The Association Between Oral Candidiasis and ABO Blood Type in Infants in Kirkuk City, Iraq

Tajer Abdullah, Iman; M. Noori, Asoda; Lateef Mohammed , Bari; Beebany, Shakhawan

doi:10.30699/ijmm.18.5.301

year 18, Issue 5 (September - October 2024) Iran J Med Microbiol 2024, 18(5): 301-307 | Back to browse issues page

‎ 10.30699/ijmm.18.5.301

Mendeley

Zotero

RefWorks

Tajer Abdullah I, M. Noori A, Lateef Mohammed B, Beebany S. The Association Between Oral Candidiasis and ABO Blood Type in Infants in Kirkuk City, Iraq. Iran J Med Microbiol 2024; 18 (5) :301-307
URL: http://ijmm.ir/article-1-2418-en.html

The Association Between Oral Candidiasis and ABO Blood Type in Infants in Kirkuk City, Iraq

Iman Tajer Abdullah¹

, Asoda M. Noori²

, Bari Lateef Mohammed¹

, Shakhawan Beebany³

1- Department of Biology, College of Science, University of Kirkuk, Kirkuk, Iraq
2- Department of Biology, College of Science, Garmian University, Sulaymaniyah, Iraq , asuda.nori@gmail.com
3- Department of Chemistry, College of Science, University of Kirkuk, Kirkuk, Iraq

Keywords: Oral candidiasis, C. albicans, Oral infection, Blood group (ABO)

Full-Text [PDF 479 kb] (237 Downloads) | Abstract (HTML) (779 Views)

Full-Text: (143 Views)

Introduction

Candida albicans (C. albicans) infection of the mouth cavities, called oral candidiasis, was initially documented in 1838. According to the GonÇAlo, de Souto Medeiros (1), immunocompromising disorders such as HIV/AIDS, chronic systemically steroid and antibiotic usage, and extremities in age (infants and elderlies) can all contribute to the immunological reduction, which is the broader cause of the syndrome (1, 2).
Oral candidiasis is diagnosed clinically, gathering health information, and evaluating risk factors for the disease. For some forms, biopsy is advised in addition to the empirical therapy. When antifungal therapy is unsuccessful, cultures are often conducted (3, 4).
Immunocompetent people's typical oral microbiota includes candida. According to the Hellstein and Marek (5), 30–60% of the mature individuals and 45–65% of babies have Candida spp within their mouths. C. albicans, which has been isolated from over 80% of the lesions, is the most frequent species of Candida that causes oral candidiasis. According to the Macias-Paz, Pérez-Hernández (6), C. albicans is a dysmorphic yeast that can appear as either a yeast or a hypha depending upon the surroundings.
Candida glabrata (C. glabrata), Candida tropicalis (C. tropicalis), Candida kruesi (C. kruesi), Candida guillermondii (C. guillermondii), Candida lusitaniae (C. lusitaniae), Candida parapsilosis (C. parapsilosis), Candida pseudotropicalis (C. pseudotropicalis), and Candida stellate (C. stellate) are additional species that have been linked, however, they are far less prevalent (5). It has been demonstrated that non-albicans Candida species invade individuals 80 years of age and older at higher rates than young people (7).
Immunocompetent and immunocompromised persons can both get oral candidiasis, although immunocompromised hosts are more likely to contract it. Oral candidiasis affects almost 90% of people with HIV at some time throughout their illness (8). Both men and women can get oral candidiasis. It usually affects newborns and neonates. Due presumably to the establishment of the host immunity, it is less prevalent in neonates who are older than six months but more widespread throughout the 4^th week of life. Hepatosplenomegaly, rashes, diarrhea, and recurrent infections are indications and symptoms of the immunosuppression in these individuals (9).
Since fungi are opportunistic microorganisms, maternity and puberty appear to be especially vulnerable times for mom as well as baby to contract fungal infections. Pregnant women (30-40%) experience vaginal Candida spp. colonization; this might be because of the elevated levels of estrogen that encourage yeast adherence and penetrating in the mucous membrane of the vagina (10). This propensity appears to persist after birth, as evidenced by the observation made by Khadija, Abbasi (11) that postpartum females are more vulnerable to oral Candida spp. colonization, which demonstrates increased virulence features. Regarding the infants, conjecture is that Candida spp. colonization takes place in the initial hours following birth. Furthermore, a few numbers of research support the theory that isolates of fungi can be passed via mother to kid (12). Simultaneously, subsequent fungal infections that frequently arise in children using diapers are commonly known in newborns as thrush in the mouth, is a common illness in children, especially until the sixth month of life (13). Researchers showed that most carriers of oral Candida had blood group A, but the difference was not statistically significant (P>0.05). These results confirm the idea that there is no relationship between A, B, and O blood groups and their secretory forms with the number of Candida colonies (9).
In Iraq/Kirkuk city, there is lack of studies about relation of blood groups (ABO) with oral Candida spp. colonization in infants. Therefore, this research was designed to identify the association between blood type antigens (ABO) and oral candidiasis in infants.

Materials and Methods

2.1. Data collection and Blood Group Identification
Specimens were taken from 110 individuals who had oral candidiasis symptoms, primarily from the Children's Hospital in Kirkuk City and a few outlying clinics. The samples included from infants aged between 1 month and 18 months. Using monoclonal antibodies against the human A, B, and Rh D antigens of the blood types, the direct hemagglutination technique was conducted to ascertain the newborns' ABO and Rh blood groups.
2.2. Sample Collection and Candida Isolation
Cotton swabs were used to gather oral specimens, which were subsequently streaked on Sabouraud dextrose agar (SDA) (Ibn Al-betar/ Iraq) plates supplemented with 0.005 g/L chloramphenicol to inhibit the development of bacteria. The incubation was conducted at 30ºC for 48 hr. Next, the isolates were inspected for the size, shape, color, and texture using both macroscopic and microscopic evaluations (14). The genus Candida w:as char:acterized through its oval or oblong form and bipolar budding, an asexual method of development. The newly formed Candida cells were cream-white in color on culture medium. Their cells showed a diameter of three to six µm, and they occasionally form pseudohyphae (15).
2.3. Species Identification by Biochemical Tests
2.3.1. Catalase Test
A small portion of a colony was added to a drop of hydrogen peroxide on a microscope slide. If bubbles or froth is formed, the organism is considered catalase-positive (16).
2.3.2. Germ Tube Formation
Serum germ tube technique uses triplicate sets of the test tubes containing 0.5–1 mL of pooled human serum. The samples were inoculated with 2-3 colonies of each isolate. The tubes were incubated at 37°C for 3 hr. Then, a drop of each suspension was examined on the labeled microscope slide (16).
2.3.3. Chromogenic Agar Candida (CAC)
Chromogenic Agar Candida (CAC) (Paris/France) was used to selectively develop the isolates with features characteristic of Candida spp (16). After growing for 24 hr on SDA, a piece of the clean colony was plotted on CAC and incubated for 24 to 48 hr at 37ºC. The color of the communities helped identify the various species. According to the results of Brawner and Cutler, (17), C. albicans is green, C. glabrata is pink to purple, C. krusei is dark pink, and C. tropicalis is blue.
2.4. Statistical Analysis
SPSS (Statistical Package for Social Science) Software version 20 was used to analyze data. Chi–square test was utilized to compare differences at P≤ 0.05 level.

Results

3.1. Distribution of Participants Based on the Fungal Infection
The results of participants’ distribution showed 65% of infants positive for oral candidiasis compared to the infants without oral candidiasis (35%) (P<0.05). Data are shown in Table 1.

Table 1. Distribution of infants according to the oral candidiasis.

Results	N	%	P value
Positive	72	65%	P<0.05**
Negative	38	35%
Total	110	100%

3.2. Distribution of infected infants based on the gender
Findings exhibited significant difference between males and females. The most infected infants were males (67%) compared to females (33%) (P<0.05) (See Table 2).

Table 2. Distribution of infants with oral candidiasis according to gender

Gender	N	%	P value
Males	48	67%	P<0.05**
Females	24	33%
Total	72	100%

3.3. Distribution of infected infants based on the age groups
The outcomes revealed the most infected infants at age groups 7-12 months (60%) and least of them at >1 years (10%). It showed significant differences (P<0.05) among age groups as summarized in Table 3.

Table 3. Distribution of infants with oral candidiasis according to age groups

Age groups	N	%	P value
1_6 moths	22	31%	P<0.05***
7_12 moths	43	60%
>1 years	7	10%
Total	72	100%

3.4. Distribution of infected infants based on the Candida types
The results indicated that the most infected infants were positive for C. albicans (85%) that showed significant differences (P<0.05) with C. glabrata (8%), C. krusei (6%), and C. tropicalis (1%) (Table 4).

Table 4. Distribution of infants with oral candidiasis according to the Candida types

Candida types	N	%	P value
*C. albicans*	61	85%	P<0.05***
*C. glabrata*	6	8%
*C. krusei*	4	6%
*C. tropicalis*	1	1%
Total	72	100%

3.5. Distribution of infected infants based on the blood groups
The most infected infants were observed positive for O+ (46%) followed by A+ (26%) and B+ (19%). Few numbers were positive for A- (4%), B- (0), and O- (4%) with significant variation (P<0.05) among blood groups as shown in (Table 5).

Table 5. Distribution of infants with oral candidiasis according to the blood groups

Blood groups	N	%	P value
A+	19	26%	P<0.05***
B+	14	19%
O+	33	46%
A-	3	4%
B-	0	0%
O-	3	4%
Total	72	100%

3.6. Distribution of infected infants based on the Rh factor
Table 6 shows significant difference between the most infected infants positive for Rh (92%) compared to Rh- (8%) (P<0.05).

Table 6. Distribution of infants with oral candidiasis according to Rh factor

Rh factor	N	%	P value
Rh+	66	92%	P <0.05***
Rh-	6	8%
Total	72	100%

Discussion

The present study aimed to diagnosis the correlation between blood type antigens (ABO) and oral candidiasis in infants in Kirkuk city. The diagnosis of oral candidiasis is often made by the microscopic evaluation of the mouth mucosa specimen exhibiting diagnostic discoveries, as well as visual inspection of detachable white plaques or erythema tissues in the mouth. The genus Candida is characterized through its oval or oblong form and bipolar budding, an asexual method of development. The newly formed Candida cells are cream-white in color on culture medium. Their cells have a diameter of 3-6 μM and they occasionally form pseudohyphae (15).
Moreover, medical and microbiological testing may be used to diagnose the oral candidiasis (18). According to the previous investigation, oral candidiasis was found in 72 (65%) out of the 110 oral swabs when examined under the light microscope. Although the regional distribution of Candida strains varies, a prior study found that their prevalence was 35% (19). These results were lower (35%) than those of the current study, which highlighted 65% of the oral swabs with Candida.
Nevertheless, in a prior investigation, it was primarily found in seniors, irrespective of genders, aged 60 or older, and the frequency of oral candidiasis was not clearly associated with those who had a dry mouth, drinking or smoking, wearing dentures, or having hormonal imbalances (20). Generally speaking, these variables are risk factors for developing oral candidiasis.
According to Keyvanfar, Najafiarab (21) oral candidiasis is uncommon in the initial week after birth but can be developed in newborns and neonates. Due presumably to the emergence of host immunity, it is less prevalent in babies who are older than six months and more frequent around the 4^th week of life. The current results, which indicate a significant incidence of oral candidiasis in babies older than six months, do not align with these outcomes. The low immunological state of newborns and babies is linked to the increased occurrence of oral candidiasis in such children.
Cook, Ferreras-Antolin (22) results, which mirrored the current data, revealed that oral candidiasis was more common in men (55%) than in women (45%). However, Chuey Chuan, Daniel (23) found that oral candidiasis was more common in women (61%) than in men (39%). The host immunological state and sample size are the factors that influence the study differences.
Even though there is a significantly higher amount and more variety of Candida species on the breastbones of nursing women, the researchers discovered a strong correlation between bottle feeding and a higher likelihood of respiratory illnesses as well as gastrointestinal tracts (GIT) illnesses. Additionally, they discovered that only a fraction of breastfed infants suffered this kind of the yeast colonized in their mouths, which supports the theory that defense variables such as mother's milk offer security toward the Candida genus colonizing in the dental cavities of exclusively breastfed infants (24).
A recent study indicates that maternal transmission plays a significant role in the oral acquisition of C. albicans in young children. It may be possible to stop fungal transfer in the early stages of infancy by including detection for mother fungal-oral carriers and putting in place oral health awareness initiatives throughout the perinatal period (12).
Almost 40% of the healthy people have commensal (or invading) Candida in their tooth cavities. Relative to the healthy people, immunosuppressed persons have been observed to have a higher incidence of Candida spp in their dental cavities. It shows that mouth yeasts were present in the salivary of 55% of hospitalized individuals with advanced cancers have Candida spp (25).
Cook, Ferreras-Antolin (22) mentioned that C. albicans showed the highest prevalence in neonates (35%), followed by C. glabrata (5%), and C. tropicalis (2%). These outcomes were close to present findings. Additionally, Cook, Ferreras-Antolin (22) mentioned that most of the Candida strains were resistant to fluconazole. Another study showed C. albicans with high prevalence in oral infants (67%), followed by C. tropicalis (30%), C. parapsilosis (15%), and C. krusei (17%) (26).
According to the present study findings, newborns with candidiasis had higher percentages of blood types O+ and A+ than other blood groups. These findings were exactly in line with those of Thanomsridetcha, Tanakittiyakul (27), who found that the largest percentage of newborns with candidiasis had A+ blood group. Numerous studies have demonstrated a correlation between individual's ABO blood type and their vulnerability to certain illnesses, such as candidiasis. Nonetheless, contradictory findings have been documented by several researchers, and there is currently no solid evidence linking ABO blood type antigens to oral candidiasis (28). The primary component of fungal development is iron, which may be transferred from the host through a variety of pathways and affect hyphae creation by influencing the development of hyphae consequences in different blood groups (29). According to a recent study, blood group A individuals had a greater germ tube development rate than blood groups B, AB, and O, and they may be more susceptible to C. albicans infection, and contain more severe cases than those in various blood groups (27).
A prior investigation revealed significant difference between blood type O persons with high frequency of C. albicans colonies in their saliva versus other categories. Furthermore, Hajimaghsoodi, Jafari Nodoushan (30) found no statistically significant difference in the number of C. albicans colonies between O+ and O- blood types.
Oral candidiasis is more prevalent in newborns belonging to blood types O+, A+, and Rh+. This is associated with the immunological state and sampling community of those persons. According to a prior study, O blood type may be more resistant to illness because of their innate immunity, but non-O blood groups may have the necessity for blood transfusions more frequently (31).

Conclusion

The prevalence of oral candidiasis in infants in Kirkuk City, Iraq is related to their impaired immune status. Thus, the weak immune system is positively associated with the occurrence of opportunistic fungal infections. Most infections were presented in males within 7-12 months with A+, O+, and Rh+ blood groups. C. albicans scored the highest prevalence in infants compared to the other Candida types due to the highest pathogenicity of this yeast.

Acknowledgment

The authors express their gratitude to Department of Biology, College of Science, University of Kirkuk for their assistance and support.

Ethical Considerations

This research work was approved by the Ethics Committee in College of Science at University of Kirkuk (code No. ScB20).

Authors’ Contributions

Conceptualization and Data curation: Bari Lateef Mohammed and Iman Tajer Abdullah, Methodology: Asoda M. Noori, Bari Lateef Mohammed and Iman Tajer Abdullah, Project administration: Asoda M. Noori, Resources: Bari Lateef Mohammed and Shakhawan Beebany, Validation: Bari Lateef Mohammed, Writing–original draft: Iman Tajer Abdullah, and Shakhawan Beebany Writing–review & editing: Iman Tajer Abdullah and Shakhawan Beebany.

Financial Support and Sponsorship

The author(s) received no financial support for the research or publication of this article.

Conflicts of Interest

The authors declare no conflict of interest.

Type of Study: Original Research Article | Subject: Medical Mycology
Received: 2024/06/26 | Accepted: 2024/09/29 | ePublished: 2024/11/30

References

1. GonÇAlo RIC, de Souto Medeiros MR, Carlan LM, de Farias Morais HG, Gonzaga AKG, de Oliveira PT, et al. Oral Candidiasis in Head and Neck Cancer Patients: A Systematic Review. Oral Surg Oral Med Oral Radiol. 2024;137(6):e316. [DOI:10.1016/j.oooo.2023.12.772]

2. Sharma M, Chakrabarti A. Candidiasis and Other Emerging Yeasts. Curr Fungal Infect Rep. 2023;17(1):15-24. [DOI:10.1007/s12281-023-00455-3] [PMID] [PMCID]

3. Hellier SD, Wrynn AF. Beyond fluconazole: A review of vulvovaginal candidiasis diagnosis and treatment. Nurse Pract. 2023;48(9):33-9. [DOI:10.1097/01.NPR.0000000000000095] [PMID]

4. Gómez-Gaviria M, García-Carnero LC, Baruch-Martínez DA, Mora-Montes HM. The Emerging Pathogen Candida metapsilosis: Biological Aspects, Virulence Factors, Diagnosis, and Treatment. Infect Drug Resist. 2024;17:171-85. [DOI:10.2147/IDR.S448213] [PMID] [PMCID]

5. Hellstein JW, Marek CL. Candidiasis: Red and White Manifestations in the Oral Cavity. Head Neck Pathol. 2019;13(1):25-32. [DOI:10.1007/s12105-019-01004-6] [PMID] [PMCID]

6. Macias-Paz IU, Pérez-Hernández S, Tavera-Tapia A, Luna-Arias JP, Guerra-Cárdenas JE, Reyna-Beltrán E. Candida albicans the main opportunistic pathogenic fungus in humans. Rev Argent Microbiol. 2023;55(2):189-98. [DOI:10.1016/j.ram.2022.08.003] [PMID]

7. Ghojoghi A, Khodavaisy S, Mahmoudabadi AZ, Nazar E, Fatahinia M. Exploring the diversity of uncommon oral yeast species and associated risk factors among substance abusers in southwestern Iran. Sci Rep. 2024;14(1):1906. [DOI:10.1038/s41598-024-52105-4] [PMID] [PMCID]

8. Taverne-Ghadwal L, Kuhns M, Buhl T, Schulze MH, Mbaitolum WJ, Kersch L, et al. Epidemiology and Prevalence of Oral Candidiasis in HIV Patients From Chad in the Post-HAART Era. Front Microbiol. 2022;13:844069. [DOI:10.3389/fmicb.2022.844069] [PMID] [PMCID]

9. Lass-Flörl C, Kanj SS, Govender NP, Thompson GR, 3rd, Ostrosky-Zeichner L, Govrins MA. Invasive candidiasis. Nat Rev Dis Primers. 2024;10(1):20. [DOI:10.1038/s41572-024-00503-3] [PMID]

10. Azevedo MJ, Araujo R, Campos J, Campos C, Ferreira AF, Falcão-Pires I, et al. Vertical Transmission and Antifungal Susceptibility Profile of Yeast Isolates from the Oral Cavity, Gut, and Breastmilk of Mother-Child Pairs in Early Life. Int J Mol Sci. 2023;24(2):1449. [DOI:10.3390/ijms24021449] [PMID] [PMCID]

11. Khadija B, Abbasi A, Khan S, Nadeem M, Badshah L, Faryal R. Isolation of pathogenic Candida species from oral cavity of postpartum females, and its association with obstetric and dental problems. Microb Pathog. 2019;131:40-6. [DOI:10.1016/j.micpath.2019.03.022] [PMID]

12. Alkhars N, Al Jallad N, Wu TT, Xiao J. Multilocus sequence typing of Candida albicans oral isolates reveals high genetic relatedness of mother-child dyads in early life. PLoS One. 2024;19(1):e0290938. [DOI:10.1371/journal.pone.0290938] [PMID] [PMCID] []

13. Ota Y, Ito T, Sashida M, Hori E, Kimijima M, Narisawa N, et al. Association between Candida albicans and childhood dental caries in Japanese children. Pediatr Dent J. 2024;34(1):1-7. [DOI:10.1016/j.pdj.2023.12.001]

14. Ihsan Hussein M, Lateef Mohammed B, Khoursheed Abbas S. IL-6 and procalcitonin levels in hemodialysis patients with fungal infection. Res J Biotech. 2024;19(11):129-34. [DOI:10.25303/1911rjbt1290134]

15. Lateef Mohammed B, Tajer Abdullah I, Hussein Mohammed S, Beebany S. Phylogenetic Analysis of Scopulariopsis Brevicaulis Isolated From Diabetic Patients in Kirkuk City, Iraq. Iran J Med Microbiol. 2024;18(4):247-56. [DOI:10.30699/ijmm.18.4.247]

16. Al-Ani DKJ, Musa FH, Buniya HK. Isolation and identification of candida albicans from children patient with candidiasis from Ramadi city, Iraq. HIV Nurs. 2023;23(2):441-9.

17. Brawner DL, Cutler JE. Ultrastructural and biochemical studies of two dynamically expressed cell surface determinants on Candida albicans. Infect and Immun. 1986;51(1):327-36.‏ [DOI:10.1128/iai.51.1.327-336.1986] [PMID] [PMCID]

18. Qadir MI, Bashir H, Ahmad MH. Human Oropharyngeal Candidiasis: From Etiology to Current Treatment. Crit Rev Immunol. 2023;43(3):15-24. [DOI:10.1615/CritRevImmunol.2023049730] [PMID]

19. Kim JH, Ahn J-M. Clinical characteristics of patients with oral candidiasis. J Oral Med Pain. 2021;46(2):33-40. [DOI:10.14476/jomp.2021.46.2.33]

20. Qiu J, Roza MP, Colli KG, Dalben YR, Maifrede SB, Valiatti TB, et al. Candida-associated denture stomatitis: clinical, epidemiological, and microbiological features. Braz J Microbiol. 2023;54(2):841-8. [DOI:10.1007/s42770-023-00952-0] [PMID] [PMCID]

21. Keyvanfar A, Najafiarab H, Talebian N, Tafti MF, Adeli G, Ghasemi Z, et al. Drug-resistant oral candidiasis in patients with HIV infection: a systematic review and meta-analysis. BMC Infect Dis. 2024;24(1):546. [DOI:10.1186/s12879-024-09442-6] [PMID] [PMCID]

22. Cook A, Ferreras-Antolin L, Adhisivam B, Ballot D, Berkley JA, Bernaschi P, et al. Neonatal invasive candidiasis in low- and middle-income countries: Data from the NeoOBS study. Med Mycol. 2023;61(3):myad010. [DOI:10.1093/mmy/myad010] [PMID] [PMCID]

23. Tan CC, Lim D, Hisham NQ, Elias NA, Azli AS, Goh YC. Clinicopathological correlation of oral candidiasis-Our experience in a tertiary centre over two decades. Malays J Pathol. 2023;45(2):237-46.

24. Bao L, Du K, Gao J, Jiang R, Li B, Liu T. An analysis of the risk factors for invasive fungal infections in preterm infants and a discussion of prevention strategies. Technol Health Care. 2024;32(1):361-7. [DOI:10.3233/THC-230218] [PMID]

25. Rajendra Santosh AB, Muddana K, Bakki SR. Fungal Infections of Oral Cavity: Diagnosis, Management, and Association with COVID-19. SN Compr Clin Med. 2021;3(6):1373-84. [DOI:10.1007/s42399-021-00873-9] [PMID] [PMCID]

26. Neamah RA. Isolation and identification of some types of yeast Candida spp and study of their sensitivity to some antifungals. Iraqi J Human Soc Sci Res. 2024;4(12A-1).

27. Thanomsridetcha N, Tanakittiyakul P, Sub-In P, Pichaipaet P, Tangwattanachuleeporn M, Kitisin T, et al. The Potential Association of Human ABO Blood Group in Candida albicans Germination. Trends Sci. 2023;20(12):7116. [DOI:10.48048/tis.2024.7116]

28. Jain S, Shigli dk, Palekar U, Awinashe V, Jain A, Chiang K. Association between Oral Candidiasis and ABO blood types. J Appl Dent Med Sci. 2016;02:30-7.

29. Weiner A, Orange F, Lacas-Gervais S, Rechav K, Ghugtyal V, Bassilana M, et al. On-site secretory vesicle delivery drives filamentous growth in the fungal pathogen Candida albicans. Cell Microbiol. 2019;21(1):e12963. [DOI:10.1111/cmi.12963] [PMID]

30. Hajimaghsoodi S, Jafari Nodoushan AA, Akhavan Karbassi MH, Yazdanparast Y. The Relationship Between Salivary Candida Albicans Colony Count and Blood Group Antigens in Dentistry Students. Int J Med Lab. 2021;8(4):284-90. [DOI:10.18502/ijml.v8i4.8099]

31. Thakur SK, Sompal S, Dinesh Kumar N, Sinha AK. Link between human ABO blood groups with diseases influencing blood donors and recipients frequency at RBTC, Delhi, India. Bioinformation. 2023;19(5):576-81. [DOI:10.6026/97320630019576] [PMID] [PMCID]