key: cord-0687349-ozif47ct authors: Klinton, Joel Shyam; Heitkamp, Petra; Rashid, Aamna; Faleye, Bolanle Olusola; Win Htat, Han; Hussain, Hamidah; Syed, Imran; Farough, Khalid; Mortera, Lalaine; Moh Lwin, Moh; Jha, Nita; Ananthakrishnan, Ramya; Mahfuza, Rifat; Chadha, Sarabjit Singh; Banu, Sayera; Mannan, Shamim; Vijayan, Shibu; Ahmed, Shahriar; Ali, Taofeekat; Oga-Omenka, Charity; Kaur, Manjot; Singh, Urvashi; Wells, William A; Stallworthy, Guy; Dias, Hannah Monica Yesudian; Pai, Madhukar title: One year of COVID-19 and its impact on private provider engagement for TB date: 2021-09-16 journal: J Clin Tuberc Other Mycobact Dis DOI: 10.1016/j.jctube.2021.100277 sha: f39ef3609c050d5ae8cb826adbcab906fa6260a0 doc_id: 687349 cord_uid: ozif47ct The COVID-19 pandemic has impacted health systems and health programs across the world. For tuberculosis (TB), it is predicted to set back progress by at least twelve years. Public private mix (PPM) is a collaborative approach to engage private providers in quality TB care. It has made a vital contribution to reach End TB targets with a ten-fold rise in TB notifications from private providers between 2012 and 2019. This is due in large part to the efforts of intermediary agencies, which aggregate demand from private providers. The COVID-19 pandemic has put these gains at risk over the past year. In this rapid assessment, representatives of 15 intermediary agencies from seven countries that are considered the highest priority for TB PPM (the Big Seven) share their views on the impact of COVID-19 on their programs, the private providers operating under their PPM schemes, and their private TB clients. All intermediaries reported a drop in TB testing and notifications, and the closure of some private practices. While travel restrictions and the fear of contracting COVID were the main contributing factors, there were also unanticipated expenses for private providers, which were transferred to patients via increased prices. Intermediaries also had their routine activities disrupted and had to shift tasks and budgets to meet the new needs. However, the intermediaries and their partners rapidly adapted, including an increased use of digital tools, patient-centric services, and ancillary support for private providers. Despite many setbacks, the COVID-19 pandemic has underlined the importance of effective private sector engagement. The robust approach to fight COVID-19 has shown the possibilities for ending TB with a similar approach, augmented by the digital revolution around treatment and diagnostics and the push to decentralize health services. It has been over a year since COVID-19 was declared a pandemic. In addition to the over 3.29 million deaths attributed to COVID-19 to date (1) , the pandemic threatens to reverse previous gains in public health outcomes, especially those in the fight against tuberculosis (TB). In a global survey by civil society organizations released in September 2020, 63% of healthcare workers from countries with grants from the Global Fund to Fight AIDS, Tuberculosis and Malaria (Global Fund) reported reductions in the number of people with TB coming to healthcare facilities for treatment (2) . Data from World Health Organization (WHO) in March 2021 shows that COVID-19 related disruptions have severely impacted over 84 countries with 1.4 million fewer people estimated to have received TB care in 2020 than in 2019 -a reduction of 21% from 2019 (3) . These COVID-19 related disruptions are estimated to cause an additional half a million TB deaths (3) and a setback of nearly 12 years (4) . Seven of the highest TB-burden countries (Bangladesh, India, Indonesia, Myanmar, Nigeria, Pakistan, and the Philippines), also known as the "Big Seven" priority countries for Public Private Mix (PPM), account for 60% of the global missing cases (5) . In these countries, 32% to 74% of the population seeks care in the private sector (6) . The proportion of total notifications contributed by the for-profit sector in these Big Seven countries has risen from 5% in 2012 to nearly 28% in 2019 (7), thereby helping countries to close the gaps in TB notification and underlining the importance of multisectoral framework to End TB (8) . This response has been enabled substantially by the emergence of Non-Governmental Organizations (NGOs) that can act as intermediaries and bridge the gaps between private providers and the government (9) . A number of these intermediary NGOs, plus the burden of TB and COVID in these countries, is outlined in Table 1 . In response to the COVID-19 pandemic, the World Health Organization (WHO) has called on member states to adopt a whole-of-government and whole-of-society approach (10) , and a wide variety of impacts and mitigation approaches have been seen for TB (11, 12) . While public-private partnerships can help support strained health systems, countries are unsure of how to optimally engage the private sector in their national response efforts to COVID (13) . This applies to TB too. To inform this area, this rapid assessment is co-authored by fifteen representatives of intermediary agencies from the big seven countries -Bangladesh (3), India (5) , Myanmar (1), Nigeria (2) , Pakistan (2) , Philippines (1) and Indonesia (1) . In the following sections, we summarize the impact of the COVID-19 pandemic on private sector providers of TB care, on TB patients, and on TB PPM intermediary agencies, plus the different adaptations to the pandemic, and opportunities seen to improve TB care (the findings are summarized in Figure 1 ). In this assessment, any reference to private providers refers to private health sector involved in service delivery including private hospitals, private laboratories and private pharmacies (14) . The authors acknowledge upfront that the data captured in this document reflects the experience between March 2020 to December 2020. Given the rapidly evolving nature of the pandemic and the roll out of vaccines starting towards the end of 2020, later experiences would necessitate a separate assessment. The private providers involved in TB service delivery faced several challenges during the pandemic in 2020 that impacted the entire cascade of TB care. In the initial months of the pandemic, when countries went into lockdowns and travel restrictions were imposed, there were disruptions in active case finding and contact tracing efforts, decreases in the demand for and use of TB diagnostics, drops in TB notifications and shutting of private practices (See Table 1 ). Although movement restrictions were slowly lifted in many regions by the end of 2020, at the time of the assessment the TB notification were nowhere near the same as in 2019 nor in line with the country targets. "We are getting around 70% of the TB notifications we saw in January/February 2020, but overall, we are at only 30-40% of our Global Fund target" (PATH, India). The several constraints that impacted TB service delivery are summarized in table 2. Some of these constraints were common for both the public and private health sectors, but private providers faced added challenges, as seen in Table 2 . Travel restrictions and fear of infection (15/15)  In Bangladesh, some providers with icddr,b, stopped chest X-rays because staff were not allowed to leave their neighborhood  In Nigeria, drug stock-outs were reported due to the impact of movement restriction on supply logistics. "The patient could not come to the health facility and the community health care worker could not go to the patient." (IHVN, Nigeria) . "People are so worried about going to hospitals and catching the infection that the whole agenda of early diagnosis and seeking care has been very badly affected". (FHI 360, Indonesia) . Difficulty in adapting to change (3/15)  Resistance among providers to use face mask  Teleconsultations were an added pressure especially for senior clinicians. "Government partners had little or no experience with virtual working." (FHI 360, Philippines) B. Constraints specific to private health sector Private sector support restricted or neglected by public sector (6/15)  In Nigeria, the Gene Xpert cartridges and microscopy reagents were procured by national program mainly for the public sector.  In Bangladesh, the government announced some incentives only for healthcare workers in the public sector. Though these constraints impacted screening for patients with TB symptoms, the intermediaries also noted more walk ins in some private clinics as patients presented directly to health facilities once their symptoms worsened, and many of these patients were diagnosed with having TB. "Only the very sick patients admitted to having cough and gave sputum to be tested for TB and a high proportion of them tested positive for TB." (SHOPS Plus, Nigeria) . However, during the period of lockdown, in most countries this rise in patients confirmed with TB was not high enough to match the reduced total patient flow, resulting in an overall drop in notifications. In addition, the intermediaries observed that many private providers had additional costs -and that those costs were passed on to patients seeking care (see next section). During the pandemic, TB treatment and diagnostics in the public sector and by government or donor-funded PPM providers continued to be free of charge or highly subsidized in all of these high burden countries. "A significant (amount of) funding is from the Global Fund to provide free TB care in the private sector [Under PPM scheme] ." (PSI, Myanmar) Despite the free TB services, patients incurred high costs for general health visits due to six main reasons. 3.1. A major cost for patients went into covering the expenses for personal protective equipment (PPE) and other infection prevention measures. "Whatever services were available became more costly because of personal protective equipment being charged to the patient." (FHI 360, Indonesia). 3.2. Some private practitioners also insisted that patients take additional tests and/or a receive a negative COVID-19 test result before they could be seen for other ailments, raising the cost for TB testing. In the Philippines, private providers were required to perform a COVID-19 test for every patient who required more than 30 minutes of interaction with the provider. 3.3. Even when patients had insurance coverage they still had to pay out of pocket in some instances, as their insurance schemes did not cover either COVID-19 expenses or COVID-19 specific health facilities. "Patients holding HMO (Health Maintenance Organization) cards also had to pay out of pocket." (FHI 360, Philippines) 3.4. Though there was a fall in the number of patients presenting at private clinics, the cost to run the clinic (rent, electricity, etc.) either remained the same or was increased due to the additional costs incurred to ensure infection prevention "The clinics that used to see 20 patients an hour can now see only about 4 patients an hour, so they charge more per patient" (FHI 360, Philippines). 3.5. Additionally, to meet the shortage of supplies, in-person consultations were charged more than virtual consultations. 3.6. Patients also incurred indirect costs due to travelling long distance and purchasing products such as soap, hand sanitizer, and masks. The most common impact of COVID-19 for the intermediary organizations was the disruption of field work and outreach activities. "Reinforcing relationships between field office staff and providers has been critically affected because of movement restrictions and lack of in-person contact." (PATH, India). The travel restrictions made it difficult for the field staff to continue active case finding, treatment monitoring, and medical camps and to monitor the progress in their projects. The field staff were also stigmatized as their neighbours and landlords were afraid of contracting COVID-19 and restricted them from going out of (or returning to) their homes. The intermediaries had to shift their budgets and tasks to accommodate the needs of the changed situation. Overall, budgets and plans for face-to-face follow-up, training, monitoring, meetings and outreach programs decreased in the periods of lockdown. By contrast, there was an increased focus on online meetings and communication, as well as increased responsibilities for field staff. Postlockdown, the regular programs resumed and were trying to catch up. Increased costs and attention were given to purchasing of PPE for private providers, training additional staff to screen patients for TB and COVID-19 and additional allowances for transport and communication for field staff. These additional tasks in turn burdened the staff who felt overworked and had to work extra hours to follow up with patients and partners. "Sometimes, I am in calls all day" exclaimed one of the stakeholders. Many field staff and laboratory staff from these intermediary agencies were also challenged by COVID-19-related morbidity and mortality, further straining the staffing. "Out of 150 field staff, [15] [16] [17] [18] but all recovered" (Greenstar, Pakistan) . All these restrictions delayed several initiatives that were planned for the year 2020 by the intermediaries. "We had wanted to expand to new geographies, but recruitment and trainings were severely delayed" (CHAI, India). In the face of these challenges, many stakeholders from the intermediary agencies were consistently appreciative of the Global Fund and other donors, mainly for non-delayed funding accompanied by flexibility within the grant to meet the additional costs such as procuring PPE. The proactive measures taken by the Global Fund and other donors to support the mitigation plans helped the intermediaries to advance funding to the service providers. In the Philippines, despite the budget cuts for the National TB Program, private hospitals were able to access Xpert cartridges because of the continued support from the Global Fund. "Funders have shown a high degree of resilience, support, and empathy to us, and they allowed adaptations to operations and timeline which was greatly appreciated" (PATH, India). In spite of the constraints that accompanied the COVID-19 pandemic, the private providers and intermediary agencies found ways to adapt to the new reality. The adaptations outlined below on the digital transformation and increase in patient-centric services were also noted in the public sector. More specifically related to private provider engagement, intermediaries provided various ancillary supports for private providers under their PPM programs. Digital tools have offered massive opportunities to connect with others from home, including doctor-patient relations, work meetings, trainings, and data-collection processes. A variety of these tools were mentioned by the respondents and are summarized in Table 3 . Many existing systems and practices were modified to better suit the patients' needs. "They (Field Staff) changed their model of TB management and prevention" (BRAC, Bangladesh) . Programs and providers have been pushed out of their comfort zone to implement the vision of patientcentered TB care as outlined in Table 4 .  AI based Chest X ray  Digital X rays  Online reports "Many centers did not have radiologists to see these x-ray reports, so BRAC introduced online systems during COVID." (BRAC, Bangladesh) Updated systems  Prescription of drugs for a longer duration at one time  Skipped sputum microscopy and conducted Gene Xpert for rapid results "Everyone was more comfortable with giving 1-2 months of medicine refills to patients, instead of daily DOTS" (WHP, India). Many intermediaries have taken this opportunity to further systematize the engagement of private providers and find new support mechanisms. The initial response of many intermediary agencies was to conduct a rapid survey to assess the ground reality and identify needs of the private providers. "We conducted a rapid assessment to understand what challenges the private providers faced and how they can be best supported to provide TB services without any interruption." (Mercy Corps, Pakistan) . Based on these assessments, the intermediaries were able to support their private providers as outlined in Table 5 .  Integration of COVID screening along with TB screening systems. e.g. TBSTARR app by SHOPS Plus  Bi-directional screening for TB and COVID in India, Bangladesh, and Indonesia  Mobile X-ray vans to screen for TB and COVID e.g. Indus Hospital and Health Network and IRD Pakistan "We pivoted our electronic data systems [in Pakistan] very quickly to capture .  Delivery of medications to client's residence  Sputum collection at client's residence "As soon as the lockdown was declared, we had to ensure that the patients were adequately stocked with treatments." (CHAI, India) Some of the initiatives under all three adaptations existed before the pandemic. Though there are no quantifiable data, the intermediaries observed a mixed response to all these adaptations. While there was either an accelerated uptake or immediate scale-up of some of these initiatives, a few initiatives were limited to certain regions within the country with limited implementation and outcome. "A policy [for bidirectional screening] The assessment has shown that the impact of COVID-19 has created many constraints to TB care programs and challenges for people affected by TB. However, the intermediaries also identified several opportunities that can pave the way for improving TB care; these are outlined in Box 1. The prioritization and scale of these of these efforts will depend on national context and plans.  "Digital advancements like utilization of internet tools to conduct virtual trainings and payment through mobile transfers are some opportunities that can be harnessed for the future" (PSI, Myanmar)  "The government's appetite and acceptance for all kinds of technology is now higher than ever before. So, we're hoping they will invest more in digital tools." (FHI 360, Philippines)  "The true spirit of public and private mix was seen especially during the COVID19 pandemic" (Mercy Corps, Pakistan)  "The potential of the private health sector must be mobilized to provide TB services to patients in the community" (Greenstar, Pakistan)  "The informal private sector could also be enhanced and leveraged as an alternative for patients when they cannot access the formal private sector." (SHOPS Plus, Nigeria)  "The availability of these multiplex platforms like Truenat and CBNAAT will further help strengthen the TB services" (FIND, India)  "For the COVID pandemic we're seeing that results can be ready much faster. We need to have a point of care test for TB that generates results during the visit." (IHVN, Nigeria)  "I think the good thing which has happened after COVID is that providers keep their premises very clean and ensure that patients wear a mask or cover their mouth and nose with a piece of cloth." (CHAI, India)  "Private providers need to be strengthened on infection prevention and emergency preparedness for any such sudden demands in the health system." (Mercy Corps, Pakistan)  "[We need to] go towards patients and the community with mobile x-ray and to ensure that testing is done" (Greenstar, Pakistan)  "TB patients' care and follow up should become easier and patient-centric" (IRD, Global) This rapid assessment of the TB intermediary agencies in seven high TB burden countries gives a good indication of the wide variety of disruptions that COVID-19 has caused in the overall health system and particularly to private TB healthcare services during 2020. Similar impacts on TB (12, (17) (18) and TB PPM (19) have also been reported in countries other than the big seven, even as performance on some quality of care indicators has been successfully maintained (20) . The work of the private health sector and the intermediaries was disrupted and caused changes in work processes and increased stress on staff. Despite the challenges, they have shown resilience and flexibility to adapt to continue to support TB services. In some instances, the contributions from the private sector increased drastically at the end of 2020, once services resumed. However, as the pandemic is still evolving and some of these countries are in the next wave of the COVID-19 pandemic, the constraints seem to continue, and the identified adaptations have not yet been scaled up and the opportunities have not yet been fully leveraged. The progress in the fight against TB that has been lost during the COVID-19 pandemic cannot be recovered overnight and will require arduous efforts from all stakeholders. PPM is essential in rebuilding the healthcare services system to end TB. The call to take engagement of private providers to scale is not something new. The PPM Roadmap for Tuberculosis that was released in 2018 captured ten key actions that are required to scale up private sector engagement (21) . The COVID-19 pandemic has only accelerated the need to prioritize those ten action items. Partnerships with private sector and intermediary agencies are crucial to build more resilient systems that can be leveraged in times of crisis and must be included in all measures recommended for countries to ensure continuity of TB services (22) . TB programs should also take advantage of the changes brought about by COVID-19 to reimagine patient-centered TB care. Declaration WAW is employed by the United States Agency for International Development (USAID), Washington DC, USA. The views and opinions expressed in this article are those of the authors 6.6. Ambitious approach towards EndTB goals  "Contact screening for COVID has brought into focus that it is possible… I don't think there will be any more excuses saying contact screening for TB cannot be done, be it public sector or private sector." (REACH, India).  "We were doing nearly ~80,000 COVID tests per day in Delhi alone with about half of them being RT-PCRs. If we are able to do this, why can't we do it for TB as well?" 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World Health Organization The views and opinions expressed in this article are those of the authors and do not necessarily reflect the view of the U.S. Agency for International Development or the U.S. Government Joel Shyam Klinton -Conceptualization, Data curation, Formal analysis, Investigation; Methodology Petra Heitkamp -Conceptualization, Data curation, Formal analysis, Investigation; Methodology Aamna Rashid -Validation, Writing -review & editing Bolanle Olusola Faleye -Validation, Writing -review & editing Han Win Htat -Validation, Writing -review & editing Hamidah Hussain -Validation, Writing -review & editing Imran Syed -Validation, Writing -review & editing Khalid Farough -Validation, Writing -review & editing Lalaine Mortera -Validation, Writing -review & editing Moh Moh Lwin -Validation, Writing -review & editing Writing -review & editing Ramya Ananthakrishnan -Validation, Writing -review & editing Rifat Mahfuza -Validation, Writing -review & editing Sarabjit Singh Chadha -Validation, Writing -review & editing Sayera Banu -Validation, Writing -review & editing Shamim Mannan -Validation, Writing -review & editing Shibu Vijayan -Validation, Writing -review & editing Shahriar Ahmed -Validation, Writing -review & editing Taofeekat Ali -Validation, Writing -review & editing Charity Oga-Omenka -Data curation, Investigation; Methodology Manjot Kaur -Data curation, Investigation; Methodology Urvashi Singh 1,17 -Writing -review & editing Writing -review & editing Guy Stallworthy -Conceptualization, Writing -review & editing Hannah Monica Yesudian Dias 20 -Conceptualization, Writing -review & editing Madhukar Pai -Conceptualization, Writing -review & editing