival time. The
analysis did not reveal any statistically significant
correlation between age, gender and survival time.
These observations are similar to most of the observations presented by other authors [31–33].
However, a 2000 study by Tachibana et al.
stated that in cases where there are no metastases
in the lymph nodes, only the depth of infiltration,
the patient’s age, the duration of the operation and
the average blood loss can be statistically significant unfavorable prognostic factors [34]. Similarly,
a 2005 study by Neuhof et al. indicated that younger age and female gender are favorable prognostic
factors [35]. Evaluating the impact of the gender
of patients on survival time, those authors asserted that there is a tendency toward longer survival
time in women than in men, although the results
were not statistically significant because of the
small number of patients in the research group.
The current research indicated that only the
presence or absence of metastases in the regional lymph nodes correlates with the survival time
of squamous carcinoma patients following an
esophagectomy.
References
[1] Holmes RS, Vaughan TL: Epidemiology and pathogenesis of esophageal cancer. Semin Radiat Oncol 2007, 17(1),
2–9.
[2] Xu XC: Risk factors and gene expression in esophageal cancer. Meth Mol Biol 2009, 471, 335–360.
[3] Sano A, Kato H, Sakurai S, Sakai M, Tanaka N, Inose T, Saito K, Sohda M, Nakayiama T, Kuwano H: CD24
expression is a novel prognostic factor in esophageal squamous cell carcinoma. Ann Surg Oncol 2009, 16(2),
506–514.
[4] Siewert JR, Feith M, Stein HJ: Esophagectomy as therapeutic principle for squamous cell cancer. Chirurg 2005,
76(11), 1033–1043.
[5] Sato M, Ando N: Standard radical esophagectomy in thoracic esophageal cancer. Nippon Geka Gakkai Zasshi
2008, 109(1), 21–25.
[6] Boone J, Livestro DP, Elias SG, Borel Rinkes IH, van Hillegersberg R: International survey on esophageal cancer:
part I surgical techniques. Dis Esophagus 2009 Jan 23. [Epub ahead of print].
[7] Li H, Zhang Y, Cai H, Xiang J: Pattern of lymph node matastases in patients with squamous cell carcinoma of the
thoracic esophagus who underwent three-field lymphadenectomy. Eur Surg Res 2007, 39(1), 1–6.
[8] Gotohda N, Nishimura M, Yoshida J, Nagai K, Tanaka N: The pattern of lymphatic metastases in superficial
squamous cell carcinoma of the esophagus. Hepatogastroenterology 2005, 52(61), 105–107.
[9] Lee J, Lee KE, Im Yh, Kang WK, Park K, Kim K, Shim YM: Adjuvant chemotherapy with 5-fluorouracil and
cisplatin in lymph node-positive thoracic esophageal squamous cell carcinoma. Ann Thorac Surg 2005, 80(4),
1170–1175.
[10] Mariette C, Piessen G, Triboulet JP: Therapeutic strategies in oesophageal carcinoma: role of surgery and other
modalities. Lancet Oncol 2007, 8(6), 545–553.
[11] Hartwig W, Strobel O, Lordick F, Büchler MW, Werner J: Multimodal therapy of esophageal cancer.
Z Gastroenterol 2008, 46(10), 1207–1213.
[12] Matsubara H: Neoadjuvant chemoradiation therapy for the treatment of esophageal carcinoma. Int J Clin Oncol
2008, 13(6), 474–478.
[13] Kunisaki C, Makino H, Takagawa R, Yamamoto N, Nagano Y, Fujii S, Kosaka T, Ono HA, Otsuka Y, Akiyama H,
Ichikawa Y, Shimada H: Surgical outcomes in esophageal cancer patients with tumor recurrence after curative
esophagectomy. J Gastrointest Surg 2008, 12(5), 802–810.
[14] Kunisaki C, Makino H, Oshima T, Fujii S, Takagawa R, Kimura J, Kosaka T, Ono HA, Akiyama H:
Clinicopathological features in N0 oesophageal cancer patients. Endo I Anticancer Res 2010, 30(7), 3063–3069.
[15] Zhang HL, Liu RL, Shi YT, Wang ZC, Wang BH, Li YJ, Zhou LY, Ping YM: Analysis of the survival in patients
after surgical resection of thoracic esophageal cancer. Zhonghua Zhong Liu Za Zhi 2009, 31(7), 541–545.
[16] Tachibana M, Dhar DK, Kinugasa S, Kotoh T, Shibakita M, Ohno S, Masunaga R, Kubota H, Nagasue N:
Long-Term Results Following Esophagectomy Due to ESCC
375
Esophageal cancer with distant lymph node metastasis: prognostic significance of metastatic lymph node ratio.
J Clin Gastroenterol 2000, 31(4), 318–322.
[17] Kunisaki C, Akiyama H, Nomura M, Matsuda G, Otsuka Y, Ono HA, Shimada H: Developing an appropriate
staging system for esophageal carcinoma. J Am Coll Surg 2005, 201(6), 884–890.
[18] Zhang H, Ping Y, Du X: Study on factors influencing survival in patients with cancer of the esophagus after resection by Cox proportional hazard model. Zhonghua Zhong Liu Za Zhi 1999, 21(1), 32–34.
[19] Dhar DK, Tachibana M, Kinukawa N, Riruke M, Kohno H, Little AG, Nagasue N: The prognostic significance
of lymph node size in patients with squamous esophageal cancer. Ann Surg Oncol 2002, 9(10), 1010–1016.
[20] Komori T, Doki Y, Kabuto T, Ishikawa O, Hiratsuka M, Sasaki Y, Ohigashi H, Murata K, Yamada T, Miyashiro I,
Mano M, Ishiguro S, Imaoka S: Prognostic significance of the size of cancer nests in metastatic lymph nodes in
human esophageal cancers. J Surg Oncol 2003, 82(1), 19–27.
[21] Hosch S, Kraus J, Scheunemann P, Izbicki JR, Schneider C, Schumacher U, Witter K, Speicher MR, Pantel K:
Malignant potential and cytogenetic characteristics of occult disseminated tumor cells in esophageal cancer.
Cancer Res 2000, 15,60(24), 6836–6840.
[22] Li SH, Wang Z, Liu XY, Liu FY, Sun ZY, Xue H: Lymph node micrometastasis: a predictor of early tumor relapse
after complete resection of histologically node-negative esophageal cancer. Surg Today 2007,37(12), 1047–1052.
[23] Shimada H, Okazumi S, Shiratori T, Akutsu Y, Matsubara H: Impact of lymph node involvement in T2 or T3
thoracic esophageal squamous cell carcinoma. Hepatogastroenterology 2009,56(93), 1039–1043.
[24] Kunisaki C, Makino H, Kimura J, Oshima T, Fujii S, Takagawa R, Kosaka T, Ono HA, Akiyama H: Impact of
lymph-node metastasis site in patients with thoracic esophageal cancer. J Surg Oncol 2010, 101(1), 36–42.
[25] Wang BY, Goan YG, Hsu PK, Hsu WH, Wu YC: Tumor length as a prognostic factor in esophageal squamous
cell carcinoma. Ann Thorac Surg 2011, 91(3), 887–893.
[26] Gaur P, Sepesi B, Hofstetter WL, Correa AM, Bhutani MS, Watson TJ, Swisher SG: Endoscopic esophageal
tumor length: a prognostic factor for patients with esophageal cancer; M.D. Anderson Esophageal Cancer Group;
University of Rochester School of Medicine and Dentistry Foregut Group. Cancer 2011, 117(1), 63–69. doi:
10.1002/cncr.25373.
[27] Griffiths EA, Brummell Z, Gorthi G, Pritchard SA, Welch IM: Tumor length as a prognostic factor in esophageal malignancy: univariate and multivariate survival analyses. J Surg Oncol 2006, 93(4), 258–267.
[28] Hirst J, Smithers BM, Gotley DC, Thomas J, Barbour A: Defining cure for esophageal cancer: analysis of actual
5-year survivors following esophagectomy. Ann Surg Oncol 2011, 18(6), 1766–1774.
[29] Zhang DK, Su XD, Long H, Lin P, Fu JH, Zhang LJ, Ma GW, Zhu ZH, Dai Y, Rong TH: Surgical treatment and
prognosis in patients with squamous cell carcinoma of thoracic esophagus. Zhonghua Wai Ke Za Zhi 2008, 46(17),
1333–1336.
[30] Hu Y, Zheng B, Rong TH, Fu JH, Zhu ZH, Yang H, Luo KJ, Li YF: Prognostic analysis of the patients with stageIII esophageal squamous cell carcinoma after radical esophagectomy. Chin J Cancer 2010, 29(2), 178–183.
[31] Kolh P, Honore P, Gielen JL, Degauque C, Azzam C, Legrand M, Jacquet N: Analysis of factors influencing
long-term survival after surgical resection for oesophageal squamous cell carcinoma. Acta Chir Belg 1999, 99(3),
113–118.
[32] Yuequan J, Shifeng C, Bing Z: Prognostic factors and family history for survival of esophageal squamous cell
carcinoma patients after surgery. Ann Thorac Surg 2010, 90(3), 908–913.
[33] Hamouda A, Forshaw M, Rohatgi A, Mirnezami R, Botha A, Mason R: Presentation and survival of operable
esophageal cancer in patients 55 years of age and below. World J Surg 2010, 34(4), 744–749.
[34] Tachibana M, Kinugasa S, Dhar DK, Shibakita M, Ohno S, Masunaga R, Kotoh T, Kubota H, Nagasue N:
Prognostic factors in node-negative squamous cell carcinoma of the thoracic esophagus. Int J Surg Invest 2000,
1(5), 389–395.
[35] Neuhof D, Neumayer F, Einbeck W, Haschemian K, Mai SK, Hochhaus A, Willeke F, Rudi J, Debus J, Wenz F:
Retrospective evaluation of combined modality treatment and prognostic factors in patients with esophageal cancer. Acta Oncol 2005, 44(2), 168–173.
Address for correspondence:
Piotr Szelachowski
Department and Clinic of Gastrointestinal and General Surgery
Wroclaw Medical University
Skłodowska-Curie 66
50-369 Wrocław
Poland
Tel.: +4871 7842752
E-mail: [email protected]
Received: 4.07.2012
Revised: 28.09.2012
Accepted: 13.06.2013