Multiple Primary Malignancies: A Clinicopathological Profile of Patients at a Tertiary Center of North India—A Retrospective Hospital-Based Observational Study
CC BY 4.0 · Indian J Med Paediatr Oncol 2024; 45(01): 052-060
DOI: DOI: 10.1055/s-0043-1768051
Abstract
Introduction The incidence, prevalence, as well as survival of cancer patients, is increasing day by day due to the use of screening and improved diagnostic modalities. Simultaneously, the development of multiple primary malignancies (MPMs) in cancer survivors is not uncommon in recent years, because of an improved understanding of biology and effective management of cancer in the form of local (i.e., surgery/radiotherapy) and systemic (chemotherapy/targeted therapy) treatment, leading to improved survival and subsequent development of more malignancies. The study was conducted to describe the clinicopathological profile of patients diagnosed with MPMs.
Objective To study the clinicopathological profile of MPMs and to look for treatment patterns of these patients.
Materials and Methods This was a retrospective hospital-based observational study. Medical records of 73 patients with MPMs, who were registered in the department of medical and surgical oncology between January 2016 and December 2018, were enrolled in the study. The statistical analysis was done by using IBM SPSS Statistics for Windows from IBM Corp. Categorical data were expressed in the form of frequencies and percentages.
Results Out of the total 73 patients, 2 patients were diagnosed to have triple malignancies and were excluded from the study for discussion purposes. Among 71 patients with double malignancies, 19 patients had synchronous and 52 had metachronous malignancies with synchronous to metachronous ratio of 1:2.73. The study included 39 men and 32 women with a male to female ratio of 1.21:1. Gastrointestinal system was the most common system involved in first primary as well as in second primary malignancy. Squamous cell carcinoma and adenocarcinoma equally were the most common histologies seen in primary, whereas adenocarcinoma was the most common histology seen in second primary malignancy.
Conclusions The phenomenon of MPMs is not an uncommon presentation due to longer survival and side effects of treatment (radiotherapy/chemotherapy). It should always be kept in consideration in any cancer survivor during surveillance in order to detect it and treat at the earliest.
Keywords
malignancy - synchronous - metachronousConsent for Publication
Not Applicable.
Authors' Contributions
A.W.M., S.P., and S.N. designed the study and oversaw the research. A.W.M., S.N., I.A., S.N., and N.A.D. developed the concept and drafted the manuscript. S.N. and N.A.D. prepared the tables and figures. A.W.M., S.N., I.A., N.S., S.P., M.H., and N.A. check data for accuracy, contributed to data preparation and analysis. A.W.M., S.N., I.A., N.S., S.P., M.M.H., and N.A. reviewed the results. A.W.M., S.N., I.A., N.S., S.P., M.M.H., and N.A.D. reviewed all versions of the manuscript. A.W.M., S.N., I.A., N.S., S.P., M.M.H., and N.A.D. finalized the manuscript. All authors reviewed the finalized manuscript. The author(s) read and approved the final manuscript.
Supplementary MaterialPublication History
Article published online:
12 May 2023
© 2023. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution License, permitting unrestricted use, distribution, and reproduction so long as the original work is properly cited. (https://creativecommons.org/licenses/by/4.0/)
Thieme Medical and Scientific Publishers Pvt. Ltd.
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Abstract
Introduction The incidence, prevalence, as well as survival of cancer patients, is increasing day by day due to the use of screening and improved diagnostic modalities. Simultaneously, the development of multiple primary malignancies (MPMs) in cancer survivors is not uncommon in recent years, because of an improved understanding of biology and effective management of cancer in the form of local (i.e., surgery/radiotherapy) and systemic (chemotherapy/targeted therapy) treatment, leading to improved survival and subsequent development of more malignancies. The study was conducted to describe the clinicopathological profile of patients diagnosed with MPMs.
Objective To study the clinicopathological profile of MPMs and to look for treatment patterns of these patients.
Materials and Methods This was a retrospective hospital-based observational study. Medical records of 73 patients with MPMs, who were registered in the department of medical and surgical oncology between January 2016 and December 2018, were enrolled in the study. The statistical analysis was done by using IBM SPSS Statistics for Windows from IBM Corp. Categorical data were expressed in the form of frequencies and percentages.
Results Out of the total 73 patients, 2 patients were diagnosed to have triple malignancies and were excluded from the study for discussion purposes. Among 71 patients with double malignancies, 19 patients had synchronous and 52 had metachronous malignancies with synchronous to metachronous ratio of 1:2.73. The study included 39 men and 32 women with a male to female ratio of 1.21:1. Gastrointestinal system was the most common system involved in first primary as well as in second primary malignancy. Squamous cell carcinoma and adenocarcinoma equally were the most common histologies seen in primary, whereas adenocarcinoma was the most common histology seen in second primary malignancy.
Conclusions The phenomenon of MPMs is not an uncommon presentation due to longer survival and side effects of treatment (radiotherapy/chemotherapy). It should always be kept in consideration in any cancer survivor during surveillance in order to detect it and treat at the earliest.
Keywords
malignancy - synchronous - metachronous
Background
Multiple primary malignancies (MPMs) in cancer patients are not very rare because of prolonged survival due to advances made in the treatment of cancer patients. The probability of recurrence or a secondary from the initial malignancy may delay treatment and impact the overall prognosis and survival, making the diagnosis of MPMs complicated. The most common presentation of MPMs is double malignancies.[1] [2] MPMs were first described by Billroth[3] in 1889 and reported in a detailed study by Warren and Gates[4] in 1932. The criteria for diagnoses of MPM, as proposed by Warren and Gates, include: (1) histological confirmation of malignancy in both the index and second primary tumors; (2) there should be at least 2 cm of normal mucosa between the tumors; if the tumors are in the same location, then they should be separated in time by at least 5 years; (3) probability of one being the metastasis of the other must be excluded.
Double primary malignancies could be divided into two categories, depending upon the interval between tumor diagnoses. Synchronous malignancies are defined where second tumor develops simultaneously or within 6 months after the diagnosis of first malignancy, whereas in metachronous malignancies, second tumor develops after 6 months or more after the diagnosis of the first malignancy.[5]
The aim of our study was to assess the clinical and pathological profile of patients diagnosed with MPMs in our region.
Material and Methods
This was a retrospective hospital-based observational study. Medical records of 73 patients with MPMs who were registered in the department of medical and surgical oncology between January 2016 to December 2018 were enrolled in the study. The patient's details were entered in a set proforma, which include age, sex, family history, smoking and drinking history, histology of synchronous and metachronous lesions, and treatment received.
Inclusion Criteria
Patients with two or more lesions at different sites with different histology or those with two lesions at different sites with similar histology but with different immunohistochemistry markers were included in the study. The tumors were divided into synchronous and metachronous lesions depending upon the time interval between the occurrence of two lesions. Synchronous tumors developed simultaneously or within 6 months of each other, whereas metachronous lesion occurred more than 6 months apart from each other.
Exclusion Criteria
Patients with malignancy at different sites but with same immunohistochemistry or disease at same site within 5 years of first malignancy were excluded from the study.
Sample Size
Sample size was calculated by using the Cochran's formula n = (1.96)[2] p(1-P)/d 2, p = 0.73%, d = 0.10%, and thus, the calculated sample size is 76. Case records of three patients were incomplete and were excluded from the study, so the final sample size of our study was 73 patients having 85%-power of study.
Primary Outcome
To study the clinicopathological profile of MPMs.
Secondary Outcome
To study the treatment patterns of MPM patients.
Statistical Analysis
The data analysis was done on a computer running Microsoft Windows. The data were initially entered into a Microsoft Excel spreadsheet to be checked for mistakes. The IBM Corp.'s IBM SPSS Statistics for Windows was used for the statistical analysis (released 2020, Version 27.0. Armonk, New York, USA). The frequency and percentage representations of categorical variables were displayed.
Results
Out of 13,852 newly diagnosed cancer cases, 73 patients were diagnosed to have MPMs comprising of 0.51%-of the total cases enrolled during the study. Two patients had triple malignancies, whereas 71 patients had double malignancies. In the two patients with triple malignancy, one had non-Hodgkin's lymphoma and developed metachronous squamous cell carcinoma of esophagus and adenocarcinoma of sigmoid colon. In another patient with index squamous cell carcinoma of skin (thigh), developed two metachronous malignancies, i.e., renal cell carcinoma and adenocarcinoma stomach. For rest of discussion purposes, we will exclude triple malignancies. Of the 71 cases of double malignancy, 39 (54.92%) were men and 32 (45.07%) were women with a male to female ratio of 1.21:1. Median age of our patients was 55 (30–80) with median time to diagnosis of second cancer of 36 months (12–228).
Among the 71 patients with MPMs, 52 patients harbored metachronous double malignancies, whereas 19 patients harbored synchronous double malignancies with metachronous to synchronous malignancy ratio of 2.73:1. The most common systems involved in primary cancer were gastrointestinal system (GI; 22; 30.99%), breast (8; 11.27%), reproductive (8; 11.27%), urinary tract (8; 11.27%), and head and neck (7; 9.86%), whereas in second primary cancer most common systems involved were GI (28; 39.43%), lung (12; 16.9%), reproductive (8; 11.27%), head and neck (8; 11.27%), and breast (4; 5.63%), with esophagus (8; 11.26%), stomach (7; 9.85%), and breast (7; 9.85%) being the most common organs involved in primary cancers, whereas lung (12; 16.90%), colorectal (9; 12.67%), and stomach (8; 11.26%) being the most common organs involved in second primary cancers ([Table 1], [Fig. 1]). Squamous and adenocarcinoma were equally distributed (16 cases each; 22.53%), the most common histologies involved in primary cancers, whereas adenocarcinoma (22; 30.99%) followed by squamous cell carcinoma (18; 25.35%) were as the most common histologies in second primary cancers ([Supplementary Fig. S1], available in the online version). Of the 71 patients with MPMs, 20 (28.17%) were treated with surgery, 14 (19.71%) with surgery + chemotherapy, 10 (14.08%) with chemotherapy + radiotherapy, whereas in second primary malignancy, 15 (21.12%) underwent surgery; 13 (18.30%) chemotherapy + radiotherapy, and 10 (14.08%) patients received surgery + chemotherapy ([Tables 2] and [3], [Supplementary Fig. S2] [available in the online version])
Site |
Primary |
% |
95% CI |
Second primary |
% |
95% CI |
||
---|---|---|---|---|---|---|---|---|
Lower |
Upper |
Lower |
Upper |
|||||
Gastrointestinal |
22 |
30.99 |
20.00 |
43.00 |
28 |
39.44 |
28.00 |
51.00 |
Reproductive |
8 |
11.27 |
4.00 |
21.00 |
8 |
11.27 |
4.00 |
21.00 |
Breast |
8 |
11.27 |
4.00 |
21.00 |
4 |
5.63 |
1.00 |
13.00 |
Urinary tract |
8 |
11.27 |
4.00 |
21.00 |
2 |
2.82 |
0.30 |
9.00 |
Head and neck |
7 |
9.86 |
4.00 |
19.00 |
8 |
11.27 |
4.00 |
21.00 |
Hematology |
6 |
8.45 |
3.00 |
17.00 |
5 |
7.04 |
2.00 |
15.00 |
Lung |
2 |
2.82 |
0.30 |
9.00 |
12 |
16.90 |
9.00 |
27.00 |
Skin |
6 |
8.45 |
3.00 |
17.00 |
4 |
5.63 |
1.00 |
13.00 |
Others |
4 |
5.63 |
1.00 |
13.00 |
0 |
0.00 |
– |
– |
S No. |
Age |
Sex |
Primary site |
Histopathology |
Treatment |
Second Primary |
Histopathology |
Treatment |
---|---|---|---|---|---|---|---|---|
1 |
48 |
F |
Esophagus (20 cm) |
SCC |
CT-RT |
Esophagus (34-37 cm) |
SCC |
CT-RT |
2 |
80 |
M |
Prostate |
Adenoca |
GnRH analogues |
Thyroid |
Papillary carcinoma |
Total thyroidectomy |
3 |
36 |
M |
Prostate |
Adenoca |
Local R/T |
Bladder |
Malignant paraganglioma |
Radiotherapy |
4 |
40 |
F |
Ovary |
Endometriod carcinoma |
TAH + BSO (OCR) +Chemo |
Uterus |
Endometrial carcinoma |
TAH/BSO done as part of ca ovarian staging |
5 |
41 |
F |
Breast |
IDC |
BCS + ALND + radiotherapy + chemo |
Thyroid |
Papillary carcinoma |
Total Thyroidectomy |
6 |
60 |
M |
Tongue |
SCC |
WLE + radiotherapy |
Gall bladder |
Adenoca |
Radical cholecystectomy |
7 |
60 |
M |
Esophagus |
SCC |
CT-RT |
Lung |
Adenoca |
CT-RT |
8 |
60 |
M |
Urinary Bladder |
TCC |
TURBT |
Lung |
Adenoca |
CT-RT |
9 |
65 |
M |
Oral cavity |
SCC |
WLE |
Thyroid |
PTC |
Total thyroidectomy |
10 |
55 |
M |
Stomach |
Adenoca |
Palliative care |
Liver |
Hepatocellular carcinoma |
Palliative care |
11 |
75 |
M |
Cervical node |
NHL |
CT + RT |
Esophagus |
SCC |
CT-RT |
12 |
67 |
M |
Esophagus |
SCC |
CT-RT |
Lung |
SCC |
CT-RT |
13 |
65 |
M |
Stomach |
Adenoca |
NACT + surgery + adjuvant chemo |
Colon |
Adenoca |
Left hemicolectomy |
14 |
60 |
M |
Esophagus |
SCC |
CT-RT |
Lung |
SCC |
CT-RT |
15 |
30 |
F |
Ovary |
HGS Ca |
Surgery/optimal cytoreduction + chemo |
Endometrium (1b) |
Endometrial Ca |
EBRT |
16 |
46 |
F |
Endometriod Ca of ovary |
TAH + BSO (OCR) |
Observation |
Endometrium |
Endometrial Adenoca (1A) |
Observation (sx already done) |
17 |
50 |
M |
GE junction |
Adenoca |
Palliative chemo |
Larynx |
SCC |
Palliation |
18 |
50 |
M |
RCC |
Clear cell |
Immunotherapy |
Lung |
Adeno |
Immuno + chemo |
19 |
55 |
F |
Breast |
IDC |
Chemo |
Ovary |
HGS Ca |
Chemo |
S.no |
Age |
Sex |
Primary site |
Histopathology |
Treatment |
Second Primary |
Histopathology |
Treatment |
Time interval (mo) |
---|---|---|---|---|---|---|---|---|---|
1 |
51 |
F |
Thyroid |
Follicular carcinoma |
Total thyroidectomy + RAIA |
Blood |
CLL |
Chemotherapy + targeted therapy |
84 |
2 |
60 |
F |
Kidney |
Clear cell carcinoma |
Right radical nephrectomy |
Left kidney |
Clear cell carcinoma |
Sunitinib |
24 |
3 |
40 |
F |
Skin |
Mycosis fungoids |
Phototherapy |
Ovary |
PSCa |
Surgery (OCR) + chemotherapy |
60 |
4 |
70 |
M |
Lymph node |
NHL(DLBCL) |
Chemotherapy + targeted |
Esophagus |
SCC |
Chemoradiation |
24 |
5 |
55 |
M |
Lymph node |
NHL (small cell type) |
Chemotherapy |
Blood |
CLL |
Chemotherapy |
12 |
6 |
50 |
F |
Colon |
Malignant carcinoid |
Right hemicolectomy + chemotherapy |
Cheek (skin) |
Basal cell carcinoma |
WLE |
12 |
7 |
55 |
F |
Cervix |
SCC |
CT-RT |
Labia majora (skin) |
SCC |
WLE |
48 |
8 |
41 |
F |
Lung |
Adenoca |
CT-RT |
Choroid |
Melanoma |
Enucleation of eyeball |
24 |
9 |
55 |
M |
Urinary bladder |
Papillary carcinoma |
TURBT + chemotherapy |
Colon |
Adenoca |
Hemicolectomy + chemotherapy |
60 |
10 |
55 |
F |
Uterus |
Adenoca |
TAH + BSO |
Rectum |
Adenoca |
Chemoradiation |
12 |
11 |
35 |
M |
Right kidney |
Chromo-phobe carcinoma |
Radical nephrectomy |
Thyroid |
PTC |
Total thyroidectomy |
12 |
12 |
58 |
F |
Skin |
SCC |
WLE |
Stomach |
Adenoca |
Supportive care |
60 |
13 |
50 |
F |
Colon |
Adenoca |
Left hemicolectomy |
Uterus |
Endometrial carcinoma |
TAH + BSO |
72 |
14 |
67 |
F |
Ovary |
Papillary carcinoma |
NACT + surgery |
Breast |
IDC |
MRM |
24 |
15 |
55 |
F |
Uterus |
Adenoca |
TAH + BSO |
Gall bladder |
Adenoca |
Chemotherapy |
24 |
16 |
65 |
M |
Skin |
SCC |
WLE |
Esophagus |
SCC |
CT-RT |
12 |
17 |
51 |
F |
Thyroid |
Follicular ca |
Total thyroidectomy |
Blood |
CLL |
Chemotherapy + targeted |
84 |
18 |
40 |
F |
Rectum |
Adenoca |
Anterior resection + CT-RT |
Uterus |
Adenoca |
TAH + BSO + radiotherapy |
192 |
19 |
52 |
M |
Esophagus |
SCC |
CT-RT |
Lung |
SCC |
Chemotherapy |
36 |
20 |
55 |
F |
Eyelid |
Merkel cell carcinoma |
WLE |
Breast |
IDC |
MRM + chemotherapy |
12 |
21 |
48 |
F |
Breast |
IDC |
MRM + chemotherapy |
Colon |
Adenoca |
Hemicolectomy + chemotherapy + radiotherapy |
48 |
22 |
70 |
M |
Colon |
Adenoca |
Hemicolectomy + chemotherapy |
Lung |
SCC |
Chemotherapy |
36 |
23 |
60 |
M |
Lung |
SCC |
CT-RT |
Skin |
SCC |
WLE |
36 |
24 |
50 |
F |
Gall bladder |
Adenoca |
Radical cholecystectomy |
Stomach |
Adenoca |
Distal gastrectomy + chemotherapy |
24 |
25 |
68 |
M |
Esophagus |
SCC |
Surgery + chemotherapy |
Lung |
SCC |
CT-RT |
192 |
26 |
55 |
M |
Bladder |
TCC |
TURBT |
Stomach |
Adenoca |
Distal gastrectomy + CT-RT |
36 |
27 |
76 |
M |
Bladder |
TCC |
TURBT + intravesical BCG |
GE junction |
SCC |
Chemotherapy |
180 |
28 |
40 |
F |
Breast |
IDC |
MRM + Chemo + RT |
Ovary |
HGS Ca |
Surgery (OCR) + Chemo |
84 |
29 |
50 |
M |
Esophagus |
SCC |
Surgery + radiotherapy |
Stomach |
Neuroendocrine tumor (G1) |
Distal gastrectomy |
96 |
30 |
75 |
M |
Lymph node |
NHL |
Chemotherapy |
Stomach |
Adenoca |
Defaulted |
36 |
31 |
56 |
M |
Blood |
CLL |
Chemotherapy |
Lip |
Merkel cell carcinoma |
WLE + radiotherapy |
228 |
32 |
60 |
M |
Skin |
SCC |
WLE + chemotherapy |
Lung |
SCC |
CT-RT |
12 |
33 |
65 |
F |
Lymph node |
NHL |
Chemotherapy |
Rectum |
Adenoca |
CT-RT |
48 |
34 |
50 |
M |
Stomach |
Adenoca |
NACT with distal gastrectomy + adjuvant chemotherapy |
Blood |
DLBCL |
Supportive care |
36 |
35 |
70 |
M |
Skin |
SCC |
WLE |
Esophagus |
SCC |
Radiotherapy |
36 |
36 |
65 |
M |
Skin |
Basal cell carcinoma |
WLE |
Lung |
SCC |
Radiotherapy |
36 |
37 |
55 |
M |
Colon |
Adenoca |
Hemicolectomy with chemotherapy |
Esophagus |
Adenoca |
Chemotherapy |
36 |
38 |
40 |
F |
Breast |
IDC |
MRM |
Brain |
Meningioma |
Observation |
12 |
39 |
62 |
M |
Spinal cord |
Ependymoma |
Laminectomy with excision |
Blood |
CML |
Imatinib |
60 |
40 |
70 |
M |
Stomach |
Adenoca |
NACT + total gastrectomy + adjuvant chemotherapy |
Rectum |
Adenoca |
Palliative care |
36 |
41 |
51 |
F |
Breast |
IDC |
MRM + chemo + RT |
Esophagus |
SCC |
CT-RT |
96 |
42 |
55 |
F |
Esophagus |
SCC |
CT-RT |
Stomach |
SCC |
Palliative care |
24 |
43 |
55 |
M |
Stomach |
Adenoca |
Chemo + surgery |
Colon |
Adenoca |
Sx + chemo |
20 |
44 |
60 |
F |
Breast |
IDC |
Sx + chemo + RT + hormones |
Gallbladder |
adeno |
Surgery |
60 |
45 |
65 |
M |
Gastric |
GIST |
Sx + imatinib |
Stomach |
Adeno |
Sx + chemo |
12 |
46 |
75 |
M |
Bone marrow |
Multiple myeloma |
Chemo + immuno |
Colon |
Adeno |
Sx + chemo |
36 |
47 |
80 |
M |
Colon |
Adenocarcinoma |
Sx + chemo |
Lung |
Adeno |
Chemo |
96 |
48 |
56 |
F |
Breast (right) |
IDC |
Sx + chemo + hormones |
Breast (Left) |
IDC |
Sx + chemo + hormones |
108 |
49 |
75 |
F |
Thyroid |
Papillary carcinoma |
Sx + RAIA |
Breast |
IDC |
Sx + chemo + radiotherapy |
204 |
50 |
45 |
F |
Uterus |
Endometrial ca |
Surgery (1A) |
Periampullary ca |
Adenoca |
Surgery |
48 |
51 |
53 |
M |
Kidney |
Clear cell ca |
Surgery (1B) |
Lung |
Squamous cell |
Chemo |
84 |
52 |
47 |
F |
Thyroid |
Papillary carcinoma |
Surgery |
Lung |
Adeno |
TKI |
96 |
Study (ref. No) |
Total no. of patients |
No. of patients with multiple primary malignancies |
Synchronous/metachronous |
Male/female |
Median age (metachronous group) |
Common site |
Median interval between index and second primary (mo) |
|||
---|---|---|---|---|---|---|---|---|---|---|
No. |
% |
Index primary |
Second primary |
Index primary |
Second primary |
|||||
Vadgaonkar et al[18] |
16,461 |
44 |
0.26 |
7/37 |
13/31 |
48 |
56 |
Gynecological |
Gynecological |
38 |
Breast |
Gastrointestinal |
|||||||||
Head and neck |
– |
|||||||||
Etiz et al[17] |
9,772 |
122 |
1.2 |
36/86 |
67/55 |
56 |
62 |
Lung |
Lung |
– |
Gastrointestinal |
Gastrointestinal |
|||||||||
Genitourinary |
Genitourinary |
|||||||||
Zhai et al[9] |
15,321 |
167 |
1.09 |
98/69 |
117/50 |
62 |
64 |
Gastrointestinal |
Gastrointestinal |
31.15 |
lung |
lung |
|||||||||
Head and neck |
Head and neck |
|||||||||
Bisht et al[7] |
3,879 |
29 |
0.74 |
8/21 |
10//19 |
54 |
56 |
Breast |
Gastrointestinal |
– |
Head and neck |
Head and neck |
|||||||||
Lung |
Lung |
|||||||||
Irimie et al[8] |
– |
63 |
– |
24/41 |
34/29 |
58.2 y in entire group |
Genital |
Breast |
– |
|
Breast |
Gastrointestinal |
|||||||||
Gastrointestinal |
Lung |
|||||||||
Present study |
13,852 |
71 |
0.51 |
19/52 |
39/32 |
55 y in entire group |
Gastrointestinal |
Gastrointestinal |
36 |
|
Breast |
Lung |
|||||||||
Reproductive |
Reproductive |
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- Zhai C, Cai Y, Lou F. et al. Multiple primary malignant tumors - a clinical analysis of 15,321 patients with malignancies at a single center in China. J Cancer 2018; 9 (16) 2795-2801
- Cheng HY, Chu CH, Chang WH. et al. Clinical analysis of multiple primary malignancies in the digestive system: a hospital-based study. World J Gastroenterol 2005; 11 (27) 4215-4219
- Curtis RE, Freedman DM, Ron E. et al. New Malignancies Among Cancer Survivors: SEER Cancer Registries, 1973-2000. Bethesda, MD: National Cancer Institute; 2006: 9-14
- Hajdu SI, Hajdu EO. Multiple primary malignant tumors. J Am Geriatr Soc 1968; 16 (01) 16-26
- Berge T, Cederqvist L, Schönebeck J. Multiple primary malignant tumours. an autopsy study of a circumscribed population. Acta Pathol Microbiol Scand 1969; 76 (02) 171-183
- Aydiner A, Karadeniz A, Uygun K. et al. Multiple primary neoplasms at a single institution: differences between synchronous and metachronous neoplasms. Am J Clin Oncol 2000; 23 (04) 364-370
- Lee TK, Barringer M, Myers RT, Sterchi JM. Multiple primary carcinomas of the colon and associated extracolonic primary malignant tumors. Ann Surg 1982; 195 (04) 501-507
- Vyas JJ, Deshpande RK, Sharma S, Desai PB. Multiple primary cancers in Indian population: metachronous and synchronous lesions. J Surg Oncol 1983; 23 (04) 239-249
- Etiz D, Metcalfe E, Akcay M. Multiple primary malignant neoplasms: a 10-year experience at a single institution from Turkey. J Cancer Res Ther 2017; 13 (01) 16-20
- Vadgaonkar RA, Nayak SS, Doni S, Digumarti L, Mullapally SK, Digumarti R. Distinct patterns of occurrence, common associations, and survival of patients with second primary malignancies: a 5-year single institute experience with review of literature. Indian J Pathol Microbiol 2021; 64 (04) 725-731
- Jena A, Patnayak R, Lakshmi AY, Manilal B, Reddy MK. Multiple primary cancers: an enigma. South Asian J Cancer 2016; 5 (01) 29-32
- Lv M, Zhang X, Shen Y. et al. Clinical analysis and prognosis of synchronous and metachronous multiple primary malignant tumors. Medicine (Baltimore) 2017; 96 (17) e6799
- Mehdi I, Shah AH, Moona MS. et al. Synchronous and metachronous malignant tumours expect the unexpected. J Pak Med Assoc 2010; 60 (11) 905-909
- Vogel VG. Identifying and screening patients at risk of second cancers. Cancer Epidemiol Biomarkers Prev 2006; 15 (11) 2027-2032
- Khan NA, Ahmad Syed N, Dar NA, Masoodi SR, Lone MM. Changing pattern of common cancers in the last five years in Kashmir, India: a retrospective observational study. Int J Med Paediatr Oncol 2021; 42: 439-443
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12 May 2023
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- Irimie A, Achimas-Cadariu P, Burz C, Puscas E. Multiple primary malignancies–epidemiological analysis at a single tertiary institution. J Gastrointestin Liver Dis 2010; 19 (01) 69-73
- Zhai C, Cai Y, Lou F. et al. Multiple primary malignant tumors - a clinical analysis of 15,321 patients with malignancies at a single center in China. J Cancer 2018; 9 (16) 2795-2801
- Cheng HY, Chu CH, Chang WH. et al. Clinical analysis of multiple primary malignancies in the digestive system: a hospital-based study. World J Gastroenterol 2005; 11 (27) 4215-4219
- Curtis RE, Freedman DM, Ron E. et al. New Malignancies Among Cancer Survivors: SEER Cancer Registries, 1973-2000. Bethesda, MD: National Cancer Institute; 2006: 9-14
- Hajdu SI, Hajdu EO. Multiple primary malignant tumors. J Am Geriatr Soc 1968; 16 (01) 16-26
- Berge T, Cederqvist L, Schönebeck J. Multiple primary malignant tumours. an autopsy study of a circumscribed population. Acta Pathol Microbiol Scand 1969; 76 (02) 171-183
- Aydiner A, Karadeniz A, Uygun K. et al. Multiple primary neoplasms at a single institution: differences between synchronous and metachronous neoplasms. Am J Clin Oncol 2000; 23 (04) 364-370
- Lee TK, Barringer M, Myers RT, Sterchi JM. Multiple primary carcinomas of the colon and associated extracolonic primary malignant tumors. Ann Surg 1982; 195 (04) 501-507
- Vyas JJ, Deshpande RK, Sharma S, Desai PB. Multiple primary cancers in Indian population: metachronous and synchronous lesions. J Surg Oncol 1983; 23 (04) 239-249
- Etiz D, Metcalfe E, Akcay M. Multiple primary malignant neoplasms: a 10-year experience at a single institution from Turkey. J Cancer Res Ther 2017; 13 (01) 16-20
- Vadgaonkar RA, Nayak SS, Doni S, Digumarti L, Mullapally SK, Digumarti R. Distinct patterns of occurrence, common associations, and survival of patients with second primary malignancies: a 5-year single institute experience with review of literature. Indian J Pathol Microbiol 2021; 64 (04) 725-731
- Jena A, Patnayak R, Lakshmi AY, Manilal B, Reddy MK. Multiple primary cancers: an enigma. South Asian J Cancer 2016; 5 (01) 29-32
- Lv M, Zhang X, Shen Y. et al. Clinical analysis and prognosis of synchronous and metachronous multiple primary malignant tumors. Medicine (Baltimore) 2017; 96 (17) e6799
- Mehdi I, Shah AH, Moona MS. et al. Synchronous and metachronous malignant tumours expect the unexpected. J Pak Med Assoc 2010; 60 (11) 905-909
- Vogel VG. Identifying and screening patients at risk of second cancers. Cancer Epidemiol Biomarkers Prev 2006; 15 (11) 2027-2032
- Khan NA, Ahmad Syed N, Dar NA, Masoodi SR, Lone MM. Changing pattern of common cancers in the last five years in Kashmir, India: a retrospective observational study. Int J Med Paediatr Oncol 2021; 42: 439-443