Extrapulmonary onset manifestations of COVID-19

Finsterer, Josef; Scorza, Fulvio A.; Scorza, Carla A.; Fiorini, Ana C.

doi:10.6061/clinics/2021/e2900

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REVIEW ARTICLE • Clinics 76 • 2021 • https://doi.org/10.6061/clinics/2021/e2900 copy

Extrapulmonary onset manifestations of COVID-19

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Coronavirus disease (COVID-19) usually starts with pulmonary signs and symptoms. However, in some cases, the initial clinical presentations are extrapulmonary. This literature review aimed at summarizing and discussing the extrapulmonary onset manifestations of COVID-19. The most frequent initial extrapulmonary manifestations include hypogeusia, hyposmia, non-specific abdominal symptoms, corneal congestion, and deep venous thrombosis. Several rarer extrapulmonary manifestations in locations such as the brain, peripheral nerves, muscles, eyes, ears, myocardium, intestines, skin, or vessels have been additionally reported as onset presentations of COVID-19. In conclusion, it is crucial for clinicians and health care providers to consider extrapulmonary presentations at the onset of COVID-19 to avoid overlooking the infection and contributing to the spread of the disease.

Clinical Presentation; COVID-19; Onset; SARS-CoV-2; Variability

Organ	Initial manifestation	Frequency	Reference
CNS	Meningitis	rare	[Naz et al. (¹³13. Naz S, Hanif M, Haider MA, Ali MJ, Ahmed MU, Saleem S. Meningitis as an Initial Presentation of COVID-19: A Case Report. Front Public Health. 2020;8:474. https://doi.org/10.3389/fpubh.2020.00474 https://doi.org/10.3389/fpubh.2020.00474... )]
	Delirium	rare	[Poloni et al. (¹⁶16. Poloni TE, Medici V, Moretti M, Visonè SD, Cirrincione A, Carlos AF, et al. COVID-19-related neuropathology and microglial activation in elderly with and without dementia. Brain Pathol. 2021;e12997. https://doi.org/10.1111/bpa.12997 https://doi.org/10.1111/bpa.12997... )]
	ADEM	rare	[Abdi et al. (¹⁴14. Abdi S, Ghorbani A, Fatehi F. The association of SARS-CoV-2 infection and acute disseminated encephalomyelitis without prominent clinical pulmonary symptoms. J Neurol Sci. 2020;416:117001. https://doi.org/10.1016/j.jns.2020.117001 https://doi.org/10.1016/j.jns.2020.11700... )]
	Epilepsy	rare	[Pinna et al. (¹⁵15. Pinna P, Grewal P, Hall JP, Tavarez T, Dafer RM, Garg R, et al. Neurological manifestations and COVID-19: Experiences from a tertiary care center at the Frontline. J Neurol Sci. 2020;415:116969. https://doi.org/10.1016/j.jns.2020.116969 https://doi.org/10.1016/j.jns.2020.11696... )]
	Headache	rare	[Pinna et al. (¹⁵15. Pinna P, Grewal P, Hall JP, Tavarez T, Dafer RM, Garg R, et al. Neurological manifestations and COVID-19: Experiences from a tertiary care center at the Frontline. J Neurol Sci. 2020;415:116969. https://doi.org/10.1016/j.jns.2020.116969 https://doi.org/10.1016/j.jns.2020.11696... )]
	Ischemic stroke	rare	[Pinna et al. (¹⁵15. Pinna P, Grewal P, Hall JP, Tavarez T, Dafer RM, Garg R, et al. Neurological manifestations and COVID-19: Experiences from a tertiary care center at the Frontline. J Neurol Sci. 2020;415:116969. https://doi.org/10.1016/j.jns.2020.116969 https://doi.org/10.1016/j.jns.2020.11696... )]
	Intracerebral bleeding	rare	[Pinna et al. (¹⁵15. Pinna P, Grewal P, Hall JP, Tavarez T, Dafer RM, Garg R, et al. Neurological manifestations and COVID-19: Experiences from a tertiary care center at the Frontline. J Neurol Sci. 2020;415:116969. https://doi.org/10.1016/j.jns.2020.116969 https://doi.org/10.1016/j.jns.2020.11696... )]
	Short term memory impairment	rare	[Pinna et al. (¹⁵15. Pinna P, Grewal P, Hall JP, Tavarez T, Dafer RM, Garg R, et al. Neurological manifestations and COVID-19: Experiences from a tertiary care center at the Frontline. J Neurol Sci. 2020;415:116969. https://doi.org/10.1016/j.jns.2020.116969 https://doi.org/10.1016/j.jns.2020.11696... )]
	Transverse myelitis	rare	[Chakraborty et al. (¹⁷17. Chakraborty U, Chandra A, Ray AK, Biswas P. COVID-19-associated acute transverse myelitis: a rare entity. BMJ Case Rep. 2020;13(8):e238668. https://doi.org/10.1136/bcr-2020-238668 https://doi.org/10.1136/bcr-2020-238668... )]
	Altered mental state	rare	[Pinna et al. (¹⁵15. Pinna P, Grewal P, Hall JP, Tavarez T, Dafer RM, Garg R, et al. Neurological manifestations and COVID-19: Experiences from a tertiary care center at the Frontline. J Neurol Sci. 2020;415:116969. https://doi.org/10.1016/j.jns.2020.116969 https://doi.org/10.1016/j.jns.2020.11696... )]
	Confusion	rare	[Alkeridy et al. (¹⁸18. Alkeridy WA, Almaghlouth I, Alrashed R, Alayed K, Binkhamis K, Alsharidi A, et al. A Unique Presentation of Delirium in a Patient with Otherwise Asymptomatic COVID-19. J Am Geriatr Soc. 2020;68(7):1382-4. https://doi.org/10.1111/jgs.16536 https://doi.org/10.1111/jgs.16536... )]
	Acute encephalopathy	rare	[Farhadian et al. (¹⁹19. Farhadian S, Glick LR, Vogels CBF, Thomas J, Chiarella J, Casanovas-Massana A, et al. Acute encephalopathy with elevated CSF inflammatory markers as the initial presentation of COVID-19. Res Sq [Preprint]. 2020;rs.3.rs-28583.https://doi.org/https://doi.org/10.21203/rs.3.rs-28583/v1. Update in: BMC Neurol. 2020;20(1):248. https://doi.org/https://doi.org/10.21203... )]
Nerves	Hyposmia	frequent	[Ramasamy et al. (⁴4. Ramasamy K, Saniasiaya J, Abdul Gani N. Olfactory and Gustatory Dysfunctions as a Clinical Manifestation of Coronavirus Disease 2019 in a Malaysian Tertiary Center. Ann Otol Rhinol Laryngol. 2021;130(5):513-9. https://doi.org/10.1177/0003489420963165 https://doi.org/10.1177/0003489420963165... )]
			[Chi et al. (²⁰20. Chi H, Chiu NC, Peng CC, Lin CH, Tai YL, Lee MD, et al. One-Seventh of Patients with COVID-19 Had Olfactory and Gustatory Abnormalities as Their Initial Symptoms: A Systematic Review and Meta-Analysis. Life (Basel). 2020;10(9):158. https://doi.org/10.3390/life10090158 https://doi.org/10.3390/life10090158... )]
	Hypogeusia	frequent	[Ramasamy et al. (⁴4. Ramasamy K, Saniasiaya J, Abdul Gani N. Olfactory and Gustatory Dysfunctions as a Clinical Manifestation of Coronavirus Disease 2019 in a Malaysian Tertiary Center. Ann Otol Rhinol Laryngol. 2021;130(5):513-9. https://doi.org/10.1177/0003489420963165 https://doi.org/10.1177/0003489420963165... )]
			[Chi et al. (²⁰20. Chi H, Chiu NC, Peng CC, Lin CH, Tai YL, Lee MD, et al. One-Seventh of Patients with COVID-19 Had Olfactory and Gustatory Abnormalities as Their Initial Symptoms: A Systematic Review and Meta-Analysis. Life (Basel). 2020;10(9):158. https://doi.org/10.3390/life10090158 https://doi.org/10.3390/life10090158... )]
	Guillain-Barre syndrome	rare	[Zhao et al. (²¹21. Zhao H, Shen D, Zhou H, Liu J, Chen S. Guillain-Barré syndrome associated with SARS-CoV-2 infection: causality or coincidence? Lancet Neurol. 2020;19(5):383-4. https://doi.org/10.1016/S1474-4422(20)30109-5 https://doi.org/10.1016/S1474-4422(20)30... )]
	Dysautonomia	rare	[Pinna et al. (¹⁵15. Pinna P, Grewal P, Hall JP, Tavarez T, Dafer RM, Garg R, et al. Neurological manifestations and COVID-19: Experiences from a tertiary care center at the Frontline. J Neurol Sci. 2020;415:116969. https://doi.org/10.1016/j.jns.2020.116969 https://doi.org/10.1016/j.jns.2020.11696... )]
	Facial palsy	rare	[Pinna et al. (¹⁵15. Pinna P, Grewal P, Hall JP, Tavarez T, Dafer RM, Garg R, et al. Neurological manifestations and COVID-19: Experiences from a tertiary care center at the Frontline. J Neurol Sci. 2020;415:116969. https://doi.org/10.1016/j.jns.2020.116969 https://doi.org/10.1016/j.jns.2020.11696... )]
Muscle	Myositis	rare	[Almadani et al. (²²22. Almadani M, Shiferson A, Swearingen B, Shih M, Jacob T, Rhee R. Compartment syndrome secondary to viral myositis as initial presentation in COVID-19 patient. J Vasc Surg Cases Innov Tech. 2020;6(4):524-7. https://doi.org/10.1016/j.jvscit.2020.08.021 https://doi.org/10.1016/j.jvscit.2020.08... )]
	Rhabdomyolysis	rare	[Anklesaria et al. (²³23. Anklesaria Z, Frankman J, Gordin J, Zhan J, Liu AK. Fatal Rhabdomyolysis in a COVID-19 Patient on Rosuvastatin. Cureus. 2020;12(10):e11186. https://doi.org/10.7759/cureus.11186 https://doi.org/10.7759/cureus.11186... )]
			[Suwanwongse et al. (²⁴24. Suwanwongse K, Shabarek N. Rhabdomyolysis as a Presentation of 2019 Novel Coronavirus Disease. Cureus. 2020;12(4):e7561. https://doi.org/10.7759/cureus.7561 https://doi.org/10.7759/cureus.7561... )]
Eyes	Pan-uveitis	rare	[Benito-Pascual et al. (²⁵25. Benito-Pascual B, Gegúndez JA, Díaz-Valle D, Arriola-Villalobos P, Carreão E, Culebras E, et al. Panuveitis and Optic Neuritis as a Possible Initial Presentation of the Novel Coronavirus Disease 2019 (COVID-19). Ocul Immunol Inflamm. 2020;28(6):922-5. https://doi.org/10.1080/09273948.2020.1792512 https://doi.org/10.1080/09273948.2020.17... )]
	Optic neuritis	rare	[Benito-Pascual et al. (²⁵25. Benito-Pascual B, Gegúndez JA, Díaz-Valle D, Arriola-Villalobos P, Carreão E, Culebras E, et al. Panuveitis and Optic Neuritis as a Possible Initial Presentation of the Novel Coronavirus Disease 2019 (COVID-19). Ocul Immunol Inflamm. 2020;28(6):922-5. https://doi.org/10.1080/09273948.2020.1792512 https://doi.org/10.1080/09273948.2020.17... )]
	Conjunctivitis	rare	[Ozturker (²⁶26. Ozturker ZK. Conjunctivitis as sole symptom of COVID-19: A case report and review of literature. Eur J Ophthalmol. 2021;31(2):NP161-NP166. https://doi.org/10.1177/1120672120946287. Erratum in: Eur J Ophthalmol. 2020;1120672120956486 https://doi.org/10.1177/1120672120946287... )]
	Conjunctival congestion	rare	[Chen et al. (²⁷27. Chen L, Deng C, Chen X, Zhang X, Chen B, Yu H, et al. Ocular manifestations and clinical characteristics of 535 cases of COVID-19 in Wuhan, China: a cross-sectional study. Acta Ophthalmol. 2020;98(8):e951-e959. https://doi.org/10.1111/aos.14472 https://doi.org/10.1111/aos.14472... )]
	Retro-orbital pain	rare	[Ruiy et al. (²⁸28. Ruiy W, Hsu SY, Tsai HL, Chen CT, Tseng CP, Chen WT. COVID-19 mimicking dengue fever with the initial manifestation of retro-orbital pain - A Rare Case. J Formos Med Assoc. 2020;119(11):1715-6. https://doi.org/10.1016/j.jfma.2020.05.039 https://doi.org/10.1016/j.jfma.2020.05.0... )]
Ears	Sensorineural hearing loss	rare	[Kilic et al. (⁵5. Kilic O, Kalcioglu MT, Cag Y, Tuysuz O, Pektas E, Caskurlu H, et al. Could sudden sensorineural hearing loss be the sole manifestation of COVID-19? An investigation into SARS-COV-2 in the etiology of sudden sensorineural hearing loss. Int J Infect Dis. 2020;97:208-11. https://doi.org/10.1016/j.ijid.2020.06.023 https://doi.org/10.1016/j.ijid.2020.06.0... )]
Heart	Myocarditis	rare	[Naneishvili et al. (⁶6. Naneishvili T, Khalil A, O'Leary R, Prasad N. Fulminant myocarditis as an early presentation of SARS-CoV-2. BMJ Case Rep. 2020;13(9):e237553. https://doi.org/10.1136/bcr-2020-237553 https://doi.org/10.1136/bcr-2020-237553... )]
Intestines	Abdominal pain, cramps, nausea	frequent	[Dietrich et al. (⁷7. Dietrich CG, Hübner D, Marx G, Bickenbach J, Bootsveld A. Primary presentation of COVID-19 solely with gastrointestinal symptoms: a problem for the containment of the disease. Eur J Gastroenterol Hepatol. 2020;32(11):1475-8. https://doi.org/10.1097/MEG.0000000000001922 https://doi.org/10.1097/MEG.000000000000... )]
			[Wu et al. (²⁹29. Wu CY, Yu XP, Ma AHY, Wang LP, Yang NB, Li GX, et al. Coronavirus disease 19 with gastrointestinal symptoms as initial manifestations: a case report. J Int Med Res. 2020;48(9):300060520952256. https://doi.org/10.1177/0300060520952256 https://doi.org/10.1177/0300060520952256... )]
			[Amaral et al. (³⁰30. Amaral LTW, Brito VM, Beraldo GL, Fonseca EKUN, Yokoo P, Talans A, et al. Abdominal symptoms as initial manifestation of COVID-19: a case series. Einstein (Sao Paulo). 2020;18:eRC5831. https://doi.org/10.31744/einstein_journal/2020RC5831 https://doi.org/10.31744/einstein_journa... )]
			[Remes-Troche et al. (³¹31. Remes-Troche JM, Ramos-de-la-Medina A, Manríquez-Reyes M, Martínez-Pérez-Maldonado L, Lara EL, Solís-González MA. Initial Gastrointestinal Manifestations in Patients With Severe Acute Respiratory Syndrome Coronavirus 2 Infection in 112 Patients From Veracruz in Southeastern Mexico. Gastroenterology. 2020;159(3):1179-81. https://doi.org/10.1053/j.gastro.2020.05.055 https://doi.org/10.1053/j.gastro.2020.05... )]
			[Khader et al. (³²32. Khader M, Al Bishawi A, Kambal A, Abdelmajid A. SARS-CoV-2 infection presenting as colitis with chest and abdomen CT findings. Radiol Case Rep. 2020;15(11):2427-32. https://doi.org/10.1016/j.radcr.2020.09.035 https://doi.org/10.1016/j.radcr.2020.09.... )]
	Hepatopathy	frequent	[Mao et al. (³³33. Mao R, Qiu Y, He JS, Tan JY, Li XH, Liang J, et al. Manifestations and prognosis of gastrointestinal and liver involvement in patients with COVID-19: a systematic review and meta-analysis. Lancet Gastroenterol Hepatol. 2020;5(7):667-8. https://doi.org/10.1016/S2468-1253(20)30126-6 https://doi.org/10.1016/S2468-1253(20)30... )]
	Mesenteric adenopathy	rare	[Noda et al. (³⁴34. Noda S, Ma J, Romberg EK, Hernandez RE, Ferguson MR. Severe COVID-19 initially presenting as mesenteric adenopathy. Pediatr Radiol. 2021;51(1):140-3. https://doi.org/10.1007/s00247-020-04789-9 https://doi.org/10.1007/s00247-020-04789... )]
	Gastrointestinal bleeding	rare	[Gulen and Satar (³⁵35. Gulen M, Satar S. Uncommon presentation of COVID-19: Gastrointestinal bleeding. Clin Res Hepatol Gastroenterol. 2020;44(4):e72-e76. https://doi.org/10.1016/j.clinre.2020.05.001 https://doi.org/10.1016/j.clinre.2020.05... )]
	Pancreatitis	rare	[Wang et al. (³⁶36. Wang K, Luo J, Tan F, Liu J, Ni Z, Liu D, et al. Acute Pancreatitis as the Initial Manifestation in 2 Cases of COVID-19 in Wuhan, China. Open Forum Infect Dis. 2020;7(9):ofaa324. https://doi.org/10.1093/ofid/ofaa324 https://doi.org/10.1093/ofid/ofaa324... )]
	Diarrhea	rare	[Yang et al. (³⁷37. Yang X, Zhao J, Yan Q, Zhang S, Wang Y, Li Y. A case of COVID-19 patient with the diarrhea as initial symptom and literature review. Clin Res Hepatol Gastroenterol. 2020;44(5):e109-e112. https://doi.org/10.1016/j.clinre.2020.03.013 https://doi.org/10.1016/j.clinre.2020.03... )]
Vessels	Deep venous thrombosis	frequent	[Erdinc et al. (⁸8. Erdinc B, Raina JS. Spontaneous Retroperitoneal Bleed Coincided With Massive Acute Deep Vein Thrombosis as Initial Presentation of COVID-19. Cureus. 2020;12(8):e9772. https://doi.org/10.7759/cureus.9772 https://doi.org/10.7759/cureus.9772... )]
	Artery thrombosis	rare	[Thompson et al. (³⁸38. Thompson O, Pierce D, Whang D, O'Malley M, Geise B, Malhotra U. Acute limb ischemia as sole initial manifestation of SARS-CoV-2 infection. J Vasc Surg Cases Innov Tech. 2020;6(4):511-3. https://doi.org/10.1016/j.jvscit.2020.07.017 https://doi.org/10.1016/j.jvscit.2020.07... )]
			[Shao et al. (³⁹39. Shao T, In-Bok Lee C, Jabori S, Rey J, Duran ER, Kang N. Acute upper limb ischemia as the first manifestation in a patient with COVID-19. J Vasc Surg Cases Innov Tech. 2020;6(4):674-7. https://doi.org/10.1016/j.jvscit.2020.08.003 https://doi.org/10.1016/j.jvscit.2020.08... )]
	Common carotid artery occlusion	rare	[Alkhaibary et al. (⁹9. Alkhaibary A, Abbas M, Ahmed ME, Khatri IA, Alkhani A. Common Carotid Artery Occlusion in a Young Patient: Can Large-Vessel Stroke Be the Initial Clinical Manifestation of Coronavirus Disease 2019? World Neurosurg. 2020;144:140-2. https://doi.org/10.1016/j.wneu.2020.08.154 https://doi.org/10.1016/j.wneu.2020.08.1... )]
Skin	Chilblain-like lesions, bullae	rare	[Rubin et al. (⁴⁰40. Rubin A, Alamgir M, Rubin J, Rao BK. Chilblain-like lesions with prominent bullae in a patient with COVID-19. BMJ Case Rep. 2020;13(11):e237917. https://doi.org/10.1136/bcr-2020-237917 https://doi.org/10.1136/bcr-2020-237917... )]
	Maculopapular rash	rare	[Falkenhain et al. (⁴¹41. Falkenhain López D, Sánchez-Velázquez A, Ortiz de Frutos J. Maculopapular rash as initial manifestation of SRAS-coronavirus-2 infection. Med Clin (Engl Ed). 2020;155(2):92. https://doi.org/10.1016/j.medcle.2020.04.008 https://doi.org/10.1016/j.medcle.2020.04... )]
Blood	Thrombocytopenia	rare	[Ahmed et al. (⁴²42. Ahmed MZ, Khakwani M, Venkatadasari I, Horgan C, Giles H, Jobanputra S, et al. Thrombocytopenia as an initial manifestation of COVID-19; case series and literature review. Br J Haematol. 2020;189(6):1057-8. https://doi.org/10.1111/bjh.16769 https://doi.org/10.1111/bjh.16769... )]
Other	Neonatal apnoea	rare	[Gonzalez-Brabin et al. (¹⁰10. González Brabin A, Iglesias-Bouzas MI, Nieto-Moro M, Martínez de Azagra-Garde A, García-Salido A. Apnea neonatal como manifestación inicial de infección por SARS-CoV-2 [Neonatal apnea as initial manifestation of SARS-CoV-2 infection]. An Pediatr (Engl Ed). 2020;93(3):215-6. https://doi.org/10.1016/j.anpedi.2020.05.008 https://doi.org/10.1016/j.anpedi.2020.05... )]
	Orofacial manifestations	rare	[Halboub et al. (¹¹11. Halboub E, Al-Maweri SA, Alanazi RH, Qaid NM, Abdulrab S. Orofacial manifestations of COVID-19: a brief review of the published literature. Braz Oral Res. 2020;34:e124. https://doi.org/10.1590/1807-3107bor-2020.vol34.0124 https://doi.org/10.1590/1807-3107bor-202... )]

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[1] *Corresponding author. E-mail: fifigs1@yahoo.de