Prevalence of Strongyloidiasis in Peru: Systematic Review

Strongyloidiasis is a disease of great public health signicance. We aimed to assess the prevalence of Strongyloides stercoralis infection in Peru. Methods. This systematic review was based on a literature search in PubMed, SciELO and Google Scholar using the key words or root words “strongyl*” AND “Peru” on 15 July 2020. Eligible studies were published from 1 January 1981 to 15 July 2020 and written in English, Spanish, Italian, or French. Results. We included 21 papers in the analysis. Studies were heterogeneous regarding the study population, diagnostic methods, and the prevalence of S. stercoralis, which ranged from 0.3–45%. Half were designed to detect parasites in general. In studies designed to detect S. stercoralis, the most widely used diagnostic method was the Baermann technique. Conclusion.


Introduction
Strongyloidiasis is an infection caused by the human parasitic roundworm Strongyloides stercoralis (1). This soil-transmitted helminthiasis is believed to affect around 370 million people worldwide (2,3).
However, this gure could actually be much higher; a 2017 study estimated global prevalence at 8.1%, or 613.9 million people (4). The helminth is endemic to tropical and subtropical regions, but it can occur in any area with an increased risk of fecal contamination due to poor sanitation, inadequate water supply, or other factors (1,2). Infection rates and risk vary among different population groups. For example, prevalence is higher in older people due to autoinfection (5,6).
In Peru, the Ministry of Health reviewed the cross-sectional prevalence studies of S. stercoralis infection from different areas of the country between 1981 and 2001 (7). Mean prevalence was 6.6%, with variations by location and diagnostic methods. Despite the high prevalence of the infection, there is limited knowledge of its epidemiology and sero-epidemiology (8).
This systematic literature review aimed to assess the prevalence of S. stercoralis infection in Peru.

Methods
We performed an electronic search in PubMed and SciELO on 15 July 2020, using the following key words or root words, grouped into two main concepts: "strongyl*" AND "Peru". Results were restricted to studies published from 1 January 1981 to 15 July 2020; performed in humans; and written in English, Spanish, Italian, or French. We sought to identify additional records through backward reference searching and electronic searches for grey literature (Google and Google Scholar).
We assessed surveys, notes, analyses, and epidemiological reports on the prevalence of intestinal protozoa and helminths in general or strongyloidiasis in particular. The rst two authors (S. O.-M. and J.-M.R.-R.) screened the titles and abstracts for relevance, and the full texts of all eligible or potentially eligible articles were retrieved. Data on the prevalence of S. stercoralis were collected regardless of the population characteristics (children, adults, immunocompromised patients, etc.), but this information was collected, along with study design, diagnostic procedure, and type of fecal examination technique (e.g. modi ed Baermann technique).

Results
The electronic search in PubMed and SciELO yielded 147 records, and 21 papers were identi ed through additional searches. After screening the titles and abstracts, we examined the full text of 42 potentially relevant papers, excluding 21 that reported the prevalence of other helminthic infections or did not report prevalence data. The remaining 21 studies were included. Figure 1 shows the ow chart for study selection.
All studies used a cross-sectional, descriptive, observational design, except one systematic review, performed by the Peruvian Ministry of Health, that collected 294 parasite prevalence studies between 1981 and 2001 (7).
Regarding sample collection, most studies collected a single stool sample; four studies used more than one (9,13,18,20). Investigators in four studies also collected blood samples, in two cases for performing S. stercoralis serology (8,11), in two for assessing anemia (11,24), and in one for evaluating eosinophilia (17). Table 1 presents a summary of the characteristics of included studies . Estimated prevalence of strongyloidiasis ranged from 0.3-45% (22,23), depending on the geographic study area, the techniques used for stool examination, and participant characteristics (e.g. those with diarrhea versus asymptomatic individuals); overall rates were stable over the study period. The highest prevalence (45%) was reported in 20 patients attended in the military hospital in Iquitos (10).
The study with the second highest prevalence (38.5%) used ve different procedures (more than any other prevalence studies in rural communities) to detect S. stercoralis in the Pasco region of the Peruvian Amazon (22). Other studies showed high prevalence in the Cusco region (24.5%) and in participants with diarrhea in Puerto Maldonado (19.5%) (20,26). Morales et al. reported a higher prevalence of Strongyloides infection at low altitudes (26.4%) compared to mountainous regions (18.6%) (26). Low prevalence, of 0.3-1.5% of the sample population, was also observed in Chacas and in children living in Jauja (Junin department) (13-15, 17, 21, 23).
Most studies discussed coinfection with various helminths. In a study in Puerto Maldonado (Peruvian Amazon), nearly half the participants (47.1%) infected with S. stercoralis were coinfected with Ancylostoma duodenale (20). In Tarapoto (12), 42% of total participants had parasitic coinfections; the most common pair was Ascaris lumbricoides and Trichuris trichura. In four provinces of the department of Lima (25), biparasitosis was 32.7%; authors did not report the most common association. The study reporting the fewest mixed parasitic infections (8.3%) involved 217 HIV patients at the Cayetano Heredia National Hospital in Lima (9).
Estimating the prevalence of S. stercoralis in Peru is complicated by the diversity of diagnostic methods used. Not all methods have the same ability to detect it. It would be necessary to systematize the studies using the gold standard to have a more precise idea of the true prevalence.
A study designed for diagnosing S. stercoralis infection in a rural community in Iquitos (8) showed that 8.7% of the stool samples were positive using one of three diagnostic methods, although the sensitivity differed between them: direct examination (sensitivity 37.7%), Baermann method (40.5%), or simple sedimentation (79.7%). Agar culture showed a sensitivity of just 60.9% due to an exuberant growth of fungi in 35% of the samples, which prevented interpretation. The ELISA was positive in 72% of the blood samples, and the negative predictive value of the serology was 98%. In another study from the same region (11) Techniques such as Baermann's or agar plate culture are cumbersome and time-consuming. Multiple samples must be collected on different days to improve the detection rate because of the irregular excretion pattern of S. stercoralis larvae, especially for low-intensity infections. Another drawback is the need for fresh and non-refrigerated stool samples. Serology is useful, but this method could overestimate the prevalence of the disease due to cross-reactivity with other nematode infections; moreover, distinguishing recent infections from past (and cured) ones is not straightforward (28).
Our review is limited by the relatively small number of included studies, the lack of standard de nitions, the use of different diagnostic techniques, and the study of multiparasitosis.

Conclusion
Prevalence of S. stercoralis in Peru ranged from 0.3-45%, with variations by geographic study area, stool examination techniques, and participant characteristics. A more precise estimate of the current prevalence of strongyloidiasis would require a standard diagnostic protocol along with adequate sampling and statistical analysis. This would be the starting point for the development of soil-transmitted helminthiasis control programs.