Exploring the Barriers Related to the Healthcare System and Healthcare Professionals in Implementing Quality Intravenous Chemotherapy: A Qualitative Study


 Purpose: This study aimed to explore barriers related to the healthcare system (HCS) and healthcare providers (HCPs) in implementing quality intravenous (IV) chemotherapy (CT) from the perspectives of cancer patients, family caregivers, and healthcare professionals.Methods: Using an explanatory descriptive qualitative method, this study was conducted in 2019. Forty-one participants (6 patients, 5 family caregivers, 12 oncologists, and 18 nurses) were selected through purposive sampling. In-depth semi-structured interviews were conducted to collect the data, which were analyzed using qualitative content analysis. Lincoln and Guba’s criteria of rigor were employed to ensure the trustworthiness of the study.Results: Data analysis showed two categories, each with three subcategories: Barriers related to HCPs that contains “educational and communication barriers”, “failure to establish trust” and “unskilled healthcare professionals”; Barriers related to the HCS, which consists of “inadequate physical and care infrastructures to provide services”, “lack of support in the disease trajectory from diagnosis to rehabilitation” and “mismanagement of CT wards/procedures”.Conclusion: The identification and removal of the barriers related to HCPs and HCS from routine care are crucial. Education of and communication with cancer patients and their family caregivers are two important pillars in the quality of intravenous chemotherapy (IV CT) and this education and communication should be based on individualized care and tailored to the unique needs of each patient.


Introduction
Cancer is an important public health concern globally. It is the second most frequent cause of death all over the world (1). It is expected the global cancer burden with a 47% rise from 2020, to be 28.4 million cases in 2040 (2). CT is one of the main methods of cancer treatment (3). Most cancer patients undergo IV CT, although there is a shift to use oral CT more (4). Nevertheless, most oncologists prefer IV CT drugs, because they can be certain of the administration of the accurate dosage of medications (5). IV CT increases survival rate (6). However, besides this privilege, it affects adherence to treatment and quality of life of patients and becomes a factor in the refusal of patients to complete the treatment course because of its side effects (3). Adherence to IV CT is assured as long as cancer patients keep their appointments for each scheduled CT cycle (7). Adherence is a complicated and multi-faceted issue that is related to many factors that affect the drug use behaviors of patients (8). Therefore, non-adherence with long-term pharmaceutical treatments is the main concern in chronic diseases (9). In the present study, the term IV CT quality means timely CT without changing the appropriate dose.
The emphasis on IV CT administration in outpatient centers requires patient adherence and acceptance to refer. So, it is important to pay attention to factors related to the quality of IV CT. In a study by Lyman, dose reduction and treatment delay were observed in all CT regimens (10). One-third of the patients who need adjuvant CT due to colon cancer start their treatments later than the time recommended by national guidelines (11). Twenty percent of all patients received CT dose reductions greater than or equal to 15%, and the dose delay was greater than or equal to 7 days (12). The failure to continue CT and delays in treatment are common (13). Since the proper administration of medications is considered as key to the success of the treatment (14), suboptimal doses of CT are associated with reduced survival and with treatment outcomes below the desired level (9,15,16). Poor adherence of the patient with the prescribed medicines and other aspects of the medical treatment can inversely affect treatment outcomes in many chronic diseases (4,17). It has been observed that, for various reasons, some patients have failed to continue with CT and therefore treatment has been unsuccessful (5), which is a signi cant problem for those involved in global and public health (17).
On the one hand, the factors associated with the delays are not clear (16). Many patients are reluctant to express their concerns and doubts about their medications because they are worried about displeasing the HCPs (18). On the other hand, we need better methods and more open and honest discussions about drugs and adherence are needed to overcome this problem (18). How can HCPs help patients by involving them in the decision-making process about the prescription and administration of drugs, so that they can make more informed decisions? How can the HCPs support patients in adhering to the prescribed medications (18)? Since healthcare providers are expected to play an important role in increasing adherence, designing and implementing interventions to in uence what they do seems like a reasonable approach (20). The identi cation of the factors related to and affecting adherence to IV CT is highly valuable in improving clinical practice (19). Studies should be conducted on the role of structural, HCP, and patient factors in CT delay to identify potential interventions (20). Understanding the potential barriers and factors that affect patient's adherence would help HCPs develop strategies to enhance/improve patients' adherence (21).
In the literature review, only two related studies were found (6, 13), in which the barriers related to the healthcare system and healthcare professionals in implementing quality IV CT have been addressed. In general, because the available knowledge and information on this problem are not su cient, it became clear that it is important to carry out this study, and the descriptive-qualitative design was selected. The descriptive-qualitative approach is appropriate for research questions focusing on discovering the who, what, and where of events or experiences and on obtaining insights related to a poorly understood phenomenon from informants (22). Moreover, one of the implications of qualitative research is to gain information in areas where the body of knowledge is not su cient.
In the present study, we intended to explore the barriers related to the HCS and HCPs in implementing quality IV CT. It was important to conduct this study because understanding these barriers can help health policymakers remove them. Given the importance of quality IV CT in increasing patient survival, this study was conducted to explore the barriers associated with HCPs and HCS in the implementation of quality IV CT from the perspective of nurses, oncologists, patients, and family caregivers.

Study design
The descriptive-qualitative (DQ) design method was used for this study. In this method, the results are a straightforward descriptive summary of the contents of the data that is organized in a logical way (23). These studies are less interpretive than other qualitative methods (24).

Participants
Participants from different settings were recruited by purposive sampling ( Table 1). The participants were selected from the four groups of family caregivers, patients, oncologists, and nurses. For the patients, the inclusion criteria were age ≥ 18 years, having taken at least one course of IV CT, awareness of the diagnosis, and having no physical or cognitive impairments affecting their participation. Inclusion criteria for family caregivers were having a close caring relationship with the patient and no physical and cognitive impairments. The only inclusion criterion for oncologists and nurses was having at least 1 year of working experience in the oncology/CT wards.  What are your experiences with regard to the personnel?
Can you explain more?
What are your impressions on the barriers to successful and timely intravenous chemotherapy?

Doctors and nurses
What are your experiences with regard to the healthcare staff-related barriers to the implementation of intravenous chemotherapy?
What experiences do you have about the health system-related barriers to the implementation of intravenous chemotherapy?
Can you explain more?

Procedure
Data were collected from July to October 2019 using semi-structured in-depth interviews with 41 participants. The interviews were conducted in a calm and quiet environment like clinic o ce room / workplace / vacant patient room taking into account participants' convenience. The sampling was stopped when data saturation was achieved. All participants had completed the written informed consent form before interviews were conducted. The mean duration of the interviews was 30-90 minutes. Some of the codes were obtained from the researcher's eld notes. A number of open-ended questions guided the researcher in gathering the information. The main question in this study was "What is your perception of the barriers to quality and timely implementation of IV CT?" Other questions were subsequently raised to attain more in-depth information. Some interview questions have been presented in Table 1.
Concurrently with data collection, data analysis was performed, too. The interviews were audio-recorded after the interviewee's agreement. At the end of each interview, the recorded statements of the participant were listened to repeatedly, and the statements were transcribed verbatim. In the present study, the second author (MS.M.) conducted face-to-face interviews with participants. She had interests in the research topic and transcribed the interviews verbatim. The rst author (S.S.) analyzed the typed transcripts.
In the present study, the four criteria proposed by Lincoln and Guba (29), including credibility, con rmability, transferability, and dependability, were used to ensure the rigorousness of the study. To ensure credibility, the extracted codes were sent to the participants for con rmation. Their con rmation indicated the validity of the codes (member check). Additionally, the researcher sent the ndings and extracted codes to be examined and validated by an expert on qualitative research (N.B.) (peer check). To improve con rmability, bracketing was used, and also the stages of the study and the decisions made during it were recorded and reported in detail so that other researchers can follow the audit trail if they so wish. More than one researcher was involved in the data analysis process to ensure dependability. In the present study, the second author (MS.M.) revised the coding process. We asked the external expert colleague (N.B.) to revise the coding and categorize. Transferability was made possible by selecting participants from various locations and with different demographic characteristics. In the present study, the participants were selected from different settings.

Data analysis
The content analysis approach proposed by Graneheim and Lundman was applied (25). Each transcript was studied several times to understand the experiences and impressions of the participants. In the transcripts, sentences containing signi cant or relevant information were underlined to highlight important statements. Then meaningful units were summarized in condensed form and the initial codes emerged. S.S. studied the initial codes thoroughly and classi ed them into subcategories based on their similarities in the concepts. Through this inductive procedure, similar subcategories were classi ed into the main categories. This coding process and the emergence of the main categories were reviewed and discussed by the second author (MS.M.) and by an experienced researcher (N.B.) with S.S. Finally, categories were determined as the expression of the implicit content of the transcripts.
All authors are faculty members of medical universities and have Ph.D./M.Sc. degrees in nursing/ English language education. The rst/second authors are female and the third author is male. All of them are trained and experienced in the methodology of content analysis. The participants were included in the present study from the target population by purposive sampling. There was no previous relationship between the researchers and the participants. Only a relationship was established prior to the commencement of the study to introduce the researcher, to explain the reasons for doing the research, and to take the written informed consent of the participants.

Results
The participants in the present study included 41 individuals, namely 6 patients, 5 family caregivers, 18 nurses, and 12 oncologists (Table 1).
Data analysis led to the emergence of 200 codes and two main categories, each with three subcategories: 1. Barriers related to HCPs consisting of "Educational and communication barriers", "Failure to establish trust", and "Unskilled healthcare professionals"; 2. Barriers related to the HCS, which consists of "Inadequate physical and care infrastructures to provide services", "Lack of support in the disease Because the lack of education or incomprehensibility of the information given to the patient and her/his family causes fear and panic and exacerbates their mental conditions, it can cause frustration and lack of follow-up with the treatment. One barrier to starting and continuing IV CT was the lack of individualized patient education, which means the "lack of speci c education appropriate to the patient's individual condition." Participants experiences showed that inaccurate and un-individualized education might lead to the patients' distrust. Moreover, wrong information received from specialists other than oncologists undercuts the patient's morale, such that he/she does not refer for CT.
Participants stated that one of the issues that cause distrust in the patients is non-native oncologists and the resulting communication problems. If patients do not trust their HCPs and HCS and they are not acceptable to them, the CT process will fail.
The participants' experiences showed that lack of technical skills and practical knowledge are effective barriers to IV CT. The participants of the present study cited unawareness of surgeons of the stages of CT, improper administration of CT drugs, delays in diagnosis, and consequently patients' delayed referrals, lack of skills in identifying patients at risk of poor adherence to treatment, and lack of experienced nurses in the wards as barriers in starting and continuing the CT process.

Category 2: Barriers related to the HCS
The participants cited inadequate numbers of beds for the timely hospitalization of patients undergoing CT, long waits for their turns, lack of a clean and calming care environment to provide favorable care, lack of desired treatment of the patient due to lack of a multidisciplinary team, absence or shortage of some CT drugs prescribed to patients, and inadequate numbers of quali ed CT nurses and specialists in the HCS as the barriers to the quality implementation of CT.
Participants described the need for the continuous and ongoing support of cancer patients from diagnosis to rehabilitation, the absence of which would challenge the CT process. The participants pointed to the importance of post-CT support and health professionals' lack of time in educating patients undergoing CT. The high cost of drugs and the scarcity of drugs are other barriers to the effective implementation of quality CT.
Participants concluded that poor management/supervision of the CT process and CT wards, the inadequate number of oncological nurses, inadequate numbers of expert HCPs in health teams to provide quality care, failure to train HCPs and its consequences, involuntary employment of nurses in CT departments, and authorities' failure to support these nurses are factors contributing to lower quality of care during CT, and which act as barriers to the quality administration of IV CT.
The shortage of quali ed HCPs in the health team to provide quality care is a barrier to the implementation of quality CT. Participants noted a lack of training courses for nurses and HCPs involved in the CT process and that this could reduce the quality of care. Inadequate training of nurses in essential work areas leads to de ciencies in their skills, for instance, in inserting an IV line and in administering IV drugs.
Participants considered disinterest in work and forced service of some nurses in oncology wards and the authorities' failure to provide support for nurses working in CT wards as barriers to successful CT. The forced employment of nurses in CT departments reduces the quality of care.

Discussion
The purpose of this study was to identify barriers related to HCPs and HCS in the implementation of quality and timely IV CT. In the present study, participants noted miscommunication between HCPs and patients, especially during patient education, and subsequently patients' distrust as barriers to the implementation of quality IV CT. Other studies con rm that one of the most important factors in the healthcare system that affects adherence is the relationship that care providers establish with patients (26). Findings from a study by Wu et al. showed that some patients reported that incidents of nonadherence occur due to inadequate training or unavailability of immediate medical guidance. One of the reasons for non-adherence includes physician-patient communication issues (27). According to Ghoshal et al., newly diagnosed cancer patients report more distressing symptoms, however, oncologists do not pay enough attention to them (28). Poor communication, lack of trust, and patient dissatisfaction and distrust in caregivers are also involved in poor adherence (21).
The purpose of education and proper communication with the patient is to empower patients in self-care and management of CT complications, which increases the patient's adaptation, tolerance, and adherence to CT and results in more successful treatment. Therefore, if the education of and communication with the cancer patient are not carried out well, this can be a barrier to implementing quality and timely CT.
In the present study, non-native HCPs and the resulting communication problems and poor attention to communication and patient education and providing inaccurate and wrong information to patients and family caregivers caused a sense of distrust in the HCS and HCPs and prevented patient referral.
Therefore, it may be a barrier to timely visits and quality of CT or the continuation of the CT process.
Dean's study showed distrust in HCS is negatively related to treatment adherence, de ned as the failure to initiate or complete physician-recommended adjuvant treatment after breast cancer (29). The barriers to adherence include physicians' failure to accurately explain the bene ts and side effects of CT, lack of attention to costs, and poor communication regarding treatment (30).
Participants noted HCPs' lack of practical knowledge and skills and lack of communication skills and training as barriers to effective chemotherapy. Evidence suggests that health professionals have poor skills in accurately identifying non-adherent patients (31,32). Sharour also showed that nurses' knowledge about chemotherapy management was insu cient, affecting the quality of care for patients with drug extravasation (33). A study by Salarvand et al. showed that nurses working in chemotherapy departments did not have su cient skills in IV line insertion and control of drug extravasation. The same study showed that oncologists' skills in establishing communication and giving bad news to patients are essential when providing care to such patients (34). These mentioned cases can lead to a decline in the quality of care and lack of quality IV CT.
Some participants mentioned a lack of clean and calming care environments. In a study by Summerhayes, nurses and pharmacists expressed the need for sanitary rooms and space (35). A study by Salarvand et al. showed that the development and improvement of care and physical environment to provide services, the need to maintain personal and environmental hygiene during the course of chemotherapy by patients and their families, emphasis on a calming chemotherapy environment in terms of structure, personnel, and facilities, and the need to maintain the privacy and respect of the patients undergoing chemotherapy were among the care needs pointed out by oncologists that were lacking (34).
Participants in the present study cited drug shortages as a barrier to timely and successful CT. Studies have shown that drug shortages are common in the United States and have increased signi cantly over the past decade (36). Delays in treatment, disruption of treatment, lack of treatment options for certain cases, and replacement of drugs in less effective and harmful regimens can adversely affect the prognosis and outcomes (37). The shortage of injectable chemotherapy drugs puts the successful treatment of cancer patients at risk (38).
Participants cited insu cient numbers of nurses and chemotherapy HCPs in the care system as a barrier to quality CT. Wise has reported that the shortage of specialist oncological nurses in the chemotherapy department caused this ward to be closed down at a hospital (39). The shortage of HCPs leads to increased workload and pressure on other staff, which will hinder the quality of care during IV CT.
Participants stated a lack of follow-up and patient support from the time of diagnosis to rehabilitation as a barrier to quality CT. Other studies con rm that a lack of patient support in various aspects can lead to failure to show up for follow-up and treatment failure (40). In a study by Salarvand et al., oncologists mentioned that one of the priorities in caring for patients undergoing CT is the existence of comprehensive support for various aspects of the cancer disease trajectory from diagnosis to rehabilitation (34). This may be due to HCPs' unawareness of the needed support or lack of infrastructure to provide the support.
The present study demonstrated that one of the barriers to patients' adherence to IV chemotherapy was a lack of cooperation among HCPs and multidisciplinary teams. Carroll's study also showed that a lack of coordination among individuals involved in cancer care can be a cause of non-compliance and treatment failure (40). If there is no multidisciplinary treatment team in the care structure, this may be a barrier to quality care during CT.
Participants mentioned poor management, including failure to employ expert healthcare professionals, compulsory employment of some nurses in chemotherapy wards and its consequences, inadequate nursing staff and lack of suitable support for nurses working in CT wards by authorities and failure to provide training to healthcare professionals and its consequences as barriers to the quality and successful implementation of IV CT. In the study by Summerhayes, nurses and pharmacists working in oncology wards pointed to HCP shortages, increased workload and stress, increased waiting times, and a signi cant imbalance between CT workloads and HCPs capacity to initiate IV CT (35).
Participants pointed to the forced employment of some nurses in chemotherapy wards and inadequate support for nurses working in these wards by authorities. No study was found on the compulsory employment of nurses in oncology and CT wards and the support and respect they received. Toh found that nurses, who worked in sub-standard work units, often expressed dissatisfaction, stress, and burnout, which encouraged them to seek a new job out of oncology (41).
Participants reported a lack of training for HCPs and, consequently, inadequate knowledge and skills of HCPs regarding the management of IV CT. No completely relevant study was found on this topic. Findings from other studies con rm this. Two studies showed that the number of nurses who were trained in the safe administration of chemotherapy before starting work is small, most nurses receiving this training while working in a CT center. For this reason, nurses experience anxiety, irritability, and fear while performing chemotherapy due to a lack of prior training on the subject (42). Many nursing programs do not teach di cult communication skills such as giving bad news or answering di cult questions (Such as "Am I dying?") . (43) In a study by Salarvand et al., oncologists stated that they had not been trained in the skills of communication with and in giving bad news (36). The fact is that many practical and theoretical skills, such as breaking bad news, the attention to patient assessment and its condition, are not taught adequately in educational curricula and retraining programs. This reduces the quality of CT care.

Conclusion
Identifying barriers related to HCPs, admission and hospitalization facilities for patients undergoing CT, as well as building trust and honest communication, providing support in various aspects of the quality implementation of IV CT and educating the patient and his family, designing effective treatment programs and providing effective follow-up with patients all play a role in improving the quality of CT and