Repeated Cross-Sectional Survey of Knowledge and Attitudes to Colorectal Cancer Screening

The continuous awareness campaigns about Colorectal Cancer (CRC) directed towards the Lebanese population in order to foster preventive medicine are on the rise. The impact has been positive and reported in previous research, although the number of victims is still high. This paper aims to perform a recent cross-sectional study of Lebanese residents’ CRC awareness by comparing the findings of two studies carried out in the years 2016 and 2018. The samples of the current study include 1140 (2016) and 993 (2018) participants who completed a simple structured questionnaire directed to assess their knowledge of colon cancer and the behavioral intentions of obtaining CRC screening. Upon comparing results, the percentage of those who know about CRC has increased significantly from 40.4% in 2016 to 78.7% in 2018, the proportion of respondents who believed that family history is the major risk factor for CRC did increase significantly from 47.7% in 2016 to 90.8% in 2018. Likewise, the proportions of respondents who believed that overweight, age, and stress are among the major risk factors for CRC increased from 26.9%, 26.7% and 11.3% in 2016 to 86.2%, 52.1% and 21.51% in 2018, respectively. On the other hand, the proportions for the risk factors related to alcohol and smoking have dropped from 37.7% and 37.3% to 27.4% and 24.2%, respectively. Moreover, the most important source of information for CRC was friends (18.4% in 2016 versus 73.8% in 2018), followed by family (18.7% in 2016 versus 56.7% in 2018), and then physicians (18.9% in 2016 and 40.2% in 2018). In fact, the efforts of the non-governmental organization (NGO) SAID (118 different major activities in the span of 3 years) did make a signifHow to cite this paper: Hejase, A.J., Hejase, H.J., Nemer, H.A., Hejase, C.A. and Trad, M.-A.M. (2020) Repeated Cross-Sectional Survey of Knowledge and Attitudes to Colorectal Cancer Screening in Lebanon. Journal of Biosciences and Medicines, 8, 178-210. https://doi.org/10.4236/jbm.2020.812017 Received: October 27, 2020 Accepted: December 27, 2020 Published: December 30, 2020 Copyright © 2020 by author(s) and Scientific Research Publishing Inc. This work is licensed under the Creative Commons Attribution International License (CC BY 4.0). http://creativecommons.org/licenses/by/4.0/


Introduction
Colorectal cancer (CRC) continues to be one of the principal global health care issues where recent studies have shown that it ranks second to breast cancer among females and third after lung and prostate cancers among males [1] [2]. In 2018 CRC was responsible for about 9.2% of all worldwide deaths caused by cancer ranking second with around 881,000 deaths worldwide [3]. As for Lebanon, in 2018, 1463 (8.5%) CRC cases out of 17,298 new cancer cases were reported for both sexes thus ranking in fifth place after breast, bladder, lung and prostate cancers [4] [5]. Specifically, CRC ranked fourth among males (8.8%) after prostate, bladder and lung cancers; and ranked second among females (8.1%) after breast cancer. In addition, CRC accounted for 7.1% of the number of cancer mortalities with 8976 deaths out of the total number of 41,843 cancer deaths in Lebanon [4].
It is noticeable that the global cancer burden has continuously been increasing whereby in 2012, there were 14.1 million new cancer cases and around 8.2 million deaths due to cancer, then the CRC cases were around 1.36 million (9.7% for both sexes) [6]. Later, the International Agency for Research on Cancer's press release indicated that "The global cancer burden is estimated to have risen to 18.1 million new cases and 9.6 million deaths in 2018. One in 5 men and one in 6 women worldwide develop cancer during their lifetime, and one in 8 men and one in 11 women die from the disease" [7]. In fact, the global burden of the CRC trend is expected to increase by 60% to more than 2.2 million new cases and 1.1 million deaths by 2030 [8]. Likewise, in the USA, the cases of CRC continue to increase yearly by 1% to 2.4% among people in the age range 20 to 40 years, and by 0.55% to 1.3% among people aged 40 to 55 years, respectively. This trend continues to prevail since 1980 [9] [10]. Along the aforementioned facts, Lebanon is not an exception where the incidence of different types of cancer is 179 new cases per 100,000 inhabitants and digestive cancers account for 14.1% of all types of cancer, with more than 50% of them located in the rectum and colon [11]. Further projection studies have revealed that by 2020, overall cancer will reach 361 and 312 cancer cases per 100,000 persons for males and females, re-spectively [12]. In fact, reported information indicates that both cancer incidence and mortality are expected to increase dramatically in the near future [5] [13].
Among those rising trends, the subject of CRC awareness remains a topic of major importance among both the medical and social communities. Indeed, various studies have shown that increasing the levels of awareness leads to an increased rate in screening for CRC and thus reduction in mortality rates [14] [ 15]. CRC is known to be curable if detected early, when it begins as a simple benign polyp at the interior wall of the colon [16] [17]. There is also a reduction in the medical and financial burdens of treatment [18]. CRC awareness has developed over the years and different nations have adopted campaigns and procedures to encourage people especially at ages above 45 years to undergo screening. Simple screening tests like FOBT (fecal occult blood test) and FIT (fecal immunochemical test) that look for occult blood (blood that cannot be seen with the naked eye) are becoming both very popular and affordable to identify blood in the stool which is a strong predictor to the presence of polyps or cancers in the digestive tract [19]. Thus undergoing an FOBT or FIT test can lead to the early detection of CRC cases which can be prevented or at least downstaged through colonoscopy. However, it has been reported that despite the ability to prevent the development of CRC and downstage the disease, the participation in CRC screening lags behind screening for other types of cancer [20] [21]. Screening through fecal testing, mainly fecal Occult blood test (FOBT) and fecal Immunochemical test (FIT) followed by colonoscopy for positive cases has led to an approximately 16% reduction in mortality caused by CRC [9] [22].

CRC Awareness and Screening
The usefulness of CRC screening in terms of reduction of incidence and mortality rates has been shown in randomized controlled trials since the nineties of the past century where early screening procedures were associated with a substantial reduction of CRC incidence and mortality [23]- [29]. In fact, it is well agreed that medical organizations and practice clinical guidelines highly recommend screening in average-risk populations [30] [31] [32].
A recent study by Dénes et al. [9], suggested that awareness efforts should go beyond the general public and extend specifically to health professionals who should be involved in CRC screening educational programs. The aforementioned study performed in Romania on a sample of 275 CRC patients showed that 41.5% of the patients declared that they have heard about cancer screening and only 6.5% about specific CRC screening procedures. Among those who have heard about screening, 85.1% perceived the information through mass media while the rest 14.9% got it from family, friends or colleagues. Unfortunately, the outcomes of the study indicated that health professionals did not contribute at all to informing about screening. ported that even though the levels of CRC knowledge and awareness were high, overall participation in CRC screening was modest. Thus, an essential step is to elaborate on mechanisms to transform public awareness and knowledge into real screening participation because recommended screening and especially colonoscopy has prevented or downstaged CRC [33] [34]. Also Inadomi and Sonnenberg [35]  By the end of the first 20 years of the twentieth first century, the issue of CRC awareness continues to be a major topic of research among medical and social professionals. A recent study regarding knowledge, practice and attitude towards CRC and its screening procedures among people of Hong Kong showed that 60.9% of the people were unaware that CRC is a very common type of cancer and 91.5% responded that there wasn't any case of CRC in their family [36].
Even in first world countries like England, a recent study among English population showed that only 10% of the participants were aware of the fact that CRC is ranked third among common type of cancers and merely 46% of the people knew some symptoms and risk factors of CRC [37].
Another study done in Kuwait demonstrated that among 675 respondents, 75% of the participants had heard about CRC [38]. A similar CRC study carried out among the population of Perak state of Malaysia concluded that 38% of the 2379 participants of the study had no knowledge regarding CRC [39]. Likewise a study performed in Saudi Arabia indicated that 53.5% of the 385 surveyed Makkah residents were unaware of CRC symptoms and 92.2% never had a CRC screening test [40]. Actually, it has been reported that CRC is one of the most common cancers in Saudi Arabia being the first most common cancer among Saudi males and third among females [41]. A study conducted among people of Oman suggested that 59.6% of them were unaware of basic symptoms and risk factors of CRC and others had poor understanding of screening procedures [42].
It can be easily concluded that around the globe there is a significant fact that people lack basic knowledge regarding CRC. This trend is also very common in western countries. In reality, the lack of knowledge on CRC happens to be a noticeable barrier to screening adherence [43].
Moreover, in a study conducted in Iran assessing the practice of Iranian physicians towards CRC showed that for 71 out of 123 physicians (57.7%), colonoscopy is the first-step screening test in average-risk individuals above 50 years; and only 22 physicians (17.9%) designated FOBTs as the first step for the above It is noticeable that even though Iran is experiencing a significant rise in the incidence of CRC over the recent decades [45] the aforementioned Iranian physicians study which was performed in 2018 did not include any reference to FIT CRC screening tests which are nowadays very popular in the health sectors. Despite its relatively high financial cost in comparison to other CRC pre-screening procedures, the surveyed physicians cited colonoscopy in first place followed by FOBT's. Actually, this information is similar to the Saudi physicians' survey where most of the physicians considered colonoscopy as the most effective screening test while only one-third of them agreed with FOBT [46]. Here, it is worth mentioning that the 5-year survival for persons with colorectal cancer is 64% in the United States. If the disease is detected at an early stage, the 5-year survival rate increases to 90%. However, because of lack of screening programs in many countries, only 39% of colorectal cancers are diagnosed at this stage [47].
Once more, in the Middle East and specifically in Oman, a study was carried out to specifically explore nurses' and physicians' (82 nurses and 60 physicians who are clinically experienced with mean service time 9.39 years and standard deviation 6.13 years) attitudes and knowledge regarding CRC screening. The findings showed that both nurses and physicians working in primary care settings have inadequate knowledge regarding CRC screening (more than 55% did not know the frequency of performing specific screening procedures, the upper age limit at which screening is not recommended, and the patients at high-risk for CRC).
Almost the same results were found in a Jordanian study where the knowledge of CRC among the majority (69.1%) of nurses and physicians working in primary care settings was very poor [48]. Actually, it looks that a principal barrier to undertake CRC screening by eligible patients is the inadequate knowledge among health care professionals.
According to Tfaily et al. [49], in a study performed in Lebanon among 371 participants (more than half of them had a university level education) who were surveyed in a major health care medical center showed that 83% and 67% of participants were not aware of CRC risk factors and warning signs, respectively, 15% have previously undergone CRC screening, 56% were aware of the necessity for screening, and 43% were willing to undergo screening. Once again, the aforementioned study did ignore existence of the popular FIT screening test where it was reported "50% of patients who were planning to get screened in the future selected FOBT as their preferred method of screening and 42% preferred colonoscopy. The remaining 8% chose neither or no preference".
In a study performed in eight Louisiana federally qualified health centers [50] among 975 patients who were 50 years or older not up to date with CRC screening (52% of them had low literacy, i.e. less than a 9 th grade level); the majority of participants had positive beliefs about the benefits of CRC screening using FOBTs, but only slightly over a third of all participants stated ever receiving a physician recommendation for CRC screening and fewer recalled being given an FOBT kit. These outcomes did not vary by literacy and clearly pointed to the limited physician recommendations.
In Hungary, the results of a study conducted among 1150 adults between the ages of 40 and 70 using quota sampling showed that 81.2% of the respondents were not well-informed about the risk factors of CRC; likewise, 79.0% were not well-informed about the symptoms of CRC, and 27.0% of respondents had not heard of CRC screening methods before [51].
In a survey administered to a representative population of the United States of America formed of 6349 participants, the term "Colonoscopy" was recognized by 80% of participants (over the age of 35); however, only 35% of the respondents perceived it as a major method for colon cancer screening. Gender played a major role in colon cancer knowledge. Women (42%) were more likely than men (27%) to understand that colonoscopy tests were for colon cancer. More women than men were aware of colonoscopy (64% versus 36%). Age did not play a major role in cancer knowledge. Older patients were more likely to know that colonoscopy detects colon cancer (50 -64 years 45%, 35 -49 years 33%).
The youngest age group (18 -34 years, 65%) was less likely to have heard of colonoscopy (82% -88% in the older age groups). Employment status did not influence colon cancer knowledge [52].
"The American Cancer Society (ACS) [19] has recently issued a qualified recommendation to initiate colorectal cancer (CRC) screening starting at age 45 years in average-risk individuals. The rationale for this recommendation is that 1) US epidemiologic data show an increase in CRC incidence in individuals younger than 50 years, 2) there is concern about a birth cohort effect with individuals aged 45 to 49 showing increasing CRC incidence rate ratios since 1949, and 3) updated simulation models show a favorable balance of benefit of risk from initiating screening at an earlier age" [53].
It is well known that behind CRC screening there are two main objectives: to reduce the incidence of CRC by detecting and removing adenomas and to reduce mortality by detecting CRC at an early stage [54]. The study performed by Larsen et al. [54] completed in Denmark aimed at assessing the effectiveness of FIT tests as an early screening tool for CRC. The reported results indicated that the FIT-based CRC screening program detects CRC in earlier stages and thereby secures a better prognosis for the patients.
In order to increase awareness and direct higher percentages of the Lebanese population towards early CRC screening, the authors in conjunction with the SAID NGO CRC awareness organization exposed the citizens to a new tool of spreading awareness being a giant inflatable, walk-through colon model equipped with physical depictions of healthy tissue, polyps and CRC [55]. The research findings showed that upon comparing results before and after making the inflatable colon tour, that the use of such a tool does increase the knowledge  [56] and results showed that "participants demonstrated that the inflatable colon increased participants' knowledge about CRC and its screening. It also improved their attitude toward discussing and undergoing CRC screening" (p. 171).
So, the main objective of the present study is to assess the levels of CRC awareness in Lebanon and how these levels were influenced by the massive NGO awareness campaigns that took place in a time span of three years, more precisely from the beginning of 2016 till the end of 2018. In reality, and as far as the authors know, this current study is a unique "Repeated Cross-Sectional" study that compares the Lebanese CRC public awareness over a span of three years.
The newest part of this current study was administered over the Lebanese territory during the last quarter of 2018. Data was collected using a simple questionnaire via face to face interviews with more than 1000 randomly selected people.

Methodology
This study adapts a Repeated Cross-Sectional research design. In longitudinal research studies participants are largely or entirely different on each sampling occasion and may analyze multiple variables at a given instance. Nonetheless, cross-sectional studies require less time to be set up, and may be considered for preliminary evaluations of association prior to embarking on cumbersome longitudinal-type studies [58]. Such a study is useful since it adds a dynamic component to the study of cross-sectional units and allows the investigation of time-varying relationships.
Thus, the aim of this study is to perform a recent cross-sectional study of Lebanese residents' CRC awareness and compare the findings with those from an

Sampling
The Repeated Cross-Sectional study is based on two randomly picked samples from different locations selected from the Lebanese territory. The newest study realized during 2018 was directed to 1028 participants based on Cochran's formula [59] with 95% confidence level, 3% of error and considering the awareness level of 59.6% achieved in 2016 [57]. Only 993 valid responses were collected to perform the 2018 study. The study that was realized in 2016 was based on a sample of 1140 participants. Both cross sectional studies were administered over the whole Lebanese territory with more emphasis on the more highly populated areas.

Informed Consent
The detailed purpose of the study and the informed consent [60] assuring the confidentiality and anonymity of the personal data as well as the optional participation were outlined in the first section of the survey. Study participants were largely or entirely different on each sampling occasion. In each previously conducted research, participants were clearly informed about the research objectives, and were transparently assured confidentiality of their responses, therefore all participants were willing to offer their responses and had no objections whatsoever or concerns either physically or emotionally while participating in this endeavor. No clinical trials, procedures, or medical testing were needed or performed.

Survey Design
A structured survey was used which included demographic data (age, gender, marital status, and education level). and based on open-ended questions and questions with a multiple-choice format. Multiple answers per question were permitted when applicable. The questionnaire was written in Arabic, which is the native language in the area of interest, and included a part pertaining to the level of participant's knowledge of said topic, followed by a demographic section.
The main questions of the survey are depicted in Exhibit 1.

Demographics of Participants
The demographics of the participants in what relates to completed years of age at last birthday, gender, marital status, educational level and working status are provided in Table 2.
The population sample of 2016 included 1140 participants, 52% of which were females, and a median age of 35 years. Table 2 shows that married university Journal of Biosciences and Medicines    Table 3.

General Results
Statistical Product and Service Solutions (SPSS) software V.26 was used to manage and analyze the data after being verified and coded [59].
As shown in Table 4 As for the questions related to knowledge about CRC risk factors, Table 5 summarizes   On the other hand, results of asking those who are aware of colon cancer if smoking and alcohol are factors associated with CRC show that the proportion of those who affirmed the association (smoking to CRC) and (alcohol to CRC) did decrease from 37.3% in 2016 to 24.2% in 2018 and from 37.7% in 2016 to 27.4% in 2018, respectively. Both results were confirmed with the Chi-Square test of independence as shown in Table 5.
In summary, the Lebanese population is becoming more aware that age, family history, stress and obesity are risk factors that are associated with increased risk of colon cancer; while smoking and alcohol are becoming less popular in what relates to their association with CRC risk.
As for symptoms of CRC, Table 6 discloses that in general the awareness about the symptoms of CRC has significantly increased from 2016 to 2018. In fact, reported results show that among those who are aware of colon cancer, the percentage who believes that abdominal distension (bloating), blood in stool, change in bowel habits, and gases are CRC symptoms did increase from 36  in 2018 for the fourth. Table 6 reports the corresponding Chi-Square tests of independence results which affirm that there is significant increase from 2016 to 2018 in the percentage of those who believe that abdominal distension, blood in stool, change in bowel habits and gases are CRC symptoms. Table 7 presents the respondents' answers for their main sources of information in what relates to knowledge about CRC. The proportion of those who chose "doctor," "nurse," "friend" and "family" did increase from 2016 to 2018.
Chi-Square tests of independence were calculated and significant dependency was found for relying on a doctor, friend and family, thus concluding that in fact there is a significant increase from 2016 to 2018. However, the Chi-Square test of independence for significant dependency failed for relying on "nurse," thus concluding that in fact there is no significant increase from 2016 to 2018 in the percentage of those who rely on a nurse as their CRC source of information.
Furthermore, results of asking those who are aware of colon cancer if a "newspaper," "magazine," and "media" are their CRC source of information show that the proportion did increase slightly from 2016 to 2018 for relying on "newspaper" and "magazine" but decrease for "media". Chi-Square tests of independence point at a significant increase from 2016 to 2018 in the percentage of those who rely on newspapers while a significant decrease for those relying on media as their CRC source of information, in addition that a no significant increase at 5% level of significance was found of those who rely on magazines as their CRC source of information. Here, it is worth to notice that the results reported for newspapers and magazines agree with the work of Hejase et al. [62] [63] which reported that Lebanon is among the countries which are suffering  from a decline in reading habits and therefore missing information about potential issues.
The proportion of those who chose "Internet" and "others" did decrease from 2016 to 2018 and the Chi-Square test of independence presents a significant decrease from 2016 to 2018 in the percentage of those who rely on the Internet as Similarly, the respondents were asked to provide the age of their relatives who suffer from CRC. Table 10 gives a brief summary of the corresponding statistics.

CRC Awareness and Gender Results
Gender has always played a principal role in colon cancer knowledge. In the 2016 survey, as depicted in Table 11, 46.6% of the females compared to 33.6% of the males were familiar with colon cancer. These figures in 2018 became 73.5% and 82.5% for females and males, respectively. The Chi-Square test of independence was used to test if CRC awareness is related to gender. Table 11

CRC Awareness and Education Level Results
Considering education, a Chi-Square test of independence for the 2016 data, resulted in χ 2 (3, 460) = 27.809 with a p-value < 0.001 indicating that the response to "Have you ever heard or read about colon cancer detection?" was in fact dependent on the level of education with more educated respondents having higher familiarity with CRC detection. Similarly, for the data corresponding to 2018.
It is worth noticing that this feature (higher CRC detection awareness among educated population) did not change through time (see Table 12 for details).

CRC Awareness and Marital Status Results
Considering the marital status of the respondents and its influence on CRC knowledge and awareness of screening, Table 13     In addition, the results of the research showed that the proportion of respondents who believed that family history is the major risk factor for CRC did in-

Conclusions and Recommendations
This paper is the first contemporary research in Lebanon to perform a cross-sectional study of Lebanese residents' CRC awareness and compare the findings with those from an earlier study.
The justification of such a study emanates from the continuous flow of reports and studies addressing the importance of Colorectal Cancer Screening.
The basis for the current research was two papers reporting the use of several  [67]. Further, this paper has its first merit from the comparative assessment of the collected and analyzed data and facts from all the aforementioned events; in addition, results and outcomes enrich the current scarcity of information about the topic.
According to Mamlouk et al. [16], CRC is naturally developed, as a malignant transformation of a benign adenoma in the majority of cases. Therefore, Bonnington and Rutter [17] argue that the aforementioned fact gives hope that the detection of adenomas and polyps with malignant potential could reduce the mortality rate. Thus, there is a continuous and urgent need to launch population-wide campaigns that assist to inform the Lebanese residents about cancer, the underlying risk factors, and the promising remedies [5] [55] [56] [57].
This study presents significant evidence that the cumulative use of more than 135 different activities by SAID NGO [68] including the use of a giant inflatable colon [tunnel like] increases knowledge of colorectal cancer and its corresponding screening practice. According to SAID's president, "These activities have directly affected 8000 people of all ages. A total of 1200 free FIT tests were performed and 95 colonoscopy procedures were performed, by the association, to anyone whose results were positive" [61]. The study shows that awareness of the importance of CRC screening did increase significantly from 40.4% in 2016 [57] [69] to 78.7% in 2018 [55] [70]. Furthermore, since 2018, the implications of the dynamism of SAID NGO and other associations continued to produce more awareness campaigns based on the fact that the lack of awareness on CRC and its common risks and symptoms terminology is a barrier to CRC screening. Accordingly, the issue needs to be more highlighted among members of the society. Dr. Jamil Jabbak, Minister of Public Health, announced that the Rafik Hariri hospital will be presenting 1000 free FIT tests to those benefiting from the Ministry of Public Health's services (those without insurance). This grant is provided by Fuji Film International. Also, this is the first time that the Ministry of Public Health has launched a national campaign to raise awareness on colon cancer, something that was deemed necessary given the increasing numbers of patients.
At the end of the announcement, an educational film prepared by the Ministry of Health, was screened, urging citizens to carry out FIT examinations every year. Furthermore, an informational pamphlet (see Figure 4) was launched to the public supported by the Lebanese Association of Gastroenterology, the Lebanese Society of Medical Oncology, the Ministry of Public Health, and surely SAID NGO (the only civil society organization in Lebanon that is specialized in raising awareness on the early detection of colon cancer) [61].
This study reflects current health education of several community groups,  which could help guide establishing local screening protocols, in addition, to inclusion in health provider curricula. Moreover, as the study guides policy makers in making and adjusting policies to achieve a more effective performance, it will help the specialized NGOs to grow, resulting in enhanced standards of living of the community at large. There is a continuous and urgent need to launch population-wide campaigns that assist to inform the Lebanese residents about cancer, the underlying risk factors, and treatments.