Effect of Statin Use on the Clinical Manifestations, Laboratory Test Results and Outcome of Lyme Neuroborreliosis
Abstract
:1. Introduction
2. Patients and Methods
2.1. Patients
2.2. Methods
2.2.1. Laboratory Evaluation
2.2.2. Serological Evaluation
2.2.3. Cultivation and Typing of B. burgdorferi sensu lato
2.3. Treatment
2.4. Definition of Outcome
- Complete recovery: complete resolution of symptoms/signs of the disease.
- Pronounced improvement: symptoms/signs of the disease are present only occasionally and/or have low intensity, not demanding regular use of analgesics and not interfering with daily activities.
- Partial improvement: symptoms/signs, although improved, still require frequent use of analgesics and/or significantly reduce daily activities.
- Failure: persistence, intensification, or appearance of new symptoms/signs, and/or a positive post-treatment CSF, skin, or blood culture for borrelia.
- Unfavorable long-term clinical outcome was defined as partial improvement or failure at 6 or 12 months after enrollment; all other patients were classified as having a favorable outcome.
2.5. Retreatment
2.6. Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
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Characteristic | Number (%, 95% CI) or Median (IQR) | p | padj | |
---|---|---|---|---|
Receiving Statins | ||||
Yes (n = 18) | No (n = 105) | |||
Sex: Male | 11 (61.1, 38.6–79.7) | 56 (53.3, 43.8–62.6) | 0.722 | >0.999 |
Age (years) Males Females | 64.5 (53.2–70.0) 54.0 (49.0–69.0) 69.0 (67.0–70.0) | 57.0 (49.0–65.0) 53.0 (46.0–65.0) 60.0 (53.0–66.0) | 0.055 0.402 0.008 | 0.565 >0.999 0.212 |
Underlying illnesses | 18 (100, 82.4–100) | 53 (50.5, 41.1–59.9) | <0.001 | 0.053 |
EM β | 15 (83.3, 60.8–94.2) | 61 (58.1, 48.5–67.1) | 0.064 | 0.565 |
Fever (>38 °C) β | 2 (11.1, 3.1–32.8) | 19 (18.1, 11.9–26.5) | 0.736 | >0.999 |
Nausea β | 5 (27.8, 12.5–50.9) | 9 (8.6, 4.6–15.5) | 0.033 | 0.437 |
Vomiting β | 2 (11.1, 3.1–32.8) | 4 (3.8, 1.5–9.4) | 0.212 | >0.999 |
Vertigo β | 4 (22.2, 9.0–45.2) | 12 (11.4, 6.7–18.9) | 0.251 | >0.999 |
Paresthesia β | 7 (38.9, 20.3–61.4) | 30 (28.6, 20.8–37.8) | 0.546 | >0.999 |
Memory disturbances β | 1 (5.6, 1.0–25.8) | 13 (12.4, 7.4–20.0) | 0.691 | >0.999 |
Concentration disturbances β | 1 (5.6, 1.0–25.8) | 13 (12.4, 7.4–20.0) | 0.691 | >0.999 |
Sleep disturbances β | 15 (83.3, 60.8–94.2) | 83 (79.0, 70.3–85.7) | >0.999 | >0.999 |
Malaise β | 6 (33.3, 16.3–56.3) | 32 (30.5, 22.5–39.8) | >0.999 | >0.999 |
Fatigue β | 9 (50.0, 29.0–71.0) | 38 (36.2, 27.6–45.7) | 0.395 | >0.999 |
Radicular pain β | 18 (100, 82.4–100) | 105 (100, 96.5–100) | >0.999 | >0.999 |
Headache β | 6 (33.3, 16.3–56.3) | 43 (41.0, 32.0–50.5) | 0.727 | >0.999 |
Neck pain β | 4 (22.2, 9.0–45.2) | 22 (21.0, 14.3–29.7) | >0.999 | >0.999 |
Lower back pain β | 3 (16.7, 5.8–39.2) | 26 (24.8, 17.5–33.8) | 0.560 | >0.999 |
Myalgia β | 3 (16.7, 5.8–39.2) | 23 (21.9, 15.1–30.7) | 0.762 | >0.999 |
Arthralgia β | 2 (11.1, 3.1–32.8) | 19 (18.1, 11.9–26.5) | 0.736 | >0.999 |
Duration of neurological symptoms (days) β | 23 (13–46) | 30 (14–45) | 0.923 | >0.999 |
Concomitant TBE | 0 (0, 0–17.6) | 2 (1.9, 0.5–6.7) | >0.999 | >0.999 |
Findings at Presentation | ||||
EM | 9 (50.0, 29.0–71.0) | 32 (30.5, 22.5–39.8) | 0.176 | >0.999 |
Ring-like EM | 4/9 (44.4, 18.9–73.3) | 15/32 (46.9, 30.9–63.6) | >0.999 | >0.999 |
Largest diameter of EM (cm) | 33.5 (21.8–43.0) | 33.5 (20.0–45.8) | 0.886 | > 0.999 |
Lymphocytoma | 0 (0, 0–17.6) | 1 (1.0, 0.2–5.2) | >0.999 | >0.999 |
Fever (>38 °C) | 0 (0, 0–17.6) | 0 (0, 0–3.5) | >0.999 | >0.999 |
Meningeal signs | 5 (27.8, 12.5–50.9) | 21 (20.0, 13.5–28.6) | 0.532 | >0.999 |
Peripheral facial palsy | 9 (50.0, 29.0–71.0) | 37 (35.2, 26.8–44.7) | 0.351 | > 0.999 |
Bilateral facial palsy | 3/9 (33.3, 12.1–64.6) | 3/37 (8.1, 2.8–21.3) | 0.079 | 0.598 |
Other cranial nerve palsy | 0 (0, 0–17.6) | 1 (1.0, 0.2–5.2) | > 0.999 | >0.999 |
Paresis | 3 (16.7, 5.8–39.2) | 10 (9.5, 5.3–16.6) | 0.404 | >0.999 |
Tremor | 0 (0, 0–17.6) | 3 (2.9, 1.0–8.1) | >0.999 | >0.999 |
CSF Laboratory Findings | ||||
Leukocyte count (×106 cells/L) α | 88.0 (30.0–373.0) | 138.0 (64.0–293.0) | 0.367 | >0.999 |
Protein concentration (g/L) Elevated (>0.45 g/L) | 1.07 (0.54–1.92) 14 (77.8, 54.8–91.0) | 1.12 (0.62–1.90) 92 (87.6, 80.0–92.6) | 0.797 0.274 | >0.999 >0.999 |
Glucose concentration (mmol/L) CSFglu/Sglu <0.33 | 3.3 (2.9–3.5) 1/17 (5.9, 1.0–27.0) | 2.9 (2.5–3.2) 5 (4.8, 2.1–10.7) | 0.026 0.999 | 0.437 >0.999 |
Albumin quotient * | 0.017 (0.008–0.025) | 0.015 (0.009–0.025) | 0.660 | >0.999 |
IgG quotient * | 0.011 (0.004–0.016) | 0.010 (0.005–0.025) | 0.311 | >0.999 |
Borrelial Serology (Liaison® or IFA) γ | ||||
Positive serum IgM | 9 (50.0, 29.0–71.0) | 48 (45.7, 36.5–55.2) | >0.999 | >0.999 |
Positive serum IgG | 16 (88.9, 67.2–96.9) | 90 (85.7, 77.8–91.1) | >0.999 | >0.999 |
Positive CSF IgM | 10 (55.6, 33.7–75.4) | 63 (60.0, 50.4–68.9) | >0.999 | >0.999 |
Positive CSF IgG | 13 (72.2, 49.1–87.5) | 86 (81.9, 73.5–88.1) | 0.448 | >0.999 |
IT synthesis of borreliaIg M antibodies present | 10 (55.6, 33.7–75.4) | 60 (57.1, 47.6–66.2) | >0.999 | >0.999 |
IT synthesis of borrelia IgG antibodies present | 12 (66.7, 43.7–83.7) | 85 (81.0, 72.4–87.3) | 0.565 | >0.999 |
IT synthesis of borrelia IgM or IgG antibodies present | 13 (72.2, 49.1–87.5) | 87 (82.9, 74.5–88.9) | 0.351 | >0.999 |
IgG AI value # | 8.1 (3.5–42.5) | 19.6 (6.0–41.3) | 0.228 | >0.999 |
Borrelia Culture Results | ||||
Positive CSF culture | 1 € (5.6, 1.0–25.8) | 14 δ (13.3, 8.1–21.1) | 0.695 | >0.999 |
Positive blood culture | 0/16 (0, 0–19.4) | 2 §/98 (2.0, 0.6–7.1) | >0.999 | >0.999 |
Positive skin culture | 4 &,$/12 (33.3, 13.8–60.9) | 17 ¥,$/40 (42.5, 28.5–57.8) | 0.741 | >0.999 |
Characteristic | Number (%, 95% CI) or Median (IQR) | p | padj | |
---|---|---|---|---|
Receiving Statins | ||||
Yes (n = 18) | No (n = 105) | |||
SS score ¥ = 0 (3 mo) | 11 (61.1, 38.6–79.7) | 56/103 (54.4, 44.8–63.7) | 0.784 | 0.968 |
SS score ¥ = 0 (6 mo) | 12 (66.7, 43.7–83.7) | 52/101 (51.5, 41.9–61.0) | 0.350 | 0.744 |
SS score ¥ = 0 (12 mo) | 13 (72.2, 49.1–87.5) | 66/100 (66.0, 56.3–74.5) | 0.807 | 0.968 |
Cranial nerve palsy (3 mo) | 4/9 (44.4, 18.9–73.3) | 9/35 (25.7, 14.2–42.1) | 0.414 | 0.744 |
Cranial nerve palsy (6 mo) | 3/9 (33.3, 12.1–64.6) | 4/34 (11.8, 4.7–26.6) | 0.147 | 0.529 |
Cranial nerve palsy (12 mo) | 3/9 (33.3, 12.1–64.6) | 2/33 (6.1, 1.7–19.6) | 0.057 | 0.516 |
Paresis (3 mo) | 2/3 (66.7, 20.8–93.9) | 3/10 (30.0, 10.8–60.3) | 0.510 | 0.744 |
Paresis (6 mo) | 1/3 (33.3, 6.1–79.2) | 3/9 (33.3, 12.1–64.6) | 0.999 | 0.999 |
Paresis (12 mo) | 0/3 (0.0, 0.00–56.1) | 3/9 (33.3, 12.1–64.6) | 0.509 | 0.744 |
CSF Leukocyte count * (3 mo) | 4 (3–8) | 6 (2–10) | 0.537 | 0.744 |
CSF Leukocyte count >10 * (3 mo) | 3/16 (18.8, 6.6–43.0) | 21/94 (22.3, 15.1–31.8) | 0.999 | 0.999 |
CSF protein concentration $ (3 mo) | 0.49 (0.40–0.58) | 0.50 (0.39–0.58) | 0.868 | 0.977 |
Borrelia IgG AI value # (3 mo) | 11.4 (3.7–25.3) | 19.7 (11.5–28.9) | 0.140 | 0.529 |
Partial improvement or failure (14 days) | 10 (55.6, 33.7–75.4) | 32/104 (30.8, 22.7–40.2) | 0.076 | 0.516 |
Partial improvement or failure (3 mo) | 4 (22.2, 9.0–45.2) | 15/103 (14.6, 9.0–22.6) | 0.481 | 0.744 |
Partial improvement or failure (6 mo) | 3 (16.7, 5.8–39.2) | 11/101 (10.9, 6.2–18.5) | 0.443 | 0.744 |
Partial improvement or failure (12 mo) | 4 (22.2, 9.0–45.2) | 8/100 (8.0, 4.1–15.0) | 0.086 | 0.516 |
Antibiotic retreatment (3 or 6 mo) | 2 (11.1, 3.1–32.8) | 25/103 (24.3, 17.0–33.4) | 0.357 | 0.744 |
Factors (Covariates) | Est | SE | Stat | p | padj | CIL | CIH | Model |
---|---|---|---|---|---|---|---|---|
Univariate Regression Model | ||||||||
Cranial nerve involvement | 1.84 | 0.51 | 1.18 | 0.236 | 0.646 | 0.66 | 5.10 | logistic |
Paresis | 1.90 | 0.71 | 0.90 | 0.369 | 0.646 | 0.39 | 7.09 | logistic |
Positive CSF borrelial culture | 0.38 | 1.07 | −0.90 | 0.368 | 0.646 | 0.02 | 2.10 | logistic |
Duration of neurological symptoms/signs | −0.10 | 0.25 | −0.42 | 0.678 | 0.791 | −0.60 | 0.39 | linear |
CSF leukocyte count | −0.22 | 0.32 | −0.68 | 0.497 | 0.696 | −0.86 | 0.42 | linear |
CSF protein conc | 0.00 | 0.18 | 0.00 | 0.999 | 0.999 | −0.37 | 0.37 | linear |
Borrelia IgG AI value # | −0.47 | 0.43 | −1.11 | 0.271 | 0.646 | −1.33 | 0.38 | linear |
Multivariate Regression Model | ||||||||
Cranial nerve involvement | 4.06 | 0.70 | 2.01 | 0.044 | 0.154 | 1.05 | 16.61 | logistic |
Paresis | 1.21 | 0.98 | 0.19 | 0.847 | 0.847 | 0.14 | 7.77 | logistic |
Positive CSF borrelial culture | 0.33 | 1.16 | −0.95 | 0.344 | 0.602 | 0.02 | 2.40 | logistic |
Duration of neurological symptoms/signs | 0.12 | 0.26 | 0.47 | 0.640 | 0.847 | −0.39 | 0.63 | linear |
CSF leukocyte count | 0.08 | 0.26 | 0.31 | 0.754 | 0.847 | −0.44 | 0.60 | linear |
CSF protein conc | 0.14 | 0.06 | 2.43 | 0.017 | 0.119 | 0.03 | 0.25 | linear |
Borrelia IgG AI value # | −0.54 | 0.51 | −1.05 | 0.297 | 0.602 | −1.57 | 0.48 | linear |
Factors (Covariates) | Est | SE | Stat | p | padj | CIL | CIH | Model |
---|---|---|---|---|---|---|---|---|
Univariate Regression Model | ||||||||
SS score * (3 mo) | −0.39 | 0.51 | −0.76 | 0.447 | 0.753 | −1.43 | 0.58 | ordinal |
SS score * (6 mo) | −0.69 | 0.53 | −1.29 | 0.196 | 0.417 | −1.80 | 0.32 | ordinal |
SS score * (12 mo) | −0.16 | 0.57 | −0.28 | 0.781 | 0.885 | −1.37 | 0.91 | ordinal |
Cranial nerve palsy (3 mo) | 2.98 | 0.67 | 1.64 | 0.101 | 0.286 | 0.73 | 10.59 | logistic |
Cranial nerve palsy (6 mo) | 4.85 | 0.81 | 1.94 | 0.052 | 0.269 | 0.88 | 24.19 | logistic |
Cranial nerve palsy (12 mo) | 9.80 | 0.95 | 2.39 | 0.017 | 0.269 | 1.51 | 79.23 | logistic |
Paresis (3 mo) | 4.17 | 0.95 | 1.50 | 0.134 | 0.325 | 0.52 | 27.08 | logistic |
Paresis (6 mo) | 1.92 | 1.18 | 0.55 | 0.581 | 0.760 | 0.09 | 16.04 | logistic |
Paresis (12 mo) | 0.75 | 1.57 | −0.18 | 0.857 | 0.911 | 0.03 | 16.36 | logistic |
CSF leukocyte count (3 mo) | −0.13 | 0.24 | −0.56 | 0.577 | 0.760 | −0.60 | 0.33 | linear |
CSF leukocyte count (3mo) > 10 × 106/L | 0.80 | 0.69 | −0.32 | 0.748 | 0.885 | 0.17 | 2.78 | logistic |
CSF protein conc (3 mo) | 0.00 | 0.09 | 0.00 | 0.999 | 0.999 | −0.19 | 0.19 | linear |
Borrelia IgG AI value # (3 mo) | −0.47 | 0.26 | −1.84 | 0.069 | 0.269 | −0.99 | 0.04 | linear |
Partial Impro + Failure (2 w) | 2.81 | 0.52 | 1.99 | 0.047 | 0.269 | 1.02 | 8.02 | logistic |
Partial Impro + Failure (3 mo) | 1.68 | 0.63 | 0.82 | 0.414 | 0.753 | 0.43 | 5.45 | logistic |
Partial Impro + Failure (6 mo) | 1.64 | 0.71 | 0.70 | 0.487 | 0.753 | 0.34 | 6.01 | logistic |
Partial Impro + Failure (12 mo) | 3.29 | 0.68 | 1.76 | 0.079 | 0.269 | 0.79 | 11.99 | logistic |
Multivariate Regression Model | ||||||||
SS score * (3 mo) | 0.83 | 0.77 | −0.24 | 0.808 | 0.884 | 0.17 | 3.61 | ordinal |
SS score * (6 mo) | 0.71 | 0.80 | −0.43 | 0.666 | 0.884 | 0.14 | 3.26 | ordinal |
SS score * (12 mo) | 0.81 | 0.87 | −0.24 | 0.814 | 0.884 | 0.13 | 4.19 | ordinal |
Cranial nerve palsy (3 mo) | 0.65 | 1.21 | −0.35 | 0.723 | 0.884 | 0.06 | 7.02 | logistic |
Cranial nerve palsy (6 mo) | 1.97 | 1.23 | 0.55 | 0.581 | 0.884 | 0.18 | 21.99 | logistic |
Cranial nerve palsy (12 mo) | 13.38 | 1.41 | 1.84 | 0.066 | 0.561 | 0.84 | 212.48 | logistic |
Paresis (3 mo) | 8.58 | 1.73 | 1.24 | 0.214 | 0.884 | 0.29 | 254.94 | logistic |
Paresis (6 mo) | 1.30 | 1.80 | 0.15 | 0.884 | 0.884 | 0.04 | 44.00 | logistic |
Paresis (12 mo) | 1.33 | 1.79 | 0.16 | 0.872 | 0.884 | 0.04 | 44.14 | logistic |
CSF leukocyte count (3 mo) | 1.04 | 1.48 | 0.70 | 0.486 | 0.884 | −1.92 | 3.99 | linear |
CSF leukocyte count (3 mo) >10 × 106/L | 1.99 | 1.21 | 0.57 | 0.571 | 0.884 | 0.18 | 21.4 | logistic |
CSF protein conc (3 mo) | 0.01 | 0.06 | 0.19 | 0.850 | 0.884 | −0.11 | 0.14 | linear |
Borrelia IgG AI value # (3 mo) | −5.14 | 6.80 | −0.76 | 0.454 | 0.884 | −18.83 | 8.56 | linear |
Partial Impro + Failure (2 w) | 1.66 | 0.76 | 0.67 | 0.502 | 0.884 | 0.38 | 7.37 | logistic |
Partial Impro + Failure (3 mo) | 1.51 | 0.86 | 0.48 | 0.631 | 0.884 | 0.28 | 8.21 | logistic |
Partial Impro + Failure (6 mo) | 4.13 | 1.02 | 1.40 | 0.162 | 0.884 | 0.56 | 30.26 | logistic |
Partial Impro + Failure (12 mo) | 15.17 | 1.20 | 2.27 | 0.023 | 0.391 | 1.46 | 157.97 | logistic |
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Ogrinc, K.; Kastrin, A.; Lotrič-Furlan, S.; Bogovič, P.; Rojko, T.; Cerar-Kišek, T.; Ružić-Sabljić, E.; Wormser, G.P.; Strle, F. Effect of Statin Use on the Clinical Manifestations, Laboratory Test Results and Outcome of Lyme Neuroborreliosis. J. Clin. Med. 2020, 9, 2995. https://doi.org/10.3390/jcm9092995
Ogrinc K, Kastrin A, Lotrič-Furlan S, Bogovič P, Rojko T, Cerar-Kišek T, Ružić-Sabljić E, Wormser GP, Strle F. Effect of Statin Use on the Clinical Manifestations, Laboratory Test Results and Outcome of Lyme Neuroborreliosis. Journal of Clinical Medicine. 2020; 9(9):2995. https://doi.org/10.3390/jcm9092995
Chicago/Turabian StyleOgrinc, Katarina, Andrej Kastrin, Stanka Lotrič-Furlan, Petra Bogovič, Tereza Rojko, Tjaša Cerar-Kišek, Eva Ružić-Sabljić, Gary P. Wormser, and Franc Strle. 2020. "Effect of Statin Use on the Clinical Manifestations, Laboratory Test Results and Outcome of Lyme Neuroborreliosis" Journal of Clinical Medicine 9, no. 9: 2995. https://doi.org/10.3390/jcm9092995