The elephant in the room: Exploring the influence and participation of patients in infection‐related care across surgical pathways in South Africa and India

The irrational use of antibiotics is a leading contributor to antibiotic resistance. Antibiotic stewardship (AS) interventions predominantly focus on prescribers. This study investigated the influence and participation of inpatients in infection‐related care, including antibiotic decision‐making, within and across two tertiary hospitals in South Africa (Cape Town) and India (Kerala).


| INTRODUCTION
Antibiotic use in human populations remains a key driver of antibiotic resistance (ABR) worldwide. 1,2 Unregulated access to antibiotics for patients and the public is an additional risk for the emergence and spread of ABR. [3][4][5][6] However, the lack of access to effective and affordable antibiotics continues to cause more harm than the risk of ABR. 7 Optimizing antibiotic use requires finding a balance between the need for regulation and control of excessive antibiotic use versus ensuring adequate access to those who need them. To do this effectively, we need to engage with the public and patients to bring about a culture of civil society responsibility for antibiotic use. 8 Whilst ABR remains a global challenge, its impact is more significant in low-and middle-income countries (LMICs). 9 In the context of surgery, addressing behaviours and practices related to infection management and antibiotic use across the surgical pathway (before, during and after surgery) is key to tackling important drivers of ABR and to decreasing the burden of surgical infections globally. [10][11][12] Currently, antibiotic stewardship (AS) interventions focus predominantly on prescribers, rarely considering the patient's role in antibiotic decision-making and consumption. 13 This is at a time when patientcentred care, including infection-related care, is becoming increasingly relevant. 14 Very few studies exist on patient involvement in AS, particularly in LMIC settings. 15 There is also a knowledge gap in healthcare professional views on patient involvement in infectionrelated care. This is an important gap to explore as patient involvement is in part dependent on the willingness of healthcare staff to participate in the process. 16,17 Managing inpatient care, in ways that recognize the patient's role as a participant, remains challenging particularly in surgical pathways. 15,18 The surgical patient's involvement in pre-and postoperative care is crucial to optimized recovery, and yet remains difficult to achieve.
Arnstein 19 provides a foundation for research into patient involvement, describing eight rungs of citizen participation from least to most inclusive: Manipulation, Therapy, Informing, Consultation, Placation, Partnership, Delegated power, Citizen control.
Different models for types of patient involvement have been described, one of which is 'co-production', or patient participation, defined as 'user co-delivery of professionally designed services'. 20 At the point of care delivery, this type of involvement describes an approach where health professionals work together with patients (and/or carers) as partners to achieve optimal care. A partnership approach may not, however, be appropriate for all patients under all circumstances, and it has been argued that 'participation should be defined by whatever level the patient is most comfortable with'. 21 To become effective participants in their own infection-related care, however, patients need to understand the basics and complexities of infection transmission and resistance and the role of AS to address ABR. Efforts to raise patient awareness have included written information on websites and leaflets and posters targeting healthcare users and the public, to mention a few.
However, patients and the public in general may be unable to grasp the immediate threat of ABR, partly due to a lack of effective communication strategies and confusion related to the advice and information provided on the subject. [22][23][24] Additionally, the social determinants of health influence clinical interactions and outcomes, 25,26 posing limitations to patients' ability to effectively participate in their own health care. 27 In relation to infection-related NAMPOOTHIRI ET AL. | 893 care, these factors and how they may influence health-seeking and health-providing behaviours remain understudied. 27 This study aims to explore patient involvement in infectionrelated care and the social and cultural factors that influence this from the perspectives of health professionals and patients and their carers in two tertiary hospitals in South Africa and India.

| Study context
South Africa is an upper middle-income country and India is an LMIC.
Over 76% of the global antibiotic consumption between 2000 and 2010 was attributable to the BRICS countries, with India leading the group as the largest consumer of antibiotics in human health. 28 Availability and accessibility to health systems are a challenge in LMICs. In South Africa, the majority (up to 70%) of patients access healthcare through the public sector. 29 In India, whilst public sector healthcare services are available free of cost to patients, due to limited staff and supplies at government facilities, many seek care from the private sector (reported up to 65%), paying out-of-pocket. 30 Annually, 3646 surgeries per 100,000 population are performed in India in comparison to the global estimate of 5000 surgeries per 100,000 patients. 31 South Africa's surgical capacity has been noted to be below international requirements, with a greater concentration of available resources in urban areas. 32,33 Kerala, the state where the study site in India is located, is an atypical state with high literacy rates and better healthcare access and infrastructure compared to the rest of the country. 34 The participating study sites were selected because despite operating in health systems with limited resources, they perform significant number of surgical interventions and have established strategies to rationalize the use of antibiotics.
Adult gastrointestinal (GI) and cardiovascular and thoracic surgery (CVTS) specialties at academic tertiary referral hospitals in South Africa (site A) and India (site B) were included in this study.
Surgical specialties were selected to represent high infection and/or mortality risks. 10

| Conceptual framework
We investigated the explicit and implicit influence and participation of patients and carers in infection-related decision-making across the participating multidisciplinary teams. Whilst we used the definition of culture coined by Spradley: 'the acquired knowledge people use to interpret, experience, and generate behaviours', 37 its application to the clinical context is built upon our existing research spanning different countries in the last 10 years. 11,12,[38][39][40][41][42] The existing research describes the role of hierarchies and the need for clinical autonomy in infectionrelated decision-making in inpatient settings, wherein senior doctor autonomy overrules policies. 11,38,40 Recognizing the gap in knowledge, we have expanded on this research to consider the role of patients and carers in infection-related decision-making. 15

| Nonparticipant observations
Data were gathered from general ward and intensive care unit (ICU) rounds. Four trained researchers and their trainer took notes of their observations, specifically on the following: place, the people involved, actions of participants, related activities carried out, tasks and results that participants tried to accomplish, emotions felt or expressed, the major events that occurred, the discussions that took place, who led the discussions, who acted upon identified plans. In Site B, additional data were gathered from the outpatient clinics, operation theatres and during departmental meetings. A previously used and tested data collection guide 39 facilitated data consistency.

| Face-to-face interviews
Study participants were recruited using convenience sampling and participation was voluntary, at a place and time convenient for the participant. A semistructured interview guide was used for the interviews, differentiated for patients and HCWs. In addition to this, questions that came up during observations were put forth for discussion. Interviews were conducted by the four trained researchers (two trained researchers at each site), with or without the study lead who had provided training.

| Study participants
All HCWs involved in patient care in the surgical specialties of interest were eligible to participate. This included HCWs with different roles, experiences and expertise in the surgical teams and those from nonsurgical teams who had input into the care of surgical patients (e.g., the AS team). Patients admitted to any of the surgical specialties of interest were eligible for inclusion in the study. For the interviews, patients who were prescribed therapeutic antibiotic(s) while under the care of the surgical team(s) were invited to participate. Participants were selected using the purposive sampling technique.

| Data analysis
Before analysis, a coding framework created by the four trained researchers and the study lead was validated through group discussions. Data from each setting were thematically analysed by researchers. Field notes and interview transcripts were analysed using the grounded theory approach-a method extensively used by the research team and published 11 -aided by NVivo 12 ® Pro software. Analyses of data were iterative and recursive, using constant comparison. Following analysis, the researchers discussed emerging themes for revision as required. Redundant themes were removed and other themes were collapsed or expanded as necessary.
The analysis process for each study site was undertaken separately to avoid analytical bias between sites.
The different data collection methods of ward round observations, face-to-face interviews and HCW and patient/care interactions

| Awareness of infections
While some of the patients knew that antibiotics are for treating infections, general awareness seemed to be lacking regarding the specific infection being treated (X1; Table 1). Some patients associated clinical improvement with antibiotic prescription and use, while others discussed the need for antibiotics to treat a virus (X2, X3, X4; Table 1). Prescribers also feel the demand for antibiotics from some patients in site B (X4; Table 1). Patients report a feeling of stigmatization with having an infection, with some demonstrating a lack of understanding of the processes involved in their care (X5; Table 1).
We observed a general lack of awareness of healthcareassociated infection (HCAI) risk among patients at site B. Patients and their carers preferred to remain in hospital as they felt they were safer there, where healthcare attention was closer than at home, despite reassurances from the surgical team that they were fit for discharge (X6; Table 1). The terms used by patients to describe infection in site A highlight how the perspectives of infection and illness differ between patients (X3, X7; Table 1). Patients referred to antibiotics as treatment for 'viruses' or 'germs' (X1, X3; Table 1).
HCWs considered the patient's socioeconomic status and/or level of education to be a factor in their understanding of antibiotic use. Surgeons at site B considered patients with higher educational qualifications to have a better understanding of antibiotic use and misuse (X8, X9; Table 1). In site B, the senior surgeons in the GI specialty took time during the rounds to speak with patients and/or their carers regarding the patient's progress and the next steps for treatment and hence the ward rounds took more time. The ward rounds led by CVTS senior surgeons were found to be much quicker, with less time spent interacting with patients and/or their carers. Across both NAMPOOTHIRI ET AL. | 895 T A B L E 1 Excerpts from study data (interviews and field notes).

Theme Excerpt ID Excerpt from data
A lack of understanding of the threat of infection and ABR

X1
'There was no reason for the presence of germs in my blood. I was told that it was due to blood transfusion. Three persons came to give blood from my son's workplace. Then younger son's friends also came. They are not bad boys. We cannot say the germs are from their blood; or cannot say the germs are in my body … I cannot blame anybody. Any way I was given antibiotic and I had it'. Patient, CVTS, India X2 'Most of the people actually they want some medicine like antibiotic … when they come for review, they will ask why I was not given an antibiotic, my wound is open and all, so the problem is there, they expect some antibiotics from us. They think that antibiotic is secure for them'. GI Surgeon, India X3 'I am getting antibiotics. They are going to give me a certain type of antibiotic … the bottle is now not here … but it is a special antibiotic for that virus'. Patient, GI, South Africa X4 '…there is always a feeling that, you know, if the patient becomes unwell and comes back to the ICU, many of them would ask you that is it because you have not given them an antibiotic'. GI Surgeon, India The consultant turns to the patient and asks if he knows when the next stage of his procedure will take place. The patient says that he does not know, adding lightly that he did not know there is another stage. The consultant tells the patient that he must ask questions about anything that is not clear to him (the patient)-to any one on his management team-and proceeds to explain the stages of the patient's management, what has been done so far and what may still need to be done. Field Notes, ICU, South Africa X14 'The patient doesn't compel us to start the medication because they are not aware of those things. They do say that they are feeling feverish. I saw the wound sores while bathing. They don't know that the medicine needs to be started for that. They tell the doctor also that the wound was wet, there was discharge and things like that, but they don't suggest an antibiotic to give them…'. GI Staff nurse, India X15 'Often, we will talk to a patient and if the patient says, "I don't want to know, just take the responsibility," and it happens more often than not … when you get to that, it just becomes habit forming … it's the only way I have known … the profile changes completely when you are dealing with private patients because they are generally much better educated and they have much higher demands'. CVTS Surgeon, South Africa 'I had a doubt since I am a nurse, I know normally after any surgery, they start with antibiotics, right? But I didn't see them giving any injection at all. When I asked the nurse, the nurse told that now without antibiotic it will heal, there is no need for antibiotics. On the fourth day, my daughter who is also a doctor, will be calling asking for the culture result. I too would ask but they would tell it has not come yet. I know, in our hospital if there is no outcome in 24 hours, they will give preliminary as no growth, but here even after four days, the results are not out yet. Even after the culture result came that night, they did not inform any doctor and they did not start any medications too. 'If I am able to convince the patient, the patient will go back happily. If I am not able to convince the patient, well the patient will go from me to another surgeon, and then to another surgeon, ultimately to a surgeon who will actually prescribe an antibiotic and then he would be happy there, so he will go off doctor shopping'. GI Surgical Resident, India X24 'I was transferred here when my funds ran out. If I had known of the wonderful care I would have received here, I would have said from the beginning, "Take me to this hospital" … There in private, it was all about the money, but here it is all about the care'. Patient, GI Surgery, South Africa X25 '….so even then in some patients, who have complete financial restraints, we will have to maybe reduce the doses or take into consideration other drugs…. the other thing that happens is they will want to go to another hospital also, so probably somewhere in medical college where the medicine is free, we would recommend that'. Pharmacist, GI surgery, India X26 'I think it is more a bit of, a case of, they're in a hurry, you know; like the lady that was helping me to eat-you know, and I've noticed-this morning when there was time, she had on an apron but when she came through now she didn't wear an apron, but, it is all right'. Patient, GI surgery, South Africa X27 'Patients' role is also there because some patients themselves ask the doctor, suppose they come to outpatients and they would have read up on something and they will be asking whether they should be on antibiotics. In such cases, the patient has to be reassured that they do not require an antibiotic'. GI Surgical Resident, India X28 'Sometimes it is just the patient's pressure, that the patient might not feel that I am a good enough doctor in case I have not satisfied the patient's prescription as well and satisfying the patient is also a very important part of our practice. Whether we satisfy them by prescribing what they want or by convincing them that they actually do not need it. Either way the patient has to be satisfied, right, and ultimately I think the patient is satisfied. The patient wants results. So with an antibiotic or without an antibiotic, if the patient actually can get well, if that convinces the patient beyond any doubt that yes, he did not need an antibiotic, or did he need an antibiotic at that point'. GI Surgical resident, India X29 'Some of the patients do tend to ask for antibiotics because they have been used to these five days of antibiotic [to be] necessary. We do tell them that we follow whatever is the standardized protocol all over the world, i.e., give prophylactic antibiotic and repeat every four hours during the surgery. Postop, unless there are signs of infection or anything, we do not give any antibiotic, in that case usually they understand. I hope they do not go back and buy it on their own'. GI Surgeon, India X30 'I find it much simpler to prescribe three days of ofloxacin to somebody rather than face a litigation based on completely unscientific allegation by somebody from outside'. GI Surgeon, India X31 'Patient expectations, I think defensive medicine, a genuine fear of harming the patient by withholding therapy, and using inadequate diagnostic tests. It's really hard, I'm not saying it's easy … most general practitioners in South Africa are in private practice and it's a business; so, if you don't give your patient what they want, they'll go somewhere else and your livelihood is at risk'. AS Physician, South Africa X32 'It is a real problem, and in India, there is an even bigger problem out in the community, so as you know, patients who go to see a clinician, a general practitioner, usually get antibiotics. So even if it is a viral fever, they might end up getting an antibiotic … you will be surprised that some of the antibiotics that you would think three times before using even in tertiary care centers, is used very frequently [in a small hospital]'. GI Surgeon, India Patients at site A expressed gratitude for the quality of care received, given their initial perceptions of care in a public healthcare environment (X24; Table 1). This awareness of the prevailing work pressures experienced by their healthcare teams as well as their gratitude for care sometimes impeded their ability to voice observed shortcomings in the care that they were receiving (X26; Table 1).

| Patient and/or carer demand for and access to antibiotics
Whilst prescribers may want to practice restraint in antibiotic prescribing, this is countered by a demand for antibiotics from patients and their families. This may be due to patients' own research on illness before seeking medical care (X27; Table 1). Prescribers in site B reported to have made efforts to educate patients and carers who demanded antibiotics (X28, X29; Table 1).
Fear of patient complaints and litigation can drive the decision to prescribe antibiotics, even though the prescriber may understand this to be irrational (X30; Table 1). The general perception, however, was that irrational prescribing is more prevalent in primary and secondary health centres than in tertiary care. Factors considered to influence inappropriate antibiotic prescribing included lack of good diagnostics and competition in community and private sectors for patients (X31; X32; Table 1).
Out-of-pocket expenses incurred to patients in healthcare systems that do not have universal health coverage act as an additional factor in suboptimal antibiotic prescribing. In site B, the high cost of antibiotics adds to the financial burden already placed on patients by surgery. As such, some patients may not be prescribed the most appropriate antibiotic. In some cases, where the most appropriate antibiotic is initiated, the course may not be finished due to cost constraints (X33; X34; Table 1), with implications for ABR.
This was generally not the case at site A, where cost was not a factor, most likely because it was a public hospital where the financial cost of care incurred to patients was minimal.
The unregulated access to and consumption of antibiotics before presentation at the hospital were recognized by participants in site B as factors in the development of ABR (X35; X36; Table 1). Patients bring their own beliefs, which need to be understood before they can be changed or influenced. While patient engagement could be affected by various clinical-and administration-related pressures, some senior surgeons, regardless of these, consistently engaged the patient in discussions related to their care, including infection care decisions. 41 Our data show that patients do not necessarily associate hospitals with infection. We need to go beyond the assumption that patient, carer and public education alone will address the identified gaps in IPC and AS and that it will foster optimized practices. 42 The identified gaps can be HCWs themselves may also benefit from context-appropriate communication skills to effectively engage patients. Depending on the context, patient carers also need to be engaged in interventions.

| DISCUSSION
Opportunities for patient and HCW engagement can provide learning, for both healthcare providers and recipients, on the effective means and outcomes of such engagement. Improving education to patient and carers on healthcareassociated infections, antibiotic use and antibiotic resistance Evidence-based educational materials should be prepared for patient and carer education. This education could be delivered through one-toone counselling, leaflets or pamphlets or other suitable means. The materials should be concise, contextually appropriate and in a language devoid of medical jargon that the patient/carer can easily understand.
Identifying role for pharmacists and nurses in providing one-toone education for patients A one-to-one education/counselling session may be beneficial for patient education. This session should take place ideally at a time that is convenient for the patient and should also be flexible as it may need to be repeated over time as needed. There may be opportunity for expanding the role of pharmacists and nurses in patient education. Limitations in resources (funding and time constraints) pose challenges to this and will need to be addressed.
| 901 facilitated multiple observations, reducing the likelihood of the Hawthorne effect. In addition, the application of a data collection guide, multiple data sources and researcher reflexivity helped to minimize subjectivity in the data collection process and to validate the findings.

| CONCLUSION
This study has provided new insight into surgical inpatients' involvement in infection-related care, including AS, across two diverse settings.
To have a valuable role in AS and make informed decisions related to their care, a better understanding and channelling of the knowledge and experiences that patients and carers bring to their own care needs is crucial. The universal patient-centred approach to care, modelled through an individualistic lens, may not be responsive to the cultural determinants of health and ABR in settings like India, where a community of individuals connected to the patient has a voice in patient care with greater access to and demand for antibiotics. More effort is required to fully integrate and channel patient and carer experiences and outlooks in initiatives to address ABR, especially as it relates to the demand for and access to antibiotics.

AUTHOR CONTRIBUTIONS
This is a multicentre study involving multiple surgical departments at each site. All the authors represent either the research team or the surgical team. All the authors have critically reviewed the manuscript and have approved the final version to be published.

ACKNOWLEDGEMENTS
We acknowledge the contributions of healthcare workers, patients and their carers across both the study sites for enabling us to conduct this study. We specifically acknowledge the insights of patient representatives (VC, SJ) at the study sites during the early discussions of this study. This study is part of the ASPIRES project (Antibiotic use

CONFLICT OF INTEREST STATEMENT
The authors declare no conflicts of interest.

DATA AVAILABILITY STATEMENT
Data on which this publication is based are available via a secure server. Access to the data can be provided upon reasonable request.
The data that support the findings of this study are available on request from the corresponding author. The data are not publicly available due to privacy or ethical restrictions.

ETHICS STATEMENT
Ethical approval was obtained from both the study sites (