The United States possesses one of the most comprehensive kidney transplant registries in the world (i.e., Scientific Registry of Transplant Recipients [SRTR] and United States Renal Data System [USRDS]). Despite the availability of such a rich data source, nationally representative data on how transplant care is structured and delivered is lacking. There are 208 adult kidney transplant centers in the United States that performed 79,756 transplants from 2007 to 2011 (www.srtr.org). As more clinical trials and observational data become available, the care of kidney transplant recipients (KTRs) has become increasingly complex and expensive. The Kidney Disease: Improving Global Outcomes (KDIGO) has proposed guidelines to assist practitioners who care for KTRs (1). These guidelines are comprehensive and based on the best available evidence. The KDIGO guidelines are less specific, however, on how this care should be delivered at specific transplant centers, and previous efforts to characterize the practice patterns in the transplant centers were not found in the literature. The variation between transplant centers in approaches to donor and recipient evaluations, inpatient health care delivery, treatment team composition, coordination of care, relationship and communication between medicine and surgery teams, and frequency of follow-up are all unknown. Furthermore, these variations in practice affect the cost of care and resources consumed by transplant programs. Through a survey distributed to the surgical and medical directors of all active transplant centers in the United States, we collected comparative data regarding these variations in the structure and delivery of care to KTRs.
The survey was completed by the surgical or medical director, or both, of 156 transplant centers (75% response rate). The characteristics of transplant centers and the providers completing the survey are shown in Tables 1 and 2, respectively. The survey results were divided into the following domains: structure and process of care, frequency of follow-up visits, and coordination of care.
Structure and Process of Care
In this domain, we assessed the availability of ancillary providers. Availability of a dedicated transplant pharmacist varied greatly between programs surveyed. Nearly as many programs had a dedicated transplant pharmacist available in both inpatient and outpatient settings as had no dedicated pharmacist available at all (Fig. 1). In a majority of centers, nephrology fellows and general surgery residents provided medical care to KTRs. Internal medicine residents were involved in 48.1% of centers (Table 3). The composition of the outpatient care team differed from the inpatient team as the presence of general surgery residents markedly decreased from 71.8% in the inpatient setting to 25.0% in the outpatient setting. In contrast, nephrology fellows were well represented on both outpatient and inpatient care teams at 59.0% and 60.3%, respectively. Physician extenders (certified nurse practitioners [CNPs] and physician assistants [PAs]) maintained a role in approximately two thirds of all care teams in both inpatient and outpatient settings.
There was significant variation in both the use of various types of hospital units and primary attending physicians for inpatient care. KTRs were fairly evenly distributed between nursing units that housed other transplant patients, other kidney (but nontransplant) patients, and on units that housed patients who did not have kidney-related disorders. The primary attending physician for a recent KTR who required intensive care unit (ICU) care was most frequently a transplant surgeon (39.1%). Slightly less frequently, the ICU attending physician was a surgical or medicine-trained intensivist (31.4%) or a transplant nephrologist (19.9%). When the need arose, regular consultations for non-renal medical issues in recipients were performed in more than 50% of transplant centers (typically by dedicated cardiologists and infectious disease specialists) (Table 3).
Frequency of Follow-Up Visits
Variation in frequency of follow-up during the first and subsequent years was reported (Table 3). During the first year posttransplant, patients were most frequently seen at least every 3 months but a near equal percentage were seen as frequently as every month. Follow-up after the first year continued to vary with nearly equal percentage of centers reporting follow-up visit frequency to be every 3, 6, or 12 months. Although timing of referral of stable patients back to their primary nephrologists varied from 0 to 12 months among centers studied, patients were most frequently referred back between 4 and 6 months after transplant. Initial contact for after-hours questions or emergencies was primarily directed to nursing staff at the transplant centers (51.9%).
Coordination of Care
Both medical and surgical teams performed pretransplant evaluations of donors and recipients in a majority of centers (Table 4). During the admission for the transplant, transplant surgery was the primary admitting team in a majority of centers (67.9%), followed by joint surgery and nephrology transplant teams (18.6%), and quite infrequently (9.6%) nephrology teams. When readmission within the first 3 months was required, surgical teams were most frequently the admitting team (45.5%). After 3 months, transplant nephrology was the admitting team in most centers. The primary outpatient follow-up team was most frequently transplant nephrology, both in the initial 3 months and after 3 months posttransplant. The overall working relationship between medical and surgical teams was characterized as either “very good” or “excellent” in total of 84% of centers. The prevalence of combined joint sit-down rounds with medical and surgical teams varied greatly between centers (Fig. 1).
The following characteristics were more frequently observed in transplant centers affiliated with a medical school compared to centers not affiliated: transplants other solid organs in addition to kidneys (pancreas [P=0.038], liver [P=0.01], heart [P=0.001], and lung [P=0.005]), onsite human leukocyte antigen (HLA) laboratory (P<0.001), patients are enrolled in a formal research protocol (P=0.037), center offers ABO-incompatible or cross-match positive transplants (P=0.009), more nephrologists and transplant surgeons have full-time academic appointments (P<0.001), more nephrologists and transplant surgeons are involved in clinical and basic research (P=0.001), more nephrologists are principal investigators (P=0.011), availability of specialty consult physicians dedicated to transplant recipients (P=0.011), more often an intensivist was the primary MD in the ICU for transplant recipients (P<0.001), and the primary physician contact after hours was not the attending surgeon or nephrologist (P=0.043) (Table S1, SDC,https://links.lww.com/TP/A963).
The following factors were more likely to be associated with increased volume of transplants performed: program transplants other solid organs in addition to kidneys (P=0.008), patients enrolled in a formal research protocol (P=0.006), use of electronic medical records (P=0.008), availability of dedicated transplant pharmacist (P=0.024), and presence of a transplant nephrology fellowship (P<0.001) (Table S2, SDC,https://links.lww.com/TP/A963).
The following factors were more likely to be associated with multi-organ transplant centers compared to kidney-alone transplant centers: presence of an HLA or tissue typing laboratory (P=0.001), formal research protocols (P<0.001), full-time research coordinators (P=0.001), offer ABO-incompatible or cross-match positive transplants (P=0.019), offer laparoscopic living donor nephrectomies (P=0.002), be affiliated with a medical school (P=0.022), more nephrology (P<0.001) and surgery (P<0.001) involvement in clinical and basic research, more full-time equivalent (FTE) surgeons (P=0.001), and more surgeons as principal investigators in industry-sponsored basic science or clinical research (P<0.001) (Table S3, SDC,https://links.lww.com/TP/A963).
The following factors were different across Organ Procurement and Transplantation Network (OPTN) regions: affiliation with a medical school (P=0.003); participation in the paired kidney exchange (PKE) (P<0.001); formal protocol for posttransplant polyomavirus screening (P=0.005); use of corticosteroids (P=0.007) and sirolimus (P=0.017) as first-line, maintenance immunosuppression regimen for low-risk patients; and use of tacrolimus for high-risk patients (P=0.014) (Table S4, SDC,https://links.lww.com/TP/A963).
Centers with financial structure organized with all resources going through departmental structures, compared to resources going to a group (transplant) practice under the same budget, were more likely to have an onsite HLA or tissue typing laboratory (P<0.001), affiliation with a medical school (P<0.001), higher number of FTE nephrologists (P=0.002), more nephrologists with full-time academic appointments (P=0.001), and the primary physician contact after hours was not the attending surgeon or nephrologist (P=0.02) (Table S5, SDC,https://links.lww.com/TP/A963).
To our knowledge, this is the first study to collect nationally representative data on how transplant care is structured and delivered, and similar data is not available for other countries. The major finding of this survey was the significant variation between different transplant centers in the domains of structure and processes of care, frequency of follow-up visits, and coordination of care. Two thirds of kidney transplant centers do not use clinical pharmacists dedicated to the outpatient setting (Fig. 1). Only two thirds of kidney transplant centers have incorporated physician extenders in their treatment teams (Table 3). Two thirds of kidney transplant centers do not see their KTRs at least monthly during the first year posttransplant (Table 3).
Despite published literature including several randomized control trials (2–4) to support the use of clinical pharmacists in the care of KTRs to minimize side effects, decrease cost, and improve adherence to immunosuppressive medications, many centers have not incorporated this vital component to their treatment team. A recent prospective, observational study demonstrated significant decreases in errors upon discharge after transplantation when the medication regimen was reviewed by a transplant pharmacist (5). Our survey found that 35% of programs used pharmacists in both inpatient and outpatient areas, and 24% used them only for the inpatient setting. Approximately two thirds of programs do not use pharmacists in the outpatient setting, where the utility has been demonstrated and where the patients are at highest risk to demonstrate non-adherence.
Numerous studies have correlated non-adherence to prescribed treatment plans with early and late allograft rejection and graft loss (6–10). In attempts to prevent this rejection and graft loss, the KDIGO guidelines recommended providing all KTRs and family members with education about the importance of medical adherence, implement preventive measures to minimize non-adherence, and increase screening for non-adherence (11). Furthermore, KDIGO has recommended a “team approach” based on literature that has shown positive outcomes associated with the use of multidisciplinary teams that combine educational, behavioral, and social support systems (12, 13). Risk factors for non-adherence such as lack of adequate follow-up with transplant specialists, multiple adverse effects from medications, and complex drug regimens have been previously identified (14, 15).
It has also been shown by Weng et al. that non-adherence varies between transplant centers (16). The present study shows that there is an opportunity to increase the utilization of physician extenders to assist in improving outcomes. It is reasonable to speculate that physician extenders may fulfill the role of educating and monitoring patients in the setting where physicians may be overextended or unavailable.
In attempts to improve patient and medical provider satisfaction, outcomes, and overall care, a multidisciplinary approach has been tried in many areas of medicine including heart failure, chronic kidney disease, and others (17–22). These studies have shown positive outcomes in mortality, metabolic and blood pressure control, readmission rates, and medication optimization (18–20, 22). Such issues have not been adequately studied in kidney transplant patients. Our study is the first to describe the variable use of pharmacists, PAs, and CNPs as members of multidisciplinary teams in this setting. To the best of our knowledge, only one previous study in 2004 addressed use of multidisciplinary teams in kidney transplant centers and focused on the integration of clinical pharmacists (23). With data from 36 centers, this study found that 73% of kidney transplant centers had pharmacists. Of these centers, pharmacists reported dedicating 43% of their time to inpatient care and only 15% to outpatient care. This finding is consistent with our data that suggests underutilization of clinical pharmacists in the outpatient care of KTRs.
Considering the previous or underlying disease and comorbidities of the patient, the complexity and hazards of ongoing immunosuppression, the risk of acute rejection, and the need for optimized general health care, adequate follow-up of KTRs is essential. The 2000 AST recommendations for outpatient surveillance of KTRs recommend routine posttransplant visits two to three times per week during the first 30 days, every 1 to 3 weeks in months 1 to 3, expanded to every 4 to 8 weeks during months 4 to 12, and ultimately every 2 to 4 months thereafter. These visits may be for laboratory tests only or may include contact with transplant nurse coordinators or physicians, or both (24). The 2009 KDIGO guidelines do not make specific recommendations on the frequency and timing of outpatient visits (25). Previous work has demonstrated significant variation in the frequency of outpatient visits between patients, centers, and regions of the country (26). Lower kidney transplant survival is associated with a lower frequency of nephrology visits (27). The survey data shows that two thirds of kidney transplant centers do not see their KTRs at least monthly during the first year posttransplant.
It is reassuring that the working relationship between transplant surgery and nephrology teams is “very good” or “excellent” in total of 84% of centers (Table 4). At a time when the patient with a recently transplanted kidney is at high risk for both medical and surgical complications, they are unfortunately shifting from surgical to medical services. For example, transplant surgery is the admitting service for 67.9% of KTRs at the time of transplantation and for 45.5% of KTRs during the first 3 months posttransplant (Table 4). However, after 3 months posttransplant, the admitting service becomes most frequently transplant nephrology (57.7%) (Table 4). A similar shift from transplant surgery to nephrology is also seen in the outpatient setting. This poses a unique challenge for patient care, and it is clear that collaboration and communication is vital. An area to increase communication could be greater utilization of joint sit-down or walking rounds between the services. However, we found that only 29.5% of centers regularly conducted sit-down rounds and 25.0% of centers regularly did joint walking rounds (Fig. 1 and Table 4). The survey did not measure the proximity of surgery and nephrology offices and clinics. It is possible that close physical proximity may reduce the need for formal interactions.
Subgroup analysis of the survey responses demonstrated several predictable trends. Programs affiliated with a medical school were more often involved in research, had more academic affiliations, and transplanted a greater variety of organs. Overall, minimal variation in delivery of care was observed across OPTN regions. Centers that distribute resources through department structures had more academic nephrologists. Not surprisingly, multi-organ transplant centers demonstrated more involvement in research. As predicted, high volume centers more often also transplanted organs other than kidneys, had available transplant pharmacists, and supported a transplant nephrology fellowship.
Our study has several limitations. At this time, it is not known if the centers that utilized pharmacists and mid-level providers such as physician extenders had better posttransplant outcomes or whether satisfactory professional relationships between nephrologist and surgeons actually were associated with better posttransplant outcomes. Our data does, however, show that the previously described differences in both treatment adherence and long-term outcomes (16) may in part be related to significant differences in the structure and coordination of care. Randomized control trials would be necessary to determine if a specific intervention, such as joint rounding between surgeons and nephrologists or increased utilization of mid-level providers, does indeed improve outcomes for KTRs. However, it is likely that the volume of transplants and number of patients per nephrologist and surgeon may make some of the interventions logistically difficult or unnecessary to use. With regards to the frequency of outpatient visits, our survey only covered visits to the transplant center and did not quantify frequency of visits to the referring nephrologist or primary care physicians. However, as previous work has shown, follow-up of recently transplanted patients by primary care physicians was quite infrequent (26), thus we can assume these primary care visits represent a minority of total outpatient visits. An additional limitation is that not all centers who responded provided completed surveys from both the medical and surgical directors. Because not all transplant physicians and surgeons were surveyed at each center, the responses reflect the opinions of only the transplant clinicians who actually filled out the survey. The nature of a particular transplant program, academic versus private, and overall budget may affect the ability of that center to support ancillary staff, including transplant-specific pharmacists. This survey did not collect data on the annual budgets of the respective programs.
In conclusion, this study determined that significant variation occurs in the structure of care, frequency of follow-up, and coordination of care between kidney transplant centers. These variations may partially explain the disparate long-term allograft outcomes that have been observed among transplant centers and between some types of KTRs (28–30). Additional research, in the form of prospective observational cohort studies and randomized control trials of interventions to increase the integration of mid-level providers or improve coordination of care between nephrologists and surgeons, are needed to determine if changes in these areas will lead to improvements in long-term allograft and patient outcomes.
MATERIALS AND METHODS
Study Design and Population
This observational cross-sectional study sought to acquire information from all active, adult, OPTN-affiliated kidney transplant programs in the United States. In total, 208 kidney transplant centers fulfilled the criteria for study inclusion at the time of first mailing (March 1, 2007). A partial contact list of medical and surgical directors of U.S. kidney transplant programs was acquired from the United Network of Organ Sharing. This list was updated using information from the internet and directly contacting eligible kidney transplant programs by telephone.
Survey Development and Content
The survey was developed by S.J.K. and N.R.P., in consultation with a transplant physician (H.R.) and transplant surgeon (L.E.R.) at the Johns Hopkins Hospital and Columbia University Medical Center, respectively. A number of the questionnaire items were adapted from a survey instrument that was developed by Loberiza et al. (31). Our questionnaire had four sections (see Appendix for the full questionnaire).
A letter describing the study was sent 1 week in advance of the first survey mailing to the medical and surgical directors of all eligible U.S. adult kidney transplant programs. Respondents were given the option of completing the self-administered questionnaire through paper or online formats. The total time from the first survey mailing to the end of the study period, which included several reminders and subsequent re-sending of surveys, was 24 weeks.
Frequency of responses was analyzed by t test for continuous variables and by chi-square test (and Fisher exact test if there are cells with less than five responses) for categorical variables. All analyses were conducted in SAS 9.4 (SAS Institute, Cary, NC) and STATA 12 (Statacorp, College Station, TX). Responses from medical directors were used first and supplemented with surgical director responses if the medical director had not responded.
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