Providing patient-centered care for patients with multidrug- or rifampicin-resistant tuberculosis in Wuhan, China

doi:10.21203/rs.3.rs-2065616/v1

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Providing patient-centered care for patients with multidrug- or rifampicin-resistant tuberculosis in Wuhan, China

https://doi.org/10.21203/rs.3.rs-2065616/v1

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Aim: This study was conducted to determine the impact of patient-centered care (PCC) on treatment adherence and outcome of patientswith multidrug- or rifampicin-resistant tuberculosis (MDR/RR-TB).

Background: Treatment adherence is critical to successful outcomes of MDR/RR-TB. However, very few studies published had addressed how to improve it.

Methods: This study retrospectivelyanalyzed treatment outcomes of MDR/RR-TB patient with two different kinds of care: clinical care for group A and PCC for group B.

Results: There were 128 patients were assigned in group A and 155 patients in group B. Patients in group B achieved a higher rate of negative 6-month sputum culture conversionthan those in group A (81.6% versus 95.3%, P = 0.0141). The treatment success rates of group A and B were 46.9% versus 68.4% (P = 0.0003), while failure, death, and default rates were4.7%, 9.4%, and 39.1% in group A, versus 1.3% (P = 0.1751), 12.9% (P = 0.3509), and 17.4% (P = 0.0000) in group B, respectively.

Conclusions: The PCC promoted MDR/RR-TB patients’ adherence and improved treatment outcomes.

Tuberculosis

Multidrug-Resistance

clinical care

patient-centered care

Multidrug-resistant tuberculosis (MDR-TB) caused by Mycobacterium tuberculosis (MTB) is resistant to at least rifampicin and isoniazid [1]. It is considered a global public health problem and a threat that blocks the control and elimination of tuberculosis (TB), particularly in low-income countries [2]. Globally, there were an estimated 465 000 (range, 400 000–535 000) incident cases of rifampicin-resistant TB (RR-TB) in 2019; 78% had MDR-TB [3]. China had the second-highest MDR/RR-TB burden behind India and approximately 833 000 TB cases in 2019 (58/100 000 population). An estimated 7.1% of new and 23% of previously treated TB cases were MDR, which meant that there were around 65 000 new cases of MDR-TB in China [3]. According to Global Tuberculosis Report 2020, the global treatment success rate for MDR-TB was 57%, far below the World Health Organization (WHO) target of curing at least 75% [3]. China, with a treatment success rate of 54%, was no exception. Nearly half of the patients were lost to follow-up, treatment failure, or death [4].

Many hurdles stood in the way of mounting an effective global response to drug-resistant TB [5]. Patients with RR-TB, commonly combined with isoniazid resistance, required longer, less effective, and less accessible regimens than the first-line, but more costly, toxic, and complicated to deliver [6]. Most second-line MDR/RR-TB regimens lasted 18 months or more in recent decades [7-10], presenting a formidable challenge to health service providers to ensure patient adherence and treatment success rates. The effective management of TB patients was essential to tackle the TB crisis [11]. To establish a well-performed Hospital-CDC cooperation mechanism could promote the performance of MDR-TB case detection and treatment [12]. The current model for TB control in most Chinese provinces had shifted away from the initial model that required the Centers for Disease Control and Prevention (CDC) to provide all services related to the treatment, diagnosis, and management of TB, to an integrated model which involves a combination of the CDC, designated hospitals and primary health care sectors [13]. Ensuring adherence to treatment was crucial to the control of MDR-TB [3, 14, 15]. A pillar of the WHO End TB strategy integrated patient-centered care (PCC) to promote treatment adherence, improve quality of life, and relieve suffering [16]. The U.S. Agency for International Development Control and Prevention of Tuberculosis (USAID CAP-TB) project led by Family Health International 360 non-governmental organization (FHI 360 NGO), partnered with the International Union Against Tuberculosis and Lung Disease, was a six-year effort to reduce the incidence and mortality of MDR-TB in China and Thailand. It was a lead case study in a global pilot project to improve PCC for MDR/RR-TB patients under the U.S. National Action Plan (NAP). With the support of USAID CAP-TB, MDR-TB patients in Yunnan Province had treatment success rates that were much higher than the China national average [17, 18]. Provinces around the country had requested to introduce these interventions, including Hubei province. Hubei is in central China along the middle reaches of the Yangtze River. It covers an area of 185,900 square kilometers with a permanent population of 59.17 million. Jinyintan Hospital (JYTH) is in Wuhan, the capital city of Hubei, is responsible for receiving patients with infectious diseases from all over the province. The majority of MDR/RR-TB patients came from 17 regions, cities, and autonomous prefectures of Hubei. Some had poor health-care services and lived more than 800 kilometers away from Wuhan. The general impression was that the hospital took no responsibility for patients in the past when they left the ward. The treatment success rate was less than 50% in JYTH due to a high default degree. To turn around, JYTH adopted the PCC based on hospital-CDC collaboration (PCC-HCC) model to complement the ongoing hospital-based treatment approach and improve continuity of care for MDR/RR-TB patients discharged from the hospital. In the present study, we shared achievements resulting from the PCC-HCC model designed for MDR/RR-TB.

Study design

It was a retrospective case-control study based on MDR/RR-TB records of JYTH from 2017 to 2018. The following variables were collected: characteristics of patients enrolled and outcomes of integrated management, including sex, age, address, patient categories, disease type, HIV status, culture results, treatment initiation site, 6-month interim outcomes, and final treatment outcomes based on guidelines. To assess the impact of the management program, we analyzed culture conversion at the end of 6-month treatment and the final treatment outcomes. Data was input into an electronic clinical management system provided by FHI360. Data were analyzed using SPSS 25.0, and a p-value less than 0.05 was considered statistically significant.

Treatment

JYTH convened an independent MDR/RR-TB expert panel before 2017 responsible for diagnosis, treatment, therapy adjustment, and outcomes judgment. MDR/RR-TB was confirmed by Xpert MTB/RIF assay or phenotypic drug susceptibility test (DST). Patients in 2017-2018 received individualized treatment regimens according to DST results and the 2016 WHO guidelines [7]. They received monthly treatment monitoring during the intensive phase and every other month in the continuous phase. Initial treatment delivery was in JYTH for 1-2 months until the patients were clinically stable and could accommodate in a separate room at home.

Management

Group A: MDR/RR-TB patients of Wuhan Jinyintan Hospital scattered in 11 tuberculosis wards before December 6, 2017. They received the hospital-based treatment and care program.

Group B (Fig 1): We strengthened screening for MDR/RR-TB in high-risk populations of JYTH and transferred confirmed patients to MDR/RR-TB unit. JYTH began to cooperate with the provincial Centers for Disease Control and Prevention in 2018. All patients’ information was input into the national electronic case register for MDR/RR-TB. CDCs at all levels in Hubei and 14 MDR-TB designated hospitals managed our outpatients together, including follow-up and injection treatment. At the same time, FHI360 helped to build a patient-centered care team, including six nurses and four peer counselors. We started to provide PCC for MDR/RR-TB patients based on clinical care and HCC. In addition to individualized treatment, patients were followed Directly Observed Therapy (DOT) during hospitalization and Virtually Observed Therapy (VOT) during staying at home. Of course, outpatients also could choose DOT provided by community doctors or family members of themself. They received peers-education, psycho-social support, and some free items provided by JYTH.

Patient-centered care (Fig 1)

Enable Partnerships, Recognize Patient Rights, Empower & Activate Patients & Communities, Engage All Stakeholders, and Monitor & Document are principles of patient-centered care [19]. Based on the above, we divided patient-centered care into five main steps and provided social support according to WHO guidelines for MDR-TB, such as information, emotion, companionship, and material support [7, 20]. Care providers accompanied patients through treatment by remaining responsible for patients from enrollment in the program until two years follow-up after the end of treatment. We had created a social media network for MDR/RR-TB consultation and communication, 57 Zone, where patients could talk about their medication, adverse drug effects, and nutrition and psycho-social concerns [21].

1st: Inpatient consultants introduced themselves and built partnerships with patients at the first meeting. After informing patients of MDR/RR-TB diagnosis and introducing the basic concept of MDR/RR-TB, inpatient consultants must assess treatment compliance of their patients to present more information at weekly clinical committee meetings.

2nd: Expert consultation meetings were due on Wednesday. Inpatient consultants told patients about the consultation results of the expert panel on the next day and conveyed views from patients about future treatment to doctors. They provided palliative care to patients rejecting treatment or with no effective therapeutic regimen and sent this information to CDC staff in time. Consultants created accounts for patients accepting MDR/RR-TB therapy.

3rd: The consultant team organized interviews which were structured around a core set of topics, including more knowledge about MDR/RR-TB, how to deal with the psychological challenges in life, how to collect qualified sputum samples, the side effects of drugs, and what patients should do if they experience side-effects. Inpatient consultants must train a community doctor or a family member as the treatment supervisor for every outpatient to ensure treatment adherence.

4th: On discharge day, inpatient consultants should teach patients how to control infection to reduce the risk of secondary transmission of MDR/RR-TB caused by home-based treatment. They notified CDC staff of the treatment information and matters needing attention about these patients.

5th: Outpatient consultants followed up with patients by telephone every week. They were also responsible for providing feedback of patients to doctors and updating treatment data in the management system. JYTH employed some cured patients as peer counselors to educated patients every day on ongoing treatment through QQ and WeChat.

Definition of Treatment outcomes

The treatment outcomes for the cohort of patients registered within the study period were assessed and assigned to the treatment category according to international consensus definitions of cure, failure, and death [7]. Patients were classified as default if they stopped treatment for two consecutive months or more due to: 1) Adverse drug reactions; or 2) Lost to follow-up; or 3) Not evaluated: A patient for whom no treatment outcome was assigned (This included cases “transferred out” to another treatment unit and whose treatment outcome was unknown). Culture conversion at month 6 was a medium-term outcome.

Characteristics and sources of patients

Retrospectively analyzed a total of 283 MDR/RR-TB patients from 2017 to 2018 accepting MDR/RR-TB therapy, with two HIV co-infected cases in 2018. 128 patients were assigned in group A (provided clinical care only) and 155 patients in group B (provided PCC). Table 1 showed that the sex, age, the origin of patients, resistance rates of fluoroquinolones, and type of patients in the two groups were not different on statistics (Table 1, P > 0.05).

Culture conversion at the end of 6-month treatment

Among patients with culture results in Group A and B, there were annually 40 (81.6%, 95% CI: 67.5-90.8) and 101 (95.3%, 95% CI: 88.8-98.3) cases gaining sputum culture conversion at the end of a 6-month intensive phase. Correspondingly, 9 (18.4%, 95% CI: 9.2-32.5) and 5 (4.7%, 95% CI: 1.8-11.2) cases remained culture-positive respectively. There were statistically differences between the two groups (Table 2, P = 0.0141).

Treatment outcomes

We recorded treatment outcomes as success (cure and treatment completion), failure, death, and default (Table 2). Of 128 patients in Group A, 60 patients(46.9%, 95% CI: 38.1-55.9) were successfully treated, 6 patients (4.7%, 95% CI: 1.9-10.4) were diagnosed with treatment failure, 12 patients (9.4%, 95% CI: 5.2-16.1) died and 50 patients (39.1%, 95% CI: 30.7-48.1) defaulted. The treatment success (68.4%, 95% CI: 60.4-75.5) and default (17.4%, 95% CI: 12.0-24.5) rates improved significantly in Group B (P < 0.01), but no differences in failure (1.3%, 95% CI: 0.2-5.1) and death (12.9%, 95% CI: 8.3-19.5) rates compared with Group A (P > 0.05). Most of the patients had bacteriological documented follow-up for 1-2 years after cure. Only one female patient with fluoroquinolone-resistance strain had a recurrent episode. She and all eight patients with treatment failure (Group A and B) were under treatment with a bedaquiline-based regimen and had culture reversion now.

A growing body of data confirmed that multidrug-resistant TB was emerging as an increasingly important cause of TB morbidity and death [3, 22 - 24]. Social and programmatic factors played an overwhelming role in treatment adherence and acquisition of MDR-TB. The lack of guidelines and responsibilities concerning patient education, clinical management, and discharge planning within the hospital were serious considerations contributing to poor continuity of care for TB patients [25]. MDR-TB programs required intensive management, clinical oversight, social support, and data management. On the one hand, county community hospitals could not make a correct MDR-TB diagnosis in time and often faced drug shortages. Although there were 14 designated MDR/RR-TB hospitals in Hubei Province, 1/4 - 1/3 refractory patients were transferred to Wuhan Jinyintan Hospital every year. On the other hand, it was difficult to improve the treatment success rate of MDR/RR-TB patients in provincial hospitals failing to follow up after discharge because of the distance. Table 1 showed that around 70% of our patients lived outside Wuhan City. More than 70% of cases had previous TB treatment history, and about 42-45% of patients infected strains resistant to fluoroquinolones. It was full of difficulty to treat and manage these patients.

Patient-centered care respected the experience, values, needs, and preferences of patients [26]. Most patients expressed feeling vulnerable and powerless in the first face of MDR-TB illness. Proper coordination of care could alleviate those feelings. Consultants must treat patients with dignity, respect, and sensitivity to their values and autonomy. In these 2nd interviews, most patients expressed their worries about their condition or prognosis. Inpatient consultants should focus on conveying information about that. Fear and anxiety associated with illness could be as debilitating as the physical effects. Caregivers should pay special attention to these concerns from patients about the impact of the disease on themselves, their families, and the economy. We supported family members or close friends as caregivers attending in decision making. Most patients expressed concern about their ability to care for themselves after discharge. Details should be informed about control of family infection, plan ongoing treatment and services, and access to financial backing. Outpatient consultants provided ease of scheduling appointments on when and how to get referrals.

The value of providing patient-centered care throughout treatment for MDR/RR-TB gone beyond minimizing default rates or even maximizing cure rates. Our PCC-HCC management model found programmatic solutions to social-psychological barriers that prevented patients from completing treatment. With the efforts of JYTH, CDCs, and the patient-centered care team, we successfully improved treatment adherence － the default rates were reduced from 39.1% to 17.4%. In the shorter treatment regimen treatment cohort that began in 2019, our loss of follow-up rate was only 2.4% (1/42, 95% CI: 0.1-14.1) [27]. The most notable achievement was that we improved success rates from 46.9% to 68.4%. Pilot work in JYTH indicated that the provision of clinical care, follow-up support through hospital-CDC collaboration and in combination with patient-centered management improved cure rates and lower default rates among patients with MDR/RR-TB. We had no bedaquiline or delamanid before 2019. Most patients bought linezolid, cycloserine, and clofazimine from smugglers without quality assurance because of the lower cost. But experience showed that we could improve treatment outcomes when patients were the center of all of our efforts, even though our treatments were imperfect. Cure rates were high than ever if patients received the medicines and the social support required to complete therapy each day.

The JYTH MDR/RR-TB management model had achieved good results. However, it was not clear about the acceptability and accessibility of this model. We also aimed to learn lessons and obtained information from the program to guide the development and future implementation of this model of care. As a result of this and other studies, the integrated patient-centered management approach is currently being scaled up across China to improve MDR/RR-TB treatment adherence [11, 28].

MDR/RR-TB is one of the most pressing health problems of our times. The airborne disease cannot be ignored or declared incurable. Our results showed that a comprehensive management approach was feasible to MDR/RR-TB diagnosis, treatment, and care, with good treatment outcomes even in resource-limited settings. JYTH offered a successful administration model that addressed many of the concerns and barriers identified by those working in the MDR/RR-TB system. We argued that this model could contribute to improving MDR/RR-TB treatment outcomes in China and elsewhere.

Ethics approval and Consent to Participate

All participants voluntarily gave their informed written consent before receiving anti-tuberculosis treatment and the patient-centered care program. Formal ethics approval from the Wuhan infectious disease Hospital Ethics Review Board was obtained before the study commencing (No. 2021-KY-16). All authors had access to information that could identify individual participants during or after data collection. All patient identifiers have been removed or disguised so the patients described are not identifiable and cannot be identified through the details of the story.

Consent for publication

All authors are satisfied and consent to submit to this journal for publication consideration. All the authors have agreed to the final contents for publication and contributed substantially to the manuscript.

Competing interests

We declare that this manuscript is an original research and has never been submitted to any journal nor is it intended to be submitted to another one. All authors declare no conflict of interest.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial or not-for-profit sectors.

Declaration of Competing interests

All authors have declared that no competing interests exist.

Acknowledgments

We are grateful to all staff and management of the National Center for Tuberculosis Control and Prevention, Chinese Center for Disease Control and Prevention (China CDC) for the excellent work done in saving lives and the collaboration during the implementation of the management model with hospital-CDC collaboration (HCC) and patient-centered care. We thank the Family Health International 360 non-governmental organization (FHI 360 NGO) for the excellent technical assistance provided at all stages of patient-centered care implementation. We also thank Dr. Chen-Yuan Chiang, consultant at International Union Against Tuberculosis and Lung Disease (The Union), for his professional advice. Our thanks go out to the CDCs in Hubei, the peer counselors and family supervisors for the excellent partnership too.

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Table 1 Characteristics of patients

Variable	Group A (N=128)		Group B (N=155)		P value
Variable	n	% [95% CI（%）]	n	% [95% CI（%）]	P value
Gender
F	31	24.2 [17.3-32.7]	40	25.8 [19.3-33.6]	0.7592
M	97	75.8 [67.3-82.7]	115	74.2 [66.4-80.7]	0.7592
Age (years old)
＜ 18	2	1.6 [0.3-6.1]	2	1.3 [0.2-5.1]	0.7544
≥ 18	126	98.4 [93.9-99.7]	153	98.7 [94.9-99.8]	0.7544
Average age	44.0 ± 15.7		46.0 ± 15.8		0.3006
Address
Wuhan	37	28.9 [21.4-37.7]	43	27.7 [21.0-35.6]	0.8285
Outside Wuhan	91	71.1 [62.3-78.6]	112	72.3 [64.4-79.0]	0.8285
DST of FQ
Resistant	55	44.7 [35.8-53.9]	61	42.4 [34.3-50.9]	0.6988
Susceptible	68	55.3 [46.1-64.2]	83	57.6 [49.1-65.7]	0.6988
Missing	5	﹘	11	﹘
Type of patient
New Case	32	25.0 [18.0-33.6]	44	28.4 [21.6-36.3]	0.5223
previously treated case	96	75.0 [66.4-82.0]	111	71.6 [63.7-78.4]	0.5223
N or n: number; CI: confidence interval; F: Female; M: Male; DST: drug susceptibility test; FQ: fluoroquinolones.

Table 2 Outcomes under PCC-HCC management model

Variable	Group A		Group B		P value
Variable	n (or n/N)	% [95% CI（%）]	n (or n/N)	% [95% CI（%）]	P value
culture conversion at month 6
negative	40	81.6 [67.5-90.8]	101	95.3 [88.8-98.3]	0.0141
positive	9	18.4 [9.2-32.5]	5	4.7 [1.8-11.2]	0.0141
Missing	79	-	49	-
Treatment outcomes
success	60	46.9 [38.1-55.9]	106	68.4 [60.4-75.5]	0.0003
failure	6	4.7 [1.9-10.4]	2	1.3 [0.2-5.1]	0.1751
death	12	9.4 [5.2-16.1]	20	12.9 [8.3-19.5]	0.3509
default	50	39.1 [30.7-48.1]	27	17.4 [12.0-24.5]	0.0000
PCC-HCC: patient-centered care (PCC) based on hospital and Centers for Disease Control and Prevention (CDC) collaboration; N or n: Number of patients.

No competing interests reported.

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Providing patient-centered care for patients with multidrug- or rifampicin-resistant tuberculosis in Wuhan, China

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