Phenotype frequencies of Rh (C, c, E, e), M, Mia and Kidd blood group systems among ethnic Thai blood donors from the north‐east of Thailand

Abstract

We here report the first study of antigen and phenotype frequencies of Rh (C, c, E, e), M, Mia and Kidd antigens in north‐east Thai blood donors. Blood transfusion services aim to ensure availability of adequate and safe blood to minimize the development of transfusion reactions. For pre‐transfusion testing, the most important blood group systems are ABO and RhD. The transfusion of ABO‐compatible otherwise unknown phenotype blood may result in alloimmunization, especially in multi‐transfused patients. Extended red blood cell (RBC) phenotyping and selection of blood negative for specific antigens reduce post‐transfusion complications and allow for effective blood transfusion regimens to be achieved. A total of 13,567 regular repeated, voluntary Thai blood donors were included for red‐cell antigen typing of Rh (D, C, E, c, e). Samples from 12,768, 9,389 and 13,059 donors were typed for Kidd, M and Mia antigens, respectively. Amongst Rh antigens, e was the most common (96.80%) followed by C (95.50%), c (34.40%) and E (32.20%) with CCDee (60.00%) being the most common phenotype. For Kidd phenotypes, Jk(a+b+) was the most common (46.73%) and Jk(a−b−) was rare (0.07%). For the M and Mia antigen, M(+) was most frequently found (94.96%) and Mia(+) was found in 17.97% of individuals. Knowledge of red‐cell antigen phenotype frequencies in a population is helpful for creating a phenotype database of blood donors which can provide antigen‐negative compatible blood to patients with multiple alloantibodies. Moreover, provision of antigen‐matched blood can prevent alloimmunization in multi‐transfused patients.

Full text

Int J Immunogenet. 2019;1–6. wileyonlinelibrary.com/journal/iji 
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© 2019 John Wiley & Sons Ltd
1 | INTRODUCTION
Blood group antigens are polymorphic antigens located on the
red‐cell membrane, able to induce an immune response in individ‐
uals potentially at risk during pregnancy [haemolytic disease of the
foetus and newborn (HDFN)] or following transfusion [haemolytic
transfusion reactions]. The probability of an individual developing an
alloimmune response depends on the incidence of the antigen in the
population (Giblett, 1961) (known to vary between different popula‐
tions and ethnic groups), on its immunogenicity and on the patient's
immune status (Daniels, 2009; Schonewille, Haak, & Zijl, 1999).
Currently, 36 blood group systems and more than 316 differ‐
ent blood group antigens have been defined by the International
Society of Blood Transfusion (ISBT) (http://www.isbtweb.org).
Received:23Octob er2018
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Revised:14January2 019
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Accepted:11Februar y2019
DOI:10.1111/iji.12420
ORIGINAL ARTICLE
Phenotype frequencies of Rh (C, c, E, e), M, Mia and Kidd
blood group systems among ethnic Thai blood donors from the
north‐east of Thailand
Amornrat V. Romphruk1 | Chalawan Butryojantho1 | Bhakwarin Jirasakonpat1 |
Ninnate Junta1 | Supawadee Srichai1 | Chintana Puapairoj1 | Piyapong Simtong2
1Blood Trans fusion Center, Facult y of
Medicine, Khon K aen Universit y, Khon
Kaen, Thailand
2Department of Clinical Immunology and
TransfusionSciences,FacultyofAss ociated
Medical Sciences, Kho n Kaen Universit y,
Khon Kaen, Thailand
Correspondence
AmornratV.Romphru k,Facult yofMedicine,
Blood Trans fusion C enter, Khon K aen
University, Khon K aen, Thailand.
Email: aromphruk@gmail.com
Funding information
Faculty of Medicin e, Khon K aen University,
Thailand,Grant/AwardNumber:MM61301
Abstract
We here report the first study of antigen and phenotype frequencies of Rh (C, c, E, e),
M, Mia and Kidd antigens in north‐east Thai blood donors. Blood transfusion services
aim to ensure availability of adequate and safe blood to minimize the development of
transfusion reactions. For pre‐transfusion testing, the most important blood group
systemsareABOandRhD.ThetransfusionofABO‐compatibleotherwiseunknown
phenotype blood may result in alloimmunization, especially in multi‐transfused pa‐
tients. Extended red blood cell (RBC) phenotyping and selection of blood negative for
specific antigens reduce post‐transfusion complications and allow for effective blood
transfusionregimens to be achieved.Atotalof13,567regular repeated,voluntary
Thai blood donors were included for red‐cell antigen typing of Rh (D, C, E, c, e).
Samplesfrom12,768,9,389and13,059donorsweretypedforKidd,MandMia anti‐
gens,respectively.AmongstRhantigens,ewasthemostcommon(96.80%)followed
byC(95.50%),c(34.40%)andE(32.20%)withCCDee(60.00%)beingthemostcom‐
monphenotype.ForKiddphenotypes,Jk(a+b+)wasthemostcommon(46.73%)and
Jk (a−b−)was rare( 0.07%).Fo rt heMan dMia antigen, M(+)wasmostfrequentlyfound
(94.96%)a ndMia(+)wasfoundin17.97%ofindividuals.Knowledgeofred‐cellantigen
phenotype frequencies in a population is helpful for creating a phenotype database
of blood donors which can provide antigen‐negative compatible blood to patients
with multiple alloantibodies. Moreover, provision of antigen‐matched blood can pre‐
vent alloimmunization in multi‐transfused patients.
KEYWORDS
blood group systems, phenotype frequency, red‐cell antigens

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ROMPHRUK et al.
ABO, Rh, Kell , Kidd, Du ffy, MNS, P, Lewis and Lu theran ar e the
major blo od group syste ms (Daniels, 20 09; Smar t & Armstrong ,
2008).Alloantibodies against Rh(E, c), MNS (Mia)and Kidd(Jka)
blood gro ups are the mo st commonl y report ed in Asian po pula‐
tions(Cheng,Lee,&Lin, 2012;Romphruk etal.,2018;Tianetal.,
2018). Moreover, these antibodies have frequently been identi‐
fied as a cause of haemolytic transfusion reac tions and HDFN in a
rangeofstudies(Chatziantoniouetal.,2017;Michalewska,Ejduk,
&Pniewska,2005).
Blood transfusion services aim to ensure availability of ade‐
quate and safe blood with regards to transfusion‐transmitted in‐
fections and compatibility testing to minimize the development
of any major transfusion reactions. For pre‐transfusion testing,
themost importantbloodgroup systemsareABO and RhD. The
transfusionofABO‐compatiblebloodwithunknownphenotypes
for clinically significant antigens may result in alloimmunization,
especially in multi‐transfused patients. Therefore, knowledge of
red‐cell antigen phenotype frequencies in regular voluntary blood
donors would help us to assess frequencies of these phenotypes
and enable us to establish a donor data bank of red blood cell
(RBC) antigens. Furthermore, it would be beneficial to provide an‐
tigen‐negative compatible blood without delay to alloimmunized
patients and to prevent alloimmunization in multi‐transfused
patients.
Thalassaemia and haemoglobinopathies are major pub‐
lic health problems in South‐East Asian countries. In Thailand,
the average frequency of α0‐thalassaemia in the population is
2.5%–10%,haemoglobin(Hb) Const ant Springand Hb Paksé are
1%–8%,  α+‐thalass aemia is 15%–20%, β‐thalassaemia is 3%–9%,
and Hb E is 30%–50% especially in the north‐eastern part of
the country (Fucharoen et al., 2002). According to the Clinical
Practice Guidelines formanagement of thalassaemiasy ndromes
in Thailand, the RBC antigen match for Rh and Mia blood group
systems is minimally required for transfusion to prevent alloim‐
munization (Fucharoen, Tanphaichitr, Torcharus, Viprakasit, &
Mekaewkunchorn,2014).T hefrequenciesofRB CantigensinThai
populations have been reported only from Bangkok (Fongsarun,
Nuchprayoon, & Yod‐in, 2002). Here, we aim to report for the
first time the RBC antigens and phenotype frequencies of various
blood groups (Rh, M, Mia and Kidd) among ethnic Thai blood do‐
nors from north‐east Thailand.
2 | MATERIALS AND METHODS
2.1 | Studied populations
This study was conducted in the Blood Transfusion Center, Faculty
of Medicine, Khon Kaen University, Thailand. Our centre is in
north‐east Thailand and supplies blood components for patients in
Srinagarind Hospital, which is a tertiary‐care multi‐specialty teach‐
ing hospital. We retrospectively examined the red‐cell phenotyping
of13, 597regular voluntary Thai blooddonors from2013to 2017.
These dat a were available on a computerized system.
2.2 | RBC phenotypes
Red blood cell phenot ypes (C , E, c, e, M, Mia and Kidd) of donors
were determined using an antigen‐typing gel test (K‐med, Khon
Kaen, Thailand) as per the manufacturer's instructions. Briefly,
red cells wereprepared as2%cell suspension in normalsaline so‐
lution. A n aliquot (25μl) was added to each well and centrifuged.
Agglutinated cellsformedared lineonthesurfaceof gelinthe mi‐
crotube or dispersed throughout the gel, indicating the presence of
the corre sponding ant igen. A compac t button of ce lls on the bot‐
tom of the microtube indicated the absence of the corresponding
antigen.
2.3 | Statistical analysis
Red‐cell antigen and phenotype frequencies of the various blood
group systems were calculated by direct counting. The results were
expressed as percentages. Data were managed and analysed using
Excel 2013 (Microsoft Corporation, Seat tle, WA). All statistical
analysiswasper formedusingGraphPadPrismsoftware(GraphPad,
Inc., La Jolla, CA, USA). The distribution of antigens/phenotypes
between this study and studies of other regional populations was
comparedusingthechi‐squaretest.Ap‐value<0.05wasconsidered
statistically significant.
2.4 | Study approval
The present study was approved by the Khon Kaen University Ethics
Committeeforhumanresearch(HE611256).
3 | RESULTS
Intota l,13, 597r egula rdono rswerein cludedforred‐ cellanti gentyp‐
ingofRh(C,E, c, e).Ofthese, only12,768,9,389and13,059were
tested for Kidd, M and Miaantigens,respectively.AmongstRhan‐
tigens, e was the most common(96.80%) followedbyC (95.50%),c
(34.40%)andE(32.20%). The antigen frequencies of Rh (C, c,E,e),
Kidd, M an d Mia systems and comparisons with other regional popula‐
tions are summarized in Table 1. Table 1 also shows 9 Rh phenotypes,
with CCDeebeing the most commoninour population (60.00%), a
significantly higher frequency than Thais in Bangkok. The distribu‐
tion of Rh blood group phenotypes differed significantly between
this study and those of the other populations, except the Chinese
in Malaysia. For the Kidd blood group system, the frequencies of
Jka andJkbwere74.14%and72.52%,respectively.Jk(a+b+)wasthe
mostc ommonphen ot ype(46.73%)o bs er ve d.Ina dd it ion,9of12, 768
(0.07%)possessedtherareJk(a‐b‐)phenotypepreviouslyunreported
from Taiwan(Lin, Broadberry,& Chang,1988). TheM(+)phenoty pe
(94.96%)was ve ry commo n in our popul ation and at a sig nificant ly
hi g her fre q u enc y tha n Tha isi nBa n gko k(8 3 .60% ),C h ine s ei n Mal ays i a
(81.50%),Taiwanese(79.70%),MainlandChinese(77.20%)andnorth
Indians (90.55%). ThefrequencyoftheMia(+)antigenwasobserved

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ROMPHRUK e t al.
in17.97% of ou rs tud yp op ul ationan dsho we dasign if ica ntdiffere nc e
fromThaisinBangkok(9.10%)(p < 0.01).
4 | DISCUSSION
Frequency of RBC phenotypes varies among different populations
and ethnic groups, and is thus of interest in the fields of anthro‐
pology and forensic medicine, as well as in transfusion medicine.
RBC incompatibilities are responsible for alloimmunization and may
cause haemolytic transfusion reactions and HDFN, with different
degrees of s everity. In addition , haemoglobin E‐β0‐thalassaemia and
homozygous β0‐thalassaemia are the most common chronic trans‐
fusion‐dependent thalassaemias in Thailand. The prevalence of al‐
loimmunization in thalassaemia patients at our Blood Transfusion
Centerhasbeendetec tedtobe19.3%(Romphruketal.,2018).Th e
detection of RBC phenotypes either among patients who required
chronic transfusions or donors would be useful to reduce alloim‐
munizationand haemolytic transfusion reactions. Although there
has been studied on RBC phenot ype frequencies in ethnic Thai
populations (Fongsarun et al., 2002), there are no data from north‐
east Thailand. Our previous studies on other aspects of molecular
genetics,suchashumanleucocyteantigens(HL A),humanneutro‐
philantigens(HNA)andkillerimmunoglobulin‐likereceptors(KIRs),
revealed significant differences in frequency of alleles/molecules
in different regions of Thailand (Chaisri et al., 2013; Romphruk et
al., 2010; Simtong et al., 2018). Here, we report for the first time
the antigen and phenotype frequencies of blood group systems
(Rh, M, Mia and Kidd) by gel technology among ethnic Thai blood
donors in the north‐east of Thailand.
TABLE 1 Comparison of phenotypic distribution of Rh (C , c, E, e), Kidd, M and Mia antigensindifferentpopulations
Populations
(Number of
subjects)
Phenotype frequencies (%)
Thais (this study) Thais in Bangkoka
Chinese in
MalaysiabTaiwanesec,dMainland ChineseeNorth Indiansf,g
(9, 389−13 ,597 ) (985 −20 , 569) (200) (1,000−1,598) (1,412) (508−51,857)
Rh system
C95.50 8 3.70✝96 .00 91.6 0✝88.00✝8 7. 10 ✝
c34.40 48.30 ✝34.50 51. 6 0 ✝57. 5 0 ✝51. 5 0✝
E32.20 38.6 0✝23.0 0✝43.50 ✝50.40✝19. 70 ✝
e96.8 0 87. 4 0 ✝97.50 93 .80 ✝91.20 ✝91.6 0✝
CCDee 60.00 4 9.4 0✝61 .50 47. 8 0 ✝41 .16 ✝40 .95✝
CcDEe 22 .10 19.9 0✝15 .00 * 34.60✝38 .87✝14 .5 4✝
CcDee 7. 4 0 10.90 ✝15.0 0* 8.20 7. 5 9 30 .91✝
CCDEe 5.40 2.20 ✝3.50 0.90 ✝0.57✝0. 32✝
ccDEE 2.50 11. 20 ✝1.00 5 .90✝7. 02 ✝0.78 ✝
ccDEe 1.70 3.90 ✝3.00 2.00 3.65✝3.69✝
CcDEE 0.50 1.20✝1.0 0 0.30 0.64 0.40
ccDee 0.30 1.10 ✝00.30 0.36 1 .15✝
CCDEE 0.10 0.20 0 0 0.14 0✝
Kidd system
Jka 74.14 76. 80 79. 0 0 72.00 67. 99 76.77
Jkb72.52 73.5 60.50 78.50 75. 57 78.89
Jk(a+ b−) 2 7.41 26.5 0 36.0 0✝21. 50✝23 .94✝30 .71
Jk(a+b+) 46.73 50.3 0✝43.00 50. 50✝44.05 46.06
Jk(a−b+) 25.79 23.20 ✝17. 5 0 ✝28.0 0 31. 52✝22.83
Jk(a−b−) 0.07 0.06 3.50✝00. 50✝0.39 *
MNS system
M+ 94.96 83.60 ✝81.5 0✝79. 70 ✝77. 2 0 ✝9 0.55 ✝
Mia + 17.97 9. 10 ✝no data 7.3NT no data no data
Note. “NT ”; no statistical testing b ecause no exact numbers of the subjects have been provided by the respec tive author.
Bold and italic = significant difference compared to this study.
aFongsarun et al., 2002, bMusa et al., 2012, cLin et al., 1988,dBroadberry et al., 1994, eYu et al., 2016, fMakroo et al., 2014, gAgarwal et al.,2013.
*p<0.05,† p < 0.01.

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ROMPHRUK et al.
The Rh blood group system is complex and contains many anti‐
gens that are highly immunogenic. These antigens are the second‐
most potent for triggering an immune reac tion, af ter those of the
ABObloodgroup.Anti‐Rhalloantibodiescancausesevereorfatal
haemolytic transfusion reaction and severe HDFN (Chatziantoniou
et al., 2017; Michalewska et al., 2005). Overall, the frequencies
of all antigens (C, c, E, e) in this study differed from those Thais
in Bangkok (Fongsarun et al., 2002), Mainland Chinese (Yu et al.,
2016), north In dians (Makroo, Gu pta, Bhatia, & Ros amma, 2014)
andTaiwane se(Lineta l.,1988).H owever,ourstu dypop ulati onh ad
frequencies of C, c and e similar to those of Chinese in Malaysia
(Musa et al., 2012). We confirmed that the e antigen is the most
frequentfollowedbythe Cantigen (87.40%–97.50%and83.70%–
96.00% , respectively)among Asian individuals.In our cohort, the
CCDee (R1R1) phenotype was the commonest (60.00%), as it is
in other A sian populat ions. Finall y,our s tudy repo rts the hi ghest
known fre quency of CCDEe phen otype (5.40%). The most com‐
mon alloantibodiesinThaipatientsareanti‐E (39.50%) and anti‐E
combinedwithanti‐c (25.30%), whichareproducedin transfused
R1R1 patients (Romphruk et al., 2018). Thus, these alloimmunized
patients should receive antigen‐negative blood (E antigen‐ and c
antigen‐negative). Fortunately, donors with the R1R1 phenotype are
very common in our region.
TheKidd bloodgroupiscomposed ofJka,JkbandJk3 antigens,
andfourphenotypes:Jk(a−b+),Jk(a+b+),Jk(a+b−)andJk(a−b−).These
antigens are associated with urea transporter UT‐B (Sands, 2003).
Thephenot ype Jk(a+b+) was the mostcommon (46.73%) and simi‐
lartothefrequenciesin ChineseinMalaysia(43.00%)(Musaetal.,
2012),MainlandChinese(44.05%)(Yuetal.,2016)andnorthIndian
populations (46.06%)(Agarwal, Thapliyal, & Chatterjee, 2013), but
significantlylowerthanThaisinBangkok(50.30%)(Fongsarunetal.,
2002)andTaiwanese(50.50%)(Linetal.,1988)(p < 0.01). The Kidd
antigenisimportant in transfusionmedicine.Anti‐Kidd antibodies
are well known for transient detectability and for their involvement
inhaemolytictransfusionreactions.Onceanti‐Jka is formed, the an‐
tibody frequently diminishes in strength so that standard antibody
screeningmethodsfailtodetect it(Kay,Poisson, Tuma,&Shulman,
2016). Thus, these antibodies are dangerous as a cause of clinically
signific ant delayed haemoly tic transfusion reaction (DHTRs) (Heddle
etal.,1995).TheJk(a‐b‐)phenotypewassignificantlylessfrequent
than in Chi nese in Malaysia (3 .50%) (Musa et al., 2012), Ma inland
Chinese(0.50%)(Yuetal.,2016)andnorthIndians(0.39%)(Agar wal
et al., 2013). Ind ividuals with t he Jk(a‐b‐) phenoty pe can develop
rareanti‐Jk3, which is likely to result in acute and delayed haemo‐
lytic transfusion reactions and difficulty in finding compatible blood
(Zhuang et al., 2013).
The M antigen belongs to the MNS blood group system and is
carriedbyglycophorinA.Phenotypingin9,389subjectsinthisstudy
revealed M(+)asthemostcommonphenotype(94.96%),afrequency
significantly higher than in many other populations (Table 1). This
implies that there are few susceptible M(−)individualswhoareatrisk
of producing anti‐M through incompatible transfusion or pregnancy.
In accordance with our previous work, anti‐M is of low frequency
intransfused patient s, representing 1.60%ofallcommon clinically
relevant antibody specificity (Romphruk et al., 2018). This contrasts
withthe10%frequencyofpositiveantibodyinpregnantCaucasian
women (De Young‐Owens, Kennedy, Rose, Boyle, & O'Shaughnessy,
1997). However, anti‐M can c ause severe haemolytic t ransfusion
reaction and HDFN ( Wikman, Edner, Gr yfelt, Jonss on, & Henter,
2007). In t he literatur e, anti‐M is identif ied freque ntly in patient s
who have never been immunized via transfusion or pregnancy (Klein
etal.,2014).
Mia antigen is previously described as the Miltenberger sub‐
system in MNS system, resulting from recombination of the GYPA
and GYPB genes (hybrid glycophorin). Surprisingly, the Mia(+) a n‐
tigen frequency in our study(17.97%) is significantlyhigher than
thatreportedinThaisinBangkok(9.10%).Anti‐Mia is the second‐
mostcommonlyfoundalloantibodyinAsiansbutisuncommonin
Caucasians. Recently, we found this alloantibody to be common
in north‐east Thailand (19.40%) (Romphruk et al., 2018). The
presence of anti‐Mia is associated with HL A ‐D RB1*0 9 (Chu et al.,
2009),anallelecommoninourpopulation(7.10%) (Romphruket
al., 2010). Following these observations, it would be interesting to
identif y any possible association between polymorphism of HLA‐
DR B1*09 and the occurrence of anti‐Mia alloantibody in the Thai
population.
At our Bloo d Transfusion Cente r,ant igen‐matched RB C pro‐
grammeforthalassaemiapatientshasbeen,since2008,65.6%of
all patients had received Rh (D, C, c, E, e) antigen‐matched and
19.2%receivedMia antigen‐matched RBCs. Based on the outcome
after implemented, a trend towards low alloimmunization rates
wasnotedintheantigen‐matchedRBCgroup,where3.5%ofpa‐
tients were alloimmunized (Romphruk et al., 2018). Moreover, a
phenotype database of blood donors also has been established at
our Blood Center which can provide the rare blood type such as
Jk(a−b−) and antigen‐negativecompatiblebloodto patientswith
multiple alloantibodies.
In conclusion, we have described the frequencies of dif ferent
blood group antigens and phenot ypes among ethnic Thai blood do‐
nors in the north‐east of Thailand. Our results indicate that the dis‐
tributions of RBC antigens differ in different ethnic groups, which
may be the result of different genetic and geographical origins. In
addition, knowledge of RBC antigen phenotype frequencies in a pop‐
ulation is helpful for creating a phenotype database of blood donors
for preparation of indigenous cell panels, and to help us to seek an‐
tigen‐negative compatible blood for patients with multiple alloanti‐
bodies and to prevent alloimmunization in multi‐transfused patients.
ACKNOWLEDGEMENTS
This work was supported by the Faculty of Medicine, Khon Kaen
University, Thailand (MM61301). We would like to thank the staf f
at Blood Transfusion Center, Faculty of Medicine, Khon Kaen
University, for the results of RBC phenotyping that was crucial for
thisstudy.Wewouldliketoacknowledge Prof.DavidBlairforedit‐
ingthemanuscriptviaPublicationClinicKKU,Thailand.

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5
ROMPHRUK e t al.
CONFLICTS OF INTEREST
The authors declare no conflicts of interest.
AUTHOR CONTRIBUTION
A. V.R. designedthestudy,analysedtheexperiment,andcritically
discusse d and finalize d the manuscr ipt. C. B., B . J., N. J. and S. S .
contributedtotheacquisitionofdata.C.P.contributedtoreagent/
material.P.S.contributedtoanalysis,interpretedthedataandwrote
the manuscript.
ORCID
Piyapong Simtong https://orcid.org/0000‐0001‐5216‐8700
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JirasakonpatB,etal.PhenotypefrequenciesofRh(C,c,E,e),
M, Mia and Kidd blood group systems among ethnic Thai
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