Introduction: Large-scale genetic studies have implicated complement factor H (CFH) in rheumatic heart disease (RHD). Together with the neighbouring factor H-related proteins (FHRs), CFH plays a critical role in complement regulation and has been linked to several complement-mediated diseases. We therefore sought to define their relative contribution to the pathogenesis of acute rheumatic fever (ARF) and RHD, which remains uncertain.
Methods: We studied a cohort of 240 children or adults with ARF or RHD and 248 healthy or alternate diagnosis controls recruited in Pakistan, and a previously reported cohort of 49 children with ARF or RHD and 99 healthy or alternate diagnosis controls recruited in Uganda. We characterised host genetic variation using a combination of targeted and genome-wide genotyping in addition to short and long-read sequencing, and measured circulating CFH and FHRs using previously developed highly specific immunoassays.
Results: Across these studies, the CFH signal replicated, localising to a known deletion of CFHR3 and CFHR1 with minor allele frequency 30-33% that conferred a 1.2-fold lower risk of ARF and RHD combined (P<0.005). Additionally, this protective deletion was highly correlated with not only reduced circulating FHR3 and FHR1 (P<10-10), but also higher circulating CFH (P<10-5), even during the inflammatory state of ARF (Percentage change per copy of CFHR3/CFHR1 deletion: FHR3 -49.6%, 95% CI -35.2 to -63.9%, P<10-10; CFH +11.4%, 95% CI +6.6 to +16.2%, P<10-5).
Conclusion: Genetic variation in the CFH locus drives risk of ARF and RHD by altering levels of key complement regulators, providing an invaluable new therapeutic target.