Genetic variation in proinflammatory and anti-inflammatory cytokine production in multiple organ dysfunction syndrome

Crit Care Med. 2002 Oct;30(10):2216-21. doi: 10.1097/00003246-200210000-00007.

Abstract

Objectives: The objectives of this study were to examine the prevalence of genetic variation for cytokine production (tumor necrosis factor [TNF]-alpha, interleukin-10, transforming growth factor-beta1) in patients with multiple organ dysfunction syndrome, to measure circulating cytokine levels and relate these to genotype, and to identify the relationship between genetic variation and outcome.

Design: Prospective analysis.

Setting: Intensive care unit of a university teaching hospital.

Patients: Eighty-eight critically ill patients with multiple organ dysfunction syndrome.

Measurements and main results: The frequency of the different interleukin-10 genotypes (corresponding to high, intermediate, and low interleukin-10 production ) were significantly different between controls and multiple organ dysfunction syndrome patients. High interleukin-10 producers were under-represented in the multiple organ dysfunction syndrome group: This genotype occurred in 30% of controls but in only 6% of patients ( <.001). There was no relationship between interleukin-10 genotype and mortality. The frequency of TNF-alpha genotypes was also significantly different between patients and controls. Intermediate TNF-alpha producers were under-represented (5.7% vs. 23%) and high TNF-alpha producers over-represented (35.2% vs. 16%) in the patient group (p <.001). TNF-alpha genotype was not related to mortality. The distribution of TNF-beta genotypes (homozygous B1, homozygous B2, and heterozygotes) was also different between controls and patients (p =.008). The B2/B2 genotype (associated with high TNF-alpha production) tended to occur less frequently in the intensive care unit population (31% vs. 50%) and was associated with a higher mortality rate than either the B1/B1 or B1/B2 genotypes (48% vs. 11% and 33% respectively, p=.115). The combination of proinflammatory (TNF-alpha/TNF-beta) and anti-inflammatory (interleukin-10/transforming growth factor-beta1) cytokine genotypes was associated with prolonged patient survival time. Patients predisposed to produce a balanced cytokine response (e.g., intermediate interleukin-10/TNF-alpha producers) demonstrated the longest survival times, although overall mortality was no different.

Conclusion: A genetic predisposition to high interleukin-10 production or intermediate TNF-alpha production may be protective of admission to the intensive care unit, although once admitted, any protection provided by these genotypes seems to be lost. TNF-beta genotype conferred no advantage to patients with multiple organ dysfunction syndrome, the TNFB2 allele being associated with increased mortality. The combination of proinflammatory and anti-inflammatory cytokine genotypes supports the idea that a balanced cytokine response is favorable and was associated with prolonged patient survival time.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Aged
  • Aged, 80 and over
  • Cytokines / biosynthesis*
  • Cytokines / genetics*
  • Female
  • Genetic Predisposition to Disease
  • Genetic Variation*
  • Genotype
  • Humans
  • Interleukin-10 / genetics
  • Interleukin-10 / metabolism
  • Male
  • Middle Aged
  • Multiple Organ Failure / etiology
  • Multiple Organ Failure / genetics*
  • Multiple Organ Failure / metabolism
  • Polymerase Chain Reaction
  • Polymorphism, Genetic
  • Prospective Studies
  • Systemic Inflammatory Response Syndrome / complications
  • Systemic Inflammatory Response Syndrome / genetics
  • Systemic Inflammatory Response Syndrome / metabolism
  • Transforming Growth Factor beta / biosynthesis
  • Transforming Growth Factor beta / genetics
  • Transforming Growth Factor beta1
  • Tumor Necrosis Factor-alpha / biosynthesis
  • Tumor Necrosis Factor-alpha / genetics

Substances

  • Cytokines
  • TGFB1 protein, human
  • Transforming Growth Factor beta
  • Transforming Growth Factor beta1
  • Tumor Necrosis Factor-alpha
  • Interleukin-10