Post-Herpetic Anti-NMDAR Encephalitis in Denmark: Current Status and Future Challenges
Abstract
:1. Introduction
2. Materials and Methods
2.1. Review of the Literature
2.2. Identification of Danish Cases of Post-HSE NMDARE
2.3. Consensus Criteria for NMDARE
2.4. Testing of Residual Samples for Autoantibodies
2.5. Incidence of Post-HSE NMDARE
2.6. Ethical Considerations
2.7. Statistics
3. Results
3.1. Danish Patients with Post-HSE NMDARE
3.2. Cases from Literature
3.3. Are Possible Adult Post-HSE NMDARE Cases Overlooked in Denmark?
3.3.1. Identifying HSE Patients in the Region of Southern Denmark
3.3.2. Screening HSE Patients for Probable Post-Viral NMDARE Using Clinical Diagnostic Criteria
3.3.3. Retrospective Screening of HSE Patients for Autoantibodies
3.3.4. Incidence of Post-HSE NMDARE in Denmark
3.4. Comparison of Danish Adult Post-HSE NMDARE Cases to Adult Literature Cases
4. Discussion
Limitations
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Literature Post-HSE NMDARE Cases | p-Value | |||
---|---|---|---|---|
All Cases n = 80 (%) | Children n = 53 (%) | Adults n = 27 (%) | ||
Demographics | ||||
Sex, Female | 42 (52) | 28 (53) | 14 (52) | >0.9999 |
Median Age, years (range) * | 3 (0.1667–84) | 1.33 (0.1667–17) | 51 (24–84) | <0.0001 **** |
Time HSV1 to NMDAR Ab n, (%) | n = 28 (35) | n = 16 (30) | n = 12 (44) | |
Median days (range) | 29.00 (4–365) | 26.5 (4–65) | 60.62 (7–365) | 0.1993 |
Clinical presentation | ||||
Prodromal symptoms | 10 (12) | 5 (9) | 5 (18) | 0.2925 |
Memory impairment | 9 (11) | 1 (2) | 8 (30) | 0.0005 *** |
Cognitive impairment | 22 (27) | 6 (11) | 16 (59) | <0.0001 **** |
Behavioral change | 52 (65) | 36 (68) | 16 (59) | 0.08665 |
Psychiatric symptoms | 29 (36) | 13 (24) | 16 (59) | 0.3473 |
Abnormal movements | 53 (66) | 47 (89) | 6 (22) | <0.0001 **** |
Altered consciousness | 40 (50) | 33 (62) | 7 (26) | 0.0041 ** |
Sleep disturbances | 25 (31) | 21 (40) | 4 (15) | 0.0398 * |
Speech abnormalities | 19 (24) | 11 (21) | 8 (30) | 0.4133 |
Autonomic dysfunction | 21 (26) | 19 (36) | 2 (7) | 0.0068 ** |
Focal neurological symptoms | 8 (10) | 4 (8) | 4 (15) | 0.4324 |
Seizures (no status epilepticus) | 23 (29) | 16 (30) | 7 (26) | >0.9999 |
Seizures status epilepticus | 9 (11) | 6 (11) | 3 (11) | >0.9999 |
CSF findings in HSE course (%) | n = 34 (42) | n = 19 (36) | n = 15 (56) | |
Abnormal CSF, n (%) | 33 (97) | 18 (95) | 15 (100) | >0.9999 |
Pleocytosis, n (%) | 32 (94) | 18 (95) | 14 (93) | >0.9999 |
Median WBC/mm3 (range) *** | 104 (0–920) | 64 (2–920) | 175 (0–730) | 0.1093 |
Protein elevation, n (%) | 20/29 (69) | 7/15 (47) | 13/14 (93) | 0.0142 * |
Median protein g/L (range) **** | 0.91 (0.34–4.44) | 0.77 (0.34–4.44) | 0.94 (0.52–3) | 0.3673 |
OCB presence, n (%) | NA | NA | NA | - |
CSF findings in NMDARE course (%) | n = 35 (44) | n = 17 (32) | n = 18 (678) | |
Abnormal CSF, n (%) | 34 (97) | 16 (94) | 18 (100) | 0.4857 |
Pleocytosis, n (%) | 28 (80) | 13 (76) | 15 (83) | 0.6906 |
Median WBC/mm3 (range) ** | 20 (0–480) | 29 (0–185) | 13 (1- 480) | 0.5898 |
Protein elevation, n (%) | 20 (57) | 7 (41) | 13 (72) | 0.0922 |
Median protein g/L (range) | 0.82 (0.39–2.56) | 0.78 (0.45–2.49) | 0.88 (0.39–2.56) | 0.7133 |
OCB presence, n (%) | 11/13 (85) | 4/4 (100) | 7/9 (78) | 0.4705 |
EEG in NMDARE course | n = 17 (21) | n = 7 (13) | n = 10 (37) | |
Abnormal EEG, n (%) | 14 (82) | 5 (71) | 9 (90) | 0.5368 |
EEG paroxysmal, n (%) ***** | 7 (41) | 1 (14) | 6 (60) | 0.134 |
EEG slowing, n (%) ***** | 9 (53) | 4 (57) | 5 (50) | >0.9999 |
EEG delta brush, n (%) | 0 (0) | 0 (0) | 0 (0) | - |
MRI changes additional in NMDARE | n = 39 (49) | n = 23 (43) | n = 16 (59) | |
Abnormal, n (%) | 12 (30.77) | 6 (26.09) | 6 (37.5) | 0.498 |
Treatment (%) | n = 73 (91) | n = 53 (100) | n = 20 (74) | |
Received any treatment, n (%) | 67 (92) | 51 (96) | 16 (80) | 0.0443 * |
Treatment—1st line a, n (%) | 67 (100) | 51 (100) | 16 (100) | >0.9999 |
Treatment—2nd line b, n (%) | 39 (58) | 30 (59) | 9 (56) | >0.9999 |
Treatment—Maintenance, n (%) | 14 (21) | 12 (23) | 2 (12) | 0.4898 |
Outcome mRS, n (%) | n = 74 (92) | n = 52 (98) | n = 22 (81) | |
Mean mRS (range) | 2.77 (0–6) | 3.04 (0–6) | 2.14 (0–6) | 0.0352 * |
Good outcome at last follow-up (mRS 0–2), n (%) | 30 (40) | 17 (33) | 13 (59) | 0.0418 * |
Poor outcome at last follow-up (mRS 3–6), n (%) | 44 (59) | 35 (67) | 9 (41) | 0.0418 * |
Dead, n (%) | 2 (3) | 1 (2) | 1 (5) | 0.5091 |
Probable + Definite (n = 16) | Not Fulfilling Criteria (n = 28) | p-Value | |
---|---|---|---|
Characteristics | |||
Sex. (male), % (n/N) | 50 (6/16) | 54 (15/28) | >0.9999 |
Age, years, median (range) | 73 (35–83) | 65 (25–88) | 0.0733 |
Prolonged/relapse, % (n/N) | 31 (5/16) | 11 (3/28) | 0.1172 |
GCS at admission, median (range) | 6 (2–13) | 13 (3–15) | <0.0001 **** |
Autoantibody Testing | |||
Tested for NMDAR-abs, % (n/N) | 37 (6/16) | 14 (4/28) | 0.1331 |
Positive NNMDAR-abs, % (n/N) | 33 (2/6) | 0 (0/4) | 0.4667 |
Timeline, days, median (range) | |||
Admission length | 30 (12–82) | 17 (6–52) | 0.0030 ** |
Symptoms to admission | 3 (0–14) | 2 (0–21) (n = 25) | 0.7526 |
Symptoms to HSE treatment | 5 (3–29) | 4 (0–22) (n = 26) | 0.1966 |
Time of Testing, % (n/N) | Autoantibody Tests n = 16 | Test Positive n = 3 | Test Negative n = 13 |
---|---|---|---|
At first admission | 37 (6/16) | 0 (0/3) | 46 (6/13) |
At relapse/prolonged admission | 25 (4/16) | 67 (2/3) | 15 (2/13) |
At re-test (CSF, Biobank) | 37 (6/16) | 33 (1/3) | 38 (5/13) |
Patient Characteristics | Patients tested n = 14 * | Positive n = 3 | Negative n = 11 |
Time admission to LP, days median (range) | 16 (−2–143) | 76 (35–143) | 7 (−2–76) |
Time symptoms to LP, days median (range) | 25 (1–147) | 90 (35–147) | 7 (1–35) |
Relapse/prolonged, % (n/N) | 36 (5/14) | 100 (3/3) | 18 (2/11) |
Probable/definite NMDARE **, % (n/N) | 43 (6/14) | 67 (2/3) | 36 (4/11) |
Literature Adults HSE (n = 27) (%) | Danish Adults HSE (n = 9) (%) | p-Value | |
---|---|---|---|
Demographics | |||
Sex, Female, n (%) | 14 (52) | 4 (44) | >0.9999 |
Age, median (range) * | 51 (24–84) | 62 (46–75) | 0.0316 * |
Time HSE to NMDAR Ab, n (%) | n = 12 (44) | n = 9 (100) | |
Days, median (range) | 61 (7–365) | 45 (25–212) | 0.7394 |
Symptoms (%) | n = 27 (100) | n = 9 (100) | |
Prodromal symptoms | 5 (18) | 2 (22) | >0.9999 |
Memory impairment | 8 (30) | 7 (78) | 0.0190 * |
Cognitive impairment | 16 (59) | 7 (78) | 0.4378 |
Behavioral change | 16 (59) | 4 (44) | 0.4697 |
Psychiatric symptoms | 16 (59) | 6 (67) | >0.9999 |
Abnormal movements | 6 (22) | 4 (44) | 0.2262 |
Altered consciousness | 7 (26) | 3 (33) | 0.6856 |
Sleep disturbances | 4 (15) | 1 (11) | >0.9999 |
Speech abnormalities | 8 (30) | 5 (56) | 0.2347 |
Autonomic dysfunction | 2 (7) | 1 (11) | >0.9999 |
Focal neurological symptoms | 4 (15) | 5 (56) | 0.0262 * |
Seizures (no status epilepticus) | 7 (26) | 5 (56) | 0.4088 |
Seizures (status epilepticus) | 3 (11) | (0) | >0.9999 |
CSF findings in HSE course (%) | n = 15 (56) | n = 8 (89) | |
Abnormal, n (%) | 15 (100) | 8 (100) | - |
Pleocytosis, n (%) | 14 (93) | 8 (100) | >0.9999 |
Median WBC/mm3 (range) ** | 175 (0–730) | 102.5 (19–360) | 0.2119 |
Protein elevation, n (%) | 13/14 (93) | 3/6 (50) | 0.0609 |
Median protein g/L (range) *** | 0.94 (0.52–3) | 0.89 (0.43–1.2) | 0.4315 |
OCB present, n (%) | NA | NA | - |
CSF findings in NMDARE course (%) | n = 18 (66.67) | n = 9 (100) | |
Abnormal, n (%) | 18 (100) | 9 (100) | - |
Pleocytosis, n (%) | 15 (83) | 9 (100) | 0.5292 |
Median WBC/mm3 (range) ** | 13 (1–480) | 23 (7–60) | 0.3176 |
Protein elevation, n (%) | 13 (72) | 8 (89) | 0.6279 |
Median protein g/L (range) **** | 0.88 (0.39–2.56) | 0.89 (0.64–1.04) | 0.9026 |
OCB present, n (%) | 7/9 (78) | 3/3 (100) | >0.9999 |
EEG in NMDARE (%) | n = 10 (37) | n = 7 (78) | |
Abnormal EEG, n (%) | 9 (90) | 6 (86) | >0.9999 |
EEG paroxysmal, n (%) ***** | 6 (60) | 1 (14) | 0.1340 |
EEG slowing, n (%) ***** | 5 (50) | 6 (86) | 0.3043 |
EEG delta brush, n (%) | 0 (0) | 0 (0) | - |
MRI changes in NMDARE (%) | n = 16 (59.26) | n = 9 (100) | |
Abnormal, n (%) | 6 (37) | 4 (44) | >0.9999 |
Treatment (%) | n = 20 (74) | n = 9 (100) | |
Any treatment, n (%) | 16 (80) | 6 (67) | 0.6424 |
1st line a, n (%) | 16 (100) | 6 (67) | 0.0365 * |
2nd line b, n (%) | 9 (56) | 0 (0) | 0.0078 ** |
Maintenance, n (%) | 2 (12) | 6 (67) | 0.0099 ** |
Outcome mRS (%) | n = 22 (81) | n= 9 (100) | |
Median mRS (range) | 2 (0–6) | 3 (1–5) | 0.3159 |
Good outcome at last follow-up (mRS 0–2), n (%) | 13 (59) | 4 (44) | 0.6927 |
Poor outcome at last follow-up (mRS 3–6), n (%) | 9 (41) | 5 (56) | 0.6927 |
Dead, n (%) | 1 (5) | 0 (0) | >0.9999 |
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Søgaard, A.; Poulsen, C.A.; Belhouche, N.Z.; Thybo, A.; Hovet, S.T.F.; Larsen, L.; Nilsson, C.; Blaabjerg, M.; Nissen, M.S. Post-Herpetic Anti-NMDAR Encephalitis in Denmark: Current Status and Future Challenges. Biomedicines 2024, 12, 1953. https://doi.org/10.3390/biomedicines12091953
Søgaard A, Poulsen CA, Belhouche NZ, Thybo A, Hovet STF, Larsen L, Nilsson C, Blaabjerg M, Nissen MS. Post-Herpetic Anti-NMDAR Encephalitis in Denmark: Current Status and Future Challenges. Biomedicines. 2024; 12(9):1953. https://doi.org/10.3390/biomedicines12091953
Chicago/Turabian StyleSøgaard, Anna, Charlotte Aaberg Poulsen, Nadia Zeeberg Belhouche, Alberte Thybo, Siv Tonje Faret Hovet, Lykke Larsen, Christine Nilsson, Morten Blaabjerg, and Mette Scheller Nissen. 2024. "Post-Herpetic Anti-NMDAR Encephalitis in Denmark: Current Status and Future Challenges" Biomedicines 12, no. 9: 1953. https://doi.org/10.3390/biomedicines12091953