key: cord-1007941-u5iwyt9p authors: Miguel, Danilo C.; Brioschi, Mariana B.C.; Rosa, Leticia B.; Minori, Karen; Grazzia, Nathalia title: The impact of COVID-19 on neglected parasitic diseases: what to expect? date: 2021-05-14 journal: Trends Parasitol DOI: 10.1016/j.pt.2021.05.003 sha: c53d3dae6a0e7e7874dfb21e069386f43a877678 doc_id: 1007941 cord_uid: u5iwyt9p Here we highlight co-infections of SARS-Cov-2 with ectoparasites, helminths and protozoa described in the literature and the urgent need to understand the conditions of these associated pathologies. We reinforce that such information is crucial for the continuity of measures that have been used for decades to control neglected parasitic diseases. On March 11, 2020 , concerned by the alarming levels of spread and severity, the WHO declared the COVID-19 outbreak as pandemic i . Since then, much has been speculated regarding forms of transmission that could effectively explain the dispersion of the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). One year later, the scientific community recognized the relevance of SARS-CoV-2 airborne transmission, setting aside the viral dissemination through objects and surfaces ii . The spread of the virus has spared no segment of the globe, but the impact on developing/poor countries, which present the highest prevalence rates for NTDs, is likely to be much more severe and prolonged. COVID-19 infections are not only expected to hinder social and economic development directly, but are also being responsible for the elimination of NTDs control programs, especially those related to mass drug administration (MDA) [1] . This widespread therapeutic intervention is highly dependent on public-private partnership investments and direct contact between health/surveillance professionals and the affected population. Regrettably, it is expected that MDA will face long-term challenges for its successful continuity once measures of social distancing, isolation and monetary crisis became our new reality. Developing/poor countries are endemic for NTDs caused by ectoparasites, helminths and protozoa, classically referred to as parasites and represent a heavy burden on malnourished population that live in unsanitary living conditions. The impact of parasitic NTDs in the additional infestations could be related to tourism activities. As travels were directly reduced by COVID-19, these cases are also expected to follow this trend. However, in terms of poor areas that are affected by ectoparasites, a Turkish study reported an increase in scabies cases in national hospitals in March, 2020. This raise may be explained by COVID-19 imposed restrictions, which exacerbated poor hygiene conditions of families that were forced to live in close quarters in rural areas favoring a primary source of Sarcoptes scabiei infestation [2] . Conversely, an interesting study by Galassi and colleagues demonstrated the impact of the current pandemic on cases of pediculosis in Latin America. This study, carried out during a strict lockdown period (Mar-Jul/2020) in Argentina from data of 1,118 school-aged children showed a decrease of head lice infestation from 70% (before lockdown) to 43% (during lockdown) [3] . As this disease is dependent on physical contact, it is not surprising that there was a significant reduction in head lice prevalence during imposed lockdown due to the restricted movement of children outside their homes and the absence of regular classes. The control of helminths infections is based on the collective effort aimed at preventing parasite-host effective transmission, encouraging MDA and public health campaign initiatives. There is a high expectation that helminth-caused NTDs will be eradicated or massively controlled by 2030 in affected tropical and subtropical regions, however, the chances of global control are threatened by the SARS-CoV-2 circulation [1, 4] . Most of African countries, for example, faced countless NTDs for many decades, including schistosomiasis, for which ideal preventive measures rely on basic sanitation systems. Unfortunatly, endemic areas were also being drastically affected by COVID-19 cases among the vulnerable population. Oyeyemi and co-authors found that the occurrence of active cases of COVID-19 was higher in endemic areas for schistosomiasis, as well as the number of deaths during the pandemic in 42 countries. Schistosomiasis endemicity appears to be associated with negative COVID-19 outcomes. Concomitantly, in regions where praziquantel treatment coverage is high, a significant reduction of COVID-19 active cases is expected, followed by the improvement on recovery rates [5] . Additionally, the continuity of control and prevention of schistosomiasis programs proved to be threatened after the establishment of the pandemic in 12 schistosomiasis-endemic provinces in China. Guo et al. observed a dramatic reduction of ~1/4 of the gross funds allocated to these programs from Jan-Mar/2020, pointing that a short-term impact on the schistosomiasis monitoring program has been seen due to COVID-19 [6] . In regard to treatment, there should be a constant concern with patients receiving high doses of corticosteroids for COVID-19 in NTDs endemic areas. There are reports in the literature pointing to the development of disseminated strongyloidiasis after immunosuppressants therapy, an expected event, given that corticosteroids promote moulting of the larvae, leading to severe hyperinfection cases. Therefore, it is essential to consider screening for Strongyloides infections in individuals with COVID-19 from endemic regions before the administration of immunosuppressants [7] . A curious recent report reinforces another example of co-infection that may require attention from health professionals. In this case, a blood smear sample was collected from a 37-yearold south Asian man with COVID-19 pneumonia, but no filariasis symptoms, despite the presence of Wuchereria bancrofti microfilaria. It is important to emphasize in such cases that mixed infections should be suspected during clinical examinations and routine lab tests in order to allow proper diseases monitoring in endemic regions [8] . Acanthamoeba and Legionella pneumophila-infected Acanthamoeba [11] . Vector-borne protozoan infections caused by Trypanosoma cruzi (Chagas Disease; CD) and Leishmania spp. (cutaneous and visceral leishmaniasis; CL and VL) may also be impacted by COVID-19. Considering that the population with CD (>6 million people worldwilde) is socioeconomically vulnerable and presents many comorbidities, the spread of the pandemic becomes a concern. Zaidel and co-authors pointed out that chronic medical conditions, such as diabetes, chronic obstructive pulmonary disease and other cardiovascular diseases increase the risk of death due to the new coronavirus. Besides, there is scientific evidence that elderly people with chronic Chagas cardiomyopathy (CCC) have a higher risk of death by COVID-19 when compared to seronegative same age patients [12] . Alberca et al. reported fatal cases of elderly Brazilian patients co-infected with CD and COVID-19 [13] . A case of a Brazilian woman with concomitant leprosy, CD, and cutaneous/mucosal manifestations of the coronavirus infection has been reported and the authors speculate that, although the patient had borderline leprosy and CCC, she did not show any recrudescence of leprosy symptoms, worsening of cardiac symptoms or severe COVID-19, a fact maybe explained by immunomodulatory properties of leprosy treatment she has previously undergone [14] . Although CD cases in the Brazilian Southeast region comprises less than 5% of the total prevalence in Brazil, COVID-19-CD cases may be an important cause of uninvestigated death in endemic regions. Parasitic disease also presents itself as an important risk factor for the development of the severe form of COVID-19, since some patients have respiratory and systemic impairment, especially in endemic areas for both diseases [12] . Leishmaniasis is a disease that also deserves attention. The incidence of CL cases can increase substantially in areas with migratory movements due to the poverty scenario that can be accentuated by COVID-19. This is extremely relevant when added to the fact that several reports have shown that middle Eastern countries facing civil conflicts are experiencing the massive displacement of refugees. As a consequence, Leishmania parasites show potential to be transmitted by permissive vectors present in other territories iii . In terms of Leishmania-SARS-CoV-2 pathogenesis modulation, Carvalho and collaborators speculated that COVID-19 may be aggravated in VL endemic areas due to innefective immune control against viral infections in VL patients [15] . In truth, it illustrates the complexity of SARS-CoV-2 coinfections, for which risks and severity of clinical symptoms interfere with the course of each disease perhaps due to immune modulation. Unfortunately, countries that concentrate parasitic NTDs have demonstrated inability in the adoption of effective control measures to curb the cases of COVID-19, such as African, Caribbean and Middle Eastern countries, Brazil and India iv . Therefore, cases of co-infection should be more frequent. Examples brought up reveal the short term impact of co-infections at the individual level. Not less important is the idea that SARS-CoV-2 co-infections may lead to serious long term consequences for entire communities, especially those requiring basic resources to guarantee their survival. The imminent possibility of resources scarcity in settings where MDA control and health surveillance programs have been used to control NTDs is threatening. Still in the pandemic scenario, where consequences must be prolonged for months/years, new cases of co-infections must be reported, bringing examples that need to be well understood biologically and epidemiologically so that the conditions of the associated pathologies are known (Box 1). Such information may provide clues to government and health professionals J o u r n a l P r e -p r o o f Journal Pre-proof to establish effective parasitic disease control and surveillance policies in endemic and nonendemic regions. As urgent measures, we reinforce the need for intragovernmental and global health agencies alliances to base their efforts on mass vaccination against COVID-19, essentially to poor/developing countries, and to reinforce the importance of measures to restrain the spread of SARS-CoV-2 to lessen negative impacts on parasitic NTDs control programs. The new COVID-19 poor and the neglected tropical diseases resurgence The effect of the "stay-at-home" policy on requests for dermatology outpatient clinic visits after the COVID-19 outbreak Head lice were also affected by COVID-19: a decrease on Pediculosis infestation during lockdown in Buenos Aires The global progress of soil-transmitted helminthiases control in 2020 and World Health Organization targets for 2030 Assessment of schistosomiasis endemicity and preventive treatment on coronavirus disease 2019 outcomes in Africa. New Microbes New Infec. 38 Challenges of schistosomiasis control in China during the coronavirus disease 2019 (COVID-19) epidemic. Zhongguo xue xi chong bing fang zhi za zhi= Strongyloides infection manifested during immunosuppressive therapy for SARS-CoV-2 pneumonia COVID-19 unfolding filariasis: The first case of SARS-CoV-2 and Wuchereria bancrofti coinfection Giardiasis reactivation during severe SARS-CoV-2 infection Wastewater-based epidemiology -surveillance and early detection of waterborne pathogens with a focus on SARS-CoV-2, Cryptosporidium and Giardia SARS-CoV-2: Disinfection Strategies to Prevent Transmission of Neuropathogens via Air Conditioning Systems COVID-19: Implications for People with Chagas Disease. Global heart 15, 69 Case Report: COVID-19 and Chagas Disease in Two Coinfected Patients The challenge of concomitant infections in the coronavirus disease 2019 pandemic era: Severe acute respiratory syndrome coronavirus 2 infection in a patient with chronic Chagas disease and dimorphic leprosy Should an intersection between visceral leishmaniasis endemicity and the COVID-19 pandemic be considered? Med. Hypotheses. 144, 110289. Box 1. Key points to be considered in the context of COVID-19 and parasitic NTDs coinfections • Certain NTDs may have their control programs affected by the COVID-19 pandemic, requiring urgent attention from governmental and non-governmental institutions. • It is important that medical and scientific communities recognize the particularities of different parasitic diseases and the impact that co-infection with SARS-Cov-2 may have on the progression in each case In non-endemic areas, attention should be given to immigrants, refugees and tourists. • Effects of immunosuppressive therapies must be monitored, as some parasites may find favorable conditions for uncontrolled proliferation We thank Dr. Cecilia F. Dupecher for critically reading the manuscript. We also thank all the professionals who have sacrificed their lives during the COVID-19 pandemic. The authors declare no competing interests.