Skip to main content

IVF laboratory COVID-19 pandemic response plan: a roadmap

Abstract

Background

The potential of COVID-19 severe pandemic necessitates the development of an organized and well-reasoned plan for the management of embryology/andrology laboratories while safeguarding the wellbeing of patients and IVF staff.

Main body

A COVID-19 pandemic response plan was proposed for embryology and andrology laboratories for pre-pandemic preparedness and pandemic management in anticipation of a possible second coronavirus wave. Preparation involves many plans and logistics before a pandemic risk rises. Many operational changes can be considered during the pandemic. This plan includes logistical arrangements, reducing labor needs, conserving supplies, and protective measures for embryologists and gametes/embryos.

Conclusion

The unpredictable emergence of the COVID-19 pandemic dictates the need for a preparedness plan for embryology/andrology laboratories, which includes an action-oriented plan to secure the safety of all stakeholders.

Background

In view of the recent worldwide COVID-19 disease and predictions suggesting the inevitability of future pandemics, the need for a disaster plan for IVF laboratories has become a compulsory requirement. COVID-19 is caused by a virus from the coronaviridae family, named severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) [1]. Coronaviruses can be transmitted through the air in respiratory droplets (> 5-μm diameter) and aerosols (≤ 5-μm diameter). Transmission is also believed to occur through direct (contaminated hands) or indirect (contaminated surfaces and fomites) physical contacts, leading to cross-infections and outbreaks [2]. According to the most recent evidence from the World Health Organization (WHO) and the US Centers for Disease Control and Prevention (CDC), the predominant transmission route for coronaviruses is through droplets as the virus is conveyed by exhaled air (through normal breathing, coughing or sneezing) rather than aerosols [3, 4]. These heavy droplets can deposit on surfaces amplifying the propagation of the virus. Surprisingly, recent data showed that the prevalence of asymptomatic individuals with COVID-19 may be as high as 50–75% which challenges the triage of infected individuals [5].

It is estimated that more than 25% of transmissions occur in the workplace [6]. The occurrence of asymptomatic coronavirus-positive patients and healthcare workers in IVF units may contribute to an environment rich in respiratory viruses, leading to potential outbreaks in the working place and spillover into the community. In this regard, it was reported that coronaviruses have been implicated in nosocomial community outbreaks originating from hospitals [7, 8].

Potential biological transmission

Several molecular characteristics of SARS-CoV-2 may justify concerns about the potential susceptibility of gametes (semen, testicular tissue) and embryos to viral infection [9, 10]. Although not universally supported [11,12,13], recent reports confirmed the presence of the virus in the semen of infected patients [14]. These findings justify calls for more vigilance in the work environment and for the need to put in place stringent measures to protect embryologists from potentially infected gametes.

The possibility of coronavirus survival in liquid nitrogen is currently not known, but it is suggested that viruses are likely to survive the freeze/thaw process [15]. During cryopreservation of gametes/embryos in liquid nitrogen, straws or vials may leak or shatter causing liquid nitrogen spill and potential cross-contamination of samples. Using an experimental model, Bielanski and colleagues confirmed the occurrence of viral cross-contamination of bovine embryos stored in liquid nitrogen by bovine airborne viruses [16]. In addition, the sterility of factory-derived liquid nitrogen is often not guaranteed, and the risk of contamination by human pathogens may theoretically exist. In theory, some airborne contaminants may contaminate liquid nitrogen during the process of gas compression [16]. When cryotanks are opened, the nitrogen vapor mixes with the atmospheric air creating ice sediments which falls into the vessel and accumulates at its bottom. During aggregation, these ice crystals may entrap various airborne microbes (bacteria, fungi…) leading to possible contamination of the cryotanks [17]. It follows that the risk of contamination and cross-contamination of cryopreserved human material in liquid nitrogen by nosocomial coronaviruses is of legitimate concern.

Occupational person-to-person transmission

Apart from direct viral transmission, the presence of patients and healthcare workers in a tight and closed working space in the presence of a variety of pathologies causes the fomites and the air to be loaded with potential viral contaminants. Occupational transmission in clinical laboratories is exceptional events rarely reported. At present no data are available for coronavirus outbreaks in IVF laboratories. Nevertheless, it is evident that in clinical laboratory settings, infection prevention and control measures are often designed to act on most pathogen’s modes of transmission.

The professional societies response

Professional societies, such as the American Society for Reproductive Medicine (ASRM) and the European Society for Human Reproduction and Embryology (ESHRE), have strongly urged to stop fertility treatments during the COVID-19 pandemic for the protection of human life (i.e., conceptus). The majority of these societies provided guidance for IVF laboratories for the gradual resumption of activities throughout the pandemic [18,19,20,21]. As COVID-19 keeps on spreading comprehensively, escalating case importation from overseas or residual infected seeds coupled with the resumption of economic activities, a second wave of COVID-19 seems plausible.

To meet these challenges, the authors, on behalf of the Middle East Fertility Society Embryology group, developed a response plan to outline the essential services and delineate the proper means to ensure the sustainability of IVF laboratory services in anticipation of a second COVID-19 pandemic wave. To that end, the authors aimed to provide a practical roadmap for a preparedness and management plan for the protection of human life (gametes/embryos and staff). It should be noted that some points raised might represent standard of practice in IVF or basic requirements for IVF laboratories accreditation. It is important to emphasize nonetheless that while these recommendations constitute appropriate guidelines for IVF laboratory management during a COVID-19 pandemic, they are not designed to dictate a rigid all-exclusive plan.

Main text

Heightened planning and logistic preparation: initial onset of a pandemic

It is widely accepted that proper pre-pandemic planning should occur at an early level, as outlined in Table 1 and discussed later. Several initial logistic preparations should be in order before the occurrence of the crisis. Although most of these preparatory steps comply with the basic emergency plan of the IVF laboratory, some important elements may require further highlighting. Basically, and as part of routine infection control practices, the IVF staff should receive adequate education and proper training on conventional infection control practices and standard operating procedures (SOP) [22].

Table 1 Early-level response plan: pre-pandemic planning recommendations for embryology and andrology laboratories

Hand hygiene compliance observation audits should be periodically performed with special focus on avoiding touching noses, mouths, and eyes [23].

In an effort to reduce the burden of the pandemic on the healthcare system, embryologists are encouraged to obtain additional vaccination namely for preventing respiratory illness caused by influenza and pertussis [24]. Personnel should also participate in a fit testing for N95 masks (FFP2 the European equivalent) which provides protection against aerosol-generated particles [28]. This test ensures that masks are properly sealed to the face.

As part of the main laboratory emergency plan, the IVF personnel should know whom to contact during an emergency crisis [25, 26]. Along this perspective, the laboratory supervisor should prepare staff emergency and suppliers contact lists and make them accessible to all staff. More importantly, duplicate records must be maintained on a secure web server and updated regularly [25].

The supervisor must also make sure to stock essential PPE supply. Facilities must consider storing cleaned spare gas cylinders in a ventilated storage room to avoid supply chain failure during pandemic times [29].

It should be noted that an on-site spare storage cryotank and reserve of liquid nitrogen (LN2) supply are critical points which constitute requirements for laboratory accreditation (College of American Pathologists (CAP) accreditation 2019 checklist; RLM.03944) [27]. The laboratory should have a written procedure to monitor and maintain adequate liquid nitrogen levels and temperatures (CAP accreditation 2019; RLM.03940). The monitoring can be through visual measurement, weight scaling, or use of an alarm system [30]. Cryopreservation consents should state the possibility of system failures during storage in case of disasters [25]. The cryotanks require periodic decontamination using approved laboratory detergents with adequate rinsing with distilled water [16]. The decontamination of cryotanks is recommended owing to the potential accumulation of sediments and contamination of liquid nitrogen [16]. However, this practice is optional and is not recommended by the regulating reproductive societies (ESHRE, ASRM, CAP).

Operational changes during the pandemic stages

Due to the nature of coronavirus transmission, the WHO advocated and enforced “social distancing” measures to maintain the 2-m “safe” distance between people in addition to the routine use of PPE [31, 32]. As previously mentioned, the high proportion of asymptomatic individuals may imply that an infected asymptomatic embryologist may infect his/her colleagues if adequate protective measures and gears are not properly used. In addition, staff should be educated to recognize early signs of viral illness, namely sore throat, fever, and cough.

As numerous plans for work have been proposed by professional societies and regulations bodies across the globe during the pandemic period, it seems reasonable for healthcare workers to adopt these measures through normal times in anticipation of new pandemic waves.

In extreme scenarios, the complete closure of IVF clinics and the total cessation of all procedures are recommended in the event of a new pandemic. However, in the “new normal” operational practices, many interventions may be changed to adapt to the pandemic risk (Table 2).

Table 2 Pandemic response plan: recommendations for embryology and andrology laboratories during the coronavirus pandemic

Operational changes reducing labor needs and conserving supplies

Several operational changes should be implemented in the IVF laboratory in order to maintain the continuity of care by ensuring the safety of the personnel and avoiding the shortage in supplies.

To meet these goals, laboratory managers are expected to identify the right people to fulfill the essential roles. In spite of a forced shut-down policy during a pandemic, some procedures such as oocyte vitrification for oncology patients are deemed to be of urgent nature. In such cases, the supervisor should also explore the option of hiring free-lancers to fulfill essential tasks. In other words, the number of embryologists reporting to work should be reduced to a minimum without compromising safety and quality. Embryologists would be expected to perform rotating shifts depending on the size of the unit and staff. The rotating schedule is created to minimize exposure time to infection while accommodating the continuity of care within the laboratory [18].

During a pandemic, manufacturing and distributing companies may lack the personnel to maintain a regular delivery schedule. This shortage would require the laboratory to increase preemptively its stock of PPE (gloves, surgical masks, and N95 masks) as well as culture and cryopreservation media batches while favoring products with longer expiration dates.

Along this perspective, supplies inventory should be updated regularly in order to match the workload. A reduction in the workload may also drive special considerations for resources management, such as the reduction of the number of operating incubators.

Operational changes protecting embryologists and gametes/embryos

It is reasonable to recommend that patients and staff be primarily triaged and regularly tested according to national recommendations and/or availability of laboratory testing. While ESHRE favored SARS-CoV-2 IgM/IgG immunologic screening, ASRM emphasized on viral molecular testing [18, 19]. One should never underestimate the importance of personal hygiene and the use of proper PPE. Laboratory staff are expected follow standard laboratory practices, including wearing surgical masks, disposable gloves, and eye protection devices. It would be reasonable to add the use of a long-sleeve impermeable gown over the scrubs when performing an aerosol-generating procedure such as testicular tissue processing. In vitro experimental studies investigating the filtering capacity of standard surgical masks and N95 masks (FFP2) [28] showed that both types of masks retained at least 95% of small particles (0.3 μm corresponding to aerosols) offering comparable effective outward protection. Toward inward protection nonetheless was superior for N95 masks. It follows that while surgical masks may not be a perfect match to N95 masks, their usage is still encouraged. While the use of surgical masks is currently standard practice, N95 masks may be encouraged during aerosol-generating procedures. In view of the global shortage in facial masks during the COVID-19 pandemic, recommendations have been modified in order to take into account the local availability of PPE supply

It also follows that unnecessary patient visits to the IVF unit for the renewal of cryopreserved biological material should be reduced. Alternatively, payments and consents may be performed online. IVF staff should wear a surgical mask and practice social distancing at all times, more so when communicating information to patients. The role for telehealth is critical during pandemic time, and has been facilitated by the widespread use of Electronic medical record (EMR) systems for tasks including online billing, e-consents, and communications [36].

When discussing indoor laboratory air environment, no clear recommendations exist for the air purification system in IVF. Although high-efficiency particulate air (HEPA) filters are 99.97% efficient at collecting the most-penetrating particles (~ 0.3 μm), they may not adequately protect against smaller entities like viruses. But, since aerosolized viruses are thought to exist as agglomerates, the increase in the particle size may consequently cause them to be efficiently captured by the filter [37]. On the other hand, activated carbon filters normally installed within HVAC filter cartridges to trap volatile organic compounds, were found to absorb viral particles as well [38]. While most IVF laboratories are equipped with positive-pressure air systems, it may be recommended to switch to negative pressure modules during airborne virus outbreaks to sink the virus. This may be technically and financially challenging to many laboratories. In view of the restricted personnel number and laboratory space within the IVF working place, the risk benefit of discontinuing positive-pressure air purification must be properly assessed. The treatment of a patient who tested positive for COVID-19 for instance warrants the turning off of positive-pressure ventilation to avoid dissemination of the virus outside the operating theater. Particular consideration should also be given to increasing the number of air changes per hour and reducing recirculation of air in favor of using 100% fresh air.

As for infection control prevention, embryologists are encouraged to follow standard practices in the IVF laboratory. Such practices include the cleaning of supply boxes and gas cylinders before entering the laboratory using approved disinfection agents [21]. In addition, the biosafety cabinet workspace should be routinely and thoroughly disinfected, with particular attention to the uncluttering of airflow outlets to avoid flow disruptive turbulence, which may increase the risk exposure of operators. Specifically, personnel should exercise laboratory housekeeping vigilance during high-risk pandemics. Cleaning practices must be diligently observed, such as disinfection of common surfaces (e.g., doorknobs, keyboards, surfaces…). Commercially available quaternary-ammonium-based formulations, labeled “embryo-safe”, were shown to be effective against coronaviruses [39]. More so, the combination of spraying and wiping with approved disinfectant, followed by UV irradiation for 30 min may completely inactivate the virus in biosafety cabinets [33].

Since coronaviruses were detected in the blood of infected patients [40] and in view of the presence of viral receptors on human spermatozoa, Sertoli cells, Leydig cells [9, 10], and oocytes [41], extra vigilance during handling biological material is highly justified. More specifically, standard precautions should be observed during routine handling of specimens, while special attention should be considered during aerosol-generating procedures such as processing of testicular tubules. The use of N95 masks, goggles or face shields may be more appropriate during sample preparatory steps that may generate aerosols or droplets and during mechanical processing of testicular tubules.

It should also be noted that universal precautions during oocyte pick up should be strictly taken, which include the collection of follicular fluid into well-sealed containers [18]. In addition, cumulus-oocyte complexes should be thoroughly and repeatedly washed with the aim of diluting viral load. While no recommendations are currently available for sperm processing during COVID-19 pandemics, precautions and procedures recommended for other viruses should be diligently followed. Semen ejaculate jars must be properly wiped prior to handling specimens. It is advisable to separate sperm using a combination of sperm density gradient techniques followed by a swim-up step to dilute the virus [42]. Sperm processing should include the frequent change of sterile pipettes and tubes prior to each washing step [43]. The use of mechanical micropipettes is recommended [26] and sterile-filtered tips pipettes are preferred to avoid aerosol generation and contamination of the micropipette. Following use, micropipettes must be disassembled and disinfected using approved laboratory agents and/or UV irradiation.

The safety of the cryopreservation process may be best observed when UV-sterilized liquid nitrogen is used [34] and when embryos and oocytes are sequentially washed. Special attention should be made to safeguarding the integrity of the zona pellucida which is considered an efficient barrier against viral contamination [35]. The use of closed system cryopreservation tools is preferred to secure the safety of the storage material [18]. Vapor tanks are also favored for cryostorage to minimize risks of viral transmission.

Conclusion

Planning for a crisis is one of the most important undertakings in a laboratory. Appropriate planning protects both personnel and gametes/embryos and ensures continuity of care. The planning process involves the prompt and proper identification of risks and the strict implementation of operational changes to address loss of staffing, shortage of supply, and changes in laboratory practices.

Availability of data and materials

Not applicable

Abbreviations

ASRM:

American Society for Reproductive Medicine

CAP:

College of American Pathologists

CDC:

Centers for Disease Control and Prevention

COVID-19:

Coronavirus disease 2019

EMR:

Electronic medical record

ESHRE:

European Society for Human Reproduction and Embryology

FFP2:

Filtering facepiece

HEPA:

High-efficiency particulate air

IgG:

Immunoglobulin G

IgM:

Immunoglobulin M

IVF:

In vitro fertilization

LN2:

Liquid nitrogen

PPE:

Personal protective equipment

SARS-CoV-2:

Severe acute respiratory syndrome coronavirus 2

SOP:

Standard operating procedure

UV:

Ultraviolet

WHO:

World Health Organization

References

  1. of the International CSG (2020) The species severe acute respiratory syndrome-related coronavirus: classifying 2019-nCoV and naming it SARS-CoV-2. Nat Microbiol 5:536

    Article  Google Scholar 

  2. Otter J, Donskey C, Yezli S, Douthwaite S, Goldenberg S, Weber D (2016) Transmission of SARS and MERS coronaviruses and influenza virus in healthcare settings: the possible role of dry surface contamination. J Hosp Infect 92:235–250

    Article  CAS  Google Scholar 

  3. World Health Organization aWho (2020) Coronavirus disease (COVID-2019) situation reports.

    Google Scholar 

  4. Prevention CfDCa. Coronavirus Disease 2019 (COVID-19) – how coronavirus spreads.

  5. Day M (2020) Covid-19: identifying and isolating asymptomatic people helped eliminate virus in Italian village. BMJ 368

  6. Koh D (2020) Occupational risks for COVID-19 infection. Occup Med 70:3

    Article  Google Scholar 

  7. Assiri A, McGeer A, Perl TM, Price CS, Al Rabeeah AA, Cummings DA, Alabdullatif ZN, Assad M, Almulhim A, Makhdoom H (2013) Hospital outbreak of Middle East respiratory syndrome coronavirus. N Engl J Med 369:407–416

    Article  CAS  Google Scholar 

  8. Guery B, Poissy J, El Mansouf L, Séjourné C, Ettahar N, Lemaire X, Vuotto F, Goffard A, Behillil S, Enouf V (2013) Clinical features and viral diagnosis of two cases of infection with Middle East respiratory syndrome coronavirus: a report of nosocomial transmission. Lancet 381:2265–2272

    Article  Google Scholar 

  9. Fan C, Li K, Ding Y, Lu WL, Wang J (2020) ACE2 expression in kidney and testis may cause kidney and testis damage after 2019-nCoV infection MedRxiv

    Google Scholar 

  10. Colaco S, K Chhabria, N Singh, A Bhide, D Singh, A Singh, A Husein, A Mishra, R Sharma and N Ashary (2020) Expression of SARS-CoV-2 receptor ACE2 and the spike protein processing enzymes in developing human embryos. arXiv preprint arXiv:2004.04935.

    Google Scholar 

  11. Corona G, Baldi E, Isidori A, Paoli D, Pallotti F, De Santis L, Francavilla F, La Vignera S, Selice R, Caponecchia L (2020) SARS-CoV-2 infection, male fertility and sperm cryopreservation: a position statement of the Italian Society of Andrology and Sexual Medicine (SIAMS)(Società Italiana di Andrologia e Medicina della Sessualità). J Endocrinol Investig 1

  12. Song C, Wang Y, Li W, Hu B, Chen G, Xia P, Wang W, Li C, Diao F, Hu Z (2020) Absence of 2019 novel coronavirus in semen and testes of COVID-19 patients. Biol Reprod

  13. Pan F, Xiao X, Guo J, Song Y, Li H, Patel DP, Spivak AM, Joseph PA, Zhang X, Xiong C (2020) No evidence of SARS-CoV-2 in semen of males recovering from COVID-19. Fertil Steril

  14. Li D, Jin M, Bao P, Zhao W, Zhang S (2020) Clinical characteristics and results of semen tests among men with coronavirus disease 2019. JAMA Netw Open 3:e208292–e208292

    Article  Google Scholar 

  15. Rademaker M (1994) Survival of virus in liquid nitrogen. N Z Med J 107:382–382

    CAS  PubMed  Google Scholar 

  16. Bielanski A, Vajta G (2009) Risk of contamination of germplasm during cryopreservation and cryobanking in IVF units. Hum Reprod 24:2457–2467

    Article  CAS  Google Scholar 

  17. Morris GJ (2005) The origin, ultrastructure, and microbiology of the sediment accumulating in liquid nitrogen storage vessels. Cryobiology 50:231–238

    Article  CAS  Google Scholar 

  18. group EC-W (2020) ESHRE guidance on recommencing ART treatments ESHRE website

    Google Scholar 

  19. (ASRM) ASFRM (2020) Patient management and clinical recommendations during the coronavirus (COVID-19) PANDEMIC.

    Google Scholar 

  20. The Association of Reproductive and Clinical Scientists aTBFS (2020) Best practice guidelines for reintroduction of routine fertility treatments during the COVID-19 pandemic.

    Google Scholar 

  21. Society for Assisted Reproductive Technology (SART) tCoRBC, and the Society for Reproductive Biologists and Technologists (SRBT) (2020) Laboratory Guidance for Commencing or Continuing ART Operations During the Ongoing COVID-19 Pandemic.

    Google Scholar 

  22. Kuhar DT, Carrico RM, Cox K, de Perio MA, Irwin KL, Lundstrom T, Overholt AD, Roberts KT, Russi M, Steed C (2019) Infection control in healthcare personnel: infrastructure and routine practices for occupational infection prevention and control services

    Google Scholar 

  23. Luangasanatip N, Hongsuwan M, Limmathurotsakul D, Lubell Y, AS Lee SH, Day NP, Graves N, Cooper BS (2015) Comparative efficacy of interventions to promote hand hygiene in hospital: systematic review and network meta-analysis. BMJ 351

  24. Organization WH. Guiding principles for immunization activities during the COVID-19 pandemic.

  25. Technology PCotSfAR and PCotASfR Medicine (2008) Guidelines for development of an emergency plan for in vitro fertilization programs. Fertil Steril 90:S131–S133

    Google Scholar 

  26. labs EGGoGPiI (2016) Revised guidelines for good practice in IVF laboratories (2015). Hum Reprod 31:685–686

    Article  Google Scholar 

  27. Tanks C (2020) Cryostorage of reproductive tissues in the in vitro fertilization laboratory: a committee opinion. https://www.reproductivefacts.org/globalassets/asrm/asrm-content/news-and-publications/practice-guidelines/for-non-members/cryostorage_of_reproductive_tissues.pdf.

    Google Scholar 

  28. van der Sande M, Teunis P, Sabel R (2008) Professional and home-made face masks reduce exposure to respiratory infections among the general population. PLoS One 3:e2618

    Article  Google Scholar 

  29. Elder K, Van den Bergh M, Woodward B (2015) Troubleshooting and problem-solving in the IVF laboratory. Cambridge University Press

  30. Schiewe M, Freeman M, Whitney J, VerMilyea M, Jones A, Aguirre M, Leisinger C, Adaniya G, Synder N, Chilton R (2019) Comprehensive assessment of cryogenic storage risk and quality management concerns: best practice guidelines for ART labs. J Assist Reprod Genet 36:5–14

    Article  CAS  Google Scholar 

  31. Hellewell J, Abbott S, Gimma A, Bosse NI, Jarvis CI, Russell TW, Munday JD, Kucharski AJ, Edmunds WJ, Sun F (2020) Feasibility of controlling COVID-19 outbreaks by isolation of cases and contacts. Lancet Glob Health

  32. Chu DK, Akl EA, Duda S, Solo K, Yaacoub S, Schünemann HJ, El-harakeh A, Bognanni A, Lotfi T, Loeb M (2020) Physical distancing, face masks, and eye protection to prevent person-to-person transmission of SARS-CoV-2 and COVID-19: a systematic review and meta-analysis. Lancet.

  33. Kariwa H, Fujii N, Takashima I (2006) Inactivation of SARS coronavirus by means of povidone-iodine, physical conditions and chemical reagents. Dermatology 212:119–123

    Article  CAS  Google Scholar 

  34. Parmegiani L, Accorsi A, Cognigni GE, Bernardi S, Troilo E, Filicori M (2010) Sterilization of liquid nitrogen with ultraviolet irradiation for safe vitrification of human oocytes or embryos. Fertil Steril 94:1525–1528

    Article  Google Scholar 

  35. Van Soom A, Wrathall A, Herrler A, Nauwynck H (2009) Is the zona pellucida an efficient barrier to viral infection? Reprod Fertil Dev 22:21–31

    Article  Google Scholar 

  36. Hernández C, Valdera C, Cordero J, López E, Plaza J, Albi M (2020) Impact of telemedicine on assisted reproduction treatment in the public health system. J Healthc Qual Res 35:27–34

    Article  Google Scholar 

  37. Helmbuch BK, JK Hodge and JD Wander (2007) Viral penetration of high efficiency particulate air (HEPA) filters. APPLIED RESEARCH ASSOCIATES INC TYNDALL AFB FL.

    Google Scholar 

  38. Reza MS, Hasan AK, Afroze S, Bakar MSA, Taweekun J, Azad AK (2020) Analysis on preparation, application, and recycling of activated carbon to aid in COVID-19 protection. Int J Integrated Eng 12:233–244

    Article  Google Scholar 

  39. Li R, Yin T, Fang F, Li Q, Chen J, Wang Y, Hao Y, Wu G, Duan P, Wang Y (2020) Potential risks of SARS-Cov-2 infection on reproductive health. Reprod BioMed Online

    Google Scholar 

  40. Ng LF, Wong M, Koh S, Ooi E-E, Tang K-F, Leong H-N, Ling A-E, Agathe LV, Tan J, Liu ET (2004) Detection of severe acute respiratory syndrome coronavirus in blood of infected patients. J Clin Microbiol 42:347–350

    Article  CAS  Google Scholar 

  41. SARS-CoV-2 host receptors ACE2 and CD147 (BSG) are present on human oocytes and blastocysts (2020) https://doi.org/10.1007/s10815-020-01952-x.

  42. Fourie JM, Loskutoff N, Huyser C (2015) Semen decontamination for the elimination of seminal HIV-1. Reprod BioMed Online 30:296–302

    Article  CAS  Google Scholar 

  43. Nicholson C, Abramsson L, Holm S, Bjurulf E (2000) Bacterial contamination and sperm recovery after semen preparation by density gradient centrifugation using silane-coated silica particles at different g forces. Hum Reprod 15:662–666

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Not applicable.

Funding

None.

Author information

Authors and Affiliations

Authors

Contributions

FC wrote the manuscript. NY critically revised the article. FC, NY, and AH provided the current recommendations. All authors have read and approved the manuscript.

Corresponding author

Correspondence to Fadi Choucair.

Ethics declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Choucair, F., Younis, N. & Hourani, A. IVF laboratory COVID-19 pandemic response plan: a roadmap. Middle East Fertil Soc J 25, 31 (2020). https://doi.org/10.1186/s43043-020-00043-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s43043-020-00043-2

Keywords