PLoS One. 2022;
17(4): e0267029. Daria Szkwarko, Conceptualization, Data curation, Formal analysis, Funding acquisition, Methodology, Project administration, Supervision, Writing – original draft, Writing – review &
editing, Hamidreza Karimi-Sari, Editor AbstractBackgroundUntreated latent tuberculosis infection (LTBI) is a major source of active tuberculosis disease in the United States. In 2016, the United States Preventive Services Task Force (USPSTF) recommended that screening for latent tuberculosis infection among individuals at increased risk be performed as routine preventive care. Traditionally, LTBI management–including both testing and treatment–has been conducted by specialists in the United States. It is believed that knowledge gaps among primary care team members and discomfort with LTBI treatment are significant barriers to LTBI management being conducted in primary care. Methods and objectivesThis qualitative study sought to evaluate the knowledge, attitudes, and skills of primary care team members regarding the LTBI care cascade, and to identify each stepwise barrier limiting primary care teams in following the USPSTF recommendations. ResultsWe conducted 24 key informant interviews with primary care providers and nurses in Rhode Island. Our results demonstrate that overall, few primary care providers and nurses felt comfortable with LTBI management, and their confidence and comfort decreased throughout the cascade. Participants felt least confident with LTBI treatment and held misconceptions about LTBI testing, such as high cost. Although participants were not confident about LTBI treatment, most were enthusiastic about treating patients if provided additional training. Participants suggested that their lack of knowledge regarding LTBI treatment led to high rates of referral to specialist providers. ConclusionThe gaps revealed in this study can inform training curricula for primary care team members in Rhode Island and nationally to shift the USPSTF policy into practice, and, ultimately, contribute to TB elimination in the United States. IntroductionIt is estimated that 13 million people in the United States (US) have latent tuberculosis infection (LTBI). Untreated LTBI is responsible for 80% of tuberculosis (TB) disease nationally [1]. Since the 1960s, preventive therapy (i.e. isoniazid) has been recognized to significantly reduce progression to TB disease. However, only three quarters of at risk individuals are screened for LTBI, and only 62% of individuals who started LTBI therapy completed treatment [2]. In 2016, the United States Preventive Task Force (USPTF) provided updated recommendations that LTBI testing be performed in populations at increased risk as part of routine preventive care [3]. Traditionally, LTBI testing and treatment in the US has often been conducted by specialists in TB clinics. The most common risk factor in the US for TB is having been non-US born; this population already faces many barriers to accessing health care [4]. As stated by Katrak and Flood in a 2018 commentary, it is believed that knowledge gaps among primary care providers (PCPs) and lack of familiarity with LTBI treatment regimens (recommended regimens in the US include 9 months of isoniazid, 4 months of rifampin, 3 months of weekly rifapentine and isoniazid) remain significant barriers to treatment for underserved populations [5]. Furthermore, non-US born populations such as refugees and asylum seekers can experience difficulty in connecting with other services, and it has been suggested that this can be worsened both by poor communication among providers as well as complex healthcare systems [6]. Task shifting LTBI testing and treatment into primary care represents a critical strategy towards TB elimination [7]; patients can be screened and treated within their primary care home, avoid the need to establish care with new specialist providers, and complete documentation of this intervention within their primary care medical record. This can all be done as part of their routine primary care preventive visits. However, prior to the USTPF guidelines update there was little impetus to include LTBI testing and treatment in routine preventive screening and primary care visits. The shift of the USPSTF screening guidelines to a Grade B recommendation ensures private insurance coverage for these activities, thus removing the cost barrier [8]. In order to design educational programs to democratize LTBI knowledge and assist primary care practices and healthcare systems to support primary care providers in LTBI testing and treatment, more information is needed to understand how PCPs and nurses perceive their knowledge, attitudes, and skills regarding LTBI testing and treatment in their practices. Given the exploratory nature of this topic, qualitative methodology can best elucidate the thematic knowledge, attitudinal, and skill gaps that exist. In this qualitative study, we aimed to explore the knowledge, attitudes, and skills (KAS) among Rhode Island (RI) PCPs and nurses regarding the latent TB infection care cascade—from recognizing and screening the at-risk population for LTBI, to evaluating for active TB disease, and to initiating, monitoring, documenting, and reporting completion of therapy. At each cascade step, there are potential KAS gaps that can influence a PCP’s or nurse’s ability to carry out LTBI testing and treatment. We set out to use qualitative research methods which are uniquely suited to exploratory research aimed at uncovering these gaps. We then aimed to apply our findings to facilitate transition of USPSTF guidelines into practice, with the ultimate goal to improve TB prevention and care. MethodsThis qualitative study was the first phase of a three-phase exploratory sequential translational study (clinicaltrials.gov ID: NCT04188041). A purposive sample of key informant PCPs and nurses working in RI were recruited to participate [9]. Key informant interviews were conducted in order to purposively include PCPs and nurses who work and have an understanding of at-risk populations. Our study reporting conforms to the Consolidated Criteria for Reporting Qualitative Research (S1 Checklist). SettingKey informant interviews (KIIs) were conducted with PCPs and nurses who work in a variety of outpatient practices throughout RI. In the United States, primary care is provided by PCPs which include both physicians as well as mid-level providers such as physician assistants or nurse practitioners. For LTBI care, PCPs can order LTBI testing, order and interpret LTBI evaluation, initiate LTBI treatment, and conduct follow up visits. Nurses work alongside PCPs on the primary care team where their role involves ordering LTBI tests, including planting and interpretation of tuberculin skin tests, and conduct treatment adherence assessment during follow up visits. The majority of interview participants work in primary care settings that serve large non-US born populations. RI has one TB specialty clinic, located in Providence, the largest city in the state, that provides treatment for both TB disease and latent TB infection [10]. In 2019, there were 14 individuals diagnosed with TB disease, and 93% of these individuals were non-US born [11]. Although LTBI is a reportable condition in RI, compliance with this reporting requirement is unclear. Traditionally, many primary care practices in RI refer people with positive LTBI screen to the TB specialty clinic; however a small proportion of patients are diagnosed and treated solely through community health centers that commonly serve LTBI-affected populations [12]. Participant recruitmentUsing purposive, criteria-based sampling to recruit PCPs and nurses, we sent emails to invite them to participate in the study [9]. Our inclusion criteria were mid-level PCPs such as nurse practitioners as well as physicians with family medicine or internal medicine training. We excluded those who did not currently have a primary care panel. We used purposive sampling to ensure inclusion of participants from Federally Qualified Health Centers in the state that serve at-risk populations, as well as other practice setting types. Authors (DS and REG) are faculty in the department of Family Medicine, and many PCPs throughout the state are alumni from this department. In addition to emailing our alumni and departmental networks, we circulated study information to medical directors at Federally Qualified Health Centers (FQHCs) and other large practices in the state that serve non-US born populations to recruit PCPs and nurses. Participants were offered a $75 gift card for their participation. Instrument and data collectionA qualitative, semi-structured interview guide was developed based on a literature review and authors’ clinical expertise regarding potential knowledge, attitude, and skill gaps. The guide included open-ended core questions that were supplemented with spontaneous probes and follow-up questions during interviews to explore the barriers impacting all LTBI steps (S1 File). We piloted the interview guide with two PCPs and modified the questions based both on their feedback and the team’s input. After obtaining consent from participants, KIIs were conducted either in person or virtually by authors SK or DS. SK is an Asian-American, cis-male fourth-year medical student and DS is a white, cis-female family medicine and preventive medicine physician. Both interviewers underwent qualitative interviewer training with REG, a qualitative research expert with more than 20 years of experience. After the training, REG also listened to the pilot interviews and provided feedback on interviewer technique. For in person interviews, written consent was obtained in person. For virtual interviews, participants were emailed a consent document in advance to review. The consent document was read aloud at the start of the virtual interview, participants were invited to ask any clarifying questions, and verbal consent was documented by the study team by signing the informed consent on the participant’s behalf and indicating that consent was obtained verbally. We continued data collection until we reached data saturation. We identified when data saturation was reached through iterative discussion of the interviews by the two interviewers throughout the interview process. During this process, we identified when the same responses were repeatedly elicited and no new content was being collected, or themes emerging [13]. Data analysisInterviews were digitally audio-recorded and then professionally transcribed verbatim. Transcripts were cleaned by SK; any identifiable data were removed, any inaudible text was identified, audio-recordings were listened to, and transcripts were edited to ensure accuracy. Two data analysis approaches were used in stepwise fashion. First, Immersion/Crystallization was used as transcripts were read in their entirety by both DS and SK, while taking notes for overall familiarity with content [14]. These notes were then used as a basis for Template Organizing Style Analysis [15]. whereby a codebook with code definitions was created based on the knowledge, attitude and skill constructs at each cascade step that informed the interview guide, as well as content categories and themes that emerged in the first stage of Immersion/Crystallization analysis of the transcripts [14]. The codebook was tested independently by SK and DS on three transcripts. Coding was compared and discussed, and the codebook was finalized. Flexible coding schemes were maintained to accommodate addition of new codes during the coding process. DS completed the coding process using the data analysis software, NVivo [16]. Following coding, DS and SK again used Immersion/Crystallization techniques to read each code report for content, patterns and themes [14]. This process, along with discussing emerging findings throughout the process with all co-authors, resulted in final interpretation of the data. Our stepwise data analysis approach, the use of NVivo, and our check-ins with all co-authors ensured rigor at each stage of analysis. Ethics approvalThis study was approved by the Kent Hospital Institutional Review Board in RI. Lifespan and Brown University entered into an IRB reliance agreement with Kent Hospital with both organizations relying on Kent Hospital, as the IRB of record, for IRB review and oversight of the project. ResultsWe conducted 25 interviews—22 PCPs and 3 nurses. One physician interview was excluded, as the interviewee had not yet started working in a primary care setting. Of the 21 PCPs included, 18 (86%) were trained in family medicine, two (9%) in medicine/pediatrics, and one (5%) in internal medicine. Seven (33%) practiced in FQHCs, five (24%) in academic practices, and nine (43%) in private practices. Three of the PCPs were resident physicians in training. The three registered nurses worked at an FQHC with a clinic that conducted health screening for immigrants to the US. Most PCPs practiced full spectrum primary care, with 19 (90%) seeing patients of all ages and 20 (95%) seeing pregnant patients. Of all PCPs and nurses, 11 (46%) reported many of their patients are Spanish speaking, 19 (79%) reported that more than one third of their panel is non-US born, and 10 (42%) reported they see many patients with lower socioeconomic status (Table 1). Table 1Demographics of primary care providers and nurses interviewed (n = 24).
Overall LTBI managementOverall, few participants (PCPs and nurses) felt comfortable with LTBI management in general, and confidence and comfort decreased as the care cascade progressed (i.e. participants felt most comfortable and confident with testing and least comfortable and confident with treatment), Fig 1.  Primary care providers’ and nurses’ knowledge, attitudes, and skills regarding LTBI management–major themes throughout the care cascade. Those with unique personal experiences with their own LTBI diagnoses, work experiences in high TB and LTBI burden settings, and/or training or mentorship regarding LTBI expressed more knowledge and comfort with LTBI management. Residents in training expressed more comfort with looking up LTBI information on resources such as UpToDate [17] than did experienced PCPs. One PCP stated:
Regarding USPSTF guidelines, 9 out of 16 participants who engaged in discussion about the guidelines were unaware of the current recommendation for LTBI screening and treatment. Most PCPs expressed discomfort with evaluating and treating LTBI in special populations such as patients living with HIV, pregnancy, children, and the elderly. For example, one PCP stated:
Another PCP mentioned, “I think if [patients] had underlying immunodeficiency, and probably the pediatric population, I would feel less comfortable diagnosing active TB or ruling out active TB.” Resident physician participants were more willing to attempt all aspects of LTBI care given that they felt supported in a training environment. One said, “I’m still a resident, meaning I’m in a learning environment. So I have multiple colleagues that I can ask questions to, but I think once you’re out of residency it’s a little harder.” We report the rest of our findings according to the LTBI care cascade steps. LTBI screeningThe majority of PCPs screened for LTBI very infrequently, with three reporting that they never screen for LTBI. The few who claimed to be screening regularly work in unique practices that see newly arrived immigrants more frequently when compared to other practices. One PCP described seeing many new immigrants from Central America in her patient panel, stating “I’ve only been working for like two months. I probably see fifteen to twenty patients a week right now. Out of those patients that come—maybe five out of fifteen are screened.” Most participants knew several factors that should prompt LTBI screening. However, few were aware of all of the factors. The majority mentioned immigration from or travel to a high TB burden country to be a reason to conduct LTBI testing. For example, one PCP mentioned:
Many PCPs identified incarceration, employment screening, exposure to active TB disease, and being a healthcare worker as reasons to screen for LTBI. Few mentioned immunocompromised conditions like HIV or starting an immunosuppressant as an indication to screen. PCPs demonstrated gaps in their knowledge regarding LTBI screening, as some mentioned symptoms of active TB disease as an indication to screen, and others were unsure about guidelines regarding screening healthcare workers. When PCPs proceeded to test for LTBI, the majority preferred the Interferon Gamma Release Assay (IGRA) over purified protein derivative (PPD). They perceived IGRA to be more accurate and easier to perform and interpret. Most acknowledged the possibility of a false-positive reaction with the PPD for patients with history of Bacillus Calmette-Guérin (BCG) vaccination. One PCP mentioned, “But if a patient has a BCG vaccine growing up in a country where that’s done, routinely the PPD is likely to have a false positive. So then the IGRA is a more accurate test. And generally I just find it somewhat more convenient [for the patient] than having two visits.” The most commonly reported benefit of the IGRA was its superior convenience for patients and team members, as it could be performed over a single visit, as opposed to two visits with the PPD. A PCP said, “I think the IGRA is great because they order labs on people all the time for less important things. I can add it on with other labs, or it’s very easy to do on a Thursday at 3:00 p.m. when you don’t want to have them come back to schedule a PPD and another visit.” A nurse commented, “We had a bunch of times where [patients] come back a week later. They’re like, ‘Oh yeah, I’m here for my [PPD read].’ It’s like, ‘We can’t read it now—you have to have it replanted.’ So we have to see them a week from their plant date and replant it.” Furthermore, PCPs often felt undertrained on PPD planting and interpretation. One PCP stated:
Another provider mentioned:
Participants who were more comfortable with the PPD had unique patient populations that necessitated more on-the-job exposure to PPDs than most of the other participants interviewed had. Additionally, nurses comprised the majority of participants who were comfortable with planting and interpreting the PPD. One nurse shared, “I feel like I was pretty comfortable, you know, just having worked at the hospital…the specific experience of immigration clinic, I definitely gained a lot more confidence [in planting and interpreting PPDs] as a result of that experience.” Despite the many benefits discussed about IGRA testing, PCPs demonstrated gaps in knowledge regarding LTBI testing in general. For example, PCPs were largely unaware that the effect of BCG on PPD wanes over time or that there are different age recommendations for LTBI testing (e.g. IGRA is not recommended under age two). One PCP said, “I think I’m recalling that if someone has had the BCG vaccine, that IGRA is better or more accurate. And I forget about the ages. I think there are age recommendations when you do one versus the other like in kids, for example.” Moreover, some PCPs expressed the misconception that patients with a positive LTBI test result can test negative later in life. PCPs were often concerned about the cost of the IGRA test compared to the PPD. Cost alone was sometimes the primary driver towards planting a PPD vs ordering an IGRA. One PCP stated, “Even though there’s the difficulties of returning, I try to start with the PPD mostly just because of the cost of the IGRA versus the PPD.” A nurse stated:
PCPs occasionally discussed treating the IGRA as a confirmatory or second line test to the PPD. One PCP stated, “So for patients who have been vaccinated with BCG’s or who previously tested positive for PPD…We would normally order a Quant Gold [IGRA] anyways and have that confirmatory backup.” Many PCPs mentioned that they report positive LTBI results to the Rhode Island Department of Health (RIDOH). Those who report consistently have nursing support to complete the reporting process. Of those who did not report LTBI to the RIDOH, most were not aware of reporting guidelines. A few assumed that the TB clinic reports to the RIDOH and referred to them without reporting. TB disease evaluationMany participants were comfortable with conducting TB disease evaluation (symptom screening and ordering a chest x-ray to rule out active TB disease) for otherwise healthy adult patients who have a positive LTBI screening test. However, the majority refer otherwise healthy adult patients to the TB clinic for final diagnosis interpretation and management. One PCP said, “I think probably the most common thing I now see is positive testing, negative chest x-ray, send them to the TB Clinic to do all other treatment and management decisions.” Some participants, particularly nurses, expressed comfort with TB disease evaluation because they use a symptom checklist either from their electronic medical record or the CDC website to conduct TB disease evaluation. One described the process as, “We have a set form in our computer system where we literally just go down a list. So I felt pretty comfortable.” A few PCPs avoided evaluation altogether and instead immediately referred to the TB clinic. One PCP stated, “Just because I don’t [do the TB evaluation] ever, I would probably send to the [TB Clinic]. If for some reason I couldn’t get them there, I don’t know, [they are] homebound or something, I would probably go to UpToDate.” A few participants mentioned language as a barrier to evaluation. The participants who expressed discomfort with LTBI evaluation also noted the lack of patients with LTBI in their practices. “I wouldn’t say super comfortable, especially after four years of not having to deal with positive test results.” LTBI treatmentGenerally, participants were not knowledgeable about or comfortable with providing LTBI treatment. While many PCPs were aware of some LTBI medications, including isoniazid and rifampin, they were less familiar with the variety of side effects and medication interactions associated with these medications. PCPs were also unsure about treatment duration and guidelines. Few knew the appropriate timing of follow up and appropriate labs or symptoms to monitor for. Very few knew about combined shorter course regimens (i.e. isoniazid and rifapentine for three months) as an available regimen. When asked about why PCPs are not treating LTBI in primary care settings, one PCP stated:
Many providers also expressed discomfort with treating patients with LTBI. One stated, “I think once you’re out of residency it’s a little harder. It’s your license on the line if you mess it up, and if you haven’t previously done it [treated LTBI], then it feels like more of a risk to try. And you know, it’s a long, extensive therapy.” Some struggled to confidently decide which patients are appropriate candidates for treatment. Other PCPs were uncomfortable treating LTBI in patients living with other medical considerations such as HIV, pregnancy, or chronic illness. Moreover, PCPs felt under-supported and under-trained to shoulder the added risk and time associated with LTBI treatment. A few PCPs mentioned that treatment would go against clinic policies or established tendencies to refer to specialists.
In addition to feeling less comfortable with LTBI treatment, PCPs also felt that specialists and the TB clinic had more resources to provide better patient care. One PCP stated:
PCPs expressed that specialists had more time, skill, and knowledge to appropriately educate and follow up with LTBI patients. One stated:
Some PCPs mentioned fear of conflict with specialists. One stated, “I think TB treatment has sort of been owned by global health and infectious disease for such a long time that I think you’re stepping on toes. You’re creating turf battles if you do it.” However, some PCPs expressed concern that patients who are referred are often unable to readily access specialist care. One commented, “But it’s a lot of work to ask [patients] to go to another doctor, and there’s transportation issues. There’s scheduling issues. And our patients don’t have stable phone numbers and don’t check their voicemail the way that I think a lot of us, if it were you or I who were going through this process.” Many participants expressed interest in being able to provide LTBI treatment to patients. One mentioned, “I mean if I could, then I would like to treat them myself because I know the patient better, and I can make sure that they are actually taking the medication.” Another said, “I’d like to learn more. I know that there’s an option for a shortened course. I believe it’s isoniazid and rifampin together. I don’t prescribe rifampin. I don’t have a lot of experience or comfort with it. I think it can turn your eyes or tears orange or something like that.” Regarding LTBI treatment follow up, many participants knew that they should be looking out for medication side effects and conducting follow-up visits with patients. However, few actually knew specific side effects or time intervals for follow-up. Many were not aware of the current guidelines regarding laboratory testing prior to and during LTBI treatment. One stated, “Yeah I mean I would have to look this up, but I think you have monthly visits to make sure there are no issues taking the medication. I forget what the recommendation is on checking liver enzymes. Maybe that would be something I would be doing.” DiscussionIn order to successfully adopt the USPSTF’s updated guidelines recommending LTBI screening as part of routine preventive screening in primary care, it is critical to understand PCPs’ and nurses’ knowledge, attitudes, and skills regarding LTBI management. The current LTBI management model depends heavily on referrals to specialists, is complicated by significant loss of patients throughout the process, and creates both time and cost burdens for patients. Benefits in recognizing the central role played by primary care teams in streamlining patient-centered care are clear, but the inclusion of primary care for LTBI screening and treatment represents a paradigm shift for public health departments, specialists, and primary care teams. As a whole, our study demonstrates that PCPs are uncomfortable with LTBI care in general, and their confidence and comfort decreases throughout each step of the LTBI management cascade—screening, evaluation for TB disease, and treatment [2]. This manuscript is the first qualitative study to our knowledge to explore this topic and sheds light on the limitations surrounding adoption of the USPSTF LTBI guidelines among primary care team members. In regard to LTBI screening, PCPs were familiar with both testing modalities—the PPD and IGRA—but many held common misconceptions about them. The most common misconception regarding the IGRA was that it is costlier to perform than the PPD. Although out-of-pocket charges for IGRA over PPD does represent a significant difference, this cost differential pertains to uninsured patients, as screening test recommendations under USPSTF guidelines are covered by insurance providers. In addition, the IGRA has actually been proven to be cost-effective for practices seeking to save costs related to screening and treating at-risk individuals such as non-US born populations [18]. The most common misconception that PCPs held regarding the PPD was that a childhood BCG vaccination can interfere with a PPD result throughout a patient’s lifetime. Though the BCG is associated with a positive PPD result in childhood, the effect wanes with time and is likely negligible at ages over 30 years old [19]. Another misconception was that a positive LTBI test result can convert to negative later in life. Misconceptions such as this one can lead to unnecessary testing and potential harm since repeating a positive PPD for example can lead to a larger, more painful, reaction. Generally, PCPs believed that though the IGRA was the more accurate test, it should be treated as a confirmatory or second line test to the PPD. On the contrary, the Centers for Disease Control recommends IGRA screening over PPD in non-US born individuals from countries with moderate to very high incidence of TB disease who have received BCG vaccination. It does not recommend utilizing both tests when testing for LTBI [20]. PCPs and nurses said they were often comfortable with evaluating young and healthy patients for TB disease. However, following a positive test result, PCPs were then hesitant to proceed to treatment, often referring at this point to specialists for further management. While most PCPs did not have the knowledge or comfort to treat LTBI in primary care, the majority expressed enthusiasm to learn and incorporate treatment into their practices, especially for otherwise healthy adults. Similar to the transition of Hepatitis C management to a primary care setting, a shift in LTBI management to primary care could allow for reduced loss to follow-up and allow specialists to focus on patients with increased risk or complicating co-morbidities [21]. Additionally, PCPs often have strong physician-patient relationships [22], and relationship strength has been shown to increase medication compliance, which may be particularly important for the vulnerable populations that LTBI disproportionately affects [23]. Diagnosing and treating LTBI prior to its progression to TB disease allows for substantial cost savings, as LTBI carries 5–10% lifetime risk of progression to TB disease, but its treatment is at least 32 times less expensive than the treatment of TB disease [24]. It is also well understood that it will be impossible to reach TB elimination without improvement in LTBI treatment completion [25]. This study has several limitations. Given that our participants were all PCPs or nurses in Rhode Island, their views may differ from PCPs and nurses in other states nationally. Most of the PCPs were family medicine trained and connected to the Warren Alpert Medical School of Brown University network. They may reflect different values when compared to PCPs trained in other specialties or in non-academic settings. Three PCPs were trained in internal medicine and two in pediatrics, and although their views were consistent with FM providers’ perspectives, future research should include a wider variety of primary care specialties including OBGYN. Moreover, most participants completed training recently. Although this suggests that LTBI training in medical school, residency and nursing school is lacking, their perspectives may not be reflective of PCPs and nurses who are further out of training. We were unable to recruit nurses beyond one health center and this health center conducted immigration screening. Therefore, nurses in our study seemed well-versed in LTBI testing which may not be consistent with nurses in clinics serving fewer non-US born patients. The major strength of this study is that it reveals specific knowledge gaps among PCPs and nurses that could be targeted in future training programs. Our study suggests that the preconceived belief that PCPs are unfamiliar with LTBI treatment is likely true. Overcoming this barrier with increased training as well as improved primary care infrastructure is key to TB elimination in our country. ConclusionPCPs and nurses in Rhode Island have limited confidence and comfort regarding LTBI management and this decreases throughout the care cascade. However, participants expressed readiness to learn how to integrate these aspects of care into their practices. The lack of knowledge regarding LTBI treatment leads to high rates of referral to specialty clinics. Non-US born populations are disproportionately impacted by barriers that decrease their ability to see a specialist, thereby increasing loss to follow-up. For the patient, it is a primary prevention intervention lost, and for the public health system, an opportunity missed to contribute toward TB elimination. Increased training focused on the gaps identified in this study has potential to move the USPSTF recommendations on LTBI screening into broad primary care adoption. Supporting informationS1 ChecklistCOREQ checklist. (DOCX) S1 FileQualitative interview guide for PCPs. (DOCX) AcknowledgmentsWe would like to acknowledge all of the busy primary care providers and nurses who took the time to participate in this study. We would also like to thank Thomas Bertrand, Jill Lamantia, and Caroline Gummo from the Rhode Island Department of Health as well as Dr. Natasha Rybak from the RISE TB Clinic for their historical perspective regarding LTBI practices in Rhode Island. Funding StatementDS is partially supported by an internal Institutional Development Award Number U54GM115677 funded by the National Institute of General Medical Sciences of the National Institutes of Health, which funds Advance Clinical and Translational Research (Advance-CTR https://www.brown.edu/initiatives/translational-research/home). Advance-CTR funded this research and members of their team provided mentorship to authors regarding Nvivo use. SK is supported by an internal program that is funded by the NIH/NIAID under R25AI140490 – Emerging Infectious Disease Scholars (EIDS https://www.brown.edu/academics/medical/plme/current-students/enrichment-activities/research-opportunities/emerging-infectious-diseases-scholars-) Program at Brown University. EIDs provided funding to support SK’s time, but otherwise did not support the research in any other way. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health, Advance-CTR, or EIDS. Data AvailabilityData cannot be shared publicly as per our Kent Hospital Institutional Review Board approved protocol and approved consent form. Our approved consent specifically states that participant data that are potentially identifiable will not be shared. Given the nature of our qualitative transcripts and coding sheets, although stripped of identifiers such as names, they contain potentially identifiable and sensitive participant information in even the most aggregate form if shared with certain individuals who are familiar with our context. For further questions regarding the IRB approved protocol and consent, you may contact Dorinda Williams, the Kent Hospital IRB coordinator at gro.enerac@smailliwrod. 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Decision Letter 010 Aug 2021 PONE-D-21-05814 Primary care providers’ and nurses’ knowledge, attitudes, and skills regarding latent TB infection testing and treatment: A qualitative study from Rhode Island PLOS ONE Dear Dr. Szkwarko, Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process. The reviewers have identified a range of concerns regarding the content and presentation of your manuscript that need to be carefully addressed in a revision. Please pay particular attention to responding to each of the points raised by Reviewer 3. Please submit your revised manuscript by Sep 23 2021 11:59PM. 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SK is supported by NIH/NIAID under R25AI140490 – Emerging Infectious Disease Scholars (EIDS https://www.brown.edu/academics/medical/plme/current-students/enrichment-activities/research-opportunities/emerging-infectious-diseases-scholars-) Program at Brown University. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health, Advance-CTR, or EIDS." Please provide an amended statement that declares *all* the funding or sources of support (whether external or internal to your organization) received during this study, as detailed online in our guide for authors at http://journals.plos.org/plosone/s/submit-now. Please also include the statement “There was no additional external funding received for this study.” in your updated Funding Statement. Please include your amended Funding Statement within your cover letter. We will change the online submission form on your behalf. 5. Please include captions for your Supporting Information files at the end of your manuscript, and update any in-text citations to match accordingly. Please see our Supporting Information guidelines for more information: http://journals.plos.org/plosone/s/supporting-information [Note: HTML markup is below. Please do not edit.] Reviewers' comments: Reviewer's Responses to Questions Comments to the Author 1. Is the manuscript technically sound, and do the data support the conclusions? The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented. Reviewer #1: Partly Reviewer #2: Yes Reviewer #3: Partly ********** 2. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: N/A Reviewer #2: N/A Reviewer #3: No ********** 3. Have the authors made all data underlying the findings in their manuscript fully available? The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified. Reviewer #1: Yes Reviewer #2: Yes Reviewer #3: Yes ********** 4. Is the manuscript presented in an intelligible fashion and written in standard English? PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here. Reviewer #1: No Reviewer #2: Yes Reviewer #3: No ********** 5. Review Comments to the Author Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters) Reviewer #1: Thank you for your valuable work. The following will be effective in improving your work. 1. Explaining the necessity of working with a qualitative method has not been done, while the questions can be answered with a quantitative method. 2. There is a need to edit and justify the lines. 3. What was the criterion for completing sampling and saturation in this study? 4. Which method was used to analyze the data? (With reference) 5. How is the data confidentiality criterion met? 6. Explain the inclusion and exclusion criteria. 7. Explain the questions used in the research (At least the basic questions) 8. Category tagging has happened with quantitative and pre-arranged visibility. Reviewer #2: This a wonderful study and is aimed at promoting ending of TB disease through not missing any LTBI untreated. It is very vital that this approach to ending TB is widely known and utilised by all countries main with high TB stats. In the background it was noted that there was no mention of LTBI treatment regimens as to be comprehensive in the clear description of the problem at hand. There is also a need to describe the distinct difference between the PCPs and Nurses as these causes confusion as to who is who. This is given the notion that nurses are primary health care provided and this is at least what is known universally. The article was well formatted Reviewer #3: Manuscript Number: PONE-D-21-05814 Article Type: Research Article Full Title: Primary care providers’ and nurses’ knowledge, attitudes, and skills regarding latent TB infection testing and treatment: A qualitative study from Rhode Island I read carefully the paper with title and manuscript list above. Beside that authors rise a thematic that is very import for healthcare institutions and hospitals, I consider that the proposal paper lacks in many aspects it orders to meet the scientific requirements for publication, especially in a journal as PLOS One is. According to my opinion and the main concern is that the number of 21 primary care providers (PCP) including in this quality study is not sufficient, in a population of Rhode Island of more than 1 Mio, and a number of physicians of more than 2500. Also, I consider that the authors, should prepare one questionnaire that is uniform and all participants in the study to answer on it and not to be based just on the interview. I consider that on this approach the authors could get much more reliable data’s for their scientific study and based on these to have much more clear picture for knowledge, attitudes and skills of PCP regarding LTBI in Rhode Island. In Introduction part there is many sentences that has not a reference; Line 62-65; Line 71-80; Line 84-86; ect… The Results part has not been clarifying fully in all study aspect and moreover is not present appropriately. There is just one table and some interviews. The Reference part is not uniform. I’m not sure for the style the authors selected and if this style has been applying to all references. See references Nb. 6,7,8,9,10,11,… Also, the English written style in some sentences was not clear and understand, so my proposal is to be check by any professional scientific experience researchers for improve. Based on all point mention above, I considered that this paper should be revise completely and after to be submitted once more. Thank you and best regards. ********** 6. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files. If you choose “no”, your identity will remain anonymous but your review may still be made public. Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy. Reviewer #1: Yes: Ebrahim Aliafsari mamaghani Reviewer #2: Yes: Prof Lufuno Makhado Reviewer #3: No [NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.] While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at gro.solp@serugif. Please note that Supporting Information files do not need this step. AttachmentSubmitted filename: Review and proposals_B.Neziri_27621.pdf Author response to Decision Letter 011 Nov 2021 Please see attached Response to Reviewers document. AttachmentSubmitted filename: PlosOne.RevisionResponses.FINAL.docx Decision Letter 121 Jan 2022 PONE-D-21-05814R1Primary care providers’ and nurses’ knowledge, attitudes, and skills regarding latent TB infection testing and treatment: A qualitative study from Rhode IslandPLOS ONE Dear Dr. Szkwarko, Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process. Please submit your revised manuscript by Mar 07 2022 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at gro.solp@enosolp. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file. Please include the following items when submitting your revised manuscript:
If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter. If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions see: https://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols. Additionally, PLOS ONE offers an option for publishing peer-reviewed Lab Protocol articles, which describe protocols hosted on protocols.io. Read more information on sharing protocols at https://plos.org/protocols?utm_medium=editorial-email&utm_source=authorletters&utm_campaign=protocols. We look forward to receiving your revised manuscript. Kind regards, Hamidreza Karimi-Sari, MD Academic Editor PLOS ONE [Note: HTML markup is below. Please do not edit.] Reviewers' comments: Reviewer's Responses to Questions Comments to the Author 1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation. Reviewer #1: All comments have been addressed ********** 2. Is the manuscript technically sound, and do the data support the conclusions? The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented. Reviewer #1: Partly ********** 3. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: No ********** 4. Have the authors made all data underlying the findings in their manuscript fully available? The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified. Reviewer #1: No ********** 5. Is the manuscript presented in an intelligible fashion and written in standard English? PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here. Reviewer #1: Yes ********** 6. Review Comments to the Author Reviewer #1: Thank you for your valuable work. The following can be effective in improving your work The necessity of the work and the reason for using the qualitative method should be highlighted in the introduction. - Explain the method of analysis and the type of qualitative method. - Explain how to achieve saturation - Explain how to ensure study rigor. - Labeling the categories with a qualitative look - At the beginning of the method, the clinical trial code is stated, but this study is descriptive and qualitative Author response to Decision Letter 122 Feb 2022 Response to Reviewers Reviewer #1: Thank you for your valuable work. The following can be effective in improving your work The necessity of the work and the reason for using the qualitative method should be highlighted in the introduction. Thank you for this comment. We have added justification for the work as well as using qualitative methodology in the introduction. - Explain the method of analysis and the type of qualitative method. This study used key informant interviews with PCPs and nurses in Rhode Island who work with at risk populations. A justification for this type of method has been added to the method section. The methods of analysis are described in the data analysis section and involved two steps – immersion/crystallization and template organizing style. We recognized that we accidentally included the immersion/crystallization reference in the wrong place and have updated this. - Explain how to achieve saturation The last line of the data collection paragraph describes how we reached data saturation. Reference 13 supports our approach. - Explain how to ensure study rigor. Our stepwise data analysis approach, the use of Nvivo, and our check-ins with all co-authors ensured study rigor. We have added a sentence reflecting this at the end of data analysis. - Labeling the categories with a qualitative look Our process of using immersion/crystallization for familiarity with content and to develop the code categories for the next phase of template style analysis using NVivo coding is outlined in the analysis section. With this method, we coded for content and then went back into the coded data, again using immersion/crystallization techniques, to identify patterns and themes in the coded data to come to final interpretation. - At the beginning of the method, the clinical trial code is stated, but this study is descriptive and qualitative This manuscript describes the results of the first aim of a three-phase exploratory sequential translational study. Aim 2 is a trial. As described in detail when the clinical trial # is searched (https://clinicaltrials.gov/ct2/show/NCT04188041), the results of the qualitative study described in this manuscript informed the design of the educational intervention studied in Aim 2. We did not provide additional details about this since the methods are outlined carefully on the trial website. AttachmentSubmitted filename: PLOSONE.R2.ReviewerResponses.FINAL.docx Decision Letter 228 Feb 2022 PONE-D-21-05814R2Primary care providers’ and nurses’ knowledge, attitudes, and skills regarding latent TB infection testing and treatment: A qualitative study from Rhode IslandPLOS ONE Dear Dr. Szkwarko, Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process. Please carefully consider the peer-review comments in the next revision. Please submit your revised manuscript by Apr 14 2022 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at gro.solp@enosolp. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file. Please include the following items when submitting your revised manuscript:
If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter. If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions see: https://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols. Additionally, PLOS ONE offers an option for publishing peer-reviewed Lab Protocol articles, which describe protocols hosted on protocols.io. Read more information on sharing protocols at https://plos.org/protocols?utm_medium=editorial-email&utm_source=authorletters&utm_campaign=protocols. We look forward to receiving your revised manuscript. Kind regards, Hamidreza Karimi-Sari, MD Academic Editor PLOS ONE Journal Requirements: Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice. Reviewers' comments: Reviewer #1: For The necessity of the work and the reason for using the qualitative method should be highlighted in the introduction: Your changes were not convincing to me. You can highlight the need to use this approach. For Explain how to ensure study rigor: Your changes were not convincing to me. Criteria as well as action for each criterion are not mentioned For Labeling the categories with a qualitative look: Your changes were not convincing to me. Needs editing, especially in the case of spacing. ********** While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at gro.solp@serugif. Please note that Supporting Information files do not need this step. Author response to Decision Letter 230 Mar 2022 Journal Requirements: Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice. -Thank you for these comments. We have not retracted any references. However, we had added several new references to support our responses in the previous revision. We have indicated relevant references below in our responses to reviewer comments. Reviewer #1: For The necessity of the work and the reason for using the qualitative method should be highlighted in the introduction: -Your changes were not convincing to me. You can highlight the need to use this approach. Thank you for your comment. Regarding the necessity of the work, we would like to highlight included references that establish the importance of LTBI screening in high risk populations (See Reference #4) and the need to task shift LTBI management into primary care (See Reference #7). You can also see the reference for the United States Preventive Services Task Force’s recommendation regarding LTBI screening (See Reference #8 and #3). As mentioned in these references, LTBI screening and treatment is critical to achieve TB elimination in the United States. As indicated in the systematic review and meta-analysis by Alsdurf et al. (reference 2) this is not successfully happening within the current health care paradigm and therefore, task shifting into primary care is an important strategy. Regarding the use of qualitative methods, we have indicated the exploratory nature of our research topic in the introduction. At this point in time, it is widely recognized that qualitative methods are uniquely suited to exploring topics or applications for which little is known because data are collected in participants’ own words. We added a sentence at the end of the introduction. As mentioned in the introduction and methods, these results were used to design an educational program geared towards primary care providers (detailed methods can be found here: NCT04188041) For Explain how to ensure study rigor: Your changes were not convincing to me. Criteria as well as action for each criterion are not mentioned -We included additional citations in our document to demonstrate reasoning behind methodology and to demonstrate that methods used are established in qualitative research. Please refer to References #9, 13, and 15. Please see S1 file for our completed Consolidated Criteria for Reporting Qualitative Research document. We hope that these criteria are what the reviewer is referring to. For Labeling the categories with a qualitative look: Your changes were not convincing to me. -As described, we used the process of immersion/crystallization (reference 14) to develop the code categories. This is an established qualitative data analysis technique. Needs editing, especially in the case of spacing. -Thank you. This may be an issue when switching between word processing software. We have gone through and eliminated all of the additional spaces and hope that this issue is now resolved. Decision Letter 31 Apr 2022 Primary care providers’ and nurses’ knowledge, attitudes, and skills regarding latent TB infection testing and treatment: A qualitative study from Rhode Island PONE-D-21-05814R3 Dear Dr. Szkwarko, We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements. Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication. An invoice for payment will follow shortly after the formal acceptance. To ensure an efficient process, please log into Editorial Manager at http://www.editorialmanager.com/pone/, click the 'Update My Information' link at the top of the page, and double check that your user information is up-to-date. If you have any billing related questions, please contact our Author Billing department directly at gro.solp@gnillibrohtua. If your institution or institutions have a press office, please notify them about your upcoming paper to help maximize its impact. If they’ll be preparing press materials, please inform our press team as soon as possible -- no later than 48 hours after receiving the formal acceptance. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact gro.solp@sserpeno. Kind regards, Hamidreza Karimi-Sari, MD Academic Editor PLOS ONE Additional Editor Comments (optional): Reviewers' comments: Acceptance letter7 Apr 2022 PONE-D-21-05814R3 Primary care providers’ and nurses’ knowledge, attitudes, and skills regarding latent TB infection testing and treatment: A qualitative study from Rhode Island Dear Dr. Szkwarko: I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department. If your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact gro.solp@sserpeno. If we can help with anything else, please email us at gro.solp@enosolp. Thank you for submitting your work to PLOS ONE and supporting open access. Kind regards, PLOS ONE Editorial Office Staff on behalf of Dr. Hamidreza Karimi-Sari Academic Editor PLOS ONE Articles from PLoS ONE are provided here courtesy of Public Library of Science |
The community health nurse prepares a teaching plan for a client with latent tuberculosis
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