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Raffetin et al. BMC Infectious Diseases (2023) 23:380 https://doi.org/10.1186/s12879-023-08352-3

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BMC Infectious Diseases

Acceptance of diagnosis and management satisfaction of patients with “suspected Lyme borreliosis” after 12 months in a multidisciplinary reference center: a prospective cohort study Alice Raffetin1,2,3*, Amal Chahour1, Julien Schemoul4, Giulia Paoletti5, Zhuoruo He1,6, Elisabeth Baux7, Solène Patrat‑Delon8, Steve Nguala1, Pauline Caraux‑Paz1, Costanza Puppo9, Pauline Arias1, Yoann Madec10, Sébastien Gallien1,3,11 and Julie Rivière2

Abstract

Introduction Because patients with a “suspicion of Lyme borreliosis (LB)” may experience medical wandering and difficult care paths, often due to misinformation, multidisciplinary care centers were started all over Europe a few years ago. The aim of our study was to prospectively identify the factors associated with the acceptance of diagnosis and management satisfaction of patients, and to assess the concordance of the medical health assessment between physicians and patients 12 months after their management at our multidisciplinary center.

Methods We included all adults who were admitted to the Tick‑Borne Diseases Reference Center of Paris and the Northern Region (TBD‑RC) (2017–2020). A telephone satisfaction survey was conducted 12 months after their first consultation. It consisted of 5 domains and 13 items rated between 0 (lowest) and 10 (highest grade): (1)Reception; (2)Care and quality of management; (3)Information/explanations given to the patients; (4)Current medical condition and acceptance of the final diagnosis; (5)Overall appreciation. Factors associated with diagnosis acceptance and man‑ agement satisfaction at 12 months were identified using logistic regression models. The concordance of the health status as assessed by doctors and patients was calculated using a Cohen’s kappa test.

Results Of the 569 patients who consulted, 349 (61.3%) answered the questionnaire. Overall appreciation had a median rating of 9 [8;10] and 280/349 (80.2%) accepted their diagnoses. Patients who were “very satisfied” with their care paths at TBD‑RC (OR = 4.64;CI95%[1.52–14.16]) had higher odds of diagnosis acceptance. Well‑delivered informa‑ tion was strongly associated with better satisfaction with the management (OR = 23.39;CI95%[3.52–155.54]). The con‑ cordance between patients and physicians to assess their health status 12 months after their management at TBD‑RC was almost perfect in the groups of those with confirmed and possible LB (κ = 0.99), and moderate in the group with other diagnoses (κ = 0.43).

*Correspondence: Alice Raffetin [email protected] Full list of author information is available at the end of the article

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Conclusion Patients seemed to approve of this multidisciplinary care organization for suspected LB. It helped them to accept their final diagnoses and enabled a high level of satisfaction with the information given by the doctors, confirming the importance of shared medical decisions, which may help to reduce health misinformation. This type of structure may be useful for any disease with a complex and controversial diagnosis.

Key messages

What is already known on this topic?

• Among patients with a suspicion of Lyme borreliosis (LB), less than 15% have confirmed LB, and more than 80% a differential diagnosis, confirming the need for multidisciplinary structures.

• To our knowledge, there are not any studies about the satisfaction of the patients with these proposed multidis- ciplinary care paths.

What this study adds?

• Acceptance of diagnosis (80.2%) was associated with satisfaction with the care paths and the current medical condition of the patients.

• The high satisfaction with the information given by the doctors was a key element of the management satisfac- tion, confirming the importance of shared medical decisions to meet the patients’ expectancies and reduce mis- information.

How this study might affect research, practice and policy?

• Provided that this satisfaction survey is externally assessed by additional studies, it could be useful to regularly assess patients’ satisfaction in the context of multidisciplinary management for suspected LB, and these multi- disciplinary structures might be generalized for other complex diseases.

Keywords Lyme borreliosis, Multidisciplinary management, Satisfaction, Concordance, Diagnostic acceptance

Introduction Lyme borreliosis (LB) is the most common tick-borne disease in Europe and in the USA. It is caused by spiro- chetes of the Borrelia burgdorferi sensu lato complex [1, 2]. Diagnosis of LB associates an exposure to tick bite, the presence of specific defined-LB manifestations (the most frequent being erythema migrans (EM) and Lyme neu- roborreliosis) and a positive microbiological test (sero- logical and sometimes PCR tests, save for EM); none of them alone makes the diagnosis of the infection certain [3–5]. European guidelines recommend a mono-anti- biotic therapy for LB treatment. The therapy should be given for 14 to 28 days according to the infection’s stage and its clinical manifestation [6, 7]. No studies have yet proven the clinical benefit of a longer antibiotic treat- ment [8–12].

The diagnosis and the management of LB may be chal- lenging for several reasons: (i) its wide range of clinical pictures, sometimes resembling other pathologies; (ii) the rare sequelae that may occur mainly after late dissem- inated LB, with most of patients being completely cured

within one month to three years in the most complicated cases [13–19]; and (iii) the possible presence of subjective symptoms (asthenia, polyalgia, cognitive complaints) at all stages of the disease [14, 20], which may persist after a well-adapted treatment, producing the post-treatment Lyme disease syndrome (PTLDS) [13, 14, 20, 21], with no clear guidelines for their management. The causative role of LB in these subjective symptoms is a source of ques- tions insofar as these non-specific symptoms may be encountered in the course of other infectious (Epstein- Barr-Virus, SARS-CoV-2, etc.) or non-infectious diseases [22]). In addition, some patients are referred for antibi- otic therapy for a suspicion of LB, sometimes at their own request, but are finally diagnosed with other diseases, mainly rheumatological, neurological, auto-immune or psychological [23–27].

Therefore, many patients suspected of having LB may experience diagnosis wandering and difficult care paths, often due to misinformation. To improve the health care organization of LB, a French national care plan for LB was started in 2016 that favored the creation of

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multidisciplinary LB centers. These centers are joint endeavors between departments of infectious diseases, internal medicine, rheumatology, neurology, algology, dermatology, psychiatry, microbiology, and physical rehabilitation to manage patients presenting a suspicion of LB, in a multidisciplinary approach. There, challenging cases are discussed in monthly multidisciplinary consul- tation meetings. One such clinic opened in December 2017 at the General Hospital of Villeneuve-Saint-Georges in suburban Paris, France. This center was labeled the Tick-borne Diseases Reference Center (TBD-RC) for Paris and the Northern region in July 2019 by the French Ministry of Health, which also established four other such clinics in France. Teams in other countries have also initiated such care organizations since 2010 [23–25], showing a European awareness of the need for the man- agement of complex LB and its differential diagnoses. These multidisciplinary experiences have revealed a low prevalence of confirmed LB (between 10 and 20%), and the multiplicity of the differential diagnoses [23–27]. We have previously demonstrated that the majority of patients (80.7%), independently of their final diagno- ses, had favorable clinical outcomes one year after their first consultation at TBD-RC of Paris and the Northern region. However, the opinions of the patients about these multidisciplinary structures, their diagnosis acceptance, especially in spite of another diagnosis than LB, and their own health status assessment after receiving care in this type of multidisciplinary structure have not been studied yet [27].

The aims of our study were to analyze the satisfaction levels of patients experiencing a multidisciplinary man- agement for suspected LB at TBD-RC of Paris and the Northern region, to identify the factors associated with their diagnosis acceptance and their global satisfaction with the management, and to assess the concordance of the medical health assessment between the physicians and the patients 12 months after their first consultation at TBD-RC.

Methods We conducted a prospective descriptive and analytic cohort study, including all adults who consulted at TBD- RC of Paris and Northern Region for a suspicion of LB, from 1 December 2017 to 1 December 2020. We followed the STROBE guidelines [28] (Additional file 1).

Population, setting, and intervention The care path at TBD-RC was previously described [27] and is summarized in Fig. 1.

Patients with diagnoses associated with LB were clas- sified as [13, 29]: confirmed LB (tick exposure, typical clinical signs and a positive serological test); possible LB

(tick exposure and/or prior erythema migrans, evoca- tive clinical signs and marked clinical improvement after 21 days of antibiotics); and post-treatment Lyme disease syndrome (PTLDS) (asthenia/polyalgia/cognitive com- plaints) or sequelae (objective impairment) after a con- firmed LB treated as recommended. PTLDS and sequelae were pooled together as they are both responsible for persistent symptoms after treatment. Therefore, com- bining them together was clinically relevant. Moreover, as sequelae are very rare, the effective would have been too small to perform statistical tests separately. The other patients were classified in the group “other diagnoses,” which were made by a doctor specialized in the field. A final orientation in the adapted medical department was offered to every patient, independently of their final diagnosis.

A telephone-based satisfaction survey was conducted, independently from the staff consulting at TBD-RC, and pseudonymized, 12 months after the first consultation at TBD-RC.

To assess the current health condition of the patients 12 months after their management at TBD-RC, the phy- sician in charge of the patient had a rating scale between 1 and 5. In the satisfaction survey, patients had a scale between 0 and 10. The current medical condition cor- responded to: complete recovery (score 1 for physicians; score 9–10 in the satisfaction survey for patients), partial improvement consisting of persistent clinical signs or symptoms allowing resumption of daily and professional activities (score 2 for physicians; score 7–8 for patients), stagnation (score 3 for physicians; score 5–6 for patients), or deterioration (score 4 for physicians; score 0–4 for patients).

Patient data and satisfaction survey Patients’ data were routinely collected in standardized medical files at the TBD-RC, independently of the study, to ensure the correct follow-up of the patients.

The satisfaction survey comprised 15 items: 12 items rated between 0 (lowest grade) and 10 (highest grade), 1 item about the acceptance with 3 categories (yes, no, and partially), and 2 free-text items. These items covered five domains: (1) reception; (2) care and quality of manage- ment (by the medical team, by the paramedical team, responsiveness and compassion to patients, care path at TBD-RC); (3) information and explanations given to the patients; (4) current medical condition after the manage- ment at the TBD-RC compared to the previous one and acceptance of the final diagnosis; and (5) overall appreci- ation (Additional file 2). This questionnaire was inspired by the MedRisk instrument, and adapted to our setting (multidisciplinary management for the suspicion of LB) [30, 31]. It was presented and discussed with patients’

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associations involved in LB on the one hand, and in other diseases such as HIV or diabetes on the other hand, to check whether this survey was adequate to their expec- tations. Their suggestions were taken into account to improve the questionnaire.

Statistical analysis The four groups of patients classified according to their final diagnosis as assessed at the TBD-RC of Paris and the Northern region (i.e. confirmed LB, possible LB, PTLDS or sequelae, and other diagnosis) were previously compared according to socio-demographic, clinical, and microbiological characteristics, and 12-month outcomes after multidisciplinary care [27]. In the present study, we compared the satisfaction levels in the four groups of patients at 12 months after the first consultation at TBD- RC. Moreover, we focused on the group “other diagno- ses” to analyze more precisely the results in patients with a bodily distress syndrome and in patients without a spe- cific diagnosis, as the diagnostic wandering could remain.

Categorical variables are reported here as proportions and percentages, and continuous variables as medians with interquartile ranges (IQR). Categorical variables were compared by chi-squared or Fischer’s exact test,

as appropriate. Continuous variables were compared between groups by ANOVA or Kruskal–Wallis test, as appropriate.

Factors associated with the acceptance of the final diag- nosis (yes vs partially or no) and those with satisfaction with the management (yes for a score ≥ 7 and no for a score < 7) were identified using logistic regression mod- els. In both analyses, factors associated with the outcome with a p-value < 0.25 in univariate analysis were consid- ered in the multivariate model. For the acceptance of the diagnosis, we chose “care and quality of management by the medical team” to avoid collinearity with the other variables and thus make them irrelevant to the multivari- ate model. For the satisfaction with the management, we focused on the medical management only, which seemed more relevant, especially as we then studied the concord- ance of the health status assessed by doctors and patients. A stepwise backward procedure was then applied to iden- tify factors that remained independently associated with the outcome. Gender and age were forced in the models.

The concordance was calculated using a simple Cohen’s kappa test (deterioration/stagnation versus partial improvement/recovery). A sensitivity analysis was per- formed with a weighted Cohen’s kappa (deterioration,

Fig. 1 Care path of the patients consulting for a suspicion of LB at TBD‑RC. TBD‑RC = Tick‑Borne Disease Reference Center; LB = Lyme borreliosis; PTLDS = Post‑Treatment Lyme Disease Syndrome

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stagnation, partial improvement, and recovery). The strength of agreement was defined as “slight” for a Cohen’s kappa between 0 and 0.20, “fair” for one between 0.21 and 0.40, “moderate” for one between 0.41 and 0.60, “substantial” for one between 0.61 and 0.80, and “almost perfect” for one between 0.81 and 1.00.

A p-value < 0.05 was defined for statistical significance. All analyses were performed using Stata version 16 (Col- lege Station, Texas, USA).

The analyses of the two free-text items will be per- formed in another study using qualitative methods.

Approval of the ethics committee The local ethics committee of the University Hospital of Créteil, France, approved this research (N°2021–02-03). All the included patients (or their legal guardian(s)) gave an informed consent to the use of their medical data for research purposes, prior to their management at TBD- RC of Paris and the Northern region and to the satis- faction questionnaire. The research sponsor signed a commitment to comply with the “Reference Methodol- ogy MR004” of the French Data Protection Authority (CNIL, 2,216,096 v 0, December 10, 2019).

Funding None.

Results Of 569 patients admitted to the TBD-RC of Paris and the Northern region between December 2017 and December 2020, 349 (61.3%) answered the satisfaction question- naire (Fig. 2).

Characteristics of the patients No statistical difference was found between the charac- teristics of patients who answered and those who did not answer the satisfaction questionnaire (Additional file 3). Characteristics of those who answered the satisfaction questionnaire are presented in the Table  1. The median age was 48 years old, and 71.4% of the patients were prac- ticing forest-based leisure activities. There were statisti- cally more patients with a history of tick-bite (p = 0.001) or EM (p < 0.001) in the three groups with a diagnosis associated with LB. The duration of the symptoms before

the initial consultation at TBD-RC was statistically longer in patients with another diagnosis (p < 0.001). Of note, 10.3% of the patients self-referred to the center with a complete medical file but with no letter from a physi- cian. They were admitted as they were in medical wan- dering. Most of the patients (66.5%) had symptoms for more than six months, except in the group of confirmed LB patients, who had a significantly shorter duration of symptoms (p < 0.001). Only 31.8% of the patients had a positive serology in ELISA and Western-Blot, regardless of the final diagnosis. Most of the patients (65.3%) had received at least one antibiotic therapy before the first consultation at TBD-RC and 17.5% had received a non- recommended one (exceeding eight weeks or associating different molecules).

Descriptive analyses of the satisfaction survey The answer rate was not different between the four groups of patients (p = 0.44). The overall median (IQR) appreciation score was 9 [8;10] (Table  2). Overall, 276 (79.1%) patients were satisfied with their final diagnosis (score ≥ 7), 280 (80.2%) accepted their final diagnoses, 296 (84.8%) were satisfied with the management and 310 (88.8%) recommended the TBD-RC (Fig. 3). Scores were significantly higher among patients with a confirmed LB than among patients with other diagnoses, except when it came to the assessment of their health condition. Those scores did not differ from those of the other groups of patients (p = 0.18).

The scores evaluating reception, the care, and the qual- ity of the management provided by the paramedical team one the one hand and by the medical team on the other hand, the responsiveness and the compassion to the patients, the care path at TBD-RC, and the informa- tion given by the doctor were significantly higher among patients with a confirmed LB than among patients with other diagnoses (p = 0.008, p = 0.009, p = 0.001, p = 0.004, p = 0.005, p < 0.001, respectively).

Patients with a confirmed LB had significantly better evaluations of their care paths at TBD-RC than patients with PTLDS/sequelae (p = 0.010). Patients with con- firmed LB accepted their diagnosis significantly bet- ter than patients with a possible LB (p = 0.006), PTLDS/ sequelae (p = 0.001), or other diagnoses (p = 0.006).

Fig. 2 Flow chart of the patients who were solicited to answer the satisfaction questionnaire at 12 months

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Satisfaction with the final diagnosis and with the global management were significantly better in patients with confirmed LB compared to other diagnoses (both p = 0.004). Patients with confirmed LB recommended the TBD-RC significantly more than patients with other diagnoses (p = 0.009).

Moreover, patients oriented in the care paths of infectious diseases, rheumatology, neurology, internal medicine, or general practice had a significant better acceptance of the diagnosis than patients oriented in psy- chology or psychiatry (p < 0.001), and had a higher level

of satisfaction with the management at TBD-RC than patients oriented in psychology or psychiatry (p = 0.009).

Among the “other diagnoses” group, we focused on patients with a bodily distress syndrome who answered the satisfaction questionnaire (n = 30): 17 (56.7%) accepted their diagnosis, 6 (20.0%) partially accepted their diagnosis, and 7 (23.3%) refused the diagnosis; 15 (50.0%) were very satisfied with the management, 4 (13.3%) were satisfied, 9 (30.0%) were moderately satis- fied and 2 (6.7%) were not satisfied; 18 (60.0%) strongly recommended the TBD-RC, 6 (20.0%) recommended

Table 1 Comparison of the characteristics of the four groups of patients who answered the satisfaction questionnaire

LB Lyme borreliosis, PTLDS Post-Treatment Lyme Disease Syndrome, IQR Inter quartile range, ELISA Enzyme-Linked Immunosorbent Assay, WB Western-Blot, TBD-RC Tick-Borne Diseases Reference Center

Characteristics of the patients Total N = 349 (%)

Confirmed LB N = 48 (%)

Possible LB N = 31 (%)

PTLDS or sequelae N = 34 (%)

Other diagnoses N = 236 (%)

P value

Age, (years), median [IQR] 48 [35,62] 48 [35,62] 49 [35,62] 48 [35,62] 48 [35,61] 0.242

Male 146 (41.8) 30 (62.5) 16 (51.6) 9 (26.5) 91 (38.6) 0.003

Lifestyle 0.287

Home in a rural area 72 (20.6) 6 (12.5) 10 (32.3) 7 (20.6) 49 (20.8) ‑

Employment in rural areas/forest 17 (4.9) 2 (4.2) 1 (3.2) 0 (0.0) 14 (5.9) ‑

Forest‑based leisure activities 249 (71.4) 40 (83.3) 20 (64.5) 26 (76.5) 163 (69.1) ‑

No exposure 11 (3.2) 0 (0.0) 0 (0.0) 1 (2.9) 10 (4.2) ‑

Past history of tick-bite 234 (67.1) 40 (83.3) 25 (80.7) 28 (82.4) 141 (59.8) 0.001

Past history of erythema migrans 97 (27.9) 29 (60.4) 11 (35.5) 16 (48.5) 41 (17.4) < 0.001

Patients referred by a physician with a letter

313 (89.7) 46 (95.8) 30 (96.8) 30 (88.2) 207 (87.7) 0.108

General Practitioner 241 (69.1) 31 (64.6) 26 (83.9) 26 (76.5) 158 (67.0)

Specialist physician 59 (16.9) 11 (22.9) 2 (6.5) 4 (11.8) 42 (17.8)

Emergency unit physician 13 (3.7) 4 (8.3) 2 (6.5) 0 (0.0) 7 (3.0)

No letter, patient self‑referral 36 (10.3) 2 (4.2) 1 (3.2) 4 (11.8) 29 (12.3)

Duration (days) of chief complaints prior to consultation at TBD-RC, median [IQ 25,75]

425.5 [140.5, 1208.5]

406.5 [135, 1171]

422 [139, 1191]

425.5 [144, 1208.5]

532.5 [167.5, 1456.5]

< 0.001

Patient’s chief complaint < 0.001

Erythema migrans 10 (2.9) 6 (12.5) 0 (0.0) 1 (2.9) 3 (1.3)

Clinical signs/symptoms evoking early dissemi‑ nated LB (< 6 months)

100 (28.7) 27 (56.3) 12 (38.7) 10 (29.4) 51 (21.6)

Clinical signs/symptoms evoking late dissemi‑ nated LB (> 6 months)

232 (66.5) 15 (31.3) 19 (61.3) 23 (67.7) 175 (74.2)

Questions after a tick‑bite 4 (1.2) 0 (0.0) 0 (0.0) 0 (0.0) 4 (1.7)

Positive serological test with no clinical signs 3 (0.9) 0 (0.0) 0 (0.0) 0 (0.0) 3 (1.3)

Serological test < 0.001

IgM and/or IgG positive in ELISA and WB 111 (31.8) 33 (68.8) 12 (38.7) 19 (55.9) 47 (19.9)

IgG positive in ELISA only 46 (13.2) 5 (10.4) 8 (25.8) 5 (14.7) 28 (11.9)

IgM and IgG negative in ELISA 163 (46.7) 7 (14.6) 11 (35.5) 10 (29.4) 135 (57.2)

No serology (suspicion of erythema migrans) 26 (7.5) 3 (6.3) 0 (0.0) 0 (0.0) 23 (9.8)

Antibiotic therapy prescribed before TBD-RC 228 (65.3) 36 (75.0) 16 (51.6) 34 (100.0) 142 (60.2) < 0.001

Antibiotic therapy > 4 weeks 71 (20.3) 12 (25.0) 2 (6.5) 14 (41.2) 43 (18.2) 0.003

Non‑recommended treatments (> 8 weeks of antibiotics and/or associated antimicrobials)

61 (17.5) 6 (12.5) 0 (0.0) 10 (29.4) 45 (19.1) 0.011

Page 7 of 13Raffetin et al. BMC Infectious Diseases (2023) 23:380

TBD-RC, 4 (13.3%) had no opinion, and 2 (6.7%) did not recommend TBD-RC.

Finally, we also focused on patients with no specific diagnosis at the end of the investigations at the TBD-RC (n = 17): 16 (94.1%) accepted their diagnosis and 1 (5.9%) did not; 15 (88.2%) were very satisfied with the manage- ment at TBD-RC, 1 (5.9%) was satisfied and 1 (5.9%) was moderately satisfied; 15 (88.2%) strongly recommended the TBD-RC, 1 (5.9%) recommended TBD-RC and 1 (5.9%) did not.

Factors associated with the diagnostic acceptance and the management satisfaction at 12 months In the multivariate analysis (Additional file  4), patients “very satisfied” with their care paths at TBD-RC had higher odds (OR = 4.64, 95% confidence interval (CI) [1.52–14.16]) of diagnosis acceptance compared to patients only “satisfied.” Patients with a possible LB had lower odds of diagnosis acceptance compared to patients with other diagnoses (OR = 0.23, 95%CI [0.07–0.77]). Patients “moderately satisfied” with the care and the management of the doctors at TBD-RC had lower odds of diagnosis acceptance compared to satisfied patients

(OR = 0.05, 95%CI [0.01–0.32]). Patients assessing their current medical state compared to the previous one as “stagnation” had lower odds of diagnosis acceptance compared to patients describing a “partial improvement” (OR = 0.16, 95%CI [0.06–0.42]).

In the multivariate analysis about management sat- isfaction (Additional file  5), patients over 48  years had marginally significant higher odds of satisfaction with management (OR = 31.98, 95%CI [1.79–571.74], p = 0.051) than patients under 35. Patients “very satisfied” with the information given by the doctors had higher odds of satisfaction with management than “satisfied” patients (OR = 23.39, 95%CI [3.52–155.54]). Patients who were moderately satisfied with their care and man- agement by the medical team had lower odds of satisfac- tion with management (OR = 0.01, 95%CI [0.00–0.10]) such as patients moderately satisfied with the care paths (OR = 0.01, 95%CI [0.00–0.08]), compared to satisfied patients. Gender, final diagnosis, responsiveness, and compassion to patients were not associated with sat- isfaction with management. Notably, in the univariate analysis, a first line of antibiotics prescribed at the TBD- RC was significantly associated with a better satisfaction

Table 2 Comparative results of the satisfaction questionnaire between the 4 groups of patients at 12 months

LB Lyme borreliosis, PTLDS Post-Treatment Lyme Disease Syndrome, TBD-RC Tick-Borne Diseases Reference Center

Domains and Items rated from 0 (worst) to 10 (best) Median, [25;75]

Total N = 349 (%)

Confirmed LB N = 48

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