|
|
|
|
Research Article
|
|
Glucose-6-Phosphate Dehydrogenase Deficiency and Sickle Cell Disease in Burkina Faso |
|
Jacques Simpore,
Denise Ilboudo,
Karou Damintoti,
Luc Sawadogo,
Esposito Maria,
Scott Binet,
Henri Nitiema,
Paul Ouedraogo,
Salvatore Pignatelli
and
Jean-Baptiste Nikiema
|
|
|
ABSTRACT
|
Where malaria is endemic, there is an unexpected association between
haemoglobinopathies and glucose-6-phosphate dehydrogenase (G-6-PD) deficiency.
Their coexistence in a patient with sickle cell disease (SCD) can lead
to hemolytic anemia, hemoglobinuria, sepsis, renal failure and vaso-occlusive
attacks (VOA). The aim of this research was to determine the impact of
G-6-PD deficiency in SCD patients. That is why, we screened haemoglobinopathies
and G-6-PD deficiency in 7 villages and at 10 primary schools in Kadiogo
Province, Burkina Faso. Hemoglobin electrophoresis was performed on blood
from 18,383 people. From these results, we chose 342 subjects for a hemogram
and the measure of the G-6-PD activity. The results were analyzed with
EpiInfo-6 and Spss-10. Statistical significance was set at p<0.05.
We found a prevalence of 28.9% of Sickle Cell Trait (SCT), 1.3% of Major
Sickle Cell Syndromes (MSCS), 12.3% of G-6-PD deficiency among women and
20.5% among men. We did not detect a statistically significant difference
for counts of erythrocytes (p = 0.773), leucocytes (p = 0.227) and reticulocytes
(0.292); hemoglobin levels (p = 0.998); annual vaso-occlusive attacks
(p = 0.869) between persons with SCD having a G-6-PD deficiency and those
with normal G-6-PD activity. According to this study, G-6-PD deficiency
does not seem to increase the severity of SCD. However, these patients
should know their G-6-PD genotype in order to avoid consuming oxidative
drugs that might provoke oxidative stress.
|
|
|
|
How
to cite this article:
Jacques Simpore, Denise Ilboudo, Karou Damintoti, Luc Sawadogo, Esposito Maria, Scott Binet, Henri Nitiema, Paul Ouedraogo, Salvatore Pignatelli and Jean-Baptiste Nikiema, 2007. Glucose-6-Phosphate Dehydrogenase Deficiency and Sickle Cell Disease in Burkina Faso. Pakistan Journal of Biological Sciences, 10: 409-414. DOI: 10.3923/pjbs.2007.409.414 URL: https://scialert.net/abstract/?doi=pjbs.2007.409.414
|
|
|
INTRODUCTION
Burkina Faso, a country in Western Africa, is bordered on the north
and the west by Mali, on the east by Niger and the south by Ivory Coast,
Ghana, Togo and Benin. In tropical area, where malaria is endemic, there
is a high prevalence of haemoglobinopathies and G-6-PD deficiency (Enevold
et al., 2005; Fleming et al., 1979). The genes for sickle
cell disease (SCD) and glucose-6-phosphate dehydrogenase (G-6-PD) deficiency
are located on chromosome 11 and chromosome X, respectively. During cell
division, the genes normally assort independently (Bouanga et al.,
1998; Luzzatto et al., 1968). Sickle cell patients experience
vaso-occlusive attacks (VOA), bacterial infections, priapism and chronic
visceral complications associated with ischemia in different organs (Jacob
et al., 2005. Singh et al., 2006. Rogers, 2005). Major Sickle
Cell Syndromes (MSCS) are the most prevalent forms of genetic disease
in the wider malaria area in tropical countries. Glucose-6-phosphate dehydrogenase
deficiency also occurs with increased frequency throughout Africa, Asia,
the Mediterranean and the Middle East. In G-6-PD deficient individuals,
anemia is usually caused by fava beans (Laosombat et al., 2006)
and other oxidative drugs (Ciftci, 2005; Ozmen et al., 2004): aspirin,
primaquine and quinine that are used during malaria attacks. In addition
to hemolytic anemia, G-6-PD deficient individuals are predisposed to prolonged
neonatal jaundice, a result of neonatal hyperbilirubinemia (Muzaffer,
2005; Kaplan et al., 2005). This is a potentially serious problem
as neonatal hyperbilirubinemia can cause severe neurological complications
and even death (Diop et al., 2005). The high prevalence of hemoglobin
S (HbS) and G-6-PD deficiency (A-type) in tropical areas is related to
the selective advantage they provide against malaria (Williams et al.,
2005; Shimizu et al., 2005). The reported prevalence of G-6-PD
deficiency in SCD patients varies. According to some authors, the incidence
of G-6-PD deficiency is higher in MSCS patients than the general population
(Bouanga et al., 1998; Lewis et al., 1966; Samuel et
al., 1986). Other authors do not agree with this association believing
rather that the mutated genes responsible for these states do not stay
on the same chromosome, so they cannot be linked (Bouanga et al.,
1998; Luzzatto et al., 1968). The potential influence of glucose-6-phosphates
dehydrogenase deficiency upon the clinical manifestation of patients with
SCD is a matter of contention as well (El-Hazmi et al., 1987; Bienzle
et al., 1975). It is known, however, that G-6-PD deficiency in
patients with SCT can express itself like symptomatic SCD. Screening of
SCD patients who are carrying the G-6-PD deficiency gene will guide physicians
in their care. Such measures allow sickle cell disease patients to enjoy
a life expectancy beyond 50 years. This study has three aims: i) to estimate
the prevalence of the association between the haemoglobinopathies and
G-6-PD deficiency genes among the population, ii) to look at patients
who carry this double mutation and to determine the evolution of any hematological
parameters that might be therapeutically helpful, iii) finally, to see
if this curious linkage of these two mutated genes causes more complications
in the pathogenesis of SCD patients.
MATERIALS AND METHODS
Blood samples were collected in 7 villages and at 10 primary schools
of the Province of Kadiogo in Burkina Faso from May 25, 1999 to June 15,
2005. A total of 18,383 subjects, ages 7-32 years, average 21.81±8.47
years, were enrolled in the SCD study. From the electrophoresis of hemoglobin
results, we chose 342 individuals for the following analyses: hemogram
and G-6-PD test. All the SCD patients agreed to answer questions concerning
their health status: number of annual transfusions, hospitalizations,
vaso-occlusive attacks (VOA) and episodes of malaria. We compared the
different evaluative elements of SCD patients who have G-6-PD deficiency
with SCD patients who do not have a G-6-PD deficit. We calculated a severity
index, a total equal to the sum of the scores obtained utilizing the following
parameters:
Number of hospitalizations in the year: 0 times at score = 0; 1 to 2 times at score = 1; more than 2 times at
score = 2
Number of vaso-occlusive attacks (VOA) in the year: 0 times at score
= 0; 1 to 2 times at score = 1; more than 2 times at score = 2
Number of transfusions in the year: 0 times at score = 0; 1 to 2 times at score = 1; more than 2 times at
score = 2
Number of malaria attacks in the year: 0 times at score = 0; 1 to 2 times at score = 1; more than 2 times at
score = 2
Number of suspensions of activity in the year: 0 times at score = 0; 1 to 2 times at score = 1; more than 2 times at
score = 2
Ethical committee: The Ethics Committee of Saint Camille Medical Center in Ouagadougou
approved the admission of prospective participants into the study only
after informed consent was obtained.
Methods: Ten milliliter of venous blood was drawn from each person and placed
in two EDTA tubes. One blood tube was used soon thereafter for the hemoglobin
electrophoresis and hematological parameters. Within 3 h of drawing blood,
plasma was separated out by centrifugation at 3,000 rpm for 10 minutes
in the 2nd tube to be used for the G-6-PD test. All subjects underwent
hemoglobin electrophoresis using cellulose acetate plates (Helena Laboratories,
Beaumont, TX, the USA) with a pH 8.6 buffer. A hemogram was carried out
utilizing the Cell-dyn®1700 automat of Abbott House while reticulocytes
were measured using new methylene blue dye. Glucose-6-phosphate dehydrogenase
quantities were measured by Quantitative G-6-PD Diagnostic Real Time Systems
Kit Test (Italy) using a spectrophotometer reader type Microlab 2000.
Statistical analysis: Demographic and clinical profiles were recorded on computer files and
analyzed by standard software SPSS-10 and EpiInfo-6. Statistical significance
was set at p<0.05.
RESULTS
Hemoglobin electrophoresis was performed on a sample of 18,383 individuals:
9,923 females (53,98%) and 8,460 males (4600%). Table 1
presents allelic frequencies calculated utilizing the genotypes observed:
p, q and r are respectively the frequency of βA, βc
and βs. The formula of Hardy-Weinberg allowed us to calculate
the genotypic and allelic frequencies: N(p+q+r)2: AA = Np2;
AC = 2Npq; AS = 2Npr; CC = Nq2; SC = 2Nqr; SS = Nr2.
N indicates the number of the sample. Table 2 presents
the G-6-PD genotypic frequencies according to age groups. The frequency
of G-6-PD deficiency in the general population is 16.3%. This percentage
increases with age: 6-9 years (8.4%), 10-19 years (20.9%) and 20-29 years
(25.0%). Table 3 shows G-6-PD activity according to hemoglobin
genotype after hemoglobin electrophoresis. The frequency of G-6-PD deficiency
among SCT, MSCS and the control population with Hb AA are, respectively:
18.57%, 27.0% and 7.81%. It is important to note that the prevalence of
the favism is higher in men (20.5%) than women (12.3%), with p = 0.041.
Table 4 presents the results of the hemogram and the
G-6-PD activity of AA, SCT and MSCS subjects. The t-TEST reveals a statistically
significant difference (p<0.001) between the control population with
Hb AA and MSCS patients for G-6-PD enzymatic activity, the number of red
blood cells (RBCs), white blood cell (WBCs), reticulocytes, the concentration
of hemoglobin and the mean corpuscular volume (MCV). Whereas the control
population with Hb AA presents a normal hemogram, there is a severe anemia,
increased amount of reticulocytes and leucocytes associated with MSCS
subjects. The SCT subjects have a moderate anemia and reticulocytosis.
Table 5 presents the influence of the G-6-PD deficiency
on the pathogenesis of SCD. In our samples, we had 74 SCD patients: 37
hemoglobin homozygote SS and 37 hemoglobin double heterozygote SC. Among
these patients, 54 had normal G-6-PD activity and 20 had deficient G-6-PD
activity. The subjects freely answered the questionnaire, the results
of which are reflected in Table 5.
Table 1: |
Genotype and allelic frequencies observed and calculated |
 |
NS = Not significant. χ2 *---> **:
p = 0.659 (NS) |
Table 2: |
G-6-PD genotypic frequencies according to age group |
 |
χ2 Test, 1-2: p = 0.029, 2-3: p = 0.542
(NS), 1-3: p = 0.003, 2- 4:
p = 0.099 (NS), 1-4: p = 0.502 Not Significant (NS), 3-4: p = 0.015 |
Table 3: |
G-6-PD frequencies and hemoglobin genotype distribution |
 |
χ2 Test: AA/G-6-PD-_ SCT/G-6-PD-:
p = 0.010; AA/G-6-PD-_ MSCS/G-6-PD-: p<0.001;
SCT/G-6-PD-_ MSCS/G-6-PD-: p<0.152 (NS),
Not Significant |
Table 4: |
G-6-PD activity and Hemogram parameter distribution |
 |
* t-test: p<0.001; ** t-test: p<0.04 |
Table 5: |
G-6-PD deficit and SCD pathogenesis score |
 |
DISCUSSION
For the 18,383 samples from the 10 schools of the town of Ouagadougou
and the 7 surrounding villages of the capital, we found 5,320 (28,9%)
SCT (HbAS, HbAC, HbCC) and 230 (1.3%) MSCS (HbSS and HbSC) (Table
1). We discovered 19.1% of the haemoglobinopathy AC. This frequency
is higher than that identified in Mali (15.8%) (Diallo et al.,
1994) and in Nigeria (0.7%) (Storey et al., 1979). According to
Trabuchet (1991) the epicenter of the HbC mutation could be in West Africa.
Indeed, studying the haemoglobinopathies among the Mossi in Burkina Faso,
Modiano et al. 2001a discovered that hemoglobin CC protected against
severe malaria. In this research, we found AS in 8.4% of subjects. This
prevalence is lower than that detected in Ghana 14,0% (Mockenhaupt et
al., 2000), Dhelki Kharia (India) 12.5% (Balgir, 2005), but very similar
to that detected in Paik (India) 7.4% (Balgir, 2005), in Karachi (Pakistan)
5.1%, (Ghani et al., 2002). Our result was quite higher than that
found in Paraja (India) 0.9% (Balgir, 2005) and in Upper Volta 4.9% by
Labie, (1984). The slight increase in the HbS percentage in our sample
compared with that of Labie in (1984) is certainly due to the additional
medical care provided in Burkina Faso since 1990 for SCD patients: vaccinations
against pneumococcus, antimicrobial prophylaxis and improved medical care.
Simpore et al. (2002) with their haemoglobinopathy research, demonstrated
that SCD patients are often sick and frequently go for medical consultation
at Saint Camille Medical Centre in Ouagadougou: 660 HbSC (6.5%), 196 HbSS
(1.9%) and 3400 SCT (33.4%). We detected 16.37% G-6-PD deficiency (Table
2). This prevalence is higher than that they found in Dakar in 2005
(12.3%) (Diop et al., 2005), in Pakistan (1.8%) (Ali et al.,
2005) and lower than that detected in both Lome in 2001 (24,1%) (Gbadoe
et al., 2001) and Vataliya Prajapati community (India) (22,0%)
(Gupte et al., 2005). However, our G-6-PD deficiency frequency
is almost the same as Modiano et al. (2001a) identified (14.9%)
(Modiano et al., 2001b). The prevalence of G-6-PD deficiency in
male subjects (20.5%) differs significantly (p = 0.04) from that found
in women (12.3%) Table 3. That is due to the fact that
the males are hemizygous and the females are dizygous for X chromosome.
As such, the probability of finding the two genes for the G-6-PD mutations
on the chromosome X is lower. In this study we found a very slight but
significant difference of G-6-PD enzyme activity between male (121.2±13.2
mU.109/Eryth) and female (123.9±12.1 mU.109/Eryth) p<0.05. This
similarity of G-6-PD enzymatic activity between male and female is due
to the fact that the phenomenon of lionization activates only one X chromosome
in each woman`s cell. G-6-PD deficiency and SCD are two genetic disorders
of red blood cells (RBCs) which predispose to hemolytic anemia. Their
presence in patients should lead those providing medical care to avoid
using oxidative drugs. In our research we found a significant difference
between G-6-PD deficiency in SCD patients (27.03%) and in the control
population with HbAA (7.81%) p<0.001 (Table 3). Similar
results were found in Congo Brazzaville (Samuel et al., 1986),
in Senegal (Diop et al., 2005), in Kenya (Rattazzi et al.,
1971), in Ghana (Lewis, et al., 1973) and in Turkey (Akoglu et
al., 1986). But other studies do not confirm this association (El-Hazmi
et al., 1987; Steinberg and Dreiling, 1974; Saad et al.,
1992). More often than not, at the time of meiosis during the cycle of
cell division, the HbS and G-6-PD deficiency genes, which are located
on two different chromosomes, independently segregate according to Mendel`s
Law. But the phenomenon of selection, due to the presence of plasmodia,
pushes these pathogenic genes to stay together and thus associated. Comparing
the profile of SCD subjects with G-6-PD deficiency and SCD subjects with
normal G-6-PD activity, no statistical difference was found between these
two groups with regard to annual VOAs (p = 0.869), annual hospitalizations
(p = 0.901), annual transfusion frequency (p = 0.805) and annual activity
suspension (0.118) (Table 5). Similarly, no statistical
difference was found for hematological parameters: RBC counts (p = 0.773),
reticulocyte counts (0.292), WBC counts (p = 0.227), hemoglobin level
(p = 0.988), hematocrit (p = 0.776) and mean corpuscular Hb (MCH) (p =
0.065). We identified a statistical difference between the two groups
only for MCV values (p<0.001). These results agree with the studies
of Bienzle et al. (1975), Steinberg,and Dreiling. (1974), Diop.
(2000) and El-Hazmi. (1986), which showed that G6PD deficiency, even in
the tropical area, seems to have no effects on the hematological data
and clinical evolution of HbSS patients. According to these authors, G6PD
deficiency does not offer any advantage or disadvantage to patients with
sickle cell disease. However, other authors like Bouanga. (1998) and Znaidi.
(1995) offer different results. And some authors argue that G-6-PD deficiency
has a protective effect in SCD patients because the absence of enzymatic
activity contributes to the elimination of premature RBCs. There is a
elevated generation of young erythrocytes in these G-6-PD deficiency persons
(Steinberg and Dreiling, 1974). There was a significant difference in
malaria attack frequency between the group of SCD patients with G-6-PD
deficiency and SCD subjects with normal G-6-PD activity (p = 0.048). SCD
subjects who have a G-6-PD deficiency suffer fewer crises of malaria.
It is known that the frequency of the G-6-PD deficit increases with age
(Table 2), which could indicate a longevity advantage
in malaria zones as compared to people with normal enzyme activity. Nonetheless,
these results should not lead us to forget that when SCD patients with
G-6-PD deficiency have malaria, there is a significant risk of developing
hemolytic anemia crises, sepsis, hemoglobinuria and renal failure after
taking anti-malarials or eating oxidative foods like fava beans. SCD,
which is responsible for a high rate of medical consultations and increased
mortality in children, remains a public health problem for tropical countries.
It remains vital to screen for G-6-PD deficiency among SCD patients in
order to provide appropriate preventive and therapeutic measures.
ACKNOWLEDGMENTS
The authors want to thank all the villages and schools that agreed
to take part in this study and the laboratory technicians of St. Camille
Medical Centre, Ouagadougou. In particular, we are grateful for the skillful
help of Mr. Bakamba Robert, Mme. Justine Yara, Mr. Emmanuel Bouda and
Mme. Angèle Sanfo Bambara. This research would not have been possible
without the friendly and constructive support of the Italian Episcopal
Conference (C.E.I.) and the RADIM House in Italy (Doctor Luigi SPARANO).
|
REFERENCES |
1: Akoglu, T., F.L. Ozer and E. Akoglu, 1986. The coincidence of glucose-6-phosphate dehydrogenase deficiency and hemoglobin S gene in cukurova province, Turkey. Am. J. Epidemiol., 123: 677-680.
2: Ali, N., M. Anwar, M. Ayyub, F.A. Bhatti, M. Nadeem and A. Nadeem, 2005. Frequency of glucose-6-phosphate dehydrogenase deficiency in some ethnic groups of Pakistan. J. Coll. Phys. Surg. Pak., 15: 137-341. Direct Link |
3: Allison, A.C., 1954. The distribution of the sickle-cell trait in east Africa and elsewhere and its apparent relationship to the incidence of subtertian malaria. Trans. Royal. Soc. Trop. Med. Hyg., 48: 312-318.
4: Balgir, R.S., 2005. The spectrum of haemoglobin variants in two scheduled tribes of Sundargarh district in northwestern Orissa, India. Ann. Hum. Biol., 32: 560-573. Direct Link |
5: Bienzle, U., O. Sodeinde, C.E. Effiong and L. Luzzatto, 1975. Glucose 6-phosphate dehydrogenase deficiency and sickle cell anemia: Frequency and features of the association in an African community. Blood, 46: 591-597.
6: Bouanga, J.C., R. Mouele, C. Prehu, H. Wajcman, J. Feingold and F. Galacteros, 1998. Glucose-6-phosphate dehydrogenase deficiency and homozygous sickle cell disease in Congo. Hum Hered., 48: 192-197.
7: Ciftci, M., 2005. Effects of some drugs on the activity of glucose 6-phosphate dehydro-genase from rainbow trout erythrocytes in vitro. J. Enzyme Inhib. Med. Chem., 20: 485-489. Direct Link |
8: Diallo, D., A.K. Traore, M. Baby, A.A. Rhaly, G. Bellis and A. Chaventre, 1994. Haemoglobinopathies C and S in the dogons. Nouv Rev. Fr Hematol., 35: 551-554.
9: Diop, S., D. Thiam, A. Sene, M. Cisse, K. Fall and A.O. Toure-All et al., 2000. Association drepanocytose-deficit en G-6-PD: Prevalence et influence sur le profil evolutif. Med. Afr. Noire., 47: 7-7.
10: Diop, S., A. Sene, M. Cisse, A.O. Toure and O. Sow et al., 2005. Prevalence and morbidity of G6PD deficiency in sickle cell disease in the homozygote. Dakar Med., 50: 56-60. Direct Link |
11: El-Hazmi, M.A. and A.S. Warsy, 1986. Glucose-6-phosphate dehydrogenase polymorphism in the Saudi population. Hum. Hered., 36: 24-30.
12: El-Hazmi M.A. and A.S. Warsy, 1987. Interaction between glucose-6-phosphate dehydrogenase deficiency and sickle cell gene in Saudi Arabia. Trop. Geogr. Med., 39: 32-35.
13: Enevold, A., L.S. Vestergaard, J. Lusingu, C.J. Drakeley and M.M. Lemnge et al., 2005. Rapid screening for glu-cose-6-phosphate dehydrogenase deficiency and haemoglobin polymorphisms in Africa by a simple high-throughput SSOP-ELISA method. Malar. J., 4: 4-61. CrossRef | Direct Link |
14: Fleming, A.F., J. Storey, L. Molineaux, E.A. Iroko and E.D. Attai, 1979. Abnormal haemoglobins in the Sudan savanna of Nigeria. I. Prevalence of haemoglobins and relationships between sickle cell trait, malaria and survival. Ann. Trop. Med. Parasitol., 73: 161-172.
15: Gbadoe, A.D., K.Atsou, O.A. Agbodjan-Djossou, E. Tsolenyanu and M. Nyadanu et al., 2001. Ambulatory management of sickle cell disease: Evaluation of the first year follow up of patients in the pediatric department of Lome, Togo. Bull. Soc. Pathol. Exot., 94: 101-105. Direct Link |
16: Ghani, R., M.A. Manji and N. Ahmed, 2002. Hemoglobinopathies among five major ethnic groups in Karachi, Pakistan. Southeast Asian. J. Trop. Med. Public Health, 33: 855-861. Direct Link |
17: Gupte, S.C., P.U. Patel and J.M. Ranat, 2005. G6PD deficiency in vataliya prajapati community settled in Surat. Ind. J. Med. Sci., 59: 51-56. Direct Link |
18: Jacob, E., J.E. Beyer, C. Miaskowski, M. Savedra, M. Treadwell and L. Styles, 2005. Are there phases to the vasoocclusive painful episode in sickle cell disease? J. Pain Symptom Manage., 29: 392-400. Direct Link |
19: Kaplan, M., M. Muraca, H.J. Vreman, C. Hammerman and M.T. Vilei et al., 2005. Neonatal bilirubin production-conjugation imbalance: Effect of glucose-6-phosphate dehydrogenase deficiency and borderline prematurity. Arch. Dis. Child Fetal Neonatal Ed., 90: F123-F127. Direct Link |
20: Labie, D., C. Richin, J. Pagnier, M. Gentilini and R.L. Nagel, 1984. Hemoglobin S and C in upper volta. Hum. Genet., 65: 300-302.
21: Laosombat, V., B. Sattayasevana, T. Chotsampancharoen and M. Wongchanchailert, 2006. Glu-cose-6-phosphate dehydrogenase variants associated with favism in Thai children. Int. J. Hematol., 83: 139-143. Direct Link |
22: Lewis, R.A., R.W. Kay and M. Harthorn, 1966. Sickle cell disease and glucose-6-phosphate dehydrogenase. Acta Haematol (Basel)., 36: 399-411.
23: Lewis, R.A., 1973. Glucose-6-phosphate dehydrogenase electrophoresis in Ghanaians with AA and SS haemoglobin. Acta Haematol., 50: 105-111.
24: Luzzatto, L. and N.C. Allan, 1968. Relationship between the genes for glucose-6-phosphate dehy-drogenase and for haemoglobin in a Nigerian population. Nature, 219: 1041-1042.
25: Mockenhaupt, F.P., B. Rong, M. Gunther, S. Beck and H. Till et al., 2000. Anaemia in pregnant Ghanaian women: Importance of malaria, iron deficiency and haemoglobinopathies. Trans. R. Soc. Trop. Med. Hyg., 94: 477-483. CrossRef | Direct Link |
26: Modiano, D., G. Luoni, B.S. Sirima, J. Simpore and F. Verra et al., 2001. Haemoglobin C protects against clinical Plasmodium falciparum malaria. Nature, 414: 305-308. CrossRef | Direct Link |
27: Modiano, D., G. Luoni, B.S. Sirima, A. Lanfrancotti and V. Petrarca et al., 2001. The lower susceptibility to Plasmodium falciparum malaria of Fulani of Burkina Faso (West Africa) is associated with low frequencies of classic malaria-resistance genes. Trans. R Soc. Trop. Med. Hyg., 95: 149-152. Direct Link |
28: Muzaffer, M.A., 2005. Neonatal screening of glucose-6-phosphate dehydrogenase deficiency in Yanbu, Saudi Arabia. J. Med. Screen., 12: 170-171. CrossRef | Direct Link |
29: Ozmen, I. and O.I. Kufrevioglu, 2004. Effects of antiemetic drugs on glucose 6-phosphate dehy-drogenase and some antioxidant enzymes. Pharmacol. Res., 50: 499-504. Direct Link |
30: Rattazzi, M.C., L.M. Corash, G.E. van Zanen, E.R. Jaffe and S. Piomelli, 1971. G6PD deficiency and chronic hemolysis: four new mutants--relationships between clinical syndrome and enzyme kinetics. Blood, 38: 205-218.
31: Rogers, Z.R., 2005. Priapism in sickle cell disease. Hematol. Oncol. Clin. North Am., 19: 917-928.
32: Saad, S.T. and F.F. Costa, 1992. Glucose-6-phosphate dehydrogenase deficiency and sickle cell dis-ease in Brazil. Hum. Hered., 42: 125-128.
33: Samuel, A.P.W., N. Saha, J.K. Acquaye, A. Omer, K. Gameshagura and E. Hassounh, 1986. Association of red cell glucose-6-phosphate dehydrogenase with haemoglobinopathies. Hum. Hered., 36: 107-112.
34: Shimizu, H., M. Tamam, A. Soemantri and T. Ishida, 2005. Glucose-6-phosphate dehydrogenase deficiency and Southeast Asian ovalocytosis in asymptomatic Plasmodium carriers in Sumba island, Indonesia. J. Hum. Genet., 50: 420-424. Direct Link |
35: Simpore, J., S. Pignatelli, S. Barlati and S. Musumeci, 2002. Biological and clinical presentation of patients with hemoglobinopathies attending an urban hospital in Ouagadougou: Confirmation of the modification of the balance between HbS and HbC in Burkina Faso. Hemoglobin, 26: 121-127. Direct Link |
36: Singh, S., D.K. Singh, R. Gupta, S. Nigam and T. Singh, 2006. Persistent splenomegaly in an adult female with homozygous sickle cell anemia. Hematology, 11: 63-65. Direct Link |
37: Steinberg, M.H. and B.J. Dreiling, 1974. Glucose-6-phosphate dehydrogenase deficiency in Sickle-cell anemia. A study in adults. Ann. Int. Med., 80: 217-220.
38: Storey, J., A.F. Fleming, R. Cornille-Brogger, L. Molineaux, T. Matsushima and I. Kagan, 1979. Abnormal haemoglobins in the Sudan savanna of Nigeria. IV. Malaria, immunoglobulins and antimalarial antibodies in haemoglobin AC individuals. Ann. Trop. Med. Parasitol., 73: 311-315.
39: Trabuchet, G., J. Elion, O. Dunda, C. Lapoumeroulie and R. Ducrocq et al., 1991. Nucleotide sequence evidence of the unicentric origin of the beta C mutation in Africa. Hum. Genet., 87: 597-601. Direct Link |
40: Williams, T.N., T.W. Mwangi, S. Wambua, N.D. Alexander and M. Kortok et al., 2005. Sickle cell trait and the risk of Plasmodium falciparum malaria and other childhood diseases. J. Infect. Dis., 1: 178-186. Direct Link |
41: Znaidi, R., R. Hafsia, A. M'Rad, R. Kastally and A. Hafsia, 1995. Association of heterozygote dre-panocytosis and G6PD deficiency: Apropos of a case. Tunis Med., 73: 415-417.
|
|
|
 |