Clinical "cytokine storm" as revealed by monocyte intracellular flow cytometry: correlation of tumor necrosis factor alpha with severe gut graft-versus-host disease

Clin Gastroenterol Hepatol. 2004 Mar;2(3):237-45. doi: 10.1016/s1542-3565(04)00011-4.

Abstract

Background & aims: Gut graft-versus-host disease (GVHD) contributes significantly to lethality after allogeneic hematopoietic stem-cell transplantation (HSCT). In murine models, macrophage secretion of interleukin 1alpha (IL-1alpha) and tumor necrosis factor alpha (TNF-alpha) contributes to gut GVHD pathogenesis. To help characterize whether human gut GVHD has similar biological characteristics, monocyte IL-1alpha and TNF-alpha production were evaluated after HSCT.

Methods: Patients with refractory hematologic malignancy (n = 17) underwent reduced-intensity conditioning, HLA-matched sibling HSCT, and cyclosporine A GVHD prophylaxis. After HSCT, monocyte IL-1alpha and TNF-alpha levels were measured using intracellular flow cytometry (IC-FCM), and results were correlated with clinical GVHD.

Results: Incidences of acute GVHD were none (n = 3), grades I-II (n = 9), or grades III-IV (n = 5; each case with stage 2-3 gut GVHD). Posttransplantation monocyte IL-1alpha production (percentage of CD14(+)IL-1(+) cells) increased significantly from 8.7% +/- 3.7% (week 2) to 40.3% +/- 7.3% (week 4; P = 0.0065) and was not associated with GVHD severity (P = 1.00). Conversely, increases in monocyte TNF-alpha were quantitatively reduced and temporally delayed, from 0.6% +/- 0.2% (week 2) to 3.6% +/- 1.4% (week 6; P = 0.076). Most importantly, elevation of monocyte TNF-alpha level correlated with increased gut GVHD severity (P = 0.0041); increases in monocyte TNF-alpha levels typically preceded the onset of gut GVHD symptoms.

Conclusions: Human gut GVHD after reduced-intensity allogeneic HSCT is associated with monocyte cytokine secretion initially involving IL-1alpha, followed by TNF-alpha. Serial measurement of monocyte cytokines, in particular, TNF-alpha, by IC-FCM may represent a noninvasive method for GVHD monitoring, potentially allowing the identification of patients appropriate for early-intervention strategies.

MeSH terms

  • Adult
  • Aged
  • Biomarkers, Tumor / blood
  • Cell Movement
  • Cytokines / analysis
  • Cytokines / biosynthesis*
  • Disease Progression
  • Female
  • Flow Cytometry
  • Graft vs Host Disease / diagnosis*
  • Graft vs Host Disease / mortality
  • Graft vs Host Disease / physiopathology
  • Hematologic Neoplasms / diagnosis
  • Hematologic Neoplasms / therapy*
  • Hematopoietic Stem Cell Transplantation / adverse effects*
  • Hematopoietic Stem Cell Transplantation / methods
  • Humans
  • Interleukin-1 / analysis
  • Interleukin-1 / biosynthesis
  • Male
  • Middle Aged
  • Monocytes
  • Prospective Studies
  • Sensitivity and Specificity
  • Severity of Illness Index
  • Survival Analysis
  • Transplantation, Homologous
  • Tumor Necrosis Factor-alpha / analysis
  • Tumor Necrosis Factor-alpha / biosynthesis

Substances

  • Biomarkers, Tumor
  • Cytokines
  • Interleukin-1
  • Tumor Necrosis Factor-alpha