Complete Remission in Paralytic Late Tick-Borne Neurological Disease Comprising Mixed Involvement of Borrelia, Babesia, Anaplasma, and Bartonella: Use of Long-Term Treatments with Antibiotics and Antiparasitics in a Series of 10 Cases
Abstract
:1. Introduction
2. Patients and Methods
2.1. Clinical and Biological Inclusion Criteria
2.2. Follow-Up
2.3. Outcome Criterion
2.4. Neurological Analysis
2.5. Infectious Involvement Criteria
2.6. Ruling Out of Other Diseases
2.7. Long-Term Treatment Regimens
3. Ethics Statement
4. Results
4.1. Cohort Description and Patient Histories (Table 1)
1 | 2 | 3 | 4 | 5 | 6 | 7 | 8 | 9 | 10 | |
---|---|---|---|---|---|---|---|---|---|---|
Age (years) | 13 | 35 | 25 | 16 | 14 | 68 | 49 | 40 | 34 | 27 |
Gender | F | F | F | F | F | F | M | M | F | F |
Identified tick bite | + | + | 0 | + | + | 0 | + | 0 | 0 | + |
Erythema migrans | + | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | + |
General disease duration at entry (months) | 6 | 20 | 10 | 65 | 21 | 36 | 84 | 12 | 12 | 20 |
Fatigue | + | + | + | + | + | + | + | + | + | + |
Subjective cognitive impairment | + | + | + | + # | + | + | + # | + | + | + |
Cephalalgia | + | + | + | + | + | + | + | + | 0 | + |
“Babesia symptoms” (night sweating, shivering, fever) | + | + | + | + | 0 | + | + | + | 0 | + |
Stretch marks | + | + | + | + | + | 0 | 0 | + | 0 | 0 |
Leucopenia | + | 0 | 0 | 0 | 0 | + | 0 | 0 | 0 | 0 |
4.2. Entry Neurological Status (Table 2)
1 | 2 | 3 | 4 | 5 | 6 | 7 | 8 | 9 | 10 | |
---|---|---|---|---|---|---|---|---|---|---|
Duration of neurological disease before treatment (months) | 6 | 13 | 6 | 48 | 9 | 16 | 60 | 6 | 6 | 12 |
Kurtzke invalidity score | 8.5 | 6 | 8 | 7.5 | 7 | 7 | 6.5 | 6 | 6 | 4.5 |
Flaccid tetraplegia | + | |||||||||
Spastic triparesis | + | |||||||||
Flaccid paraplegia | + | |||||||||
Spastic paraplegia | + | |||||||||
Spastic paraparesis | + | + | + | + | ||||||
Isolated limb palsy | + | + | ||||||||
Wheelchair before treatment | + | - | + | + | + | + | - | - | - | - |
Walking with 1 or 2 stick(s) | - | + | - | - | - | - | + | + | + | 0 |
Permanent pain score: 0–10 | 8 | 8 | 9 | 9 | 8 | 6 | 9 | 8 | 5 | 7 |
Interruption of work or school attendance | + | + | + | + | + | + | + | + | + | + |
Duration of work (w)/school (s) attendance interruption before treatment (months) | 6 s | 13 w | 6 w | 36 s | 12 s | 16 w | 60 w | 2 w | 4 w | 12 w |
4.3. Entry Neurological Explorations (Table 3)
1 | 2 | 3 | 4 | 5 | 6 | 7 | 8 | 9 | 10 | |
---|---|---|---|---|---|---|---|---|---|---|
MRI T2-weighted image hyperintensities: | 0 | + | 0 | + | 0 | + | 0 | 0 | 0 | nd |
Encephalon Spinal cord | 0 | 0 | 0 | + | 0 | 0 | 0 | 0 | 0 | nd |
Pleocytosis > 4 cells/cc | 0 | 0 | 0 | 0 | nd | 0 | + | nd | 0 | nd |
Protein concentration > 0.45 g/L | 0 | 0 | 0 | 0 | nd | 0 | + | nd | 0 | nd |
CSF Oligoclonal pattern | 0 | + | 0 | 0 | nd | 0 | 0 | nd | + | nd |
Inferior limb EMG anomalies | 0 | 0 | 0 | 0 | nd | 0 | 0 | 0 | 0 | 0 |
4.4. Microorganism Involvement Status (Table 4)
1 | 2 | 3 | 4 | 5 | 6 | 7 | 8 | 9 | 10 | |
---|---|---|---|---|---|---|---|---|---|---|
ELISA Borrelia s. lato IgG | 0 | + | + | + | 0 | + | 0 | 0 | 0 | 0 |
IgM | 0 | 0 | 0 | + | 0 | + | 0 | 0 | + | 0 |
ELISA positivity | 0 | + | + | + | 0 | + | 0 | 0 | + | 0 |
Immunoblot Borrelia s. lato IgG signif. band(s) | 0 | ± | +(5) | 0 | +(2) | +(2) | +(1) | +(1) | 0 | +(1) |
p41 excluded IgM signif. band(s) p41 included | 0 | 0 | 0 | +(3) | +(6) | +(1) | 0 | 0 * | 0 | +(6) |
Immunoblot positivity | 0 | 0 | + | + | + | + | + | + | 0 | + |
Neuroborreliosis-correlated antigens (IgG/IgM) p18 | - | 0 | + | + | + | + | + | 0 | 0 | + |
p100 | - | 0 | + | 0 | 0 | 0 | 0 | + | 0 | + |
OspC | - | 0 | 0 | + | + | 0 | 0 | 0 | 0 | + |
VlsE | - | 0 | + | 0 | 0 | + | 0 | 0 | 0 | 0 |
Cumulated Borrelia stigmata (Bo) | 0 | + | + | + | + | + | + | + | + | + |
Babesia divergens (Bb) | + | + | + | + | + | + | 0 | + | + | 0 |
Anaplasma (A) IgG | + | 0 | 0 | 0 | 0 | + | 0 | 0 | + | 0 |
phagocytophylum IgM | 0 | 0 | 0 | 0 | + | + | 0 | 0 | 0 | 0 |
Bartonella (Bt) henselae IgG | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | + | 0 |
quintana IgG | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 |
Co-involvement status | Bo | Bo | Bo | Bo | Bo | Bo | Bo | Bo | Bo | |
Bb | Bb | Bb | Bb | Bb | Bb | - | Bb | Bb | - | |
A | A | A | A | |||||||
Bt | ||||||||||
Intrathecal Borrelia antibody synthesis | 0 | 0 | 0 | 0 | - | 0 | 0 | - | 0 | - |
4.5. Realization of the Long-Term Treatments (Table 5)
1 | 2 | 3 | 4 | 5 | 6 | 7 | 8 | 9 | 10 | |
---|---|---|---|---|---|---|---|---|---|---|
Number of ceftriaxone–oral doxycycline cycles | 3 | 8 | 4 | 4 | 3 | 7 | 3 | 4 | 3 | 3 |
Number of 2–3-month doxycycline–azithromycin c. | 1 | 4 | 4 | 3 | 3 | 4 | 4 | 3 | 3 | 2 |
Number of 2–3-month doxy–azithro-rifampicin c. (possibly continuous) | 3 | 0 | 0 | 3 | 4 | 0 * | 3 | 5 | 0 * | 0 |
Number of atovaquone– azithromycin cycles | 4 | 5 | 4 | 1 | 2 | 3 | 2 ** | 4 | 3 | 1 |
Duration of treatment to first motor remission (months) | 8 | 4 | 3 | 23 | 12 | 10 | 26 | 31 | 4 | 10 |
Cumulated duration of active treatment (months) | 18 | 19 | 19.5 | 23 | 26 | 22 *** | 26 | 31 | 14.5 | 10 |
4.6. Lines and Inserted Devices
4.7. Treatment Outcomes (Table 6)
1 | 2 | 3 | 4 | 5 | 6 | 7 | 8 | 9 | 10 | |
---|---|---|---|---|---|---|---|---|---|---|
Complete motor remission at 2 years after treatment end | 0 | + | 0 | + | + | 0 | + | + | + | + |
Kurtzke Invalidity score at 2 years after treatment end8 | 8 | 0 | 8 | 0 | 0 | 8 | 0 | 0 | 0 | 0 |
Kurtzke Ivalidity Score at entry (reminder) | 8.5 | 6 | 8 | 7.5 | 7 | 7 | 6.5 | 6 | 6 | 4.5 |
Wheelchair after treatment | + | 0 | + | 0 | 0 | + | 0 | 0 | 0 | 0 |
Number of motor recurrences during treatment course | 1 | 6 | 2 | 0 | 1 | 4 | 0 | 0 | 1 | 0 |
Cumulated duration of c. active treatment in successful cases (months) | - | 19 | - | 23 | 26 | - | 26 | 31 | 14.5 | 10 |
Time from treatment onset to final motor remission (months) | - | 41 | - | 23 | 36 | - | 26 | 31 | 17 | 10 |
Return to work or school | 0 | + | 0 | + | + | 0 | + & | + | + | + |
Cumulated duration of work(w)/school (s) interruption in successful patients at final evaluation (months) | - | 54 w | - | 54 s | 14 s | - | 87 w | 33 w | 10 w | 16 w |
4.8. Side Effects
5. Discussion
5.1. High Rate of Complete Remission with Long-Lasting Treatments in a Cohort with Intractable Neurological Deficits and Significant Elements of Tick-Borne Involvement
5.2. Long-Term Treatment Aspects and Results
5.2.1. Ceftriaxone Administration Duration and Remission
5.2.2. Importance of Coadministration of Doxyxycline, Azithromycin, and Rifampicin for Borrelia and Anaplasma
5.2.3. Importance of Coadministration of Repeated Anti-Babesia Atovaquone–Azithromycin Regimens
5.3. Treatment Decision and the Nosological Situation of the Cohort
5.3.1. Borrelian Involvement
5.3.2. Mixed Borrelia–Babesia Involvement
5.3.3. Non-Borrelia Involvement, with Babesia–Anaplasma Positivity
5.3.4. Low Rate of MRI Neural Hyperintensities
5.3.5. Treatment Decision Basis
5.4. Responsibility of Coinfection in the Severity of the Neurological Status
5.5. Factors of Failure
5.6. Indications for Future Studies
5.7. Moral and Economic Considerations
6. Limitations
7. Conclusions
Author Contributions
Funding
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
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Trouillas, P.; Franck, M. Complete Remission in Paralytic Late Tick-Borne Neurological Disease Comprising Mixed Involvement of Borrelia, Babesia, Anaplasma, and Bartonella: Use of Long-Term Treatments with Antibiotics and Antiparasitics in a Series of 10 Cases. Antibiotics 2023, 12, 1021. https://doi.org/10.3390/antibiotics12061021
Trouillas P, Franck M. Complete Remission in Paralytic Late Tick-Borne Neurological Disease Comprising Mixed Involvement of Borrelia, Babesia, Anaplasma, and Bartonella: Use of Long-Term Treatments with Antibiotics and Antiparasitics in a Series of 10 Cases. Antibiotics. 2023; 12(6):1021. https://doi.org/10.3390/antibiotics12061021
Chicago/Turabian StyleTrouillas, Paul, and Michel Franck. 2023. "Complete Remission in Paralytic Late Tick-Borne Neurological Disease Comprising Mixed Involvement of Borrelia, Babesia, Anaplasma, and Bartonella: Use of Long-Term Treatments with Antibiotics and Antiparasitics in a Series of 10 Cases" Antibiotics 12, no. 6: 1021. https://doi.org/10.3390/antibiotics12061021