Background: Within a dramatic socio-political context, cancer represents a growing health burden in the Gaza Strip. We investigated the survival experience of people diagnosed with breast (BC) or colorectal (CRC) cancer from 2005 to 2014. Methods: Data included 1360 BC cases (median age 55.1 years) and 722 CRC cases (median age: 59.5 years; 52.5% men) recorded by the Gaza Cancer Registry according to a standard protocol. Clinical information was available for cases diagnosed in 2005–2006 only. Survival probabilities were estimated by Kaplan-Meyer method, while hazard ratios (HRs) and 95% confidence intervals (CI), adjusted for age and sex, were computed to assess factors associated with the risk of death. Results: Five-year survival was 65.1% for women with BC and 50.2% for patients with CRC. Advanced age (> 65 years), stage, and grade increased the death risk. Full access to therapies was associated with a reduced risk of death as compared with patients who had limited access (HR = 0.26, 95% CI:0.13–0.51 for BC; and HR = 0.11, 95% CI: 0.04–0.31 for CRC). Conclusion(s): The 5-year survival after BC or CRC in the Gaza Strip was in line with estimates from surrounding Arab countries, but it was much lower than in developed Mediterranean countries (e.g., in Italy or in Jewish people in Israel). Keywords: Gaza Strip, Cancer survival, Breast cancer, Colorectal cancer Background of death, after cardiovascular diseases, and it accounts The Gaza Strip, a narrow land located in the southern for 20% of the whole expenditure for drugs [5, 6]. part of the Occupied Palestinian Territory (OPT), is an In the OPT, two population-based cancer registries overcrowded area with a population of 1.8 million were established in 1996 by the Palestinian Ministry of people (i.e., 5000 persons per km ). Although most Health (MoH) -one in the West Bank, and one in the of the population in the Gaza Strip has a challengeable Gaza Strip . Given the geopolitical context of the life, with a high rate of poverty - 74% of families were es- Gaza Strip [7, 8], the data collection process cannot fully timated to live below the poverty line [2, 3] - life expect- reflect the whole cancer burden in the area. As a conse- ancy at birth reaches 71.5 years in males and 74.4 years quence, the World Health Organization (WHO) has re- in females . Cancer is the second most common cause cently given support to the Palestinian MoH in improving cancer registration . Of all cases recorded between 2005 and 2014, breast cancer (BC) was the most common cancer among women (26.0% -skin can- * Correspondence: email@example.com Chiara Panato and Khaled Abusamaan contributed equally to this work. cers included), while colorectal cancer (CRC) was the Cancer Epidemiology Unit, IRCCS Centro di Riferimento Oncologico, Aviano, second most common cancer in men (9.7% of all cases). Italy The Italian MoH promoted the “EUROMED Cancer Friuli Venezia Giulia Cancer Registry, IRCCS Centro di Riferimento Oncologico, Aviano, Italy Network” with the general aim to support extra-European Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Panato et al. BMC Cancer (2018) 18:632 Page 2 of 10 Union Mediterranean countries in the development of ef- for these cases a multivariate analysis was conducted to fective anti-cancer programs [9, 10]. The ongoing collab- estimate the risk of death. oration with the Gaza Cancer Registry (GCR) was conducted by the National Cancer Institute “Centro di Statistical methods Riferimento Oncologico”, Aviano (notheastern Italy); the The crude survival time was calculated as the time Italian network of cancer registries (AIRTUM); and the elapsed from date of cancer diagnosis to date of death, Italian National Health Institute (ISS), Rome. or to end of follow-up –whichever came first. At univar- Herein, we describe the general characteristics and the iate analysis, the survival time for the totality of BC or crude survival experience of patients diagnosed with BC CRC patients diagnosed from 2005 to 2014 was esti- or with CRC between 2005 and 2014 in the Gaza Strip. mated by means of the Kaplan-Meier method . Furthermore, as selected clinical data were available only For cases diagnosed in 2005–2006 only, a multivariate for cases diagnosed in 2005–2006, we estimated the risks analysis was carried out to statistically assess the role of of death for patients with BC or CRC according to type selected clinical variables on survival. To this end, haz- of therapy, disease, grade, or stage. ard ratios (HRs) for all-cause mortality, and the corre- sponding 95% confidence intervals (95% CIs), were estimated using the Cox proportional hazard model ad- Methods justed for age at diagnosis (< 35, 35–44, 45–54, 55–64, Study population 65–74, 75+ years) and gender, as appropriate . The We described the general characteristics and the cancer proportional hazard assumption was assessed through survival experience of people living in the Gaza Strip, di- Schoenfeld residuals, including interactions with agnosed with BC or CRC in 2005–2014, according to follow-up time . the information recorded in the population-based GCR. Cancer Registries are identified as collectors of personal Results data for surveillance purposes without the need of expli- Breast cancer cit individual consent. The approval of a research ethic The median age of the 1360 women diagnosed with BC committee is not required because neither direct nor in- in the Gaza Strip between 2005 and 2014 was 55.1 years direct intervention on patients took place. Nonetheless, (Inter Quartile Range -IQR: 45.8–64.8 years). The abso- the General Director of the Primary Health Care, MoH, lute number of cases more than doubled, from 178 in (Dr. Fouad Elissawi) cleared the use of the registry data 2005–2006 up to 396 in 2013–2014 (Table 1), with slight for study purposes. The data collection process used by variations in median ages –from 53.0 years (in 2005– GCR is an active one, carried on by GCR trained 2006) to 55.4 years (in 2013–2014). Overall, 76.1% (95% personnel who regularly visit the pathology departments and oncology clinics to collect newly detected cases and Table 1 Description of breast and colorectal cancer incident to update the already recorded ones. The update of the cases diagnosed from 2005 to 2014 in the Gaza Strip vital status is manually checked by means of the death Breast cancer Colorectal cancer registry. Cases Deaths Cases Deaths For the aims of this analysis, to ensure data validity, N = 1360 N = 486 (%) N = 722 N = 361 (%) each case was reviewed by a member of the GCR and Sex co-author of this article (FE). The vital status and – Female 1360 486 (35.7) 343 169 (49.3) eventually – the date of death were ascertained from the Male –– 379 192 (50.7) death registration database at Palestinian MoH. The last follow-up time was December 31st, 2016. Overall, from Age at cancer diagnosis (years) 2005 to 2014, 1495 women were diagnosed with BC (no ≤ 44 331 108 (32.6) 97 33 (32.0) cases of BC were recorded in men during the study 45–54 371 120 (32.4) 163 69 (40.5) period), and 878 people were diagnosed with CRC. This 55–64 319 112 (35.1) 221 114 (49.3) analysis was restricted to 1360 BC and 722 CRC patients ≥ 65 339 146 (43.1) 241 145 (59.3) after exclusion of: cases lacking the full date of birth (7 Calendar year at cancer diagnosis BCs and 21 CRCs); children under 15 years of age (2 BCs and 3 CRCs); and those patients with coincident 2005–2006 178 93 (52.3) 80 58 (72.5) dates of diagnosis and death (126 cases of BC and 132 2007–2008 207 73 (35.3) 124 53 (47.7) cases of CRC). 2009–2010 223 101 (45.3) 136 72 (52.9) Information on therapy, grade, and stage of disease 2011–2012 356 143 (40.2) 165 91 (55.2) was available for cases diagnosed in 2005–2006 only 2013–2014 396 76 (19.2) 217 87 (40.1) (i.e., 178 cases of BC and 80 cases of CRC). Accordingly, Panato et al. BMC Cancer (2018) 18:632 Page 3 of 10 CI: 73.7–78.3) of these women was alive after 3 years, disease were statistically lower than those with a local- 65.1% (95% CI: 62.1–67.4) after 5 years, and 51.9% (95% ized BC stage (p of log-rank test = 0.0314) (Fig. 2b). Con- CI: 47.9–55.7) after 10 years from BC diagnosis (Fig. 1a). cerning HR, advanced stage of disease was associated The probability of survival after BC was strongly influ- with an elevated risk of death as compared with those enced by age, with women aged 65 years or older show- with a localized disease – of borderline statistical signifi- ing the lowest survival rates (i.e., 66.0% after 3, 57.4% cance – (HR = 1.93, 95% CI: 0.98–3.80). Likewise, the after 5, and 45.1% after 10 years from diagnosis) (p < survival probabilities stratified by grade of disease were 0.001) (Fig. 1b). different from each other (p-value = 0.0078) (Fig. 2c), Selected clinical data available for the 178 women with and women diagnosed with poorly or undifferentiated BC diagnosed in 2005–2006 are discussed in detail BC were at 1.67-fold higher risk of death than women (Table 2). The majority of them (60.1%) was diagnosed with well/moderate grade of cancer (HR:1.67, 95% with an advanced stage of disease, but no difference was CI:1.04–2.69) (Table 2). noted between the percentage of women diagnosed with Surgically treated women (87.6%) had the best progno- well or moderately differentiated BC and those diag- sis, and those treated with two or more anti-cancer ther- nosed with a poorly differentiated or undifferentiated apies presented a statistically significant 70% reduction disease. Among these 178 patients with BC, 83.7% in the risk of death, as compared with those who had lit- underwent two or more therapies, in particular surgery tle (i.e., only one type of treatment) or no access (2.9%) (87.6%) and chemotherapy (76,4%). to anti-cancer therapies (Table 2). The 178 women diagnosed with BC between 2005 and 2006 were followed-up to December 31st, 2016 for a Colorectal cancer median period of 63.3 months (IQR: 23.0–100.3 months). The median age of the 722 individuals (47·5% women) During such period, 93 of them (52.2%) died, and 85 diagnosed with CRC in the Gaza Strip between 2005 and were censored. The estimated median survival time was 2014 was 59.5 years (IQR: 51.2–68.6 years), and the ab- 83.7 months (95% CI: 61.3–106.9) (Fig. 2a). Grade and solute number of cases ranged from 80 in 2005–2006 to stage of disease influenced the prognosis. Indeed, the 217 in 2013–2014 (Table 1). The median ages at CRC survival probabilities of women with advanced stage of diagnoses remained stable over time (58.7 years in Fig. 1 Kaplan-Meier estimates of survival probabilities among cases 1360 women diagnosed with breast cancer: overall (a) and according to age class (b). Gaza Strip, 2005–2014 Panato et al. BMC Cancer (2018) 18:632 Page 4 of 10 Table 2 Hazard ratios (HR) of all-cause deaths, with corresponding 95% confidence intervals (CI), among 178 incident breast cancer cases diagnosed in 2005–2006 in the Gaza Strip according to clinical characteristics Cases Deaths (N = 93) N N (%) HR (95% CI) Age at diagnosis (years) < 55 98 47 (48.0) 1 ≥ 55 80 46 (57.5) 1.39 (0.93–2.09) Stage Localized 33 10 (30.3) 1 Regional/Distant 107 57 (53.3) 1.93 (0.98–3.80) Missing 38 26 (68.4) 2.32 (1.10–4.91) Grade Well and Moderately differentiated 75 31 (41.3) 1 Poorly differentiated and Undifferentiated 70 42 (60.0) 1.67 (1.04–2.69) Missing 33 20 (60.6) 1.33 (0.72–2.44) Surgery No 18 14 (77.8) 1 Yes 156 76 (48.7) 0.29 (0.16–0.53) Chemotherapy No 38 23 (60.5) 1 Yes 136 67 (49.3) 0.58 (0.36–0.94) Radiotherapy No 81 46 (56.8) 1 Yes 93 44 (47.3) 0.89 (0·57–1·39) Hormone therapy No 109 63 (57.8) 1 Yes 65 27 (41.5) 0.53 (0.33–0.84) Number of therapies 0–1 25 20 (80.0) 1 2 55 29 (52.7) 0.32 (0.18–0.58) 3 56 23 (41.1) 0.25 (0.13–0.48) 4 38 18 (47.4) 0.26 (0.13–0.51) a b c Estimated using the Cox proportional hazard model adjusted for age; Reference category; The sum does not add up to the total because of missing values 2005–2006, 59.9 years in 2013–2014). Overall, 59.8% As per clinical protocols, 88.8% of these 80 cases diag- (95% CI: 56.0–63.3) of them were alive after 3 years, nosed in 2005–2006 underwent surgery, 87.5% received 50.2% (95% CI: 46.3–54.0) after 5 years, and 40.7% (95% chemotherapy, and only 27.5% radiotherapy. More than CI: 35.6–45.8) after 10 years from diagnosis (Fig. 3a). three quarters of patients underwent two or more thera- The survival probabilities after a CRC diagnosis were peutic regimens (Table 3). not influenced by sex (Fig. 3b). Conversely, survival after Figure 4a shows the overall survival of patients with CRC diagnosis was strongly influenced by age, with pa- CRC diagnoses, the median survival time was tients aged 65 years or older showing the lowest survival 43.3 months (95% CI: 31.4–60.0), and 34 patients were rates (i.e., 49.0% after 3, 40.1% after 5, and 33.8% after censored. Cases with a localized disease had a higher 10 years from diagnosis) (p < 0.001) (Fig. 3c). survival rate (i.e., 61.0% 5-years survival) than those with Women accounted for 60.0% of the 80 patients diag- regional/distant disease (i.e., 27.1% 5-years survival) nosed in 2005–2006 with a CRC (Table 3). Advanced (p-value = 0.0041) (Fig. 4b). Furthermore, CRC patients stage of disease was documented in 49 out of 80 patients with a regional/distant stage of disease had an elevated (61.3%), and a well or moderately differentiated grade of risk of death, as compared to those with a localized dis- cancer was documented in 53 out of 80 patients (66.3%). ease (HR = 3.38, 95% CI: 1.57–7.29) (Table 3). Similarly, Panato et al. BMC Cancer (2018) 18:632 Page 5 of 10 Fig. 2 Kaplan-Meier estimates of survival probabilities among 178 women diagnosed with breast cancer: overall (a); according to stage (b); and grade (c). The Gaza Strip, 2005–2006. The sum does not add up to the total because of missing values survival rates between patients with a well/moderate types of treatments), as compared with those who had grade of CRC (i.e., 53.9% 5-years survival) and those little (i.e., only one type of treatment) or no access (one with a poorly or undifferentiated grade (i.e., 13.6% patient) to anti-cancer therapies (Table 3). 5-years survival) were significantly different (p-value< 0.0001) (Fig. 4c). Likewise, CRC cases diagnosed with Discussion poorly or undifferentiated CRC were at 3.57-fold (95% Female BC and CRC are among the most common can- CI:1.87–6.81) higher risk of death than cases with well/ cers diagnosed every year worldwide in both more- and moderate grade of disease (Table 3). less-developed WHO regions . These cancers are Patients who had been treated with two or more very common also in the Gaza Strip, where the present anti-cancer therapies presented a reduction in the risk of study attempted -for the first time- to estimate the sur- death (HR = 0.36 for those who received 2 out of three vival of people diagnosed with cancer in the Gaza Strip. modalities; HR = 0.11 for cases who underwent all 3 Our findings indicate that 65.1% of women with BC, and Panato et al. BMC Cancer (2018) 18:632 Page 6 of 10 Fig. 3 Kaplan-Meier estimates of survival probabilities among cases 722 cases diagnosed with colorectal cancer: overall (a), according to sex (b) and age class (c). Gaza Strip, 2005–2014 50.2% of patients with CRC were alive after 5 years the luminal B sub-type had a 5-year survival around from diagnosis. In the subgroup of patients with avail- 30%. A possible explanation of these results could be the able clinical information, the majority of patients were small sample size . diagnosed at an advanced stage. Concerning survival after CRC, a study conducted in In agreement with our results, a Jordanian study dis- Israel among Bedouin Arab and Jewish patients with closed a five-year survival for BC patients of 59.3%, CRC is worth mentioning . The five-year overall sur- showing that grade and stage had a significant effect on vival was about 65% in both ethnic groups. However, the survival rates . Mean age at breast cancer diagnosis mean age at diagnosis was lower for the Bedouin Arab was similar in Jordan , in Egypt , and in the Gaza population (i.e., 57 years) than for the Jewish population Strip. The median survival time after BC in Egypt (i.e., (i.e., 69 years), pointing to a survival disadvantage for 83.8 months) was equal to the estimate in the Gaza Strip the Bedouin Arab ethnic group . The 40% five-year (i.e., 83.7 months)  in 2005–2006. Furthermore, in survival for patients living in the Gaza Strip indicated a Uganda 5-year survival probability was between 50 and greater disadvantage in comparison with both Israeli 60% after a BC diagnosis, and in particular women with ethnic groups. Panato et al. BMC Cancer (2018) 18:632 Page 7 of 10 Table 3 Hazard ratios (HR) of all-cause deaths, with corresponding 95% confidence intervals (CI), among 80 cases of colorectal cancers diagnosed in 2005–2006 in the Gaza Strip according to clinical characteristics Cases Deaths (N = 46) N N (%) HR (95% CI) Age at diagnosis (years) < 60 44 23 (52.3) 1 ≥ 60 36 23 (63.9) 1.38 (0.77–2.48) Sex Male 32 20 (62.5) 1 Female 48 26 (54.2) 0.88 (0.48–1.59) Stage Localized 27 10 (37.0) 1 Regional/Distant 49 35 (71.4) 3.38 (1.57–7.29) Grade Well and moderately differentiated 53 23 (43.4) 1 Poorly differentiated and Undifferentiated 22 19 (86.4) 3.57 (1.87–6.81) Surgery No 9 9 (100.0) 1 Yes 71 37 (52.1) 0.27 (0.13–0.62) Chemotherapy No 10 8 (80.0) 1 Yes 70 38 (54.3) 0.37 (0.16–0.87) Radiotherapy No 58 38 (65.5) 1 Yes 22 8 (36.4) 0.24 (0.10–0.56) Number Therapies 0–1 18 16 (88.9) 1 2 40 22 (55.0) 0.36 (0.17–0.74) 3 22 8 (36.4) 0.11 (0.04–0.31) a b c Estimated using Cox proportional hazard model adjust for sex and age; Reference category; The sum does not add up to the total because of missing values The comparison of data from the GCR with those 71.1% in Izmir, Turkey, in women diagnosed from 1995 from highly-developed countries highlighted substantial to 1997 and followed-up to 2003, or to 61.3% in Saudi differences. In the Gaza Strip, the percentage of BC pa- Arabia, among women diagnosed in 1994–1996 and tients with localized disease at diagnosis was about half followed-up to 2001 . Similar variations emerged, at than that recorded in most European countries, and population level for survival after CRC diagnosis, from a similar to the picture described in eastern European raw 5-year survival of nearly 23% in Setif to 52% in Izmir countries . For CRC cases, the proportion of lo- . calized diseases in the Gaza Strip was about two-fold Among the study strengths, the survival of cancer pa- higher than that documented by Italian cancer regis- tients living in the Gaza Strip was assessed at a popula- tries . With respect to treatment, the proportion tion level, while other studies were previously conducted of patients in the Gaza Strip who underwent chemo- in clinical setting [22, 23]; moreover, we described the therapy and/or radiotherapy was higher than the propor- heterogeneity survival. On the other hand, accuracy and tion of Italian patients (88% vs. 39 and 28% vs. 10%, completeness of data collection, in this study, might respectively). have suffered of potential limitations. With regards to In contrast with widely available estimates of cancer the accuracy of information, the data from the GCR may incidence rates, survival estimates at population level in have suffered of limitations due to the socio-economic less developed countries -including the WHO EMR- are situation and to the conflicts in the Gaza Strip, which less common . The 5-year raw survival after BC var- may have limited the activity of the health personnel ied substantially, from 38.8% in Setif (Algeria) to working in the West Bank and in Gaza. Furthermore, Panato et al. BMC Cancer (2018) 18:632 Page 8 of 10 Fig. 4 Kaplan-Meier estimates of survival probabilities among 80 cases diagnosed with colorectal cancer: overall (a); according to stage (b); and grade (c). The Gaza Strip, 2005–2006. The sum does not add up to the total because of missing values because of cultural taboos (e.g., negative and false per- updated indications on the state of oncologic health care ception toward cancer patients with a consequent isola- in the Gaza Strip. Moreover, it tries to address the prob- tion from family members), cancer patients tend to lematic cancer care situation in this population. conceal their disease, which hinders their access to local The closure policy of the Gaza Strip for security rea- hospitals. Concerning completeness, although cancer sons has caused an isolation of Gaza citizens. This isola- registration in the Gaza Strip started in 1996, it still faces tion has affected the possibility to have adequate cancer several obstacles such as lack of appropriate hardware and care for many cancer patients living in the Gaza Strip. In software, insufficient staff, and training of health particular, the denial or delay of permits to travel outside personnel. All these concerns represent key issues in the Gaza Strip for cancer patients referred to its two neigh- accurate assessment of the cancer burden in the Gaza bouring countries (namely, Israel and Egypt) limits the Strip. opportunity of adequate diagnosis and/or treatment. Notwithstanding this lack of completeness, our study Moreover, a number of antineoplastic medications are results represent one of the first attempts to provide denied to patients due to the embargo [5, 24]. Panato et al. BMC Cancer (2018) 18:632 Page 9 of 10 Conclusions Friuli Venezia Giulia Cancer Registry, IRCCS Centro di Riferimento Oncologico, Aviano, Italy. In view of this already acknowledged difficult social, pol- itical, and economical context, the results from the Received: 3 October 2017 Accepted: 24 May 2018 present oncologic investigation further stresses the need to thoroughly re-assess and overcome the obstacles to a proper delivery of health care to the people living in the References Gaza Strip. 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