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Originally published online as doi:10.1189/jlb.0503245 on October 13, 2003

Published online before print October 13, 2003
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(Journal of Leukocyte Biology. 2004;75:157-162.)
© 2004 by Society for Leukocyte Biology

Physiologic variations in granulocytic surface antigen expression: impact of age, gender, pregnancy, race, and stress

M. Tarek Elghetany*,1 and Francis Lacombe{dagger}

* Division of Hematopathology, Department of Pathology, University of Texas Medical Branch, Galveston; and
{dagger} Laboratory Hematology, Hospital Haut-Lévêque, CHU Bordeaux, France

1 Correspondence: Department of Pathology, University of Texas Medical Branch, 301 University Blvd., Galveston, TX 77555-0743. E-mail: melgheta{at}utmb.edu


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 IMPACT OF PHYSIOLOGIC CONDITIONS...
 BIOLOGICAL CORRELATION
 CRITICAL ASSESSMENT OF RESULT...
 CONCLUSION
 REFERENCES
 
There is a growing interest in the use of granulocytic surface markers for the diagnosis of some inherited and acquired disorders, such as Shwachman-Diamond syndrome and myelodysplastic syndromes. Understanding the impact of physiologic factors, such as age, gender, pregnancy, race, and stress on granulocytic surface markers is essential for appropriate interpretation of results. Some surface markers show marked variations at the very early and the very late stages in life. Fetal granulocytes tend to have a lower expression of CD11b, CD11c, CD18, and CD32. Term neonatal granulocytes are frequently associated with a lower expression of CD10, CD11b, CD13, CD33, and CD62L and a higher expression of CD55 and CD64. Elderly individuals have shown a higher expression of CD64. Pregnancy is associated with temporary changes in granulocytic surface markers, such as a lower expression of CD16 and a higher CD64, partially mimicking an inflammatory response. Stress also has an impact on some surface markers, particularly adhesion molecules, such as CD62L and CD54. These factors need to be taken in consideration for the optimal interpretation of granulocytic surface marker studies.

Key Words: flow cytometry • neonates • aging


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
IMPACT OF PHYSIOLOGIC CONDITIONS...
 BIOLOGICAL CORRELATION
 CRITICAL ASSESSMENT OF RESULT...
 CONCLUSION
 REFERENCES
 
The study of surface antigens of granulocytes has received less attention compared with other hematopoietic cells. Earlier studies of granulocytic surface antigens have focused on the diagnosis of certain inherited disorders, such as leukocyte adhesion molecule deficiency (LAD) [1 ]. Recently, there has been a growing interest in the use of surface-antigen studies to support the diagnosis of other inherited and acquired bone marrow disorders, such as paroxysmal nocturnal hemoglobinuria, myelodysplastic syndromes, and Shwachman-Diamond syndrome [2 3 4 5 ]. The lack of understanding of the impact of physiologic variations on granulocytic surface antigens may potentially pose a diagnostic pitfall. In this report, we review the literature regarding the impact of various physiologic conditions on granulocytic surface markers and provide a critical assessment and explanation of result variability. Table 1 provides a concise summary of the results of literature reports.


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  		Table 1. Changes in the Expression of Granulocytic Surface Markers in Different Physiologic Groups Compared with Healthy Adults

 

   IMPACT OF PHYSIOLOGIC CONDITIONS ON SURFACE MARKERS
TOP
 ABSTRACT
 INTRODUCTION
 IMPACT OF PHYSIOLOGIC CONDITIONS...
BIOLOGICAL CORRELATION
 CRITICAL ASSESSMENT OF RESULT...
 CONCLUSION
 REFERENCES
 
CD10 (CALLA, neutral endopeptidase)
It is normally expressed on terminally differentiated neutrophils, i.e., segmented neutrophils [4 ]. Term neonates have shown a decreased percentage of CD10+ granulocytes in their peripheral blood (PB) compared with healthy adults in the absence of increased bands or left shift. This may be related to immaturity of cell development [6 ]. No other physiologic group has been studied for the expression of this antigen.

CD11a (lymphocyte function antigen-1)
It is expressed on all leukocytes, including granulocytes. In utero, CD11a intensity on fetal granulocytes in early pregnancy was less than that of adults. However, its level increased with gestational age until it became comparable with that of adults during the third trimester [7 ]. The intensity of expression of CD11a in preterm and term neonates and elderly individuals was comparable with that of healthy adults [8 , 9 ]. In pregnancy, the intensity of CD11a on neutrophils was reported to be increased and decreased compared with a control group [7 , 10 ]. Brief exercise induced no change in the intensity of CD11a expression or the percentage of CD11a+ granulocytes [11 , 12 ]. However, regular and moderate exercise was associated with decreased intensity of CD11a expression [13 ]. Brief psychological stress caused no change in the intensity of expression of CD11a [12 ]. LAD is a condition that is associated with defects in the ß2 subunit (CD18), which heterodimerizes with CD11a. This mutation causes decreased or absent expression of CD11a on leukocytes [14 ]. Age seems not to be an interfering factor in the diagnosis of LAD when CD11a expression is relied on. Yet, when studying patients with obstructive jaundice for LAD, caution should be exercised, as obstructive jaundice has been reported to cause low expression of CD11a [15 ].

CD11b (complement receptor 3, CR3)
This antigen is expressed on myelocytes and more mature granulocytes. The impact of age on CD11b expression has been debatable. Numerous studies of fetal, premature neonatal, and term neonatal granulocytes showed CD11b expression to be less than, equal to, or higher than adult values, although the majority of studies indicated a lower value in early life [7 , 8 , 16 17 18 19 20 ]. Most studies did not consider the impact of neonatal stress in their study design. Using a different approach, one study quantified the amount of CD11b in term neonatal granulocytic lysates rather than its surface expression. This study concluded that term neonatal neutrophils contained ~66% of adult neutrophil CD11b [21 ]. Inconsistent results of CD11b expression have also been encountered in pregnant women and elderly individuals. CD11b expression has been reported to be normal or increased in these populations [7 , 9 , 10 , 22 23 24 25 26 ]. However, pregnant women delivering prematurely have consistently shown a higher expression of CD11b [27 ]. Regular and moderate exercise was associated with decreased intensity of CD11b expression [13 ]. Conversely, marathon racers and exhaustive treadmill runners had increased CD11b intensity on their granulocytes [28 ]. The difficulty of assessing surface expression of CD11b may be related to the fact that this antigen has an extensive, intracellular storage pool, which could be released to the surface with activation or excessive manipulation [29 ]. As CD11b forms a heterodimer with CD18, it is also decreased or absent in LAD. Considering literature reports of variable CD11b results, its use for diagnosis of LAD in early life may be more difficult compared with CD11a.

CD11c (CR4)
This antigen is expressed at the myelocytic stage of development and is maintained at the more mature stages of neutrophilic development. Fetal granulocytes were reported to show a low expression of CD11c compared with adults. Although the expression of CD11c gradually intensified with more progression in intrauterine fetal age, its in utero expression at term remained lower than adult expression [7 ]. Premature labor was associated with a higher percentage of fetal neutrophils expressing CD11c, suggesting neutrophilic activation [30 , 31 ]. The elderly population showed a higher percentage of CD11c+ cells but with normal intensity [32 , 33 ]. CD11c has been reported to have normal and higher intensities of expression in pregnancy [7 , 10 ]. Regular and moderate exercise was associated with decreased intensity of CD11c [13 ]. This antigen has not been studied in other physiologic groups. CD11c expression is also decreased or absent in LAD. As surface expression of CD11c increases with activation, this fact should be taken in consideration for appropriate interpretation of the result [34 ].

CD13 (aminopeptidase N)
This antigen is a myelomonocytic antigen expressed on most PB granulocytes. In utero studies have shown that fetal neutrophils express CD13, and premature labor causes a more intense expression. The enhanced expression of CD13 was thought to be in response to premature parturition [30 , 31 ]. The percentage of CD13+ neutrophils in term neonates was lower than that of adults [24 ]. Granulocytes have intracellular storage pools of CD13 that are releases with activation, which could explain the changes in its surface expression under some activation conditions [29 , 35 ]. No other physiologic groups have been studied for this antigen.

CD14
It is expressed mostly on monocytes. Granulocytes, particularly when activated, may express CD14. This antigen was reported to be expressed on a higher percentage of preterm neonatal granulocytes compared with healthy adults but with similar intensity [36 ]. The intensity of CD14 on granulocytes in pregnancy was increased compared with control subjects [25 , 26 ]. There was no significant difference in its expression between pregnant women undergoing term labor and those undergoing premature labor [27 ].

CD15 (X-hapten)
CD15 and its sialylated form (CD15 s) are expressed on adult granulocytes. CD15 is also expressed on fetal and neonatal granulocytes. However, premature and prolonged labor was associated with higher percentages of CD15+ fetal and preterm neonatal neutrophils [17 , 30 , 31 ]. Although the intensity of expression of CD15 on maternal neutrophils was normal in term pregnancy, premature delivery caused a higher intensity of its expression [26 , 27 ]. It is clear that premature and prolonged labor affects the expression of CD15 on neutrophils from mother and baby. The intensity of expression of CD15 was also higher in the elderly population [9 , 37 ]. Obstructive jaundice has been reported to cause reduced expression of CD15 [15 ]. Measuring CD15 s may play a role in the diagnosis of LAD II, which is characterized by defective fucosylation of various cell-surface proteins [14 ]. No literature is available on the impact of various physiologic conditions on the expression of CD15 s.

CD16 [FC receptor for immunoglobulin G (Fc{gamma}RIII)]
CD16 is expressed on granulocytes at the metamyelocytic stage and is maintained throughout maturation. When fetal blood was studied, one study reported a lower intensity and a lower percentage of CD16+ granulocytes compared with adults [38 ]. However, these results were complicated by the fact that fetal blood was rich in eosinophils, which showed no expression of CD16 [39 ]. When this fact was taken into consideration, the expression of CD16 on fetal neutrophils was reported to be similar to that of the adults [19 ]. Variable results were also obtained when preterm and term neonatal granulocytes were studied. However, most studies indicated a lower expression compared with adults [18 , 19 , 36 , 38 , 40 , 41 ]. Increased expression of CD16 has been positively correlated with increased birth weight, and decreased expression was observed in septicemia and respiratory distress [36 , 40 ]. Gender and race had no impact on CD16 expression on granulocytes [33 ]. Yet, pregnancy was associated with a lower intensity of expression of CD16 [25 ]. This expression did not change during premature or term labor [27 ]. Previous studies suggested that CD16 antigen was lost from the surface of neutrophils as a result of inflammation [42 ]. Conversely, excessive manipulation of granulocytes may release the intracellular storage pools of CD16, causing an artificial increase in its surface expression [34 ]. Familial absence of CD16 has been reported in some patients with higher prevalence of autoimmune diseases. However, the absence of CD16 was not associated with an increased risk for infections [43 ].

CD18 (integrin ß2 subunit)
This antigen forms a heterodimer with members of the CD11 group and is expressed on all leukocytes. The intensity of CD18 expression on fetal granulocytes was less than adults, although it increased with fetal age [7 ]. The intensity of expression of CD18 was higher in the elderly population [9 , 37 ]. Most studies suggested that pregnancy, term labor, and premature labor had no effect on CD18 expression [7 , 10 , 24 25 26 27 ]. Regular and moderate exercise was associated with decreased intensity of CD18 expression [13 ]. However, marathon racers and exhaustive treadmill runners had no change in CD18 expression on their granulocytes [28 ]. As mentioned earlier, LAD is an autosomal, recessive disorder caused by decreased expression or function of CD18 and accompanied by concomitant, decreased expression of the {alpha} subunits of all members of the CD11 family [14 ]. As CD18 is not affected by labor, it may prove to be a reliable marker for LAD in early life.

CD29 (integrin ß1 subunit)
This antigen heterodimerizes with many integrin {alpha} subunits, including CD49a–f and CD51. It is normally expressed on all leukocytes but with lower expression on the more mature granulocytes. A small number of studies reported decreased intensity of CD29 in pregnancy and no change in its expression with regular and moderate exercise [10 , 13 ].

CD32 (FC{gamma}RII)
This antigen is expressed on all leukocytes. Several studies reported that fetal and preterm neonatal granulocytes had a lower expression of CD32 in percentage of positive granulocytes and intensity compared with adult granulocytes [36 , 38 ]. The expression of CD32 on term neonatal granulocytes has been controversial. Various studies have reported a higher, similar, and lower expression of CD32 in term neonates compared with adults [18 , 36 , 38 ]. Gender and race were not associated with any change in the expression of CD32 [33 ].

CD33
CD33 is a myelomonocytic antigen that is expressed by all granulocytes but at a lower intensity than monocytes. The percentage of granulocytes expressing CD33 in preterm and term neonates was lower than adults and was not influenced by gestational age [6 , 17 ].

CD35 (CR1)
This antigen is normally expressed on neutrophilic bands and segmented neutrophils. Fetal, preterm neonatal, and term neonatal granulocytes expressed CD35 in an intensity that was similar to adult granulocytes [18 , 19 ], although one study has reported a higher intensity on neonatal granulocytes [44 ]. The latter study applied the lysing step before antibody incubation, suggesting excessive manipulation. CD35 has a large intracellular pool that could be easily translocated to the plasma membrane with manipulation or activation [45 ]. When the CD35 content of neonatal granulocytes was quantified, it was not different from adult granulocytes [21 ].

CD49d (very late antigen-4)
It is expressed on early neutrophilic granulocytes and is absent on bands and segmented neutrophils. The expression of CD49d on granulocytes was not changed in pregnancy, including those ending with premature labor [25 26 27 ]. Similarly, brief exercise caused no change in CD49d expression [11 , 12 ].

CD54 (intracellular adhesion molecule-1)
This antigen is normally very weakly expressed on granulocytes beyond the promyelocytic stage. Brief exercise and psychological stress induced no change in the intensity of CD54 expression but were associated with an increased percentage of CD54+ granulocytes [11 , 12 ]. As CD54 is expressed on granulocytes on activation, this pattern of expression may reflect some degree of granulocytic activation with stressful conditions.

CD55 and CD59
Both antigens are complement-regulatory proteins that are normally expressed by granulocytes. Resting neonatal neutrophils had a higher intensity of CD55 expression but a similar intensity of CD59 expression compared with adult neutrophils [44 ]. No other physiologic groups have been studied for these antigens.

CD62L (L-selectin)
This antigen is normally expressed on all granulocytes. The intensity of CD62L on fetal and preterm neonatal granulocytes was similar to adults but higher than term neonates [8 , 20 , 39 ]. The intensity of expression of CD62L was not changed in pregnancy whether associated with term or premature labor [7 , 24 25 26 27 ]. Brief exercise also induced no change on the percentage of granulocytes expressing CD62L, but the intensity of its expression was increased [11 , 12 ].

CD64 (FC{gamma}RI)
CD64 is normally expressed at the early stages of granulopoiesis and is lost at the band stage of development. Fetal expression of CD64 was similar to that of adults [38 ]. In preterm neonates, one study reported a higher percentage of CD64+ cells than adults but a similar intensity of expression [36 ]. However, a more recent study showed the absence of any difference in the intensity of CD64 expression between preterm neonates (stressed and nonstressed) and adults [18 ]. In term neonates, most studies indicated a higher expression of CD64 compared with healthy adults [38 , 41 ]. The expression of CD64 in centenarians was higher in percentages and intensity, which may be related to the higher level of interferon-{gamma} (IFN-{gamma}) in the elderly population [32 ]. Gender had no impact on CD64 expression. However, Africans expressed a higher level of CD64 on their granulocytes compared with Caucasians [33 ]. The expression of CD64 on neutrophils during pregnancy was reported to be of higher intensity compared with nonpregnant subjects [25 , 26 ]. Premature labor caused no further change in CD64 expression [27 ].

CD66b
This antigen is normally expressed on granulocytes. The expression of CD66b in intensity and percentages of positive cells in preterm neonates was comparable with that of adults [36 ]. Gestational age of neonates had no effect on the percentage of CD66b+ cells [17 ]. The expression of CD66b did not change in pregnancy [25 , 26 ]. However, pregnant women, who delivered prematurely, had a higher intensity of CD66b expression on their granulocytes [27 ].

HLA-DR
Despite its very low, normal expression, there were reports of lower intensity of HLA-DR expression on granulocytes during pregnancy compared with nonpregnant control [25 , 26 ]. Premature labor had no effect on HLA-DR expression in pregnant women [27 ].


   BIOLOGICAL CORRELATION
TOP
 ABSTRACT
 INTRODUCTION
 IMPACT OF PHYSIOLOGIC CONDITIONS...
 BIOLOGICAL CORRELATION
CRITICAL ASSESSMENT OF RESULT...
 CONCLUSION
 REFERENCES
 
The weak expression of some antigens in early life may be related to immaturity, as antigen expression improves with age. For instance, CD11a expression in early fetal life is weak. However, it reaches adult level late in the third trimester. Other antigens, such as CD10, CD16, and CD32, gradually increase their expression during the neonatal period [6 ]. Some physiologic conditions may simulate an inflammatory environment that is associated with neutrophil activation. It has been hypothesized that during pregnancy, placental products or humoral substances such as prostaglandins and cytokines may induce changes, which are similar to inflammation, in leukocytes in the peripheral circulation [17 , 25 , 27 ]. The impact is more pronounced in premature labor, which influences fetal and maternal granulocytes. Premature labor is associated with a higher percentage of fetal neutrophils expressing CD11c, CD13, CD15, and CD66b compared with fetal neutrophils of term labor [30 , 31 ]. Similarly, neutrophils of pregnant women, who delivered prematurely, had a higher intensity of expression of CD11b, CD15, and CD66b [27 ].

Furthermore, the higher level of IFN-{gamma} in centenarians has been linked to the higher expression of CD64 on their neutrophils [32 ]. Some of the changes detected during exercise, such as the increased intensity of CD62L expression, could be explained on the basis of increased demargination of neutrophils. The margination pool of neutrophils is known to have a higher expression of CD62L [11 ].


   CRITICAL ASSESSMENT OF RESULT VARIATION IN THE LITERATURE
TOP
 ABSTRACT
 INTRODUCTION
 IMPACT OF PHYSIOLOGIC CONDITIONS...
 BIOLOGICAL CORRELATION
 CRITICAL ASSESSMENT OF RESULT...
CONCLUSION
 REFERENCES
 
In our review of various literature reports, we came to the conclusion that contradictory results may be caused by technical or study design-related factors.

Technical factors
The following technical factors may play a role in result variation: first, the methodology of granulocytic preparation, such as density gradient separation, which tends to change surface expression of several antigens including CD35 and CD16 compared with whole blood lysis technique [8 , 34 , 36 ]; second, the variability in data acquisition and analysis, as some studies are based on absolute fluorescence intensity, relative fluorescence intensity, the number of surface molecules, or the percentage of positive or negative cells; third, the presence of a high eosinophilic count in fetal blood within the granulocytic gate, which can interfere with the assessment of antigens that are normally absent on eosinophils, such as CD16 and CD10 [39 ]; and finally, the presence of a population of immature cells in neonatal blood could skew the results, particularly for antigens that appear late in granulocytic maturation, such as CD35 [4 , 16 ].

Study design
The definition of premature babies has varied markedly among various reports. Some studies have used <32 weeks [18 ], <37 weeks [17 ], 22–31 weeks [36 ], 27–37 weeks [8 ], and 26–35 weeks [19 ] as their definition of prematurity. Some studies have also included premature infants shortly after their recovery from respiratory distress or septicemia [19 ], which are known to influence the expression of some markers such as CD16 [40 , 42 ]. The postnatal interval for these studies also varied from several hours to several days. The length of labor was not taken into consideration, despite the fact that prolonged labor has been associated with a higher percentage of cells expressing CD11b, CD11c, CD15, CD33, and CD66b on preterm infants [17 ].


   CONCLUSION
TOP
 ABSTRACT
 INTRODUCTION
 IMPACT OF PHYSIOLOGIC CONDITIONS...
 BIOLOGICAL CORRELATION
 CRITICAL ASSESSMENT OF RESULT...
 CONCLUSION
REFERENCES
 
Physiologic conditions have a strong impact on neutrophilic surface antigens. Understanding this impact would help in the diagnosis of various conditions, particularly those associated with decreased expression of some antigens. Standardization of granulocytic processing and preparation and study design should provide a better means for result assessment and comparison.

Received May 28, 2003; revised August 20, 2003; accepted August 22, 2003.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 IMPACT OF PHYSIOLOGIC CONDITIONS...
 BIOLOGICAL CORRELATION
 CRITICAL ASSESSMENT OF RESULT...
 CONCLUSION
 REFERENCES
 

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