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Journal of Cardiovascular Development and Disease
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  • Systematic Review
  • Open Access

23 April 2024

Associations of Atrioventricular Blocks and Other Arrhythmias in Patients with Lyme Carditis: A Systematic Review and Meta-Analysis

,
and
1
BronxCare Health System, Bronx, NY 10457, USA
2
Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA
*
Author to whom correspondence should be addressed.
J. Cardiovasc. Dev. Dis.2024, 11(5), 131;https://doi.org/10.3390/jcdd11050131
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Abstract

Lyme disease often leads to cardiac injury and electrophysiological abnormalities. This study aimed to explore links between atrioventricular blocks and additional arrhythmias in Lyme carditis patients. This systematic review and meta-analysis of existing literature was performed from 1990 to 2023, and aimed to identify cases of Lyme carditis through serology or clinical diagnosis with concomitant arrhythmias. Pubmed and Web of Science were searched using appropriate MESH terms. Patients were divided into groups with atrioventricular blocks and other arrhythmias for cardiovascular (CV) outcome assessment. A total of 110 cases were analyzed. The majority (77.3%) were male, with mean age = 39.65 ± 14.80 years. Most patients presented within one week of symptom onset (30.9%). Men were more likely to have first-degree atrioventricular blocks (OR = 1.36 [95% CI 1.12–3.96], p = 0.01); these blocks tended to be reversible in nature (OR = 1.51 [95% CI 1.39–3.92], p = 0.01). Men exhibited a higher likelihood of experiencing variable arrhythmias (OR = 1.31 [95% CI 1.08–2.16], p < 0.001). Ventricular and supraventricular arrhythmias were more likely to exhibit instability (OR = 0.96 [95% CI 0.81–1.16] p = 0.01) and variability (OR = 1.99 [95% CI 0.47–8.31], p < 0.001). Men with Lyme carditis are likely to present with various atrioventricular blocks. These atrioventricular blocks are benign, and follow a predictable and stable clinical course. Further large-scale studies are warranted to confirm these associations.

1. Introduction

Lyme disease is a prevalent global vector-borne illness, particularly in Europe, Eurasia, and the US. In Europe and Eurasia, the yearly incidence rate is approximately 0.21%, with higher rates in specific areas like northeast Moscow and Western Siberia [1,2,3,4]. In the US, between 2008 and 2015, the CDC documented 208,834 confirmed cases and 66,755 probable cases, with July being the peak month for onset [5]. Lyme disease can lead to cardiac complications, with about 1% of patients developing Lyme carditis, typically between June and December of the year following exposure [6,7]. This condition can manifest as atrioventricular block or left ventricular dysfunction, along with ECG abnormalities like T wave irregularities and prolonged QT intervals [8,9,10,11,12]. While antibiotics are effective in treating Lyme disease, they seem less critical in reversing cardiac manifestations, suggesting inflammation as a driving factor in Lyme carditis [13,14,15]. However, data on risk factors and treatment for Lyme carditis remain limited, highlighting the need for further research.
The objective of the study was to determine associations of atrioventricular blocks and other arrhythmias in patients with Lyme carditis. The study also focuses on demographic characteristics, clinical presentations, treatment, and outcomes of both cohorts with Lyme carditis.

2. Materials and Methods

2.1. Protocol Development and Search Strategy

The protocol was registered in PROSPERO (ID# CRD42023448732) and followed the guidelines of the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) [16]. We implemented the patient, intervention, comparison, and outcomes (PICO) approach for our research query in this study. The keywords employed were: “lyme” [All Fields] AND (“myocarditis” [MeSH Terms] OR “myocarditis” [All Fields] OR “carditis” [All Fields]) AND (“arrhythmia s” [All Fields] OR “arrhythmias, cardiac” [MeSH Terms]) OR (“arrhythmias” [All Fields] AND “cardiac” [All Fields]) OR (“cardiac arrhythmias” [All Fields] OR “arrhythmia” [All Fields] OR “arrhythmias” [All Fields]).

2.2. Data Extraction

Our search was conducted on PubMed and Web of Science using Boolean operators (“OR”, “AND”). This systematic review incorporated articles written in English over the past three decades that met the following inclusion standards: (1) articles that addressed Lyme carditis or arrhythmias in patients with a confirmed Lyme disease diagnosis via serology or clinical symptoms; and (2) articles that specifically detailed interventions used for patients with arrhythmias in Lyme carditis and their results. Employing the PICO approach, we evaluated patients diagnosed with Lyme carditis. The interventions referred to the treatment strategies applied (such as antibiotic treatments and pacemaker implantation). The outcome variables included mortality, arrhythmia reversibility, clinical symptoms, and reversibility duration, which were compared with patients without AV block arrhythmias. To reduce population bias and enhance qualitative variable measurements, the systematic review included observational studies and case reports. The initial search yielded 164 articles from PubMed and 9300 articles from Google Scholar. After removing duplicates, two independent reviewers screened the remaining studies based on the inclusion criteria, initially reviewing abstracts and then full-text articles if criteria were met (N.J. and J.N.B.). Zotero (version 6) and Rayyan (version 2016) software were used for this process. A third reviewer was brought in to resolve any possible disputes (E.S.). One reviewer (N.J.) extracted details about the study design, publication year, study location, journal of publication, demographic data, initial symptoms, diagnostic characteristics, types of arrhythmias, management, and outcomes from the records. The collected data was then double-checked for its accuracy and completeness. Studies were excluded from the analysis if translations or complete articles were unavailable, or if the information about device-specific characteristics was incomplete. Non-peer-reviewed papers were also omitted. The initial data was logged into an Excel spreadsheet, and the final analysis included 68 studies. These findings are illustrated in Figure 1.
Figure 1. PRISMA diagram reviewing all studies.
STATA version 18 was used to perform the statistical analysis. Continuous variables were expressed as mean ± standard deviation. Qualitative variables were represented by frequencies or percentages. Statistical tests such as chi-square, independent t-test, and analysis of variance were employed. To identify predictors for multiple outcomes, logistic regression models were utilized. A p-value of less than 0.05 was deemed significant.

3. Results

3.1. Demographic and Clinical Characteristics

The analysis encompassed a total of 68, comprising 5 case series and 63 case reports. The cumulative number of cases considered in the review amounted to 110. Predominantly, the cases were male, accounting for 78.10% of the total. The mean age of the study population was 39.65 ± 14.80 years. Detailed information regarding data extraction from the articles is provided in Table S1 [17,18,19,20,21,22,23,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81,82,83,84]. Most commonly, patients had presented with electrophysiological abnormalities within 2 weeks of initial symptoms (40.9%). Prior comorbidities had been discussed for 27 cases; hypertension was present in 13.6% of the cases. Syncope was present in 32/110 cases (29.1%), followed by palpitations in 14/110 cases (12.7%) and dizziness in 8/110 cases (7.3%).

3.2. Laboratory Investigations, Electrocardiogram- and Echocardiogram-Based Features

As can be seen in Table 1, most of the cases were hemodynamically stable on presentation (104/110 cases). Echocardiographic findings were not documented for many cases (55/110 cases).
Table 1. Features on presentation.
Troponinemia was observed in 4/110 cases. Increased inflammation was observed in 9/110 cases. Diastolic dysfunction was observed in 11/110 cases. Systolic dysfunction was observed in 5/110 cases. Most of the patients presented with first-degree (25/110) or complete atrioventricular block (24/110).

3.3. Management

As may be seen in Table S2, most of the cases were managed with antibiotics (70/110; 63.6%). Pacing was needed for 22/110 cases. The arrhythmias resolved with treatment in 88/110 cases. Six patients died during the course of illness.

3.4. Subgroup Analysis

The subgroup analyses are detailed in Table 2 and Table 3.
Table 2. Characteristics of atrioventricular blocks in men.
Table 3. Characteristics of atrioventricular blocks and other arrhythmias.
Men were more likely to present with syncope, had a shorter time to resolution, and presented with variable arrhythmias. However, atrioventricular blocks were likely to be stable and reversible. Patients with atrioventricular blocks were likely to present with syncope and had a shorter time to resolution. The abnormalities were more stable and reversible in nature. However, the type of atrioventricular blocks varied.

4. Discussion

Our study had a few key findings. First, the majority were young men with mean age = 39.65 ± 14.80 years. Male sex has been identified has one of the independent predictors of developing Lyme carditis [85,86,87]. In the US, men and women have been found to have similar odds of developing Lyme disease (50% in men and 50% in women) [88]. In European studies, a preponderance for the female population in developing Lyme disease has been noted. As per the literature, these differences could not be explained by attire, usage of deodorant/perfume, or activities at the time of the tick bite [89]. One of the hypotheses suggested in the study included a variation in neurochemical hormones that leads to varying rates of tick bites [89]. However, this has not been discussed in the literature. Even in studies with relatively equal gender distributions, the risk of developing carditis was higher in men [90]. In our study, younger individuals were at a higher risk of developing Lyme carditis. However, it was not an independent predictor of development of cardiac abnormalities. This is similar to another study mentioning older age as one of the independent predictors for Lyme carditis [86], particularly due to an increase in comorbidities.
Second, the majority of the patients had presented with atrioventricular blocks (50.9%). A few hypotheses can be considered for this finding, as described by previous models. One of the borrelial proteins, P66, binds to the integrin receptors, resulting in greater extracutaneous dissemination of bacteria and cardiac tropism [91]. Similarly, one of the proteoglycans called decorin-binding protein causes colonization of the heart. However, this impact has been studied in murine models, and more investigations are needed to determine the long-lasting effects of the proteins [92,93]. Men were more likely to have atrioventricular blocks that were stable and reversible. As observed in another study, men had a longer AV block cycle in supraventricular arrhythmias (371 ± 76 ms vs. 330 ± 52 ms, p = 0.02) compared to women [92]. More ventriculoatrial dissociation was observed in men [94]. Additionally, the previous literature also suggests that men have a preponderance to develop atrioventricular block regardless of age, as discussed in a Chinese study. Men were 2.44-fold more likely to develop atrioventricular block after adjusting for age [95]. This implies that, in men, PR interval representing both autonomic and structural cardiac abnormalities indicated progressive fibrosis, which is also a measure of advanced age, might be hypothesized to be the causative factor [96].
Limited data exist on antibiotic guidelines for Lyme carditis management. UK guidelines recommend oral doxycycline or amoxicillin for stable patients, and intravenous ceftriaxone for those with hemodynamic compromise or systemic illness, typically for 14 to 21 days. Once-daily administration of ceftriaxone is advantageous [97], but most patients in our study were hospitalized regardless of atrioventricular block type, suggesting a need for revised guidelines. Apart from use of antibiotics, one algorithm discussed use of pacemaker implantation and subsequent explantation. Pacemaker implantation is common for symptomatic bradycardia, especially with high-grade AV blocks, as these are associated with cardiac arrest [7,98]. In Lyme carditis, brief periods of asystole are associated with a worse prognosis, along with escape rhythms featuring a wide QRS complex and fluctuating bundle branch blocks [99]. Pacemaker interrogation should be performed after completion of antibiotic therapy. In cases of refractory ventricular pacing, the pacemaker is usually long-term. In other cases, the Wenckebach point comes into play, with heart rates <80 beats per minute warranting long-term pacemaker placement [100].
Three patients with atrial fibrillation and first-degree atrioventricular block died, while those remaining had associated ventricular arrhythmias; limited data explain this distribution, but prior studies suggest that men with ventricular arrhythmias have a worse prognosis [100].
The main strengths of the study include a gender-based comparison of disease pattern in Lyme carditis, as well as a comparison of the electrophysiological abnormalities. There are a few limitations to the study. Men were in higher numbers in the study, which can produce bias in analysis, despite being adjusted for. Therefore, these findings need to be interpreted in appropriate context. Multiple studies used qualitative measures that could not be compared in a pair-wise fashion, despite producing significant results in the studies discussed. Data about prior histories of comorbidities and echocardiographic findings were limited.

5. Conclusions

The study explored the relationship between Lyme disease and cardiac complications, specifically focusing on atrioventricular blocks and other arrhythmias in Lyme carditis patients. Men were more likely to develop first-degree atrioventricular blocks, often reversible in nature. Additionally, men showed a higher likelihood of experiencing various arrhythmias, with ventricular and supraventricular arrhythmias associated with instability and variability. The study suggests a potential predisposition of men with Lyme carditis to atrioventricular blocks, highlighting the need for further comprehensive research to confirm these associations.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/jcdd11050131/s1, Table S1: Demographic and clinical characteristics, Table S2: Management and outcomes.

Author Contributions

Conceptualization, N.J. and E.S.; methodology, N.J.; software, N.J.; validation, E.S. and J.N.B.; formal analysis, N.J.; investigation, N.J.; resources, E.S. and J.N.B.; data curation, N.J.; writing—original draft preparation, N.J.; writing—review and editing, N.J., E.S. and J.N.B.; visualization, N.J.; supervision, J.N.B. and E.S.; project administration, E.S. and J.N.B. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

Data is available on request addressed to the corresponding author.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Smith, R.; Takkinen, J. Lyme borreliosis: Europe-wide coordinated surveillance and action needed? Eurosurveillance 2006, 11, 2977. [Google Scholar] [CrossRef]
  2. Korenberg, E.I. Comparative ecology and epidemiology of lyme disease and tick-borne encephalitis in the former Soviet Union. Parasitol. Today 1994, 10, 157–160. [Google Scholar] [CrossRef] [PubMed]
  3. EpiNorth. A Co-Operation Project for Communicable Disease Control in Northern Europe. EpiNorth Data: Lyme Borreliosis. 2014. Available online: http://www.epinorth.org (accessed on 4 January 2024).
  4. WHO Workshop on Lyme Borreliosis Diagnosis and Surveillance, Warsaw, Poland, 20–22 June 1995 (who/cds/vph/95141-1); World Health Organization: Geneva, Switzerland, 1995.
  5. Hu, L.T. In the clinic: Lyme disease. Ann. Intern. Med. 2012, 157, ITC2-2–ITC2-16. [Google Scholar] [CrossRef]
  6. Shen, R.V.; McCarthy, C.A. Cardiac Manifestations of Lyme Disease. Infect. Dis. Clin. N. Am. 2022, 36, 553–561. [Google Scholar] [CrossRef]
  7. Krause, P.J.; Bockenstedt, L.K. Cardiology patient pages. Lyme disease and the heart. Circulation 2013, 127, e451–e454. [Google Scholar] [CrossRef]
  8. Forrester, J.D.; Mead, P. Third-degree heart block associated with lyme carditis: Review of published cases. Clin. Infect. Dis. 2014, 59, 996–1000. [Google Scholar] [CrossRef] [PubMed]
  9. Kubánek, M.; Šramko, M.; Berenová, D.; Hulínská, D.; Hrbáčková, H.; Malušková, J.; Lodererová, A.; Málek, I.; Kautzner, J. Detection of Borrelia burgdorferi sensu lato in endomyocardial biopsy specimens in individuals with recent-onset dilated cardiomyopathy. Eur. J. Heart Fail. 2012, 14, 588–596. [Google Scholar] [CrossRef]
  10. Costello, J.M.; Alexander, M.E.; Greco, K.M.; Perez-Atayde, A.R.; Laussen, P.C. Lyme carditis in children: Presentation, predictive factors, and clinical course. Pediatrics 2009, 123, e835–e841. [Google Scholar] [CrossRef] [PubMed]
  11. Cox, J.; Krajden, M. Cardiovascular manifestations of Lyme disease. Am. Heart J. 1991, 122, 1449–1455. [Google Scholar] [CrossRef]
  12. McAlister, H.F.; Klementowicz, P.T.; Andrews, C.; Fisher, J.D.; Feld, M.; Furman, S. Lyme carditis: An important cause of reversible heart block. Ann. Intern. Med. 1989, 110, 339–345. [Google Scholar] [CrossRef]
  13. Shen, R.V.; McCarthy, C.A.; Smith, R.P. Lyme Carditis in Hospitalized Children and Adults, a Case Series. Open Forum Infect. Dis. 2021, 8, ofab140. [Google Scholar] [CrossRef] [PubMed]
  14. van der Linde, M.R.; Crijns, H.J.; Lie, K.I. Transient complete AV block in Lyme disease: Electrophysiologic observations. Chest 1989, 96, 219–221. [Google Scholar] [CrossRef] [PubMed]
  15. Lantos, P.M.; Rumbaugh, J.; Bockenstedt, L.K.; Falck-Ytter, Y.T.; Aguero-Rosenfeld, M.E.; Auwaerter, P.G.; Baldwin, K.; Bannuru, R.R.; Belani, K.K.; Bowie, W.R.; et al. Clinical Practice Guidelines by the Infectious Diseases Society of America (IDSA), American Academy of Neurology (AAN), and American College of Rheumatology (ACR): 2020 Guidelines for the Prevention, Diagnosis and Treatment of Lyme Disease. Clin. Infect. Dis. 2021, 72, e1–e48. [Google Scholar] [CrossRef] [PubMed]
  16. Page, M.J.; McKenzie, J.E.; Bossuyt, P.M.; Boutron, I.; Hoffmann, T.C.; Mulrow, C.D.; Shamseer, L.; Tetzlaff, J.M.; Akl, E.A.; Brennan, S.E.; et al. The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. BMJ 2021, 372, n71. [Google Scholar] [CrossRef]
  17. Wan, D.; Blakely, C.; Branscombe, P.; Suarez-Fuster, L.; Glover, B.; Baranchuk, A. Lyme Carditis and High-Degree Atrioventricular Block. Am. J. Cardiol. 2018, 121, 1102–1104. [Google Scholar] [CrossRef] [PubMed]
  18. Zainal, A.; Hanafi, A.; Nadkarni, N.; Mubasher, M.; Lingutla, D.; Hoefen, R. Lyme carditis presenting as atrial fibrillation. BMJ Case Rep. 2019, 12, e228975. [Google Scholar] [CrossRef]
  19. Gazendam, N.; Yeung, C.; Baranchuk, A. Lyme carditis presenting as sick sinus syndrome. J. Electrocardiol. 2020, 59, 65–67. [Google Scholar] [CrossRef] [PubMed]
  20. Esfandiari, N.; Beebe-Peat, T.; Quinlan, A.; Wagner, B.; Wark, T.; Lobel, R. Lyme Carditis Complicated by Polymorphic Ventricular Tachycardia and Cardiac Arrest: A Case Report. J. Investig. Med. High Impact Case Rep. 2022, 10, 23247096221098333. [Google Scholar] [CrossRef] [PubMed]
  21. Franco-Avecilla, D.; Yeung, C.; Baranchuk, A. Lyme carditis presenting with an atypical rash. CMAJ 2020, 192, E584. [Google Scholar] [CrossRef]
  22. Bamgboje, A.; Akintan, F.O.; Gupta, N.M.; Kaur, G.; Pekler, G.; Mushiyev, S. Lyme Carditis: A Reversible Cause of Acquired Third-Degree AV Block. Am. J. Case Rep. 2021, 22, e927885. [Google Scholar] [CrossRef]
  23. Zaid, J.M.; Lingel, J.M.; Scheinthal, E.; Foster, M.; Ragupathi, L.; Russo, A.M. Lyme Carditis Presenting With Complete Heart Block and Wide Complex Escape Rhythm. Tex Heart Inst. J. 2022, 49, e207515. [Google Scholar] [CrossRef] [PubMed]
  24. Arroja, J.D.; Fassa, A.A.; Zimmermann, M. Atteinte cardiaque de ta maladie de Lyme [Lyme carditis]. Rev. Med. Suisse 2015, 11, 563–568. [Google Scholar] [PubMed]
  25. Kannangara, D.W.; Sidra, S.; Pritiben, P. First case report of inducible heart block in Lyme disease and an update of Lyme carditis. BMC Infect. Dis. 2019, 19, 428. [Google Scholar] [CrossRef] [PubMed]
  26. Rojas-Marte, G.; Chadha, S.; Topi, B.; Hollander, G.; Shani, J. Heart block and Lyme carditis. QJM 2014, 107, 771–772. [Google Scholar] [CrossRef] [PubMed][Green Version]
  27. Khetpal, V.; Wark, T.W.; Masel, R.; Tran, C.T.; Haines, P. A 34-Year-Old Woman with Third-Degree Heart Block and Atrial Flutter Associated with Lyme Carditis: A Case Report. Am. J. Case Rep. 2021, 22, e933789. [Google Scholar] [CrossRef] [PubMed]
  28. Wang, C.; Chacko, S.; Abdollah, H.; Baranchuk, A. Treating Lyme carditis high-degree AV block using a temporary-permanent pacemaker. Ann. Noninvasive Electrocardiol. 2019, 24, e12599. [Google Scholar] [CrossRef] [PubMed]
  29. Yoon, E.C.; Vail, E.; Kleinman, G.; Lento, P.A.; Li, S.; Wang, G.; Limberger, R.; Fallon, J.T. Lyme disease: A case report of a 17-year-old male with fatal Lyme carditis. Cardiovasc. Pathol. 2015, 24, 317–321. [Google Scholar] [CrossRef] [PubMed]
  30. Dobbs, L.B.; Mugmon, M.A. Wenckebach responsive to cephalosporins—It must be Lyme carditis. J. Community Hosp. Intern. Med. Perspect. 2013, 3, 23013. [Google Scholar] [CrossRef]
  31. Beach, C.M.; Stewart, E.; Marcuccio, E.; Beerman, L.; Arora, G. Lyme carditis presenting as paroxysmal junctional tachycardia and complete atrioventricular block in an adolescent. J. Electrocardiol. 2023, 76, 14–16. [Google Scholar] [CrossRef]
  32. Shabbir, M.A.; Saad Shaukat, M.H.; Arshad, M.H.; Sacco, J. Lyme carditis presenting as atrial fibrillation in a healthy young male. BMJ Case Rep. 2019, 12, e229261. [Google Scholar] [CrossRef]
  33. Kennel, P.J.; Parasram, M.; Lu, D.; Zisa, D.; Chung, S.; Freedman, S.; Knorr, K.; Donahoe, T.; Markowitz, S.M.; Halazun, H. A Case of Lyme Carditis Presenting with Atrial Fibrillation. Case Rep. Cardiol. 2018, 2018, 5265298. [Google Scholar] [CrossRef] [PubMed]
  34. Brunner, F.J.; Blankenberg, S.; Sydow, K. Digital camera revealed infection with Borrelia burgdorferi as a cause of reversible total AV block in a 42 year old man. Int. J. Cardiol. 2014, 177, e165–e166. [Google Scholar] [CrossRef] [PubMed]
  35. Greenberg, Y.J.; Brennan, J.J.; Rosenfeld, L.E. Lyme myocarditis presenting as fascicular tachycardia with underlying complete heart block. J. Cardiovasc. Electrophysiol. 1997, 8, 323–324. [Google Scholar] [CrossRef] [PubMed]
  36. Siebenlist, D.; Hahn, M.; Gattenlöhner, W. Transitorischer AV-Block als kardiale Manifestation der Lyme-Krankheit [Transitory AV block as a cardiac manifestation of Lyme disease]. Dtsch. Med. Wochenschr. 1991, 116, 1549–1552. (In German) [Google Scholar] [CrossRef] [PubMed]
  37. Rostoff, P.; Konduracka, E.; El Massri, N.; Gackowski, A.; Kruszec, P.; Zmudka, K.; Piwowarska, W. Boreliozowe zapalenie serca manifestujace sie jako ostry zespół wieńcowy [Lyme carditis presenting as acute coronary syndrome: A case report]. Kardiol. Pol. 2008, 66, 420–425. (In Polish) [Google Scholar] [PubMed]
  38. Aringer, M.; Pirich, C.; Wenger, S.; Kiener, H.P.; Machold, K.; Stanek, G.; Graninger, W.B. AV-Block II und Arthritis als Manifestationen der Lyme-Borreliose [AV-block II and arthritis as manifestations of Lyme borreliosis]. Wien Med. Wochenschr. 1995, 145, 195–196. (In Germany) [Google Scholar]
  39. Vasiljević, Z.; Dmitrović, R.; Naumović, Z.; Ostojić, M.; Radosavljević, M.; Karadzić, A.; Prostran, M.; Colić, M. Common form of Lyme borreliosis carditis--complete heart block with syncope: Report on 3 cases. Cardiology 1996, 87, 76–78. [Google Scholar] [CrossRef]
  40. Panic, G.; Stanulovic, V.; Popov, T. Atrio-ventricular block as the first presentation of disseminated Lyme disease. Int. J. Cardiol. 2011, 150, e104–e106. [Google Scholar] [CrossRef]
  41. Dam, E.P.; Jonker, D.R.; Hoorntje, J.C. Temporary decrease in heart rate in Lyme carditis during treatment with antibiotics. Heart 1996, 76, 289–290. [Google Scholar] [CrossRef][Green Version]
  42. Manek, M.; Kulkarni, A.; Viera, A. Hint of Lyme, an uncommon cause of syncope. BMJ Case Rep. 2014, 2014, bcr2013201547. [Google Scholar] [CrossRef]
  43. Nutt, C.T.; Bersell, K.R. Syncope Due to Complete Heart Block-A Ticking Time Bomb. JAMA Intern. Med. 2021, 181, 113–114. [Google Scholar] [CrossRef]
  44. Khalil, S.; Padala, S.K.; Hui, C.M.; Steckman, D.A.; Sidhu, M.S.; Torosoff, M.T. Lyme Carditis in the Fast Lane: From Alternating Bundle Branch Block to Asystole in 12 Hours. Conn. Med. 2015, 79, 517–520. [Google Scholar] [PubMed]
  45. Mayer, W.; Kleber, F.X.; Wilske, B.; Preac-Mursic, V.; Maciejewski, W.; Sigl, H.; Holzer, E.; Doering, W. Persistent atrioventricular block in Lyme borreliosis. Klin. Wochenschr. 1990, 68, 431–435. [Google Scholar] [CrossRef] [PubMed]
  46. Jensen, T.B.; Dalsgaard, D.; Johansen, J.B. [Cardiac arrest due to torsades de pointes ventricular tachycardia in a patient with Lyme carditis]. Ugeskr. Laeger 2014, 176, V03140168. (In Danish) [Google Scholar]
  47. Jiménez-Castillo, R.A.; Carrizales-Sepúlveda, E.F.; Vera-Pineda, R.; Herrera-Elizondo, J.L.; García-Sarreón, A.; Reyes-Mondragón, A.L.; Mercado-Domínguez, E.; Marfil-Rivera, L.J. A tick beat in the electrocardiogram: Persistent third degree block as only manifestation of Lyme disease. J. Electrocardiol. 2019, 52, 109–111. [Google Scholar] [CrossRef]
  48. Lórincz, I.; Lakos, A.; Kovács, P.; Várvölgyi, C.; Polgár, P.; Wórum, F. Temporary pacing in complete heart block due to Lyme disease: A case report. Pacing Clin. Electrophysiol. 1989, 12, 1433–1436. [Google Scholar] [CrossRef] [PubMed]
  49. Vlay, S.C.; Dervan, J.P.; Elias, J.; Kane, P.P.; Dattwyler, R. Ventricular tachycardia associated with Lyme carditis. Am. Heart J. 1991, 121, 1558–1560. [Google Scholar] [CrossRef]
  50. Munk, P.S.; Ørn, S.; Larsen, A.I. Lyme carditis: Persistent local delayed enhancement by cardiac magnetic resonance imaging. Int. J. Cardiol. 2007, 115, e108–e110. [Google Scholar] [CrossRef]
  51. Dernedde, S.; Piper, C.; Kühl, U.; Kandolf, R.; Mellwig, K.P.; Schmidt, H.K.; Horstkotte, D. Borrelien-Myokarditis als seltene Differentialdiagnose des akuten Vorderwandinfarktes [The Lyme carditis as a rare differential diagnosis to an anterior myocardial infarction]. Clin. Res. Cardiol. 2002, 91, 1053–1060. (In German) [Google Scholar] [CrossRef]
  52. Isath, A.; Padmanabhan, D.; Naksuk, N.; Kella, D.; Friedman, P. Leadless pacemaker used as long-term temporary therapy in Lyme carditis with high-grade atrioventricular block. Europace 2019, 21, 8. [Google Scholar] [CrossRef]
  53. Timmer, S.A.; Boswijk, D.J.; Kimman, G.P.; Germans, T. A case of reversible third-degree AV block due to Lyme carditis. J. Electrocardiol. 2016, 49, 519–521. [Google Scholar] [CrossRef] [PubMed]
  54. Clinckaert, C.; Bidgoli, S.; Verbeet, T.; Attou, R.; Gottignies, P.; Massaut, J.; Reper, P. Peroperative cardiogenic shock suggesting acute coronary syndrome as initial manifestation of Lyme carditis. J. Clin. Anesth. 2016, 35, 430–433. [Google Scholar] [CrossRef]
  55. van der Zande, J.M.J.; Baarsma, M.E.; Grundeken, M.J.; Verhaar, N.; Kok, W.E.M.; Hovius, J.W. Tweedegraads atrioventriculair blok door lymeziekte [Second-degree atrioventricular block caused by Lyme disease]. Ned. Tijdschr. Geneeskd. 2020, 164, D4214. (In Dutch) [Google Scholar] [PubMed]
  56. Matthiae, D.; Kriatselis, C. Kurzatmigkeit und Herzstolpern bei einem 39-jährigen Patienten [Dyspnea and palpitations in a 39-year-old male patient]. Internist 2021, 62, 871–875. (In German) [Google Scholar] [CrossRef]
  57. Xanthos, T.; Lelovas, P.; Kantsos, H.; Dontas, I.; Perrea, D.; Kouskouni, E. Lyme carditis: Complete atrioventricular dissociation with need for temporary pacing. Hell. J. Cardiol. 2006, 47, 313–316. [Google Scholar]
  58. Rosenfeld, M.E.; Beckerman, B.; Ward, M.F.; Sama, A. Lyme carditis: Complete AV dissociation with episodic asystole presenting as syncope in the emergency department. J. Emerg. Med. 1999, 17, 661–664. [Google Scholar] [CrossRef]
  59. Wenger, N.; Pellaton, C.; Bruchez, P.; Schläpfer, J. Atrial fibrillation, complete atrioventricular block and escape rhythm with bundle-branch block morphologies: An exceptional presentation of Lyme carditis. Int. J. Cardiol. 2012, 160, e12–e14. [Google Scholar] [CrossRef]
  60. Bhattacharya, I.S.; Dweck, M.; Francis, M. Lyme carditis: A reversible cause of complete atrioventricular block. J. R. Coll. Physicians Edinb. 2010, 40, 121–122. [Google Scholar] [CrossRef] [PubMed]
  61. Lo, R.; Menzies, D.J.; Archer, H.; Cohen, T.J. Complete heart block due to lyme carditis. J. Invasive Cardiol. 2003, 15, 367–369. [Google Scholar]
  62. Semmler, D.; Blank, R.; Rupprecht, H. Complete AV block in Lyme carditis: An important differential diagnosis. Clin. Res. Cardiol. 2010, 99, 519–526. [Google Scholar] [CrossRef]
  63. Chauhan, V.; Chauhan, N.; Chauhan, C.G.; Vaid, M. A young healthy male with syncope and complete heart block. Scott. Med. J. 2013, 58, e13–e17. [Google Scholar] [CrossRef] [PubMed]
  64. Franck, H.; Wollschläger, H. Symptomatische Sinusknotendysfunktion bei Lyme-Karditis [Lyme carditis and symptomatic sinus node dysfunction]. Clin. Res. Cardiol. 2003, 92, 1029–1032. (In German) [Google Scholar] [CrossRef]
  65. Brownstein, A.J.; Gautam, S.; Bhatt, P.; Nanna, M. Emergent pacemaker placement in a patient with Lyme carditis-induced complete heart block and ventricular asystole. BMJ Case Rep. 2016, 2016, bcr2016214474. [Google Scholar] [CrossRef] [PubMed]
  66. Prochnau, D.; Kühnemund, J.; Heyne, J.P. Reversible high-grade atrioventricular block with septal myocardial edema in Lyme carditis. Herzschrittmacherther. Elektrophysiol. 2022, 33, 327–329. [Google Scholar] [CrossRef] [PubMed]
  67. Semproni, M.; Rusk, R.; Wuerz, T. Fatal Lyme carditis presenting as fluctuating high-grade atrioventricular block. CMAJ 2020, 192, E574–E577. [Google Scholar] [CrossRef]
  68. Konopka, M.; Kuch, M.; Braksator, W.; Walczak, E.; Jakuciński, M.; Lipowski, D.; Dłużniewski, M. Unclassified cardiomyopathy or Lyme carditis? A three year follow-up. Kardiol. Pol. 2013, 71, 283–285. [Google Scholar] [CrossRef]
  69. Marx, G.E.; Leikauskas, J.; Lindstrom, K.; Mann, E.; Reagan-Steiner, S.; Matkovic, E.; Read, J.S.; Kelso, P.; Kwit, N.A.; Hinckley, A.F.; et al. Fatal Lyme Carditis in New England: Two Case Reports. Ann. Intern. Med. 2020, 172, 222–224. [Google Scholar] [CrossRef]
  70. Kaczmarek, K.A.; Szwabe, K.; Urbanek, I.; Ptaszynski, P.; Strzelecki, A.; Wranicz, J.K.; Cygankiewicz, I. Prevalence of Lyme Carditis in Patients with Atrioventricular Blocks. Int. J. Environ. Res. Public Health 2022, 19, 14893. [Google Scholar] [CrossRef]
  71. Patel, L.D.; Schachne, J.S. Lyme Carditis: A Case Involving the Conduction System and Mitral Valve. Rhode Isl. Med. J. 2017, 100, 17–20. [Google Scholar]
  72. Reznick, J.W.; Braunstein, D.B.; Walsh, R.L.; Smith, C.R.; Wolfson, P.M.; Gierke, L.W.; Gorelkin, L.; Chandler, F.W. Lyme carditis. Electrophysiologic and histopathologic study. Am. J. Med. 1986, 81, 923–927. [Google Scholar] [CrossRef]
  73. Cary, N.R.; Fox, B.; Wright, D.J.; Cutler, S.J.; Shapiro, L.M.; Grace, A.A. Fatal Lyme carditis and endodermal heterotopia of the atrioventricular node. Postgrad. Med. J. 1990, 66, 134–136. [Google Scholar] [CrossRef] [PubMed]
  74. Steere, A.C.; Batsford, W.P.; Weinberg, M.; Alexander, J.; Berger, H.J.; Wolfson, S.; Malawista, S.E. Lyme carditis: Cardiac abnormalities of Lyme disease. Ann. Intern. Med. 1980, 93, 8–16. [Google Scholar] [CrossRef] [PubMed]
  75. Muhammad, S.; Simonelli, R.J. Lyme Carditis: A Case Report and Review of Management. Hosp. Pharm. 2018, 53, 263–265. [Google Scholar] [CrossRef] [PubMed]
  76. Baron, S.; Nepal, S.; Lamichhane, M.; Roseman, H. Unresolved Heart Block in Lyme Carditis: A Case Report. Cureus 2022, 14, e29661. [Google Scholar] [CrossRef] [PubMed]
  77. Büscher, A.; Doldi, F.; Eckardt, L.; Müller, P. Lyme carditis manifesting with sinoatrial exit block: A case report. Eur. Heart J. Case Rep. 2022, 6, ytac022. [Google Scholar] [CrossRef]
  78. Rubin, D.A.; Sorbera, C.; Nikitin, P.; McAllister, A.; Wormser, G.P.; Nadelman, R.B. Prospective evaluation of heart block complicating early Lyme disease. Pacing Clin. Electrophysiol. 1992, 15, 252–255. [Google Scholar] [CrossRef]
  79. Wagner, V.; Zima, E.; Gellér, L.; Merkely, B. Krónikus Lyme-infekcióban észlelt akut atrioventricularis blokk [Acute atrioventricular block in chronic Lyme disease]. Orvosi Hetil. 2010, 151, 1585–1590. (In Hungarian) [Google Scholar] [CrossRef]
  80. Kaczmarek, K.; Deroń, Z.; Janiszewski, T.; Supeł, K.; Ptaszyński, P.; Ruta, J.; Cygankiewicz, I. Całkowity blok przedsionkowo-komorowy jako pierwszy objaw boreliozy: Antybiotykoterapia zamiast wszczepienia rozrusznika serca [Complete atrio-ventricular block as a first symptom of borreliosis: Antibiotic treatment instead of pacemaker implantation]. Kardiol. Pol. 2013, 71, 205–207. (In Polish) [Google Scholar] [CrossRef] [PubMed]
  81. Batalla Celorio, A.; González Camino, F.; Suárez Suárez, E.; Martínez González, J.; Hevia Nava, S.; Barriales Alvarez, V. Bloqueo auriculoventricular completo transitorio en la enfermedad de Lyme [Complete transitory atrioventricular block in Lyme disease]. Rev. Esp. Cardiol. 1999, 52, 529–531. (In Spanish) [Google Scholar] [CrossRef]
  82. Kashou, A.H.; Braiteh, N.; Kashou, H.E. Reversible atrioventricular block and the importance of close follow-up: Two cases of Lyme carditis. J. Cardiol. Cases. 2018, 17, 171–174. [Google Scholar] [CrossRef][Green Version]
  83. Riaz, S.; Garel, A.; Subedi, A.; Mogadam, E.; Weinberg, A. Third-Degree Atrioventricular Block as the Initial Presentation of Lyme Disease. Cureus 2020, 12, e9574. [Google Scholar] [CrossRef] [PubMed]
  84. Legatowicz-Koprowska, M.; Gziut, A.I.; Jezierski, J.; Zabek, J.; Lipowski, D.; Walczak, E.; Prochorec-Sobieszek, M.; Gil, R.J.; Wagner, T. Borelioza serca—Gorzka lekcja czy spóźniony sukces diagnostyczny? Opis przypadku [Lyme carditis—A bitter lesson or a delayed diagnostic success—A case report]. Kardiol. Pol. 2007, 65, 1228–1230. (In Polish) [Google Scholar] [PubMed]
  85. Schwartz, A.M.; Hinckley, A.F.; Mead, P.S.; Hook, S.A.; Kugeler, K.J. Surveillance for lyme disease—United States, 2008–2015. MMWR Surveill. Summ. 2017, 66, 1–12. [Google Scholar] [CrossRef] [PubMed]
  86. Uzomah, U.A.; Rozen, G.; Hosseini, S.M.; Shaqdan, A.; Ledesma, P.A.; Yu, X.; Khaloo, P.; Galvin, J.; Ptaszek, L.M.; Ruskin, J.N. Incidence of carditis and predictors of pacemaker implantation in patients hospitalized with Lyme disease. PLoS ONE 2021, 16, e0259123. [Google Scholar] [CrossRef]
  87. Strle, F.; Wormser, G.P.; Mead, P.; Dhaduvai, K.; Longo, M.V.; Adenikinju, O.; Soman, S.; Tefera, Y.; Maraspin, V.; Lotrič-Furlan, S.; et al. Gender disparity between cutaneous and non-cutaneous manifestations of Lyme borreliosis. PLoS ONE 2013, 8, e64110. [Google Scholar] [CrossRef] [PubMed]
  88. Kugeler, K.J.; Mead, P.S.; Schwartz, A.M.; Hinckley, A.F. Changing Trends in Age and Sex Distributions of Lyme Disease-United States, 1992–2016. Public Health Rep. 2022, 137, 655–659. [Google Scholar] [CrossRef] [PubMed]
  89. Bennet, L.; Stjernberg, L.; Berglund, J. Effect of gender on clinical and epidemiologic features of Lyme borreliosis. Vector Borne Zoonotic Dis. 2007, 7, 34–41. [Google Scholar] [CrossRef]
  90. Moon, K.A.; Pollak, J.S.; Poulsen, M.N.; Heaney, C.D.; Hirsch, A.G.; Schwartz, B.S. Risk factors for Lyme disease stage and manifestation using electronic health records. BMC Infect. Dis. 2021, 21, 1269. [Google Scholar] [CrossRef]
  91. Radesich, C.; Del Mestre, E.; Medo, K.; Vitrella, G.; Manca, P.; Chiatto, M.; Castrichini, M.; Sinagra, G. Lyme Carditis: From Pathophysiology to Clinical Management. Pathogens 2022, 11, 582. [Google Scholar] [CrossRef]
  92. Brown, E.L.; Wooten, R.M.; Johnson, B.J.; Iozzo, R.V.; Smith, A.; Dolan, M.C.; Guo, B.P.; Weis, J.J.; Höök, M. Resistance to Lyme disease in decorin-deficient mice. J. Clin. Investig. 2001, 107, 845–852. [Google Scholar] [CrossRef]
  93. Caine, J.A.; Coburn, J. A short-term Borrelia burgdorferi infection model identifies tissue tropisms and bloodstream survival conferred by adhesion proteins. Infect. Immun. 2015, 83, 3184–3194. [Google Scholar] [CrossRef] [PubMed]
  94. Liu, S.; Yuan, S.; Kongstad, O.; Olsson, S.B. Gender differences in the electrophysiological characteristics of atrioventricular conduction system and their clinical implications. Scand. Cardiovasc. J. 2001, 35, 313–317. [Google Scholar] [CrossRef] [PubMed]
  95. Shan, R.; Ning, Y.; Ma, Y.; Liu, S.; Wu, J.; Fan, X.; Lv, J.; Wang, B.; Li, S.; Li, L. Prevalence and risk factors of atrioventricular block among 15 million Chinese health examination participants in 2018: A nation-wide cross-sectional study. BMC Cardiovasc. Disord. 2021, 21, 289. [Google Scholar] [CrossRef]
  96. Cheng, S.; Keyes, M.J.; Larson, M.G.; McCabe, E.L.; Newton-Cheh, C.; Levy, D.; Benjamin, E.J.; Vasan, R.S.; Wang, T.J. Long-term outcomes in individuals with prolonged PR interval or first-degree atrioventricular block. JAMA 2009, 301, 2571–2577. [Google Scholar] [CrossRef] [PubMed]
  97. National Guideline Centre (UK). Evidence Review for the Management of Lyme Carditis: Lyme Disease: Diagnosis and Management: Evidence Review I. London: National Institute for Health and Care Excellence (NICE); 2018 Apr. (NICE Guideline, No. 95.). Available online: https://www.ncbi.nlm.nih.gov/books/NBK578170/ (accessed on 9 March 2024).
  98. Wamboldt, R.; Wang, C.N.; Miller, J.C.; Enriquez, A.; Yeung, C.; Chacko, S.; Foisy, M.; Baranchuk, A. Pacemaker Explantation in Patients with Lyme Carditis. JACC Case Rep. 2022, 4, 613–616. [Google Scholar] [CrossRef]
  99. Lelovas, P.; Dontas, I.; Bassiakou, E.; Xanthos, T. Cardiac implications of Lyme disease, diagnosis and therapeutic approach. Int. J. Cardiol. 2008, 129, 15–21. [Google Scholar] [CrossRef]
  100. Ehdaie, A.; Cingolani, E.; Shehata, M.; Wang, X.; Curtis, A.B.; Chugh, S.S. Sex Differences in Cardiac Arrhythmias: Clinical and Research Implications. Circ. Arrhythmia Electrophysiol. 2018, 11, e005680. [Google Scholar] [CrossRef]
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