Taenia solium taeniasis/cysticercosis in Guatemala: a prevalent public health problem?

ABSTRACT

In Guatemala, neurocysticercosis (NCC) was first recognized in 1940; since then, cases of NCC have been reported in all Guatemalan departments. However, epidemiological studies on Taenia solium infections are scarce and most information remains unpublished. This study aims to provide evidence of T. solium infections as a public health problem in Guatemala. All information available, either published or unpublished, on T. solium infections in the country was compiled. Official data from the Ministry of Health for the period 2003–2019 were reviewed and analyzed, and all cases of T. solium infections were classified and counted. In total, 5246 cases of taeniasis and 454 cases of human cysticercosis were recorded. On the other hand, 44 studies were identified, mostly from local journals, which included 1951 cases of taeniasis, 2873 cases of human cysticercosis of which 543 were classified with complete diagnosis, and 2590 cases of porcine cysticercosis. Cases were classified by geographic region, patient sex, and Taenia species in taeniasis cases when information was available, and the departments with the highest number of taeniasis and cysticercosis cases were identified. Meanwhile, in Zacapa, a northeastern department of Guatemala with one the highest number of taeniasis cases, a young man diagnosed with a severe form of NCC and two cases of porcine cysticercosis (both confirmed by necropsy) were identified. Taken together, the data herein reported indicate that T. solium infections are a major health problem in Guatemala that needs to be addressed.

1. Introduction

The life cycle of Taenia solium requires two hosts: humans, the only definitive host of the adult tapeworm, and pigs, the intermediate host of the larval stage, known as cysticerci [1]. Humans acquire T. solium infection (taeniasis) by ingesting raw or undercooked pork containing viable cysticerci. Pigs become infected (porcine cysticercosis) by ingesting viable T. solium eggs found in the feces of human tapeworm carriers. In humans, cysticercosis occurs when T. solium eggs are accidentally ingested; after hatching from the egg, the larval stage is lodged in various organs and tissues (brain, eyes, muscles, and subcutaneous tissue) [2]. Neurocysticercosis (NCC), a common cause of epilepsy, occurs when cysticerci are located in the central nervous system (CNS) [2]. Human cysticercosis is a major public health problem and results in economic losses in low-income areas of Latin America, Africa, and Asia, where poor sanitary conditions, poor hygiene, open defecation practices, free-roaming pigs, and poverty prevail [3,4]. According to the World Health Organization, cysticercosis was the leading cause of death out of all foodborne parasitic diseases in 2015, resulting in 2.8 million disability-adjusted life years (DALYs). It is also the leading cause of late-onset epilepsy in developing countries [5].

Guatemala has among the lowest human development indices in Latin America [6], with 59.3% of the population below the national poverty line. As a result, a significant part of the population, especially in rural indigenous communities, lacks basic sanitation and is affected by neglected tropical diseases (NTDs). Half of the total population lives in rural areas, and more than 70% of this population lives in poverty, with no access to health services [7,8]. A literature search yielded only one study on the epidemiology of T. solium infections in Guatemala, conducted 25 years ago [9]. Given the current lack of information, the urgent need for more accurate data has already been expressed [10]. Knowing the extent of T. solium transmission is crucial for local health authorities to implement control measures, and it is also a matter of global concern. In fact, the incidence of NCC is increasing in the United States, especially among immigrants from endemic Central American countries [11,12].

All available reports on S. solium infections in Guatemala, and the treatment provided, are compiled in this work. In addition, official reports from the Ministry of Health were retrieved to update our data on the status of T. solium infections in the country. Finally, by reviewing official data, a possible endemic locality in the department of Zacapa was identified, and a case of human cysticercosis and two cases of porcine cysticercosis are described.

2. Methods

2.1. Systematic review

A literature search was performed following the PRISMA guidelines, from July 2019 to May 2020. Articles published in English and Spanish indexed in PubMed, ScienceDirect, Scopus, SciELO, LILACS, and Google Scholar were considered, using the following keywords: Taenia solium + Guatemala; cysticercosis + Guatemala; swine/porcine cysticercosis + Guatemala; taeniasis + treatment + Guatemala, and cysticercosis + treatment + Guatemala. Research articles on cysticercosis, T. solium and swine cysticercosis; published cross-sectional studies; reports; reviews and retrospective clinical characterizations, all conducted in Guatemala, were retrieved. No limits were set as to the dates of the articles due to the scarcity of journal-published works. A manual search was also conducted in the archives of Revista Médica del Colegio de Médicos y Cirujanos de Guatemala – COLMEDEGUA and Revista de la Asociación Guatemalteca de Parasitología y Medicina Tropical – AGPMT. Databases from universities with medical science careers and Google scholar were included.

2.2. Official data review

Information was retrieved from the Sistema de Información Gerencial de Salud – SIGSA [13], of the Ministry of Health and Social Assistance of Guatemala (MSPAS), to obtain official epidemiological data on taeniasis and cysticercosis. The SIGSA data are classified according to the International Statistical Classification of Diseases and Related Health Problems (ICD-10). The following codes were considered: B680: T. solium taeniasis; B68: T. saginata taeniasis; B689: unspecified taeniasis; B690: CNS cysticercosis; B691: ocular cysticercosis; B698: cysticercosis in other locations; B699: unspecified cysticercosis.

2.3. Clinical cases

2.3.1. Swine

In March 2018, two sows (aged 1 and 2 years) from Azacualpa (15°4ʹ16.3562″ N, 89°25ʹ8.292″ W), a village in Gualán, acapa Department, were identified with cystic lesions on the tongue, compatible with cysticerci. They were confined for examination, but the owners said that they used to roam freely. The sows were necropsied, and muscle tissue and organs were inspected in 0.5 cm sections. Cysticerci were recovered and counted in 1 kg of mixed muscle tissue. All animal inspection procedures were performed by professional veterinarians in accordance with the Animal Welfare and Bioethics Committee, Faculty of Veterinary Medicine and Zootechnics, Universidad de San Carlos de Guatemala (Permit No. EAP.15.2019).

2.3.2. Human case report

In March 2019, a 20-year-old male from the village Guasintepeque (15°7ʹ10.272″ N, 89°21ʹ25.955″ W), Gualán, Zacapa, complained of mild headaches. As the severity of headaches progressed, vomiting and convulsions appeared 23 days later. Upon sudden loss of consciousness, the patient was admitted to the Regional Hospital of Zacapa, Guatemala. The patient was evaluated and treated following standard clinical procedures. Written informed consent was obtained from the patient for the publication of this case report and authorization to publish images.

3. Results

3.1. Search results of human taeniasis/cysticercosis, swine cysticercosis, and treatment provided

In total, 258 search results were obtained: 14 in PubMed, 17 in LILACS, 200 in ScienceDirect, 2 in Rev. COLMEDEGUA, 15 in AGPMT, 7 in university databases and 3 in Google Scholar. Of these, 44 met the inclusion criteria and were selected (Figure 1).

Figure 1.

Search strategy in electronic databases and additional resources.

The occurrence of swine cysticercosis is an indicator of active transmission of T. solium [14]. In 2014, there were an estimated 2.7 million pigs in Guatemala, and the Regional Agricultural Health Agency (OIRSA) estimated that at least 55% of swine production in Central American countries relied on backyard rearing [15,16]. Only six pig slaughterhouses in Guatemala are certified by the Ministry of Agriculture, Livestock and Food (MAGA). Others operate under municipal supervision, and several others are clandestine. There were no reports of swine cysticercosis in any of the certified slaughterhouses in the period 2010–2019, and municipal slaughterhouses do not report official data, as only some of them have veterinary inspection. While the national swine health surveillance and monitoring program (PRONASPORC-MAGA: Programa Nacional de Sanidad Porcina, Ministerio de Agricultura Ganadería y Alimentación) is in place, porcine cysticercosis is not included in this program. Cases of porcine cysticercosis found in published and unpublished literature are summarized in Supplementary material.

Three commercial anthelmintics, albendazole, praziquantel and niclosamide, have been widely used with great efficacy against taeniasis. Niclosamide and albendazole are registered and approved by the IGSS (Guatemalan Social Security Institute) as anthelmintic drugs. Allan et al. [17] used niclosamide in a mass drug administration (MDA) program against T. solium in two rural communities in Guatemala. The prevalence of human taeniasis before MDA was 3.5% (56/1582), but it decreased to 1% (11/1116) 10 months later. All tapeworms collected were identified as T. solium. Parallel to human taeniasis, the high seroprevalence (55%, 148/269) of porcine cysticercosis before MDA decreased to 7% (22/300) 10 months after the intervention. Despite its success in these communities, the effect of these actions was not followed up. In addition, there are no standardized national protocols for the treatment of patients with taeniasis in Guatemala. With respect to NCC, although albendazole is widely used in the country, there are no standard protocols for the care, management, and treatment of NCC patients.

3.2. Official data results

The number of cases of taeniasis and cysticercosis is reported annually, but the criteria used to diagnose both infections are unclear, and they are often misreported. In particular, most cases of taeniasis are reported as ‘unspecified’ (B690); therefore, it is not possible to differentiate between T. solium and T. saginata infections. On the other hand, the anatomical location of cysticerci is not reported in most cases (B699), but they are reported instead as ‘unspecified’ by SIGSA. The official reports of human taeniasis and cysticercosis in the period 2002–2019 are shown in Table 1. The number of cases of taeniasis and human cysticercosis according to official data in the geographic regions of Guatemala is shown in Figure 2. Official data on swine cysticercosis are not available, as case registration is not mandatory.

Table 1.

Official reports of taeniasis and human cysticercosis (2002–2019, SIGSA [13]) in the eight geographical regions of Guatemala.

Taeniasis					Cysticercosis
Region of the country	Taenia sp.	T. solium	T. saginata	Total	NCC	Unspecified	Ocular	Total
Region 1-Metropolitan (Guatemala, Guatemala City)	1499	33	2	1534	16	41	1	58
Region 2-North (Alta Verapaz, Baja Verapaz)	76	2	0	78	13	16	0	29
Region 3-Northeast (Izabal, Zacapa, Chiquimula, El Progreso)	864	11	1	876	21	37	0	58
Region 4-Southeast (Jalapa, Jutiapa, Santa Rosa)	384	1	0	385	17	67	0	84
Region 5-Central (Chimaltenango, Sacatepéquez, Escuintla)	213	3	0	216	4	10	4	18
Region 6-Southwest (San Marcos, Quetzaltenango, Totonicapán, Retalhuleu, Suchitepéquez, Sololá)	1697	4	0	1701	9	65	0	74
Region 7-Northeast (Huehuetenango, Quiché)	313	3	3	319	18	57	3	78
Region 8-Petén	131	4	2	137	29	25	1	55
Total	5177	61	8	5246	127	318	9	454

Figure 2.

Regions in Guatemala with cysticercosis (asterisks) and taeniasis cases during 2002–2019, SIGSA (2020). A blue triangle indicates the location of Gualán (municipio/municipal district), where the cases of swine cysticercosis and the case of NCC herein reported were found. The square shows the location of the dry corridor.

Taeniasis and human cysticercosis cases found in published and unpublished literature are summarized in the Supplementary material. In the period 2002–2019, 5246 cases of taeniasis and 454 cases of cysticercosis were reported in the official statistics of Guatemala. In the period 2015–2019, 99.95% (3648) of taeniasis cases were reported without specifying the causative agent, and only 0.05% (20) were reported as caused by T. solium. Most cases occurred in female patients (2274; 67%). Regarding geographic distribution, the highest number of taeniasis cases was reported in Sololá (1376; 41%), followed by Guatemala (455; 13%), Chiquimula (398; 12%), Zacapa (258; 8%), and Huehuetenango (174; 5%). As for cysticercosis, the location of the parasite was not specified in 167 cases (67%); 77 cases (31%) were NCC; and 4 (2%) were ocular cysticercosis. Most cysticercosis cases were reported in female patients (166, 67%). The departments with the highest number of cysticercosis cases were Petén (39, 16%), Guatemala (40, 17%), Santa Rosa (43, 17%), Huehuetenango (20, 8%), and Baja Verapaz (18, 7%) [13]. In the period 2015–2019, of the 214 reported cases of human cysticercosis, 143 (67%) were females and 71 (33%) were males. The dynamics of taeniasis and cysticercosis cases in the period 2002–2019 is shown in Figure 3. The higher number of cases observed in 2019 could be due to improvements in data recording by SIGSA.

Figure 3.

Reported cases of taeniasis and cysticercosis during 2002–2019 in Guatemala, SIGSA (2020).

3.3. Case reports of human and swine cysticercosis in Zacapa

3.3.1. Swine cysticercosis

Each sow was estimated to be infected with more than 25,000 T. solium cysticerci (Figure 4). Numerous viable cysticerci were found in the striated muscles, brain, and even in the muscle layer of the intestines. The characteristics of the village (lack of drainage, poor sanitary facilities, lack of drinking water, and free-roaming pigs) favor the continuity of T. solium life cycle (Figure 5).

Figure 4.

Necropsy of a sow with cysticercosis from Zacapa. T. solium cysticerci were found in striated muscle (a), brain (b), and heart muscle tissue (c).

Figure 5.

Conditions favoring the persistence of the life cycle of T. solium in the village of Azacualpa, Gualán, Zacapa: Many households lack latrines, and open defecation allows consumption of human feces by free-roaming pigs; a cylindrical concrete latrine (center) with no walls or roof (a). Free-roaming pigs forage for organic material and drink water directly from household drains (b).

3.3.2. Human case of intraventricular and parenchymal NCC

The patient’s vital signs were normal. He was drowsy and had isochoric, nonphotoreactive pupils. Brain computed tomography (CT) showed inflammation throughout the ventricular system, with communicating hydrocephalus (Figure 6(a)). In addition, throughout the brain parenchyma there were hypodense, round lesions, without edema, most of them with a hyperintense nodule; calcified granulomas were also observed (Figure 6(a,b)). A ventriculoperitoneal shunt (VPS) was placed and the patient’s symptoms improved immediately. Cerebrospinal fluid (CSF) examination showed a moderate elevation in protein level (68 mg/dL), and Gram stain was negative after 72 h of incubation. Specific antibodies and antigen (HP10) were detected by ELISA in serum and CSF samples [18,19]. Fecal examination was performed, but no T. solium eggs or proglottids were found in the feces. Albendazole (400 mg/8 h for 3 weeks), corticosteroids (prednisolone 5 mg/8 h for 5 days) and anticonvulsants (phenytoin 100 mg/8 h) were administered. One month after treatment, migraine, nausea, vomiting, and seizures recurred. The patient was hospitalized again, and noncontrast MRI images revealed persistent inflammation of the fourth ventricle. Sagittal T1 sagittal MRI images suggested the presence of an intraventricular cysticercus (Figure 6(c)), and the same chemotherapy (albendazole + corticosteroids + anticonvulsant) was administered. During follow-up (September 2019), a brain MRI revealed degeneration of the intraventricular cyst and normalization of the size of the fourth ventricle (Figure 6(d)). Since then, the patient’s condition gradually improved and the symptoms of NCC disappeared. Although the reported clinical case had a favorable outcome, his family had suffered severe psychological (depression in his mother) and economic difficulties in paying for treatment and hospitalization expenses.

Figure 6.

CT scans show global hydrocephalus, as well as calcified (a) and vesicular (b) cysticerci. Sagittal T1 MRI image shows persistent swelling of the fourth ventricle after VPS placement due to the presence of a cysticercus (red arrow) (c). Sagittal T1 MRI image three months after the second albendazole treatment shows a reduction in volume of the fourth ventricle after degeneration of the cyst (red arrow) (d).

The family reported that they have never raised pigs and occasionally eat pork; however, pig raising is a common practice in the village of Guasintepeque. The household (17°7ʹ10.272″ N, 89°25ʹ9.55″ W) has a latrine in good condition. All family members and neighbors were asymptomatic, and only one neighbor had specific Ig-G (ab-ELISA) to T. solium. No fecal examinations were performed on family members or neighbors.

4. Discussion

The data reported here confirm that T. solium infections are a prevalent and widely distributed health problem in Guatemala. While most of the reports included were found in the gray literature, they are nevertheless our main source of information. This is one of the reasons why T. solium infections are often ignored, and our study aimed to fill this gap in our knowledge of T. solium in Guatemala. Developing countries where T. solium infection is endemic face several serious problems and have very limited resources, personnel, and infrastructure for research. This impacts on epidemiological surveillance efforts.

Of particular interest is the region known as the ‘dry corridor’, a drought-stricken area with the highest levels of food insecurity in the country, very limited health infrastructure, and extreme poverty. Due to irregular rainfall, the dry corridor has become one of the most susceptible regions in the world to the effects of climate change [20,21]. On the other hand, T. solium infection is endemic in this area, according to García Noval et al. [9] and SIGSA reports from the last five years. Pork is reportedly by locals to be the main source of protein in Zacapa, a department located in the dry corridor. Coincidentally, a high number of cases of taeniasis have been reported in Zacapa (SIGSA).

In turn, the few studies conducted to date on porcine cysticercosis in Guatemala (Supplementary material) have detected the infection in rural areas of the country. This is to be expected, as pigs typically roam freely in rural areas and have access to human feces. Unfortunately, official veterinary inspection is only performed in MAGA-registered slaughterhouses and a few municipal slaughterhouses. Therefore, in rural areas where free-range/backyard pig farming predominates, pork is consumed without prior veterinary inspection. In the two cases of swine cysticercosis reported here, one 1-year-old and one 2-year-old sow had severe infections, indicating that one or more T. solium carriers live in the community. No tapeworm carriers could be identified, but it is of utmost importance to implement a specific epidemiological program that includes a campaign to diagnose T. solium carriers in this area.

The patient diagnosed with NCC was a young individual presenting a severe case that required urgent placement of a VPS. While the parenchymal location is generally susceptible to cysticidal therapy, cysticerci located in the ventricles are more resistant to treatment, as our case illustrates. In total, one neurosurgery, two cysticidal treatment cycles, and two hospitalizations were required to treat the patient. This entails a high economic cost, often unaffordable for the rural population of Guatemala, which highlights the socioeconomic problem posed by the disease.

We are aware of the limitations in our data. For instance, the diagnosis criteria and tests used are often unclear. This is evident in official statistics, where taeniasis cases are reported as Taenia sp. and most cysticercosis cases are labeled as ‘unspecified’, although most cases probably correspond to NCC, as it is the case in other endemic countries [3]. A single molecular study confirmed the African/Latin American genotype of T. solium in Guatemala [22]; however, no molecular methods have been used to date in epidemiological studies to differentiate Taenia species.

Considering the information reported here, several actions could be implemented to improve the situation. First, a national epidemiological survey should be conducted to assess the real burden of T. solium infections and identify endemic areas. If such a study confirmed the extent of the problem, T. solium should be considered as a top priority health problem and included in the MSPAS epidemiological surveillance protocols for zoonoses and NTDs [23,24]. This would require the development and application of diagnostic protocols for taeniasis (formalin ether concentration, Kato-Katz, ELISA of coproantigens, observation of proglottids) [25–27].

Immunodiagnostic tests for NCC are scarce in Guatemala, and only one private laboratory located in Guatemala City performs immunodiagnosis of cysticercosis. The cost of an ab-ELISA is 150 quetzales (about USD 20) (Laboratorio Clínico Biomédico, 20 June 2021). Therefore, immunological surveys have only been used in some epidemiological studies for research purposes [9,28]. In addition to immunodiagnosis, increased coverage and availability of neuroimaging studies (CT and MRI) are required to diagnose NCC. Currently, these studies are only available in private medical centers, with costs ranging from 400 to 2,600 quetzales (about 50–350 USD). Therefore, a vast majority of NCC sufferers living in impoverished rural areas (in extreme poverty, with less than 1.90 USD per day) will never receive a proper diagnosis.

Furthermore, as Guatemala is a multiethnic country, an inclusive approach is required, in which all protocols and measures related to the prevention and control of T. solium are translated into the 22 Mayan and non-Mayan (Xinca and Garifuna) languages currently spoken in the country. If the severity of the problem is confirmed, various approaches and measures should be taken. Different studies have shown that MDA is effective in reducing taeniasis infections in rural communities [17,29,30]; therefore, once endemic foci have been identified through national epidemiological surveys, this strategy should be implemented as a priority. Vaccination of pigs, either alone [31] or accompanied by anthelmintic treatment (oxfendazole) [32], has proven to be a valuable tool to prevent porcine cysticercosis, indirectly reducing the occurrence of T. solium infections in humans. Thus, the feasibility of vaccinating and treating pigs as part of a control program could be evaluated for implementation in resource-poor communities. Other recommendations for T. solium control should include official veterinary meat inspection at the local level, education on pig husbandry and the importance of a thorough cooking of pork, limiting free-roaming pigs, improving the use of latrines, and implementing hygiene and sanitation education programs [33].

Due to the lack of structured information on the epidemiological status of T. solium in Guatemala, none of the above strategies have been implemented to date. It is crucial to improve our epidemiological knowledge and delineate future actions and control measures, as a plan by PAHO to eliminate NTDs, including T. solium, in Latin America is currently underway [34].

5. Conclusions

A literature search and a review of official data in Guatemala suggest that Taenia solium infections are frequent and pose a serious health problem. In fact, T. solium infections have been reported in all departments of the Republic. However, due to the lack of epidemiological surveillance, the actual status and burden of T. solium infections remain unknown, and cysticercosis is not recognized as a priority preventable disease and is not included in national health programs. On the other hand, taeniasis and cysticercosis are frequently reported as ‘unspecified’ due to a failure to diagnose them properly; the species of Taenia and the specific location of parasites in cysticercosis cases are often not reported, making it impossible to have real casuistry data. This should be improved, and efforts should be made to conduct epidemiological studies to detect foci of T. solium. As a starting point, reliable data recording methods for T. solium infections should be established as part of a nationwide surveillance system by public health authorities, considering the cultural and socio-demographic characteristics of vulnerable populations living in rural communities.

Funding Statement

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Supplementary material

Supplemental data for this article can be accessed online at https://doi.org/10.1080/20477724.2022.2083757