International Journal of Laboratory Hematology

The Official journal of the International Society for Laboratory Hematology

REVIEW INTERNAT IONAL JOURNAL OF LABORATO RY HEMATO LOGY

Reporting and grading of abnormal red blood cell morphology

B. T. CONSTANTINO

Mississauga, ON, Canada S U M M A RY

Correspondence: In spite of the continual standardization of test result formats, the

Benie T. Constantino, 5591 improvements of laboratory technologies, publications of reference
Haddon Hall Road, Mississauga,
ON L5M 5G4, Canada.
guidelines, and the advancements in hematology analyzers, the
E-mail: btconstantino@hotmail. methods of reporting or grading abnormal red blood cell morphol-
com ogy still vary among laboratories everywhere. This article describes
the methods or systems of reporting abnormal red cell morphology
doi:10.1111/ijlh.12215 and the conditions associated with the abnormalities.

Received 3 December 2013;

accepted for publication 24
February 2014

Keywords
Red blood cell morphology,
grading system, standardization

blood film (PBF). For example, one reference textbook

INTRODUCTION
[11] grades elliptocytes/ovalocytes as slight (2–5%),
More than four decades ago, equipped with the earliest moderate (6–15%), and marked (>16%) compared to
automated hematology Coulter Counter Model S to other reference [4] which rates the same abnormality as
count blood cells and to determine the size (MCV) and 1+ (6–10%), 2+ (10–25%), 3+ (25–50%), and 4+
hypochromia (MCH) of the red cells, an attempt was (>50%). Moreover, other laboratory [9] reports the
made to promote uniformity (standardization) in grad- same red cell changes as + (1–5%), ++ (5–25%), and +++
ing hematologic abnormalities [1]. In spite of this, and (>25%).
the continual standardization of test result formats, pub- Undoubtedly, the lack of a uniform grading system
lications of reference guidelines, the improvements of can lead to inconsistent and confusing results as
laboratory (lab) technologies, and the advancements in reflected in these examples. The grading system and
hematology instrumentations [1–7], the methods of grading level vary; three types of grading systems can
reporting or grading abnormal red blood cell morphol- be observed. The grading level shows two varying for-
ogy (RBC-M) still vary among laboratories everywhere mats: one with three levels and the other, four grade
[8, 9]. This is probably because some reference textbooks levels format. The grading level differences, however,
and laboratories have different grading systems and are statistically significant, although they may not be
grading levels of reporting results [1–4, 10]. The grading clinically.
system represents the method for reporting results, Currently, there are two systems or methods of
whereas the grading level indicates the relative percent- grading RBC-M [2–4, 11]. While some laboratories
age (%) or fraction of abnormal cells in the peripheral report or grade the degree of morphologic abnormalities

© 2014 John Wiley & Sons Ltd, Int. Jnl. Lab. Hem. 2015, 37, 1–7 1
2 B. T. CONSTANTINO | REPORTING AND GRADING OF ABNORMAL RBC MORPHOLOGY

numerically (plus) from 1+ to 4+, others used descrip- thermal injury. Since different types of abnormal red
tive terms, such as slight (few), moderate, or marked, cells arise by different etiologic processes, the diagno-
and/or ‘rare’ or ‘occasional’. At times, others just sis of a disease can be made by assessing PBF in con-
report the abnormal morphologic findings as ‘present’. junction with clinical and other automated laboratory
Because there is no evidence that either system is data such as numerical and graphical data [22, 23].
better than the other, the author emphasizes that The interpretation of the reference guide (Table 1)
maintaining consistency within a chosen system is a shown for illustration of the grading system of RBC-M
good laboratory practice and is also recommended by is self-explanatory. This simplified reference guide is
laboratory accrediting services. For the grading system presented in a two-system or three-graded format: 1+
(numerical or descriptive) to be clinically meaningful, or slight, 2+ or moderate, and 3+ or marked. Notice
it should be clearly defined by their corresponding there is no 4+, ‘rare’, or ‘occasional’ comment. The
grading levels and be understood by the technologists clinical interpretation or significance of grade 3+ and
and clinicians. Tables 1 and 2 show the condensed 4+ is almost the same – markedly increased, thus it is
reference guide for grading abnormal RBC-M and practical to merge them into one grade and simply
the conditions associated with different grade levels, reports 3+. The ‘rare’ or ‘occasional’ comment is
respectively. These tables are handy and can be meaningless or redundant. Although the grading of
easily used as a reference guide when performing abnormal results looks simple, the grading itself is
microscopy. complicated as it requires experience and expertise to
This article describes the grading systems or meth- identify and distinguish many abnormal cells.
ods of reporting RBC-M and the conditions associated Specific details on some morphological disorders
with the abnormalities, and explains the reasons for such as burr cells, Howell-Jolly bodies, stomatocytes,
standardizing the method of reporting RBC-M nation- teardrops, agglutination, microcytes, sickle cells and
ally or internationally. others and how to examine and grade abnormal RBC-
M and their mechanisms of formation are discussed
elsewhere [see Refs. 4, 8, 13–18]. As a rough guide,
A N A LYS I S A N D I N T E R P R E TAT I O N S O F
the size of the nucleus of normal lymphocyte and
R E S U LT S
normal red cell is almost the same. Any deviation in
The reporting or grading of abnormal RBC-M is an size, shape, and staining properties represents abnor-
essential component of hematology process and can mal red cells.
serve as an invaluable aid in the diagnosis of a variety Schistocytes/fragments are small pieces (fragments)
of disorders (Tables 1 and 2). The grading of RBC-M of red cells with irregular outline characterized by tri-
represents the magnitude or degree of morphological angular, crescentic, and half-moon-shaped cells. They
changes brought about by intrinsic or extrinsic factors are seen especially in syndromes of microangiopathic
involved in the pathogenesis of a specific disease (ane- hemolytic anemia such as thrombotic thrombocytope-
mia) [21]. Some specific red cell aberrations including nic purpura and hemolytic uremic syndrome. The
spherocytes, target cells, elliptocytes, macrocytes, and presence of <1% fragments in the PBF is considered
hypochromic microcytes are indicative of a particular normal. However, the finding of >1% schistocytes
disorder. They appear in varying percentages or with accompanying low platelets and absence of addi-
fractions of cells at certain stages of many anemias tional severe RBC morphological abnormalities may
(disorders), thus they may not be regarded as signify an underlying pathological disorder and should
distinguishing features of a single disease. However, never be ignored. Put simply, for the schistocyte count
they are significant for they reflect common pathways to be considered clinically meaningful, it should repre-
of red cell destruction, altered function and structure, sent the main morphological alteration in the PBF
or abnormal production and metabolism. For exam- [24]. Some hematology analyzers are capable of
ple, spherocytes (decreased surface membrane redun- detecting and producing a red cell fragments count,
dancy) may be seen in varying percentages in patients the presence of which may be reflected as a high
with autoimmune hemolytic anemia, microangiopath- takeoff on the left baseline side of the histogram curve
ic hemolytic anemia, hemoglobinopathies, or after [23]. The count, however, must be correlated with

© 2014 John Wiley & Sons Ltd, Int. Jnl. Lab. Hem. 2015, 37, 1–7
 B. T. CONSTANTINO | REPORTING AND GRADING OF ABNORMAL RBC MORPHOLOGY 3

Table 1. Reference guide for grading red blood cell morphology [1–4, 9–12]

Red blood cells (cell type) Normal (nonspecific) 1+ (%) (Slight/few) 2+ (%) (Moderate) 3+ (%) (Marked)

Hypochromasia 5–15 16–40 >40

(MCH – pg) 27–34 pg 22–26 18–21 <18
Polychromasia 3–5 6–20 >20
Microcytes (MCV – fL) 80–99 fL 70–79 60–69 <60
Macrocytes (MCV – fL) 80–99 fL 100–110 111–125 >125
Schistocytes (Fragments) 1–5 6–15 >15
Elliptocytes/Ovalocytes 6–20 21–50 >50
Rouleaux 11–50 >50
Spherocytes 1–5 6–20 >20
Target cells 5–10 11–25 >25
Acanthocytes 1–10 11–30 >30
Burr cells 30% Report if present
Irregularly contracted
red cells (Bite cells) 4%
Stomatocytes 30%
Teardrop cells* 4%
Agglutination
Dimorphic red cells
Dual population
Howell-Jolly bodies
Oval macrocytes
Pappenheimer bodies
Parasites
Sickle cells

pg, picogram; fL, femtoliter.

*Teardrop cells accompanied by NRBCs can be reported even <4%.

the morphologic grading level. Although identification Rouleaux are red cell aggregates resembling a
of RBC fragments apparently seems straightforward, stack of coins. They are caused by an increase of
there is no precise consensus definition of schisto- asymmetric macromolecules, such as globulin and
cytes, hence the variability in the morphological inter- fibrinogen. Associated clinical conditions include
pretation and reporting between laboratories and multiple myeloma, acute infection/inflammation, and
observers [25]. macroglobulinemia. These alterations will result in an
Elliptocytes/ovalocytes are cells with oval or ellipti- increased ESR and a moderate-to-marked rouleaux in
cal shapes. Often times, these terms are interchange- the PBF [28]. Slight rouleaux formation is of normal
able. In normal subjects, <15% of red cells may be occurrence especially in patients with low red cell
slightly oval or elliptical, whereas in patients with counts because of the relative fibrinogenemia; so in
hereditary elliptocytosis (or sometimes in thalassemia this case, their slight presence be reported as nonspe-
trait), >25–75% of red cells are elliptical [26]. cific.
Although elliptical cells of around 15% have been Spherocytes are small dense spheroidal red cells
considered as normal, recent studies indicate no with normal volume enclosed within greatly dimin-
higher than 5% is normal [27]. ished surface area, hence the decreased surface–volume
Elliptical cells are also present in patients with dys- ratio and the decreased deformability and filterability.
erythropoiesis, such as megaloblastic anemia and They are usually absent in the blood films of healthy
severe iron deficiency. Infiltrative disorders of the bone individuals. It is useful to distinguish red cell variations
marrow such as in metastatic carcinoma are associated between hereditary spherocytosis (HS) and acquired
with formation of elliptocytes and teardrop cells. one. In HS, large numbers of almost the same size of

© 2014 John Wiley & Sons Ltd, Int. Jnl. Lab. Hem. 2015, 37, 1–7
4 B. T. CONSTANTINO | REPORTING AND GRADING OF ABNORMAL RBC MORPHOLOGY

Table 2. Conditions associated with abnormal RBC morphology based on their grading [4, 8, 13–20]

Cell type Slight* (1+) to Moderate* (2+) Marked 3+

Schistocytes Hypersplenism Thalassemia major Microangiopathic hemolytic

(Fragments) Myeloid metaplasia Severe burns anemia
Megaloblastic anemia Mechanical hemolytic anemia Disseminated intravascular
Iron deficiency anemia (prosthetic heart valve) coagulation
Cancer cytotoxic Hereditary pyropoikilocytosis Vasculitis syndromes
chemotherapy Metastatic carcinoma
Enzymes deficiencies Chronic renal failure
Premature infants Unstable hemoglobin
Renal graft rejection Malignant hypertension
Infection
Severe sepsis
Myelofibrosis
Elliptocytes/ Megaloblastic anemia Hereditary pyropoikilocytosis Hereditary elliptocytes
Ovalocytes Severe iron deficiency Myelofibrosis
anemia Hemoglobin C trait
Sickle cell anemia South East Asian
Hypersplenic state ovalocytosis
Metastatic carcinoma
Sideroblastic state
Thalassemia trait
Rouleaux Hyperfibrinogenemia Multiple myeloma
Hyperglobulinemia Waldenstrom’s
Chronic inflammatory Disorders Macroglobulinemia
Spherocytes Post splenectomy Microangiopathic hemolytic anemia Hereditary spherocytosis
Liver disease Hereditary pyropoikilocytosis Autoimmune hemolytic
Hemoglobinopathies Severe burns anemia
Older population of Hypersplenism Hemolytic transfusion
transfused red cells Clostridium perfringens reaction
Heart valve prosthesis ABO incompatibility
Heinz body hemolytic
anemia
Premature infants
Myelofibrosis
Target cells Newborn/Premature infants A-C and A-S trait C-C disease
Thalassemia minor Thalassemia major S-C disease
Postsplenectomy Sickle cell anemia Hb. E disease
Severe iron deficiency Sickle-thalassemia Liver disease
Acanthocytes Newborn/Old age Renal disease Abetalipoproteinemia
Severe burns Postsplenectomy Alcoholic liver disease
Sideroblastic anemia Neonatal or acquired hepatitis
Enzymes deficiencies Uremia
Anorexia nervosa/ McLeod phenotype
starvation Myxedema
Vitamin E deficiency
Hypothyroidism

*Note the grading level of some conditions may vary from slight to moderate and even to marked depending on the
severity, intensity, and duration of the disorders.

spherocytes are present without other abnormal cells may be high normal or increased [29], whereas, in
other than the signs of erythropoietic regeneration. The acquired one, small to large numbers of spherocytes in
automated MCV is within normal range, but the MCHC varying sizes are present together with other red cell

© 2014 John Wiley & Sons Ltd, Int. Jnl. Lab. Hem. 2015, 37, 1–7
 B. T. CONSTANTINO | REPORTING AND GRADING OF ABNORMAL RBC MORPHOLOGY 5

abnormalities as seen in pyropoikilocytosis, immune review of patient’s complete blood count and periph-
hemolytic anemia, or hemoglobinopathies. The MCHC eral blood film (PBF) remains the mainstay of hema-
is usually normal. tologic diagnosis. In other words, the automated
Target cells (TC) are the morphologic expression of findings of microcytic or fragmented red cells have yet
increased surface-to-volume ratio which signify either to be verified microscopically.
excessive surface membrane formation or excessive Note, however, that because of the tremendous
loss of volume or hemoglobin (Hb) content of the red improvements in both the precision and accuracy as well
cells. The red cells may look like a ‘bull’s-eye’, hence as flagging of many abnormal red cells by modern hema-
the name target. TC may be microcytic, normocytic, tology analyzers, automated results including slightly
or macrocytic. Major causes of microcytic TC or hypochromic microcytic red cells and slightly reduced
decreased Hb content include severe iron deficiency platelets can be autoreleased. Depending on laboratory
anemia, thalassemia trait, and certain hemoglobinopa- protocol, a qualifying comment can be affixed to the
thies such as Hb C and Hb E. Some causes of normal results, such as ‘microcytosis, consider iron deficiency
TC include sickle cell anemia and sickle cell thalasse- and/or thalassemia’. This modification allows technolo-
mia. Macrocytic TC are uncommon, but may be gist to focus more on significant abnormalities, resulting
observed in patients with liver disease, postsplenecto- in reduce overall workload and operating costs, decrease
my, and in premature infants. It must be emphasized, turnaround time, and increase productivity in the labo-
however, that TC may be an artifact of blood film ratory. The ability to microscopically verify or grade
preparation due to slow air drying or over anticoagu- other abnormal RBC-M and use technology to help sort
lation of blood sample. through that process is inherently subjective and thus
Acanthocytes are spheroidal dense cells with multiple may be prone to variation as it is influenced by the skill
unevenly distributed spikes of varying length. The pres- and experience of the technologists. A simpler and more
ence of few acanthocytes is significant, particularly consistent reporting/grading format may not only be a
when it is associated with target cells and Howell-Jolly cost-effective way but also a more systematic and effi-
bodies, as it may indicate asplenia [12]. In some asplenic cient laboratory process that improves the level of repro-
cases, an unusual increased of lymphocyte counts ducibility between observers in the laboratory and thus
resembling chronic lymphocytic leukemia may be may lessen or preclude variability in reporting results.
observed. The purpose of a red cell morphology report is to con-
In all these examples, the grading level of red cell vey to the physician the abnormal findings in a legible,
abnormalities depends on the relative fraction or per- comprehensible, and concise manner that will enable
centage of red blood cells with abnormality and/or the judgment on the clinical significance of the abnormali-
relative degree of abnormality in individual cells seen ties. Thus, the reporting or grading of abnormal RBC-M
in the PBF [4]. Their degree or rate of variability, how- should be based on clinical significance and age of the
ever, is influenced by the severity, intensity, and dura- patients. Some morphologic alterations, including sickle
tion of the illness, rapidity and extent or stage of the cells, fragments, oval macrocytes, Howell-Jolly bodies,
(hemolytic) process, and/or whether the abnormality is acanthocytes, and spherocytes, are quite specific and sig-
due to intracellular or extracellular causes such in the nificant even when they occur in small numbers. In
RES or in the spleen. When reporting hematologic small numbers, other morphologic variations, including
abnormalities, the total morphologic picture must be target cells, ovalocytes/elliptocytes, round macrocytes,
presented in conjunction with automated numerical teardrop cells, polychromasia, stomatocytes, and burr
and graphical pictures so that the physicians can relate cells, are ambiguous and of little diagnostic significance.
this picture to the clinical picture of the patient for They become significant only when they appear in con-
better diagnosis and health care. siderable numbers (Table 2). Moreover, there are some
other red cell abnormalities, such as dimorphic red cells,
dual population, or agglutination, which do not need
COMMENTS
to be quantified and should be reported merely as
Despite the modern hematology instrumentation and ‘present’. This quantitative descriptor ‘present’ can be
technical advancement in the clinical laboratory, used only if the abnormal red cells in questions meet the

© 2014 John Wiley & Sons Ltd, Int. Jnl. Lab. Hem. 2015, 37, 1–7
6 B. T. CONSTANTINO | REPORTING AND GRADING OF ABNORMAL RBC MORPHOLOGY

necessary numbers required (Table 2) or as per labora- anemia or the fragmented red cells of hemolytic anemia
tory protocol so as to avoid misinterpretation of results can have the same morphological alterations seen
by the clinicians. virtually in all patients whether in the Philippines, in
Be aware that the morphological characteristics of Canada, or in other countries.
the newborn’s erythrocytes differ considerably from It is undeniable that the clinical laboratory is experi-
their counterpart in older infants, children, and adults encing globalization by virtue of ever faster travel,
[30]. Children and adult may show up to 1% red cell improve laboratory technologies and communications
fragments, whereas full-term infants may show 3% and thus the need to harmonize and standardize clini-
fragments, some polychromasia, spherocytes, tear- cal laboratory reporting of results has increased in
drops, acanthocytes, target cells, nucleated red blood importance. The clinical implications of such globaliza-
cells, or Howell-Jolly bodies. Premature infants may tion include the comparability of results so that a
even show increased red cell abnormalities. Because of patient and/or his physician may compare results
this, the grading of abnormal RBC-M should take into obtained in one region or country to another results
consideration these distinctions to ensure an accurate obtained in a different location. For example in report-
interpretation of results and their use in patient care. ing spherocytes, one laboratory location may grade
Ideally, standardized definitions and reporting format result of 9% spherocytic cells as 1+ or slight [10] while
should be employed within all laboratories. Although others report or grade the same result of 9% as ++ or
standardization would take much time and energy to moderate [9] and 3+ or marked [4]. Without standardi-
conform laboratories throughout the world to this sys- zation, the differences between two results may be con-
tem, it would be more pragmatic and beneficial if all lab- fusing which may lead to inconsistent diagnostic
oratories in one country in particular and the whole interpretation, thereby affecting treatment and clinical
world used a uniform or standardized method of report- outcome. This lack of standardization and the virtual
ing abnormal RBC-M. The benefits of standardization similarities of abnormal RBC morphological findings
are enormous including reducing costs (cost-produc- everywhere as well as the benefits of standardization
tive), increasing efficiency, protecting the health of the further reinforce the importance of standardization of
patients, improving the quality of health care, and pro- reporting abnormal RBC-M results in all laboratories.
moting the global harmonization of medical reporting of In view of the foregoing statements, therefore, the
results – so you can be sure your clinical laboratory standardization of reporting abnormal RBC-M is
result interpretations will be same everywhere. essential and can be accomplished not only within a
Everywhere in the world you will find that the laboratory, but also in laboratories within a country
same morphological alterations in size, shape, color, and internationally. In addition, with standardization
and staining properties of the red cells, or even the and increased sophistication of hematology instru-
pathophysiologic mechanisms in their formations can mentation, the evaluation of red cell morphology is
be observed – there is no racial barrier. Simply put, the becoming more systematic and consistent among labo-
hypochromic microcytic red cells of iron deficiency ratory professionals.

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