Oocyte isolation techniques from the ovary samples of slaughtered animals: A review

Introduction

Assisted Reproductive Technology (ART) like In-Vitro Embryo Production (IVEP) is a tedious process and influences several factors, including the oocyte collection technique. In vitro produced embryos have great demand in the market and are used for studies on IVM, IVF, IVC, commercial embryo transfer, embryo cloning, production of transgenic animals, and research purposes (Gordon I, 2003) [12] . Slaughtered ovary samples are cheap, abundant, reasonable, inexpensive, and various kinds of non-invasive oocyte isolation techniques are employed to collect oocytes from the ovary sample. The oocyte retrieval techniques include slicing, aspiration, puncture, dissection, and other techniques (Alm et al., 2008; Ciptadi et al., 2019) [2,7] . Domestic animals play a vital role in livestock production and economics to contribute to the country's total GDP (Dash S, 2017) [9] . India is the world largest population country in the world and needs to produce a sufficient amount of food and food products from the livestock sector. So, genetically superior animal production and their maintenance which can be possible through IVEP is required. Different domestic animals include Cattle (Faheem et al., 2011) [11] , Buffalos (Mishra et al., 2014) [25] , Goats (Sigh et al., 2013) [37] , Sheep (Davachi et al., 2012) [10] , and Equines (Vazquez et al, 1993) [41] slaughter ovary samples are practically employed for the IVEP. In addition to ovum collection techniques, some other factors like breed, season, age, stage of the oestrus cycle, size of the ovary, type of the ovary, transportation time, and skill of the person influence the oocyte recovery rate (Wania et al., 1999) [46] . This review detailly addresses the different types of oocyte collection techniques for slaughter samples of domestic animals.

The aspiration method not only recovers the maximum number of oocytes compared to the slicing technique and also influences the association of increases in the maturation rate of oocytes in goats (Majeed et al., 2011) [23] . Even though the recovery rate of oocytes is minimal in the aspiration technique compared with the slicing technique, the Advantage is this technique mainly has a chance of recovering a maximum number of good-quality oocytes (Rahman et al., 2016) [29] . The method of aspiration plus slicing is best among the oocyte collection methods because through aspiration technique can get the floating oocytes from the follicle and some follicles embedded in the deeper cortex have the oocytes recovered by the slicing technique (Hammad et al., 2014) [13] . Ultrasound-Guided Follicular Aspiration (UGFA) used to collect the oocytes from ovaries in live animals. The recovery percent and morphologically good quality of oocytes aspirated up to the maximum level by aspiration method from the ovaries of slaughtered animals (Majeed et al., 2019) [22] , whereas the UGFA method is perfect for the higher developmental competence of in vitro culture embryos (Landeo et al., 2022) [20] . Quality oocytes (an ample amount of A and B-grade) are in most demand for in-vitro experiments and the aspiration technique is superior to producing the quality oocytes, but the oocyte retrieval is not only affected by various collection techniques but also influenced by the type of breed, reproductive status of animals, climatic conditions, poor body condition, and specimen processing factors (Raziq et al., 2008; Chaudhari et al., 2014) [32,6] . The aspiration technique is good for the collection of A-grade quality oocytes within less time and debris.

Puncture

Puncture is a technique used to collect the oocytes from the slaughterhouse samples of ovaries. The Puncture method was applied to the abattoir ovaries of the Holstein cow results analysed that puncture is the perfect method to recover a higher number of good-quality oocytes and the oocyte developmental competence is not significant when compared to the other techniques (Wang et al., 2007a) [45] . The Slicing and Puncture techniques are associated isolation of A-grade (4-5 layers of cumulus cells and evenly distributed cytoplasm) cumulus oocytes complexes at maximum levels compared to Aspiration-1 and Aspiration-2 techniques, although the maturation rate of Boer goat is more than the slicing technique this is due to the recovery of the higher number of preantral oocytes from the ovaries (Wang et al., 2007) [44] . The sheep and goats are small ruminant domestic animals with small ovary size and Puncture is the best technique to collect the COC from the slaughtered animals (Bonde et al., 2000) [3] . Moreover, these techniques have a disadvantage in that recovery of more debris along with the oocytes and the techniques of Puncture, Slicing, or Aspiration don't affect the oocyte developmental competence during in-vitro studies (Hoque et al., 2011) [14] . If the slicing and puncture oocyte collection methods are taken, the highest COC may come from slicing, but the debris is much less in the puncture technique. Examining oocytes from the media is easy with this method, and oocyte maturation is more than slicing (Sofi et al., 2012) [38] . Among the aspiration, puncture, and slicing methods the puncture technique is associated with the collection of a greater number of good-quality due to the oocyte surrounding layers of cumulus cells stable and not disturbed at the time of retrieval and in the aspiration and slicing methods, it is opposite (Borah et al., 2018) [4] . Irrespective of quality the retrieval rate of oocyte yield is higher possibly by the slicing technique. Simultaneously, the majority of normal COC (A and B grade) production is associated with the puncture technique (Raihan Ratul, 2020) [30] . The Puncture or Slicing technique is prominently used for the retrieval of good-quality oocysts from the caprine slaughterhouse ovaries.

Slicing

The IVEP is important for the rearing of small ruminants and in which the basic oocyte isolation techniques like aspiration and slicing play a major role, especially in ovine seasonal breeders slicing enhances the recovery rate of oocytes in Ewe and Lambs (Shirazi et al., 2005) [35] . The comparison among the methods of slicing, aspiration, and puncture of oocyte retrieval concluded that slicing is the best technique for the isolation of oocytes and timeconsuming processes associated with aspiration and puncture but, yielded a higher number of good-quality oocytes compared to puncture and aspiration techniques (Das et al., 1996; Nuaimi et al., 2020) [8,27] . The slicing method dominates the other methods including puncture, aspiration, and aspiration after slicing of the oocyte isolation from the abattoir ovaries and not only affects the collection technique along with the transportation time from the slaughterhouse to the experimental lab but plays a vital role in the developmental competence of oocytes during in vitro conditions like prolonged time reduced oocyte competence and vice versa (W.M. Saleh, 2017) [43] . The goat ovaries are small and help properly handle oocyte collection by the slicing method. Employing aspiration and puncture or other techniques for oocyte isolation may be time-consuming and laborious (Pawshe et al., 1994) [28] . The ovarian stroma of buffalo species is strong and bottomless follicles are embedded in it so slicing is the method appropriate for the isolation of the oocytes even to get chance of debris like blood clots and fibrin shreds (Kumar and Mourya, 2000) [19] . A large number of primordial follicles and antral follicles are present in the prepubertal stage of buffalo and the slicing procedure to recover the deeper section of ovaries is one of the reasons to get a higher number of oocytes (Kumar et al., 1997) [18] . The recovery of oocytes is influenced by the size of the ovary and the mean recovery of oocytes per ovary is highest in the slicing technique in contrast with the aspiration (Sianturi et al., 2002) [36] . Even if the slicing method recovers a greater number of oocytes, eventually, the getting of quality oocytes is less due to the more debris associated with the oocytes and requires a long time to wash results the denudation of cumulus cells leading to less quantity of oocytes (Mahesh et al., 2014) [21] . The slicing method is associated with a high quantity of oocyte isolation and oocyte quality is not that much appropriate.

Dissection

Dissection is a simple technique to perform oocyte collection from the ovaries. The blunt dissection technique is easy to handle and an inexperienced person efficiently can collect the maximum number of oocytes (A and B grade) in contrast with the slicing technique from the goat abattoir ovary sample (Mamy et al., 2016) [24] . In addition, it yielded the maximum number of oocytes in contrast with the puncture and aspiration technique (Jamil et al., 2008) [17] .

The dissection method is used to recover a good quality and quantity of oocytes from the slaughterhouse ovaries, especially bovines. The aspiration and dissection techniques are used for retrieving ovaries from domestic animals but dissection attained significant value due to the retrieval of more ovaries compared to the aspiration technique (Carolan et al., 1994) [5] . However, a minor difference was observed in the oocyte recovery processes between the dissection and aspiration techniques but the oocyte maturation rate in TCM-199 media is higher in case of the dissection technique (Hussain et al., 2015) [15] . The highest number of oocyte collection is associated with the dissection technique but the maximum number of normal oocyte collection is not (Tarikul Islam, 2019) [39] . The puncture and aspiration techniques are appropriate for the collection of oocytes from larger follicles visible on ovaries and the dissection method approaches the small, embedded follicles within the ovary. So, through the dissection method getting a high chance of quality oocytes.

Other techniques

The commonly employed techniques include slicing, aspiration, and puncture for slaughtered domestic animal oocyte retrieval for IVEP, and some other techniques are rarely used in labs. The involvement of these techniques are slicing plus aspiration in bovine (Udin et al., 2020) [40] , follicular puncture plus slicing and scoring in buffalos (Varma et al., 2008; Shahid et al., 2014) [42,33] , slashing in Ewe Lambs (Shirazi et al., 2004) [34] , and aspiration by a vacuum pump in camel (Nowshari, 2005) [26] . These techniques are a combination of two techniques or modifications of actual techniques and are not prominent in the practice of oocyte collection in in-vitro laboratories. As per the available review of the literature, these individual techniques are very efficient in the recovery of a bulk quantity of oocytes from slaughtered samples, even if these methods are not employed due to retrieval of a large number of debris, time-consuming process, and recovery of less quality of oocytes. So, each and every drawback effectively influences the oocyte developmental competence and further embryo developmental competence leads to a large impact on the IVEP.

Conclusion

There is no species-specific oocyte isolation technique or the most preferable ovum retrieval technique in the animal reproduction field and every technique has advantages and disadvantages. The oocyte retrieval techniques are influenced by several factors associated with oocyte number and morphology of oocyte but not early embryonic developmental competence. The availability of literature indicates that the slicing, dissection techniques are connected with the recovery of a higher number of oocytes, and the aspiration technique is related to the good quality of oocytes. Based on individual choice and circumstances of the laboratory oocyte isolation techniques are popular in the reproductive field.

References

1. Ahmed JA, Dutta D, Nashiruddullah N. Recovery of Different Cumulus Oocyte Complex (COC) Grades from Bovine Ovaries by Aspiration Method. Journal of Animal Research. 2015;5(3):631-634.
2. Alm H, Torner H, Kanitz W, Roschlau K. Influence of oocyte recovery method, in vitro fertilization method and serum source on embryonic development of in vitro matured bovine oocytes. Arch Tierz. 2008;51(3):224234.
3. Bonde SW, Naqvi SMK, Mittal JP. Comparison of oocyte recovery from surface follicles of sheep and goat ovaries. International Journal of Animal Sciences. 2000;15(1):1-4.
4. Borah D, Biswas RK, Deka BC, Sinha S, Barkalita L, Borah RS, Nath KC, Kalita MK, Dewry RK. Effect of Retrieval Techniques on the Quality of Abattoir Ovarian Follicular Oocytes in Assam hill Goats. Indian Journal of Animal Reproduction. 2018;39(2).
5. Carolan C, Monaghan P, Gallagher M, Gordon I. Effect of Recovery Method on Yield of Bovine Oocytes per Ovary and their Developmental Competence after Maturation, Fertilization and Culture In vitro. Theriogenology. 1994;41:1061-1068.
6. Chaudhari CF, Derashri HJ, Chaudhary SS, Puri G. Quantitative and qualitative study of buffalo oocytes recovered by different oocyte harvesting techniques. Indian Journal of Animal Sciences. 2014;84(9):958961.
7. Ciptadi G, Rahayu S, Putri AI, Karima HN, Budiarto A, Susiati, Putri PF, Mudiwamah. Utilization of local goat ovary waste from slaughter house as a material source for in vitro culture, conservation and freezing of oocyte cells. International Conference on Science and Technology for Environmental Protection; 2019, doi:10.1088/1755-1315/259/1/012007.
8. Das GK, Jain GC, Solanki VS, Tripathi VN. Efficacy of Various Collection Methods for Oocyte Retrieval in Buffalo. Theriogenology. 1996;46:1403-1411.
9. Dash S. Contribution of Livestock Sector to Indian Economy. Indian Journal of Research. 2017; 6 (1).
10. Davachi ND, Zeinoaldini S, Kohram H. A novel ovine oocyte recovery method from slaughterhouse material. Small Ruminant Research. 2012;106:168-172.
11. Faheem MS, Carvalhais I, Chaveiro A, Moreira da Silva F. In vitro oocyte fertilization and subsequent embryonic development after cryopreservation of bovine ovarian tissue, using an effective approach for oocyte collection. Animal Reproduction Science. 2011;125:49-55.
12. Gordon I. Laboratory production of cattle embryos. Wallingford, UK: CAB International; 2003.
13. Hammad ME, Gabr SA, El-Ratel IT, Gad MA. Efficacy of Different Collection Techniques on Yield and Quality of Egyptian Buffalo Oocytes. J. Animal and Poultry Prod. 2014;5(7): 413-422.
14. Hoque SAM, Kabiraj SK, Khandoker MA, Mondal A, Tareq KMA. Effect of collection techniques on cumulus oocyte complexes (COCs) recovery, in vitro maturation and fertilization of goat oocytes. African Journal of Biotechnology. 2011;10(45):9177-9181.
15. Hussain M, Chakravarty P, Soren S, Deori S, Begum SS. Effect of recovery technique and culture media on in vitro maturation of indigenous cattle oocytes of Assam. Indian J. Anim. Res. 2015;49(1):51-54.
16. Jaayid TB, Fahid TA, Jasim NY. Oocytes Extraction from Iraqi Local Goat Ovaries by Using Aspiration and in vitro Fertilization Techniques. Basrah J. Agric. Sci. 2013;26(1):28-42.
17. Jamil H, Samad HA, Qureshi ZI, Rehman NU, Lodhi LA. Harvesting and Evaluation of Riverine Buffalo Follicular Oocytes. Turk. J. Vet. Anim. Sci. 2008;32(1):25-30.
18. Kumar A, Solar VS, Jindal SK, Tripathi VN, Jain GC. Oocyte retrieval and histological studies of follicular population in buffalo ovaries. Animal Reproduction Science. 1997;47:189-195.
19. Kumar S and Mourya SN. Evaluation of oocyte retrieval methods from Bubaline ovaries. Indian Journal of Animal Research. 2000;34 (2):130-132.
20. Landeo L, Zuniga M, Gastelu T, Artica M, Ruiz J, Silva M, Ratto MH. Oocyte Quality, In vitro Fertilization and Embryo Development of Alpaca Oocytes Collected by Ultrasound-Guided Follicular Aspiration or from Slaughterhouse Ovaries. Animals. 2022;12(1102).
21. Mahesh YU, Rao MM, Sudhakar P, Sambasiva Rao KRS. Effect of harvesting technique and presence or absence of corpus luteum on in vitro development after parthenogenetic activation of oocytes recovered from buffalo ovaries. Veterinary World. 2014;315-320.
22. Majeed AF, Al-Timimi IH, Al Saigh MN. In vitro embryo production from oocyte recovered from live and dead Iraqi black goat: A preliminary study. Res. J. Biotech. 2019;14(I).
23. Majeed AF, Saied IH, Al-Saigh MN. Effect of collection techniques on recovery and in vitro maturation of Black Iraqi Goats oocytes. Al-Anbar J. Vet. Sci. 2011;4(2).
24. Mamy K, Atiqah NF, Ariani N. Effect of ovarian types and collection techniques on the number of follicles and the quality of cumulus-oocyte-complexes in cow. Bang. J. Anim. Sci. 2016;45(3):10-16.
25. Mishra SK, Maurya SK, Anand M, Yadav S, Saxena A. Recovery follicular oocytes in Murrah Buffalo by Slicing method. 2 nd annual meeting of Society of veterinary science and Biotechnology National Seminar on Biotechnological approaches to challenges in animal health and production. 2014 March 6-7; DUVASU, Mathura (UP).
26. Nowshari MA. The effect of harvesting technique on efficiency of oocyte collection and different maturation media on the nuclear maturation of oocytes in camels (Camelus dromedarius). Theriogenology. 2005;63:2471-2481.
27. Nuaimi AJ, AL-Rubaei HM, AL-Gebouri FG. Influence of Oocyte Collection Techniques on Oocyte Retrieval and Quality from Ovaries of Iraqi Goats (Capra Hircus). Sys Rev Pharm. 2020;11(11):1160-1163.
28. Pawshe CH, Totey SM, Jain SK. Methods of Recovery of Goat Oocytes for In vitro Maturation and Fertilization. Theriogenology. 1994;42:117-125.
29. Rahman ANMI, Asad L, Hossain MM. Collection Techniques and Corpus Luteum Effects on Quality and Quantity of Goat Follicular Oocytes for In vitro Studies. Wayamba Journal of Animal Science. 2016;1346-1350.
30. Raihan Ratul MDA. Relative Efficiency of Oocytes Collection Techniques and Evaluation from Goat Ovaries. Thesis of Sher-E-Bangla Agricultural University, Dhaka. 2020.
31. Rakshitha P, Abhilash RS, Kurien MO, Metilda J, Pratheesh MD, Revathy MM. Effect of Aspiration Technique on Oocyte Yield and Quality in Crossbred Cattle of Kerala. The Pharma Innovation Journal 2019; 8(3):102-104.
32. Raziq A, Rehman Z, Khan S, Ali J, Shah I. Oocyte recovery and gradation from buffalo ovaries slaughtered in Peshawar slaughter house. Life science: an international journal. 2008;2(1):533-536.
33. Shahid B, Jalali S, Khan MI, Shami SA. Different Methods of Oocytes Recovery for in vitro Maturation in Nili Ravi Buffalo's Oocytes. APCBEE Procedia. 2014;8:359-363.
34. Shirazi A, Esfandabadi NS, Hosseini SM. A Comparison of Two Methods of Oocyte Recovery in Ewe Lambs for in vitro Maturation. 11th International Conference of the Association of Institutions for Tropical Veterinary Medicine and 16th Veterinary Association Malaysia Congress; 2004 August 23-27; Malaysia.
35. Shirazi A, Shams-Esfandabadi N, Hosseini SM. A comparison of two recovery methods of ovine oocytes for in vitro maturation. Small Ruminant Research. 2005;58:283-286.
36. Sianturi RG, Thein M, Wahid H, Rosnina Y. Effect of Collection Technique on Yield of Bovine Oocytes and The Development Potential of Oocytes from Different Grades of Oocytes. Jurnal Ilmu Ternak dan Veteriner, 2002;7(3).
37. Singh RL, Sadasiva Rao K, Murali Mohan K. Oocyte Retrieval Methods, Grade and Percentage of Oocytes in Goats. International Journal of Molecular Veterinary Research. 2013;3(2):4-6.
38. Sofi KA, Khan MZ, Islam R, Lone FA. Effect of collection methods on the recovery rate and in vitro maturation rate of oocytes. Indian journal of animal science. 2012;82(10):1190-1192.
39. Tarikul Islam MD. Evaluation of Oocytes Recovered from Ovaries of Black Bengal Goat under Different Retrieval Methods. Thesis of Sher-E-Bangla Agricultural University, Dhaka. 2019.
40. Udin Z, Masrizal, Hendri and Nanda S. Evaluation of Different Techniques in Recovering of Oocytes and Storage Duration of Ovaries on the Quality and Quantity of Bovine in vitro Maturation. Bulletin Animal Science. 2020;44(2):1-7.
41. Vazquez JC, Moreno JF, Hanneman R, Evans JW, Kraemer DC. Evaluation of Three Techniques (Follicular Aspiration and Flushing and Slicing of the Ovaries) for Recovery of Equine Oocytes from Excised Ovaries. Equine Nutrition and PhysiologySociety, Refereed Papers from the13 th Symposium.1993;13(9).
42. Verma VK, Saxena A, Yadav S, Adesh K, Verma AK, Bhati SK. Effect of retrieval methods CL, and side on oocyte recovery from buffalo slaughterhouse ovaries. conference paper. Feb 2008.
43. W.M. Saleh. Assessment of different methods of bovine oocytes collection, maturation and In vitro fertilization of abattoir specimens. Iraqi Journal of Veterinary Sciences. 2017;(31)1:55-65.
44. Wang ZG, Xu ZR, Yu sd. Effects of oocyte collection techniques and maturation media on in vitro maturation and subsequent embryo development in Boer goat. Czech J. Anim. Sci. 2007; 52(1):21-25.
45. Wania NA, Wani GM, Khan MZ, Sidiqi MA. Effect of different factors on the recovery rate of oocytes for in vitro maturation and in vitro fertilization procedures in sheep. Small Ruminant Research. 1999;34:71-76.