INTRODUCTION

Parasitic zoonoses are neglected diseases that are naturally transmitted from vertebrate animals to humans, the most important being zoonoses caused by helminths such as Fasciola hepatica, Echinococcus granulosus and Taenia solium¹. In humans, T. solium cysticercus infection mainly affects the central nervous system (CNS), F. hepatica infection affects the bile ducts of the liver, and E. granulosus infection affects the liver and lungs. All these tissue parasitosis are asymptomatic until the chronic phase of the disease, where the main signs and symptoms begin to manifest, significantly deteriorating health ².

These zoonoses are mainly distributed in Africa, Asia, Southern Europe and South America ^(3-5. In Peru, seroprevalence rates in humans of up to 20% of cystic echinococcosis were reported in Cerro de Pasco ⁶, 24% of T. solium cysticercus in Saylla (Cusco) ⁷ and up to 31% of fascioliasis in Puno ⁸, which are rural and cattle-raising areas of the central and southern highlands. It is estimated that, in Peru, the burden of disease per disability-adjusted life years (DALY) for human cystic echinococcosis is 1139 years with a total annual cost of 2,420,348 US dollars ⁹; however, there are no DALY estimates for T. solium cysticercus and human fascioliasis.

The main risk factors associated with human cystic echinococcosis, which have been reported in the Peruvian population, are exposure to infected dogs, contact with infected cattle and consumption of food contaminated with eggs of E. granulosus, which is the infecting form of the parasite ¹⁰. Human fascioliasis is associated with determinants such as exposure to infected cattle and consumption of raw vegetables exposed to irrigation water contaminated with metacercariae of F. hepatica, which is the infecting form of the trematode ¹¹. On the other hand, the risk factors associated with T. solium cysticercus are the consumption of raw or undercooked pork contaminated with T. solium cysticercus larvae, consumption of food and water contaminated with feces of people with taeniasis through direct transmission of T. solium eggs, which is the infecting form of T. solium cysticercus¹². In addition, there are common determinants for the three zoonoses such as deficient hygienic habits and unfavorable socioeconomic conditions, such as the lack of access to adequate health services, education and basic sanitation ^10-12.

There are studies on the distribution of zoonoses at the national level focused on school-age children; however, neither the communities at high risk of zoonoses in the Peruvian territory nor the magnitude of the disease in the general population have been determined. For this reason, this study aimed to determine seropositivity to anti-IgG antibodies for E. granulosus, F. hepatica and T. solium cysticercus infection and to describe the characteristics of those infected in 13 regions of the Peruvian highlands between 2016 and 2019.

MATERIALS AND METHODS

RESULTS

Of the 9389 epidemiological files identified, 1578 were excluded due to lack of information. A total of 7811 epidemiological files obtained from inhabitants of 13 highland regions of Peru were included (Figure 1).

Figure 1 Flow chart of the analyzed epidemiological files. 

Table 1 describes the sociodemographic characteristics of the population; 36.7% were adults, 65% were male, and 41.4% were students. Likewise, most the participants had primary education (44.4%), had adobe as a housing wall material (85.2%), had water supply through a sink or pipe (52.3%), had access to boiled water (86.1%), a bathroom with a drain (50.5%) and were from Apurimac (26.2%).

The frequency of cases of cystic echinococcosis, T. solium cysticercus infection and fascioliasis was 4.9%, 2.3% and 7.9%, respectively. In addition, the highest number of cases of cystic echinococcosis was found in adults (5.5%), most cases of T. solium cysticercus infection were found in older adults (4.1%), and most cases of fascioliasis were reported in adolescents and older adults (9.7%). The occupational groups most affected by cystic echinococcosis were housewives and farmers (5.7%), housewives had the most cases of T. solium cysticercus infection (4.1%), and farmers had the most cases of fascioliasis (9.7%). Significant positivity for fascioliasis was found predominantly in people with primary and secondary education (8.0%). Likewise, the highest frequency of fascioliasis was found in participants residing in hut dwellings (11.1%), as well as in those who received accessed water by wells (12.3%), and defecated in the open field (13.2%). The highest frequency of cystic echinococcosis was found in Cerro de Pasco (24.5%), of cysticercosis in Ayacucho (4.5%), and of fascioliasis in Puno (40.6%) (Table 1).

In terms of people’s habits and activities, significant positivity for cystic echinococcosis was found in participants who raised pigs (5.4%) and sheep (3.8%); and for fascioliasis, in farmers who raised goats (7.2%), cows (6.2%) and sheep (6.5%). The highest frequency of cysticercosis was found in participants who raised free-range pigs (4.1%), and those who slaughtered their pigs near their homes (2.4%). People with did not deworm their dogs had a higher frequency of cystic echinococcosis (6.0%), while cysticercosis cases were higher in those who sold meat contaminated with T. solium cysticercus (5.7%) (Table 2).

Regarding consumption of foods and beverages, most cases of cysticercosis were found among participants who consumed pork (2.9%); however, this difference was not statistically significant. In addition, participants who consumed emollients and vegetable extracts had a higher frequency of fascioliasis and cystic echinococcosis (p<0.05). Additionally, we evidenced a difference in cases of cystic echinococcosis by consumption of vegetables in juices (p<0.05) (Table 3).

The main symptoms for cystic echinococcosis were weight loss (4.3%), chest pain (4.2%), and abdominal pain (4.4%). For cysticercosis, the main symptoms were headache (1.8%), dizziness (2.0%), and nausea (2.2%), while for fascioliasis they were weight loss (7.6%), abdominal pain (8.0%), fever (7.9%), and jaundice (7.8%). Regarding the assessment of family history, a statistically significant difference was found in the frequency of cases (p<0.05) for the three parasitic zoonoses (Table 4).

DISCUSSION

The National Referral Laboratory for Parasitic Zoonoses of the National Institute of Health decided to conduct laboratory-based surveillance to determine the extent of infection of fascioliasis, cystic echinococcosis, and T. solium cysticercosis in 7811 samples from 13 regions of Peru. Data from this activity have identified a seropositivity of 4.9% for cystic echinococcosis, 7.9% for human fascioliasis, and 2.3% for T. solium cysticercosis.

Cerro de Pasco (24.5%), Ayacucho (8%), Huancavelica (7.1%), Provinces of Lima (6.1%), Junín (5.3%) and Cusco (4.3%) had the highest cystic echinococcosis seropositivity, this maybe be due to the fact that they are considered endemic areas, as evidenced by other studies conducted in the Peruvian Andes ^21-24. In addition, cases of cystic echinococcosis were found in Huánuco (1.9%), Tacna (0.8%), Arequipa (3.7%), Apurímac (3.3%) and Puno (3.1%). It is worth mentioning that we only obtained a small number of samples from the regions of Puno and Moquegua because these regions did not have adequate logistics to obtain a larger number of samples for laboratory-based surveillance of parasitic zoonoses.

The regions of Huánuco (8.6%), Ayacucho (6.2%) and Apurímac (5.9%) had the highest frequency of cases of human fascioliasis; however, we should also highlight the presence of cases in Cerro de Pasco (1.3%), Huancavelica (3.6%) and Tacna (1.5%), which is important because our study is the first report of cases of human fascioliasis in these regions. Therefore, it is of utmost importance to carry out further studies to identify risk areas for the control and prevention of this zoonosis.

The frequency of human fascioliasis was higher in Puno (40.6%), Cajamarca (20.0%), Arequipa (15.4%), Junín (5.5%) and Cusco (6.9%), which have been identified as endemic for this infection, as evidenced by Marcos et al. in their report of human cases between 1995 and 2005 ²⁵, and by other studies that identified these areas as endemic ^16,26,27. In addition to the aforementioned regions, we also found high seropositivity (13.1%) in Lima provinces. This finding is consistent with previous studies; a prevalence of 12.1% has been previously reported in Vichaycocha, Huancapón and Cajamarquilla, in the highlands of Lima ²⁸. Likewise, the presence of this parasite has also been reported from coprological samples obtained in Huarochirí (16.7%) ²⁹ and Oyón (1.12%) ³⁰.

We found a 2.3% seropositivity rate of T. solium cysticercosis, which is lower than the estimated prevalence in Latin America (4.08%) ³. In addition, we identified cases of this infection in regions where it had not been previously reported, such as Huánuco (1.9%) and Huancavelica (0.5%). A seropositivity rate lower than pre-existing reports was evidenced in some regions, such as Cerro de Pasco which previously reported 4.2%, Cusco with 24.0% in Saylla, Junín with 7.0% in Huancayo, Apurímac with 12.0% in Andahuaylas, Tacna with 1.85% and Puno with 1.64% ⁷. On the other hand, there were regions with higher seropositivity rates than previously reported, such as Ayacucho, which had reports of 3.3% in Pampa Cangallo, Lima with previous seropositivity of less than 1%, and Arequipa, which previously had 1.01% ¹⁹. This variation in results may be due to the number of samples obtained and the sampling areas.

The sociodemographic characteristics that had a higher seropositivity for these parasitic zoonoses were age and occupation. We found a higher frequency of IgG type antibodies against cystic echinococcosis and T. solium cysticercosis in adults and older adults, respectively, compared to human fascioliasis, which was found mainly in adolescents and older adults. The increase in cystic echinococcosis and T. solium cysticercosis seropositivity with age found by our study is consistent with that found by previous studies ^31,17. The most affected occupational groups for these zoonoses were housewives and farmers; a higher cystic echinococcosis seropositivity in housewives has been reported by other studies ³². Likewise, the housing material, source of water for human consumption, consumption of unboiled water and defecating outdoors presented a difference in the seropositivity of human fascioliasis, where poverty and deficient sanitary conditions allow the perpetuation of this disease; this has been found by previous studies ^8,26,33.

The habits and activities of the settlers in the studied areas that showed a difference in the seropositivity of these zoonoses were the raising of animals such as pigs and sheep for cystic echinococcosis; goats, cows and sheep for human fascioliasis, and the raising of pigs in free range for T. solium cysticercosis. These animals act as hosts in the biological cycle of zoonotic parasites. In this regard, Ghatee et al.³⁴ found that the population density of sheep, cattle and goats significantly influences the distribution of cystic echinococcosis. In addition, there was a relationship between the higher frequency of T. solium cysticercosis and the slaughter of pigs in the peridomicile. This finding could be explained by the fact that raising pigs in unsanitary conditions and consuming their meat without proper inspection may cause greater exposure to T. solium³⁵. On the other hand, dogs are used for raising cattle, sheep and goats in the countryside. This means that non-dewormed dogs that consume raw viscera from animals slaughtered in the peridomicile are a primary source of cystic echinococcosis infection for humans and animals, which has been demonstrated by our study since we found a difference in the frequency of cases between having non-dewormed dogs and the slaughter of animals in the peridomicile with cystic echinococcosis.

Parasitic zoonoses can be acquired by consuming water and plants contaminated with eggs of E. granulosus, T. solium, or metacercariae of F. hepatica. This fact could explain our results, which show that consuming raw vegetables in juices, extracts and emollients had a difference in the seropositivity of cystic echinococcosis and human fascioliasis. This finding has been reported by previous studies with similar results ^11,35.

We found a statistically significant difference in the frequency of cases between weight loss and chest pain with cystic echinococcosis seropositivity. Himsawi et al. found that weight loss is associated with cystic echinococcosis ²⁰. In addition, another study found an increased frequency of abdominal pain and chronic cough ³⁶, which is similar to our findings. Symptoms such as headache, dizziness and nausea had higher T. solium cysticercus seropositivity as shown in previous studies ^37,38. However, although cysticercosis is associated with epilepsy, we did not identify a difference in case frequency. This finding could be attributed to the fact that we only evaluated data focused on the detection of circulating IgG-type antibodies, which did not allow us to determine neurocysticercosis. A significant difference was found between the frequency of fascioliasis cases and the decrease in weight; which has also been reported by Orfanos et al. ³⁹ in a study carried out in children from three provinces of Cajamarca. On the other hand, abdominal pain and fever were frequent symptoms in cases with seropositivity to fascioliasis, which is consistent with previous research ^40,41.

Likewise, we found that participants with a family history had a higher frequency of the three parasitosis, which has been previously reported by Carmona et al⁴². This finding could be due to the fact that people living together in the same environment and sharing the same food and habits could facilitate the transmission of these zoonoses. Therefore, it is recommended to screen the whole family once a case of these etiologies is confirmed. These findings demonstrate the importance of early detection in order to start effective treatment as well as to avoid complications, thus improving public health.

It is important to point out that the main limitation of our study is the use of secondary data, which was obtained previously as part of surveillance activities that do not have a definition established in any manual or guide related to the collection instrument; however, most of the data are clear and have reduced subjectivity. Also, due to the very nature of the study regarding secondary data, it was not possible to include other variables that could be of epidemiological interest, such as the variable “Occupation”, which was collected in an open form in the instrument, and was categorized by the authors in an ad hoc manner according to affinity and similarity of the responses. Additionally, the data collected through the epidemiological files were used to establish, in an exploratory manner, a difference in the number of cases identified for each of the parasitic infections. Another important limitation is the representativeness of the analyzed data, given the limited number of subjects screened per region, as well as the non-probabilistic selection made. These data collection limitations were caused by logistical difficulties, since the sampling points were located in rural areas far from the city. Due to the low representativeness of the sample and the methodological design of the screening process (aspects that affect the external validity of the data), it was not possible to establish prevalence and/or seroprevalence estimators, but only case frequency estimators. These limitations should be considered during the critical reading of this article. However, despite the limitations of the sample and design of this study, it should be noted that no previous similar study with a such a large sample size has been found. For this reason, our results are very useful to understand the distribution of these infections. It should also be considered that these parasitic zoonoses are underreported in Peru because they are neglected diseases frequently found in rural areas with extreme poverty, and the Peruvian Ministry of Health (MINSA) has not implemented mandatory notification for their surveillance, prevention and control.

In conclusion, we were able to obtain a better overview of the distribution and characteristics of these parasitic zoonoses in 13 regions of Peru, through the serological analysis of 7811 samples obtained through epidemiological surveillance activities. Our findings could be a useful tool for decision-makers in different sectors, such as Health, Agriculture and Environment, to define strategic areas and/or policies with prioritization or differentiated focus for the control and prevention of these zoonoses.