By definition, anemia refers to an absolute reduction of the total number of circulating red blood cells (RBCs). For practical purposes, anemia is considered when one or more of the following are decreased: hemoglobin concentration, hematocrit, or RBC count. This condition is a laboratory finding that signifies the presence of illness or disease; anemia itself should not be considered a diagnosis.
Anemia usually is grouped into three etiologic categories: decreased RBC production, increased RBC destruction, and blood loss. Anemia of chronic illness and anemia of chronic kidney disease (CKD) both fall under the category of decreased RBC production. When the classification of anemia is based on the morphology of the RBCs, both anemia of chronic illness and anemia of CKD usually fall under the classification of normochromic, normocytic anemia.
See Anemia and Chronic Kidney Disease for more complete information on those topics. For patient education information, see Anemia and Kidney Disease.
Anemia of chronic illness traditionally encompassed any inflammatory, infectious, or malignant disease of a long-standing nature. The modern definition includes rheumatoid arthritis, severe trauma, heart disease, diabetes mellitus, and inflammatory bowel disease.[1] Anemia of chronic disease is characterized primarily by the following[2] :
Hepcidin, an endogenous antimicrobial peptide secreted by the liver, has been identified as controlling the level of plasma iron by regulating the intestinal absorption of dietary iron, as well as the release of iron from macrophages and the transfer of iron stored in the hepatocytes. Increase in hepcidin level in the course of inflammatory disease may be a significant mediator of the accompanying anemia.[3, 4, 5]
Another proposed mechanism for anemia of chronic illness involves cytokines, such as interleukins (IL-1 and IL-6) and tumor necrosis factor (TNF-alpha). These are believed to cause the destruction of RBC precursors and decrease the number of erythropoietin receptors on progenitor cells.[6, 7, 8]
The severity of anemia of CKD is directly related to the degree of loss of kidney function, as the kidneys are responsible for approximately 90% of erythropoietin production.[9] Whereas hypoxia in an individual with normally functioning kidneys leads to erythropoietin gene transcription, and hence increased RBC production, CKD results in primary deficiency of erythropoietin production by the interstitial fibroblasts, also known as type I interstitial cells.
In individuals with advanced stages of CKD, the etiology of anemia tends to be multifactorial and include the following:
In general, anemia is more common in women, in particular, those in their childbearing years. In the latter decades of life, anemia tends to occur without any particular sex predilection. However, in patients with chronic kidney disease (CKD), the risk of developing anemia is 30% higher in males than in females. Although males have higher hemoglobin values, they also have higher rates of advanced CKD. The prevalence of anemia is lower in current smokers, which has been attributed to secondary erythrocytosis.
Anemia is common in patients with CKD. The landmark study by Obrador et al showed that among predialysis patients, 68% of those with advanced CKD who required renal replacement therapy had a hematocrit of less than 30%; of those, 51% had a hematocrit less than 28%.[10] Furthermore, although anemia is not as common in earlier stages of CKD, the prevalence of concurrent anemia was 5.2% in patients with stage III disease, rising to 44.1% in those with stage IV disease.[11]
The prevalence of anemia of CKD is also greater in those older than 60 years, as compared with those age 46 to 60 years (see Anemia in Elderly Persons). This is probably secondary to the greater rate of CKD in older individuals, as well as the lower estimated glomerular filtration rates (GFRs) that are associated with aging.
Blacks have not only a 4-fold increased risk of developing CKD relative to whites[12] but also an increased prevalence of anemia.
Although the diseases that lead to anemia, such as malignancy or chronic kidney disease (CKD), may cause obvious symptoms, the anemia itself tends to cause quite nonspecific symptoms. Clinicians must be wary of the tendency to dismiss these symptoms as insignificant—for example, as being due to old age—when in fact they should serve as alarming signals of disease or pathology.
Patients with anemia of chronic disease or CKD may present with the following symptoms:
The following physical findings may be noted:
Other causes of normochromic, normocytic anemia and decreased RBC production (hypoproliferative) should be noted, and conditions involving the bone marrow and secondary conditions involving the liver (eg, cirrhosis) and endocrine system should be assessed.
The following diseases, which primarily involve the bone marrow, should be included in the differential diagnosis:
Bone marrow biopsy can be useful in establishing the etiology of anemia in patients with decreased production of RBCs. The results can confirm whether the marrow is aplastic or hypoplastic; hyperplastic; or infiltrated with nonhematopoietic elements.
The following endocrine disorders should be included in the differential diagnosis:
The following laboratory tests are vital in the evaluation of anemia of chronic illness or chronic kidney disease:
Laboratory tests that may help eliminate other common causes of anemia include the following:
Measurement of serum erythropoietin levels is of no current diagnostic utility in patients with chronic kidney disease, as it is expected to be low. Neither does it influence the starting dose or any adjustment in dosing of erythropoiesis-stimulating agents (ESAs) in such patients
A low reticulocyte count usually points to decreased RBC production as the primary mechanism responsible for anemia, whereas an elevated reticulocyte count points to increased RBC destruction or hemolysis as the most likely cause.
Although decreased RBC production is the main mechanism in both anemia of chronic illness and anemia of chronic kidney disease, oftentimes the anemia is due to a combination of events, including concomitant blood loss. Therefore, a reticulocyte count should always be interpreted with caution.
In general, patients with anemia of chronic illness or of chronic kidney disease can be treated on an outpatient basis. Confounding factors that need to be addressed in both diseases include concomitant blood loss, iron deficiency, or deficiencies of vitamin B12 and/or folic acid.
The preferred initial form of therapy for anemia of chronic illness is treatment of the underlying disease. Erythropoiesis-stimulating agents (ESAs) and blood transfusions are reserved for severe and symptomatic cases. Administration of ESAs is usually best done under the auspices of a hematologist or nephrologist, who may be more informed regarding the latest guidelines on the uses of such agents, as well as for insurance policy coverage.
The preferred initial therapy for anemia of chronic kidney disease (CKD) is the use of erythropoiesis-stimulating agents (ESAs). ESAs available in the United States include epoetin alfa and darbepoetin alfa (Aranesp).
The US Food and Drug Administration (FDA) advises clinicians to consider starting ESA treatment for patients with CKD when the hemoglobin level is less than 10 g/dL, but does not define how far below 10 g/dL would be an appropriate threshold for initiating ESA treatment in an individual patient.[13] Kidney Disease: Improving Global Outcomes (KDOGI) guidelines suggest basing the decision whether to initiate ESA therapy in non–dialysis-dependent CKD patients with a hemoglobin concentration < 10.0 g/dL on the following:
To evaluate response to ESA treatment, the KDIGO guidelines recommend measuring hemoglobin at least monthly during the initiation phase. During the maintenance phase, measurement is recommended at least every 3 months in patients with non–dialysis-dependent CKD patients, and at least monthly in CKD 5D patients.[14]
The optimal level of hemoglobin correction with ESA therapy in patients with anemia of CKD was addressed in two landmark trials published in 2006: the Cardiovascular Risk Reduction by Early Anemia Treatment with Epoetin Beta (CREATE) study[15] and the Correction of Hemoglobin and Outcomes in Renal Insufficiency (CHOIR) study.[16] Both provided evidence against full correction of the hemoglobin concentration (ie, to at least 13 g/dL).
As a result of the CREATE and CHOIR studies, in March 2007, the FDA added a black box warning to the labeling of epoetin alfa and darbepoetin alfa to emphasize that use of these ESAs may increase the risk of serious cardiovascular events and death when they are dosed to achieve a target hemoglobin of greater than 12 g/dL. In November 2007, the FDA stated that "ESAs should be used to maintain a hemoglobin level between 10 g/dL to 12 g/dL. Maintaining higher hemoglobin levels in patients with chronic kidney failure increases the risk for death and for serious cardiovascular reactions such as stroke, heart attack or heart failure."[17]
In 2011, the FDA abandoned the concept of a target range for the hemoglobin level in ESA treatment. Instead, the FDA recommended using the lowest dose of ESA sufficient to reduce the need for red blood cell transfusions for each patient, and adjusting the dose as appropriate.[13]
The 2012 KDIGO guidelines recommend that in general, the hemoglobin level in adult patients with CKD should not be maintained above 11.5 g/dL; some patients may have improvements in quality of life at hemoglobin concentrations above 11.5 g/dL (115 g/l) and will be prepared to accept the risks, but hemoglobin should not exceed 13 g/dL.[14] These goals are associated with lower mortality and less frequent hospitalization rates.
In pediatric CKD patients receiving ESA therapy, the KDIGO guidelines suggest a hemoglobin concentration in the range of 11.0 to 12.0 g/dL. However, National Kidney Foundation–Kidney Disease Outcomes Quality Initiative (NKF-KDOQI) commentary on the guidelines recommends a range of 11-13 g/dL, to avoid the need for multiple dosing adjustments.[14]
A post-hoc analysis of the CHOIR study showed that a high hemoglobin target may be associated with a greater risk of progression of CKD, which is apparently augmented by concurrent smoking.[18] The Trial to Reduce Cardiovascular Events With Aranesp® Therapy (TREAT) resulted in two reports raising concern about the use of target-based strategies in managing anemia of chronic kidney disease. The initial report, conducted in patients with type 2 diabetes melitus, CKD, and moderate anemia, indicated an increased risk of stroke and no reduction in the risk of death or a cardiovascular or renal event with darbepoetin alfa.[19]
The second report noted that when doses of darbepoetin alfa were increased to meet target hemoglobin levels in patients with a poor initial hematopoietic response, the subsequent risk of death or cardiovascular events increased.[20] (See Cardiovascular disease under Complications of Anemia of Chronic Disease and CKD.)
A systematic review and meta-analysis published in 2016 found that ESA treatment of anemia to obtain higher hemoglobin targets did not result in important differences in health-related quality of life in patients with CKD.[21]
The NEPHRODIAB2 Prospective Randomized Controlled Open-Labelled Trial Comparing Effect of Two Haemoglobin levels, which was conducted in patients with type 2 diabetes mellitus and stage 3-4 CKD, found that raising hemoglobin to the normal range (13-14 g/dL) with ESA treatment was safe but did not significantly slow renal function decline and increased treatment cost.[22]
Methoxy polyethylene glycol-epoetin beta (Mircera) is a third-generation, pegylated epoetin (PEG-EPO) beta under the new category of a continuous erythropoietin receptor activator (CERA) that was approved by the FDA in 2007 for the treatment of anemia of CKD. In phase 3 trials, methoxy polyethylene glycol-epoetin beta was given every 2 or 4 weeks, with both regimens achieving hemoglobin targets. Disadvantages of this agent include concerns about possibility of pure red cell aplasia (PRCA). In addition, in 2009, the FDA upheld a 2008 injunction against the marketing of methoxy polyethylene glycol-epoetin beta by Roche due to infringement of several Amgen patents.
In the MIRcerA CLinical Evidence on Renal Survival in CKD patients with anemia (MIRACLE-CKD) study, a multicenter prospective observational study in 2851 non–dialysis-dependent Japanese patients treated with a CERA, kidney outcome was superior in patients who achieved a hemoglobin concentration of ≥11 g/dL by week 12 of therapy. The kidney survival rate in patients in the ≥11 g/dL group was 51.47%, significantly higher than the 37.57% rate in the < 11 g/dL group (P < 0.0001).[23]
Peginesatide (Hematide) is a pegylated, peptidic ESA (also called an erythropoietin mimetic [EPO mimetic]) that binds to the erythropoietin receptor, thereby activating intracellular signaling pathways.[24] This agent was approved in the United States in March 2012 for treatment of anemia of CKD, but was discontinued in February 2013 following postmarketing reports of severe hypersensitivity, including fatalities.[25]
In kidney transplant recipients, the Correction of Anaemia and Progression of Renal Failure on Transplanted Patients found that correction of hemoglobin values to 13 g/dL or higher reduces progression of chronic allograft nephropathy. No increase in cardiovascular events was noted.[26]
The studies on ESA use in anemia of CKD and the FDA actions have been followed by a change in clinical practice. Between 2006 and 2015, CKD patients in the US were increasingly less likely to be treated with ESAs and more likely to receive intravenous iron supplementation and blood transfusions.[27]
Long-term treatment with ESAs has been associated with increased systemic blood pressure and occurrence of seizures; hypertension has been documented to be a common side effect of intravenous use of ESAs. For this reason, blood pressure should always be closely monitored in patients administered with such agents. The postulated mechanism is believed to be an imbalance between endothelin and proendothelin that leads to hyperresponsiveness to the effects of norepinephrine (vasoconstriction) and hyporesponsiveness to the effects of nitric oxide (vasodilatation).
Reports of neutralizing "anti-epoetin antibodies" have been linked to the unusual occurrence of PRCA in European cohorts, but this finding has been attributed to the difference in immunogenicity of the ESAs marketed between the US and Europe.
The working definition of ESA resistance is the requirement for greater than 150 units/kg of ESA at least 3 times per week or the sudden response refractoriness to a previous stable maintenance dose, such that hemoglobin levels fall below target levels.
The most common cause of ESA resistance is iron deficiency. Therefore, it is imperative that iron stores are adequate during ESA treatment. The second most common cause of ESA resistance is a chronic infection/inflammatory state, and such resistance is attributed to inflammatory cytokines (eg, IL-1).
Other less common causes of ESA resistance include hyperparathyroidism (the mechanism appears to be related to bone marrow fibrosis), as well as severe malnutrition.
As noted above, iron deficiency is the most common identifiable cause of ESA resistance. The 2 most important tests to order to assess iron deficiency are transferrin saturation (TSAT) and serum ferritin.
The importance of these tests lies in the fact that even the diagnosis of iron deficiency anemia is not truly straightforward. In anemia of CKD, there is primarily an imbalance between the iron required for erythropoiesis versus the amount released by the reticuloendothelial tissues. This is referred to as functional iron deficiency, which is characterized by a TSAT less than 20% and a ferritin level less than 100 ng/mL. Iron therapy should be considered in patients with CKD whose TSAT is ≤30%, as iron therapy has the potential to increase the hemoglobin concentration or permit a decrease in the ESA dose.[14]
However, clinicians must be aware that ferritin is an acute phase reactant that can be elevated in states of chronic infection or inflammation. Therefore, an elevated ferritin does not necessarily imply iron store adequacy or overload. Current guidelines recommend against use of iron products when ferritin is 500 ng/mL or greater.
At present, various new potential markers of iron status are being developed and experiments are under way to identify every component that may be involved in the mobilization of iron throughout the body. One of these markers is an endogenous antimicrobial peptide, hepcidin. The possible central role of hepcidin in the pathogenesis of anemia of chronic disease has been the subject of numerous publications.[3, 4, 5]
There are some newer agents that hold great promise in the treatment of anemia in chronic illness or chronic kidney disease.[28] Some of these have been approved by the FDA, while others are undergoing clinical trials.
In January 2015, the FDA approved ferric pyrophosphate (Triferic), a soluble iron replacement therapy, which is added to the hemodialysate solution. Approval was based on the PRIME study that showed soluble ferric pyrophosphate to be ESA sparing. Patients (n=103) were randomized to receive ferric pyrophosphate in dialysate or standard dialysate. The researchers found that ferric pyrophosphate was able to maintain hemoglobin and not increase ferritin, while significantly reducing the use of ESAs by 37.1% compared with regular dialysate.[29]
For CKD patients who require iron supplementation, intravenous (IV) iron is generally recommended, as IV iron consistently achieves higher TSAT and ferritin values than oral iron.[14] Examples of intravenous iron replacement therapies include the following:
An alternative to the administration of exogenous ESAs is the use of agents that stimulate endogenous erythropoietin production in renal and nonrenal tissues. One class of investigational agents under development works to stabilize hypoxia-inducible factor (HIF) by inhibiting prolyl hydroxylase (PH) enzymes.[30] HIF is a key regulator of erythropoietic gene expression, iron absorption, energy metabolism, pH, and angiogenesis; as its name indicates, HIF is induced by hypoxia.
HIF-PH inhibitors improve iron mobilization to the bone marrow and induce considerably lower but more consistent blood erythropoietin levels than ESAs. They also promote erythroferrone production by erythroblasts which reduces hepcidin interference, allowing for greater utilization of iron. As well, these agents have the advantage of being administered orally.
Four HIF-PH inhibitors are currently under development: roxadustat, vadadustat, daprodustat, and molidustat.[30] In a phase 2a trial, vadadustat increased hemoglobin levels and improved biomarkers of iron mobilization and utilization in patients with anemia secondary to stage 3 or 4 CKD. Phase 3 trials of vadadustat in non–dialysis-dependent patients are ongoing.[31] . In 2019, the Phase 2 DIALOGUE 1,2 & 4 trials were released. DIALOGUE 1 and 2 showed that over a period of 16 weeks, hemoglobin increase in patients that received molidustat compared to those that received darbepoetin or placebo. DIALOGUE 4 did not show signifcant improvement verses epoetin, but it was a small cohort and hemoglobin levels were maintained within the treatment goals. Further Phase 3 trials are planned with larger cohorts. [38]
Oral iron products may also be helpful for management of iron deficient anemia in patients with CKD who are not on dialysis. Ferrous sulfate is inexpensive, but other oral iron products are also available (eg, carbonyl iron, ferric citrate). Ferric citrate is an oral phosphate binder for the control of serum phosphorus levels in patients with CKD on dialysis. It also approved by the FDA for adults with iron deficiency anemia who have CKD and are not on dialysis.[32]
Hypoxia is the most potent stimulus to the production of erythropoietin by the kidneys. In the healthy individual, erythropoietin exerts its effects in the bone marrow to help in the production of RBCs, thereby improving oxygen concentration in the blood, relieving the hypoxia.
Another complication that commonly occurs in those with chronic kidney disease is that of secondary hyperparathyroidism and the development of renal osteodystrophy. In these patients, the bone marrow tends to be fibrotic and, hence, less responsive to the effects of erythropoietin.
Silverberg et al described the "cardiorenal syndrome," which refers to a vicious cycle whereby decreased kidney function, as seen in chronic kidney disease, leads to decreased erythropoietin production and, thence, anemia.[33] Severe anemia leads to a compensatory left ventricular hypertrophy (LVH). Such compensatory LVH eventually precipitates chronic heart failure (CHF), which causes a decline in blood perfusion to the kidneys, resulting in further kidney damage.
Levin et al estimated that for every 1-g decrease in hemoglobin concentration, there is an increased 6% risk of LVH in patients with chronic kidney disease.[34] Foley et al estimated that such a 1-g decrease in hemoglobin concentration also translated into a 42% increase in left ventricular dilatation in patients with stage 5 chronic kidney disease.[32] Regression of LVH is a known benefit of treatment with ESAs.
The risk of death from cardiovascular disease also increases with advancing age, and the impact of anemia on cardiovascular disease and chronic kidney disease (CKD) in this elderly population cannot be understated. Cardiovascular disease remains the most common cause of mortality in these patients, much higher than in the general population.[35] Anemia has been shown to be an independent risk factor for increased cardiovascular morbidity and mortality.
The Dialysis Outcomes Practice Pattern Study (DOPPS), which involved several countries, showed that as hemoglobin concentrations decreased to less than 11 g/dL, there was a corresponding increase in the rates of hospitalization and mortality in patients with CKD.[36] Ofsthun et al analyzed the databases from Fresenius Medical Care of North America (FMCNA) (selection restricted to patients in the census for 6 consecutive months from July 1, 1998, through June 30, 2000) and showed that the longer it took for these patients with stage 5 CKD resolve their hemoglobin concentrations from less than 11 g/dL, the more dramatic an increase in their mortality hazard ratio.[37] The investigators further added that lower hemoglobin concentrations clearly correlated positively with adverse events in these patients.
In summary, one can derive that maintenance of hemoglobin levels at the recommended target goals translates into decreased LVH, decreased hospitalizations related to cardiovascular disease, and decreased mortality from cardiovascular disease. Moreover, quality of life tends to improve, in the following ways:
This blood film at 1000X magnification demonstrates a leukoerythroblastic blood picture with the presence of precursor cells of the myeloid and erythroid lineage. In addition, anisocytosis, poikilocytosis, and polychromasia can be seen. Courtesy of U. Woermann, MD, Division of Instructional Media, Institute for Medical Education, University of Bern, Switzerland.
Peripheral smear from a patient with agnogenic myeloid metaplasia. This image shows the presence of teardrop red blood cells (RBCs) and a leukoerythroblastic picture with the presence of nucleated RBC precursors and immature myeloid cells. Courtesy of Wei Wang, MD, and John Lazarchick, MD; Department of Pathology, Medical University of South Carolina.
This blood film at 1000X magnification demonstrates a leukoerythroblastic blood picture with the presence of precursor cells of the myeloid and erythroid lineage. In addition, anisocytosis, poikilocytosis, and polychromasia can be seen. Courtesy of U. Woermann, MD, Division of Instructional Media, Institute for Medical Education, University of Bern, Switzerland.
Peripheral smear from a patient with agnogenic myeloid metaplasia. This image shows the presence of teardrop red blood cells (RBCs) and a leukoerythroblastic picture with the presence of nucleated RBC precursors and immature myeloid cells. Courtesy of Wei Wang, MD, and John Lazarchick, MD; Department of Pathology, Medical University of South Carolina.