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ORIGINAL ARTICLE The Prevalence of Cytomegalovirus, 2
3
4
5
Hepatitis B, Hepatitis C, and HIV Infections 4
5
6
7
among Hemophilic Patients in Sanandaj in 6
7
8
9
2017 8
9
10 10
11 11
12 Mostafa Zoorpaikar1, Reza Khalili Dizaji2, Ali Maleki3, Mohsen Zhaleh3, 12
13 Sajjad Babaei3, Nasrollah Sohrabi3 13
14 1
Department of ???, School of Medicine, Kurdistan University of Medical Sciences, Sanandaj, Iran, 14
AQ2
15 2
Department of Internal Medicine, Kurdistan University of Medical Sciences, Sanandaj, Iran, 3Department 15
16 of Laboratory Sciences, School of Paramedical Sciences, Kermanshah University of Medical Sciences, 16
17 Kermanshah, Iran 17
18 18
19 Abstract 19
20 20
21 Background and Objective: As Cytomegalovirus (CMV) has been distributed widely and great number of people 21
22 are affected by it, such as hemophilic patients, and given the prevalence and complications of CMV, hepatitis B, 22
23 hepatitis C, and HIV and lack of study in Kurdistan province in this regard, this study was conducted to evaluate 23
24 the prevalence of CMV infection and other viruses among the hemophilic patients. This study can be used to 24
25 reduce and solve the problem of hemophilic patients and health system plans. The objective of this study was to 25
26 evaluate the prevalence of mentioned infections among hemophilic patients in Besat Hospital in Sanandaj in 2017. 26
27 Materials and Methods: This is a descriptive study in which its population included all 121 hemophilic patients, 27
28 diagnosed in Besat Hospital of Kurdistan province. They were examined in terms of infection of four viruses, 28
29 including hepatitis C, hepatitis B, CMV, and HIV. It should be noted that the definition of infection was based 29
30 on global criteria. Results: Of 121 patients, 95 cases were tested for hepatitis C, which 22 of them (23.1%) were 30
31 positive in terms of HCV-Ab, and 13 people (13.6%) were suspected. In addition, 88 of them were tested for CMV, 31
32 which 70 of them (79.5%) were positive in terms of CMV-Ab. In terms of HIV and HBV, all tested patients were 32
33 seronegative. Among these patients, 48 ​​patients had severe hemophilia, who recurrently received coagulation 33
34 factor. Among them, 14 people (29.1%) were seronegative in terms of HCV-Ab, and 43 people (89.5%) were 34
35 seronegative in terms of CMV-Ab. In addi t ion, nine of them (18.7%) were suspected in terms of HCV-Ab. 35
36 Conclusion: The recent study showed that the prevalence of hepatitis C among hemophilic patients is higher than 36
37 that in other people of the community. In addition, among hemophilic patients, the prevalence of hepatitis C is 37
38 higher in patients who received coagulation factor recurrently than that in other patients. The prevalence of CMV 38
39 is also more in patients receiving factor recurrently than that in rest of the patients. Therefore, patients receiving 39
40 blood and blood products should be periodically evaluated for virology. 40
41 41
42 Key words: Cytomegalovirus, hemophilia, hepatitis B, hepatitis C, HIV 42
43 43
44 44
45 hemophilia. This disease is mainly seen in males and females 45
INTRODUCTION
46 are generally asymptomatic. Clinically, hemophilia A and B 46

O
47 47
wing to impaired coagulation factors
48 48
(depending on the level of factors in
49 Address for correspondence: 49
the blood), hemophilic patients should
50 Nasrollah Sohrabi, Department of Laboratory Sciences, 50
receive blood product exogenously to maintain
51 School of Paramedical Sciences, Kermanshah University 51
their homeostasis. Hemophilia is a chromosome
52 of Medical Sciences, Kermanshah, Iran. 52
X-dependent disorder, making the person prone
53 Tel: +918 339 9344. E-mail: ??? AQ3
53
to bleeding due to coagulation factor 8 or factor
54 54
9 deficiencies. Type A hemophilia prevalence
55 Received: 10-05-2018 55
is 1 per 10,000 people, and type B hemophilia
56 Revised: 15-06-2018 56
prevalence is 1 per 60,000 people. Almost
57 Accepted: 21-06-2018 57
80% of hemophilic patients suffer from type A

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Zoorpaikar, et al.: Running title missing??? AQ1
1 are not distinguishable, and the severity and phenotype of the in the Sanandaj in 2017. As an epidemiological study, its 1
2 disease are influenced by the level of remaining factors 8 and results can be used for health promotion planning and as a 2
3 9. Patients need to receive the required factors during their base for future studies. 3
4 lifetime based on the severity of the disease and the level of 4
5 factors.[1,2] Hemophilia patients are exposed to the blood of 5
6 thousands of donors and are prone to blood-borne diseases METHODOLOGY 6
7 during their lives due to the frequent need to receive the 7
8 blood products. Blood-borne diseases are the leading cause The study type 8
9 of mortality in hemophilic patients. Approximately 7–10% 9
10 of hemophilic patients have a severe disease, that is, their This research was a descriptive, cross-sectional study. 10
11 coagulation factor is <1% (1 and 3). Therefore, there is always 11
12 a concern that the patient to be infected with blood-borne 12
13 infections. As these infections, which the most important of Population of the study 13
14 them is viral infections, are followed by bad consequences and 14
15 increase morbidity and mortality in patients[3,4] and preventing All hemophilic patients admitted to Sanandaj Besat Hospital 15
16 the transmission of these viruses is vital. Hence, medical in 2017, whose files were reviewed by written consent of the 16
17 science is always looking for a solution for this problem.[5] patients or first-degree relatives of the patients and according 17
18 to the Ethical Code of Kermanshah Medical Science 18
19 The risk of transmission of hepatitis and human retroviruses, University. Personal information and the name of patients 19
20 such as HIV, has been reduced through screening of antibodies remained confidential. Patients with intravenous drug users 20
21 before transfusion. However, Cytomegalovirus (CMV) can (IDU), patients with high-risk sexual behaviors, diseases 21
22 be transmitted through blood transfusion[6-8] due to the lack of cases transmitted from mother to embryo, and suspicious 22
23 routine screening of all blood donors. The CMV is a member of needling were excluded from the study. 23
24 the herpesviruses family and betaherpesvirus subfamily, causing 24
25 various syndromes in children and adults. It is also the most Data collection 25
26 common cause of congenital and neonatal viral infections in the 26
27 world. The prevalence of this infection in human communities 27
In this study, 121 hemophilic patients who had a medical file
28 varies from 40% to 99%. Recent studies on neonatal CMV 28
in Besat Hospital of Sanandaj and had no exclusion criteria
29 infection followed by transfusion have proved that donors with 29
were selected and examined. To obtain information required
30 antibody are the source of CMV infection after transfusion in 30
for this study, a checklist was prepared. It included general
31 recipient patients without antibodies against the CMV.[9] Das 31
information and virology of hemophilic patients. In this
32
AQ4 et al. published an article entitled “CMV prevalence in blood 32
study, the results of the individual tests conducted within the
33 donors and recipients.” In this prospective study, 2100 blood 33
last 6 months were recorded, and these tests were performed
34 donors and 200 blood recipients were studied, and serum level 34
for those test date was older than 6 months. Serologic tests
35 of the patients was examined in terms of antibodies against 35
were performed using the ELISA method and diagnostic kits
36 CMV using ELISA method. Based on the results obtained from 36
(eBioscience Inc, United States).
37 2100 blood donors, 98.6% of the people had IgG, and only one 37
38 person had IgM. Among 200 blood recipients, 100% of the 38
39 people had IgG, and only one person had IgM.[10] Data analysis 39
40 40
41 In this regard, other studies conducted in different countries This study data entered into the STATA-11 software. 41
42 on the prevalence of these infections among people who Quantitative descriptive goals were calculated by calculating 42
43 received blood or blood products for any cause showed the mean and standard deviations and, if needed, other 43
44 different results.[6,11,12] A part of these differences is due quantitative indicators such as the mode and median. 44
45 to the social and cultural conditions, lifestyle and literacy Qualitative descriptive goals were calculated by calculating 45
46 level of people, and the prevalence of these infections in the the ratios along with the confidence interval. 46
47 target community, so the results of a single study cannot be 47
48 generalized to all communities. Based on what was stated, 48
49 the prevalence of the mentioned infections needs to be RESULTS 49
50 examined at the national and even at the smaller scale of 50
51 the province level. Given that what was stated, conducting Demographic characteristics 51
52 research in this regard seems to be an essential, since based 52
53 on the role of early prevention in modern medicine, it is In our study, 121 patients with coagulation disorder, which 53
54 necessary to identify all risk factors of various diseases majority of them were hemophilic patients, were evaluated. 54
55 to prevent the disease and its complications. This study Their demographic characteristics are presented in Table 1a. 55
56 examined the prevalence of hepatitis B, hepatitis C, and HIV The place of birth and living place of the studied patients are 56
57 57
and CMV viral infections among the hemophilic patients also presented in Table 1b.

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Zoorpaikar, et al.: Running title missing??? AQ1
1 Family history Virologic findings 1
2 2
3 Family history information of coagulation disorders was Out of a total of 121  patients, whose medical files were records 3
4 reported in medical files of 113 patients. In this regard, at Besat Hospital in Sanandaj, 90–95 of them participated in 4
5 58 (51.3%) patients had no family history of coagulation the study to perform the test. The patients, who did not admit 5
6 disorders. About 25 (22.2%) patients had at least one brother to this center, were mostly those patients whose medical files 6
7 affected this disorder, and 10 (8.8%) patients had at least one could not be examined or those who had not received factor. 7
8 sister affected this disorder. Five (4.5%) patients had mother Finally, the virology tests were taken from the patients, and 8
9 with this disorder, and one patient had father with coagulation following results were obtained. 9
10 disorder. The results of the family history of patients in terms 10
11 of coagulation disorders are presented in Table 2. 11
Prevalence of Hepatitis B (HBs-Ag)
12 12
13 13
Frequency of blood groups Out of 95 HBs-Ag patients underwent HBs-Ag test, no
14 14
patient had positive HBs-Ag.
15 15
The frequency of different types of blood groups of patients
16 16
was also examined, and the results of this examination are
17 Status of HBs-Ab 17
shown in Table 3.
18 18
19 Out of the 92  patients underwent HBs-Ab, 65  (70.6%) patients 19
20 Frequency of coagulation disorders were positive, and 27 (29.3%) were negative [Table 5]. 20
21 21
22 With regard to the frequency of coagulation disorders in Table 3: Frequency of blood group types among 22
23 patients, the investigations revealed that among the patients, hemophilic patients studied 23
24 hemophilia A with 67 people (55.3%) ranked first in terms of Blood group type n (%) Confidence interval 24
25 prevalence and it accounts for 85.9% of the total hemophilia 25
A+ 30 (24.7) (13.4–31.5)
26 cases. The results of this study are presented in Table 4. 26
27 B+ 17 (13.9) (6–21.7) 27
28 O+ 55 (45.5) (34–56.7) 28
29 Table 1a: Frequency of gender in patients studied 29
AB+ 7 (5.7) (1.7–8)
30 Variable  n (%) Confidence Mean of
Other 12 (10.2) (4.3–15.4)
30
31 (gender) interval age (SD) 31
32 Total 121 (100) 32
Male 85 (70.2) (61.9–78.2) 24.9 (14.8)
33 Female 36 (29.8) (21.4–38) 27.4 (13.3) 33
34 Table 4: Frequency of types of hemophilia among 34
Total 121 (100)
35 patients studied 35
36 Coagulation n (%) Confidence interval 36
37 disorder 37
Table 1b: Living place of the participants
38 38
Variable n (%) Confidence interval A 67 (55.3) (43.2–69.9)
39 39
40 City 103 (88.6) (81.4–95.7) B 11 (9) (6.2–17.8) 40
41 Village 18 (11.4) (4.2–18.5) 7a 11 (9) (6.2–17.8) 41
42 Total 121 (100) VWF 15 (12.4) (4.6–18.9) 42
43 Others 17 (14) (6.8–21.8) 43
44 44
45 45
Table 2: Family history of patients in terms of Table 5: Immunity status against hepatitis
46 46
coagulation disorders B (HBs‑Ab) among patients studied
47 47
48 Positive family n (%) Confidence interval ??? Prevalence AQ548
history
49 n (%) Confidence 49
50 No 58 (51.3) (43.1–59.5) interval 50
51 Father 1 (0.8) (−0.2–4.2) Variable 51
52 Mother 5 (4.5) (0.8–11.8) 52
Positive 65 (70.6) (62.3–77.1)
53 53
Brother 25 (22.2) (12.4–32.1) Negative 27 (29.3) (21.9–37.5)
54 54
55 Sister 10 (8.8) (3.7–14.1) All people tested 92 (100) ‑ 55
56 Others (uncle …) 14 (12.4) (4.4–17.6) Unknown 29 (13.2–31) 56
57 Total 113 (100) (without test) (24 out of patients) 57

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1 Prevalence of hepatitis C (HCV-Ab) Table 6: The prevalence of hepatitis C among 1
2 patients studied 2
3 With regard to HCV-Abs, out of 95 patients tested, 22 (23.1%) AQ5 3
??? Prevalence
4 people were positive, and 60 (63.1%) patients were negative, 4
5 and 13 (13.6%) people had suspected result [Table 6]. n (%) Confidence 5
6 interval 6
7 Variable 7
Prevalence of HIV-AIDS
8 Positive 22 (23.1) 15.9–31.6 8
9 Negative 60 (63.1) 54.2–71.8 9
In the case of HIV-Ab, all of 93 tested patients were negative.
10 10
Suspected 13 (13.6) 4.2–22.4
11 11
12 Prevalence of CMV All people tested 95 (100) ‑ 12
13 Unknown 26 11.8–25.9 13
14 In terms of CMV-Ab, out of 88 patients tested, 70 (79.5%) (without test) (21.4 out of patients) 14
15 were positive and 18 (20.5%) were negative [Table 7]. 15
16 16
17 Table 7: The prevalence of CMV among patients 17
Virology tests in patients with severe hemophilia
18 studied 18
19 ??? Prevalence AQ5 19
Due to the non-admitting to the center by a number of
20 20
patients for performing virology tests, a number of tests did n (%) Confidence
21 21
not complete. Hence, we decided to prepare a table using the interval
22 22
information of those patients who admitted to the center to Variable
23 23
receive the factor as well as those who received the factor
24 Positive 70 (79.5) 71.7–95 24
with other coagulation disorders patterns for more precise
25 Negative 18 (20.5) 12.3–28.8 25
examination of the virology status of the patients.
26 All people tested 88 (100) ‑ 26
27 27
This group of patients is, in fact, the group who had severe Unknown 33 30.1–42.3
28 28
coagulation disorders. Their approximate number was 55 in  (37.5 out of patients)
29 29
the province of Kurdistan. Based on the medical files of them CMV: Cytomegalovirus
30 30
in Besat Hospital in Sanandaj, 50 people were available at
31 31
first, which after contacting and following up them, 48 of
32 32
them were tested for virology and their results are presented Table 8: Status of HBS‑Ab among severe
33 33
below. hemophilic patients
34 34
35 HBs‑Ab n (%) Confidence interval 35
36 Frequency and prevalence of hepatitis B Positive 34 (70.8) 62.4–81 36
37 Negative 14 (29.1) 22.3–38.5 37
38 Out of 48 patients, no patient had hepatitis B. Total 48 (100) ‑ 38
39 39
40 40
Status of HBs-Ab
41 41
Table 9: Frequency and prevalence of hepatitis C
42 42
Out of 48 patients, 14 (70.8%) patients do not have adequate among severe hemophilic patients
43 43
immunity against hepatitis B [Table 8]. HCV‑Ab n (%) Confidence interval
44 44
45 Positive 14 (29.1) 22.8–35.5 45
46 Frequency and prevalence of hepatitis C Negative 25 (52) 44.4–60.1 46
47 47
Suspected 9 (18.7) 10.3–23.2
48 About 14 patients (29.1%) are seropositive in terms of 48
49 Total 48 (100) ‑ 49
hepatitis C, indicating a high prevalence of hepatitis C among
50 patients with severe hemophilia. Moreover, 9 (18.7%) of 50
51 patients had suspected serology [Table 9]. 51
Frequency and prevalence of CMV-Ab
52 52
53 53
Frequency and prevalence of HIV About 43 (89.5%) patients have positive CMV-Ab, indicating
54 54
that the prevalence of CMV infection is more among these
55 55
No patient was seropositive in terms of HIV-Ab. patients than that in other patients [Table 10].
56 56
57 57

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Zoorpaikar, et al.: Running title missing??? AQ1
1 Table 10: Frequency and prevalence of CMV‑Ab viral infection and seronegative CMV, these patients should 1
2 among severe hemophilic patients not be exposed to blood products or liquids of the body of 2
3 donors with seropositive CMV.[15] 3
CMV‑Ab n (%) Confidence interval
4 4
5 Positive 43 (89.5) 83.5–97.2 In another study conducted by Jacson et al. in 1988, the 5
6 Negative 5 (10.4) 2.9–17.2 prevalence of antibody against CMV was examined in 6
7 Total 48 (100) ‑ the serum of non-homosexual hemophilic patients and 7
8 CMV: Cytomegalovirus
homosexual hemophilic male patients with HIV-1. The 8
9 results showed that 57% of hemophilic patients with HIV-1 9
10 had positive antibody. In addition, 65% of hemophilic 10
11 DISCUSSION AND CONCLUSION patients with HIV-1 infection had symptomatic-HIV-1 and 11
12 CMV-positive antibody.[16] However, in our study, 79.5% of 12
13 This research was a descriptive study in which 121 patients patients were seropositive, and among patients who received 13
14 with coagulation disorders in Kurdistan province, which most factor recurrently, 89.5% (n = 43) were seropositive. Based 14
15 of them were hemophilic, were examined in terms of infection on the current research, the prevalence of hepatitis C and 15
16 with several viruses. It was found that 23.1% of total patients CMV in a group of patients received factor recurrently is 16
17 and 29.1% of patients with the factor level <1% had positive higher than that in total number of patients. Moreover, the 17
18 HCV-Ab. With regard to CMV antibody, these values were prevalence of hepatitis C among hemophilic patients is higher 18
19 79.5% and 89.5%, respectively. HBs-Ab was also positive than that in other people of the community. If confirmed 19
20 in 70.6% and 70.8% of patients in both groups, respectively. by other studies, appropriate and practical plans should be 20
21 In addition, no patient was positive in terms of HBs-Ag developed in this regard to reduce its transfusion rate and to 21
22 and HIV-Ab. Blood and blood products, long-term chronic treat patients. The prevalence of anti-CMV antibody in this 22
23 hemodialysis, and IDU have been reported as important risk study (most parts of Iran and worldwide) shows high level, so 23
24 factors for the transmission of many infectious diseases in complementary studies and planning are required for patients 24
25 hemodialysis and hemophilia patients.[13] Moreover, viral and those people who are at risk for this virus. In addition, 25
26 hepatitis in developing countries is considered as a problem the prevalence of hepatitis B and HIV in patients of our study 26
27 in hemophilic patients.[14] The clinical importance of the was zero, indicating the proper screening of blood and blood 27
28 infection with hepatitis B and C and HIV in humans is well products. 28
29 known; however, the clinical importance of the infection 29
30 with the CMV virus and its association with acute or chronic 30
31 hepatitis and liver enzymes have not yet been well studied. ACKNOWLEDGMENT 31
32 32
33 One of the epidemiological issues discussed in this regard is We thereby appreciate the Besat Hospital of Sanandaj city for 33
34 the question of whether blood donors should be screened for providing an opportunity to conduct this study. 34
35 viruses, which have been discovered in human blood but have 35
36 not been yet recognized as the cause of the disease. To answer 36
37 this question, many factors are involved, including knowing REFERENCES 37
38 the prevalence of the virus in blood donors and recipients 38
39 of that community, the probability of the virus transmission 1. Sona PS, Lingam CM. Hemophilia-an overview. Int J 39
40 by blood transfusion, the virus’s role in the development of Pharm Sci Rev Res 2010;5:18-26. 40
41 acute and chronic hepatitis, and the ability to produce long- 2. Zimmerman B, Valentino LA. Hemophilia: In review. 41
42 term viremia. This requires examining the prevalence of the Pediatr Rev 2013;34:289-94. 42
43 above-mentioned viruses among blood recipients and donors 3. Unim B, Veneziano MA, Boccia A, Ricciardi W, La 43
44 at first step and then comparing them with other people in Torre G. Haemophilia A: Pharmacoeconomic review of 44
45 the community especially the donors of these products. prophylaxis treatment versus on-demand. Sci World J 45
46 Thus, the results of this study can be helpful in achieving 2015;2015:596164. 46
47 the final answer for the asked questions by gaining a better 4. Ragni MV, Triulzi DJ, Bass D, Duerstein S. Transfusion 47
48 understanding of the prevalence of these viruses among high- and Cytomegalovirus-associated AIDS-defining 48
49 risk individuals. In a study conducted by Rabkin et al. in 1993 disease in hemophiliacs. Hemophilia malignancy study. 49
50 on more than 390 hemophilic patients, it was found that 49% Transfusion 1996;36:681-4. 50
51 of the patients had IgG antibodies for CMV in their serum 5. Herve P. Transfusion safety: Emergent or hypothetical 51
52 (1983). They were older than the rest of the participants. In risks. Transfus Clin Biol 2000;7:30-8. 52
53 addition, it was revealed that people with seropositive CMV 6. Furui Y, Satake M, Hoshi Y, Uchida S, Suzuki K, 53
54 are more suspected to AIDS compared to other people. Older Tadokoro K. CMV seroprevalence in Japanese blood 54
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56 serum samples. The results of this study indicated that to elderly donors. Transfusion 2013;53:2190-7. 56
57 7. Hecker M, Qiu D, Marquardt K, Bein G, Hackstein H. 57
prevent more deaths among hemophilic patients with HIV

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6 DNA, RNA and antibody in normal donor blood. J Infect Middle East. Saudi J Kidney Dis Transpl 2011;22:1-9. 6
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8 9. Stuart PA. Transfusion-associated Cytomegalovirus Hilgartner MJ, et al. Cytomegalovirus infection and risk 8
9 infections. Rev Infect Dis 1983;5:977-93. of AIDS in human immunodeficiency virus-infected 9
10 10. Das B, Gagandeep K, Sabita B. Seroprevalence of hemophilia patients. J Infect Dis 1993;168:1260-3. 10
11 Cytomegalovirus antibodies among blood donors and 16. Jackson JB, Erice A, Englund JA, Edson JR, 11
12 multitransfused recipients–a study from North India. Balfour HH Jr. Prevalence of Cytomegalovirus antibody 12
13 Transfus Apher Sci 2014;50:438-42. in hemophiliacs and homosexuals infected with 13
14 11. Bate SL, Dollard SC, Cannon MJ. Cytomegalovirus human immunodeficiency virus type 1. Transfusion 14
15 seroprevalence in the United States: The national health 1988;28:187-9. 15
16 and nutrition examination surveys, 1988-2004. Clin 16
17 Infect Dis 2010;50:1439-47. 17
18 12. Hejazi S, Abaszadeh AM, Karamiyar M. Prevalence of Source of Support: Nil. Conflict of Interest: None declared. 18
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AQ3:Kindly provide email id
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AQ4:Kindly check the edit made.
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