An unusual presentation of strongyloidiasis in a patient on chronic dialysis causing clinical deterioration

Abstract

Background

Strongyloidiasis is a parasitic infection caused by the helminth Strongyloides stercoralis. Strongyloidiasis is endemic in tropical regions, including Mali. Diffuse forms of the disease occur in seriously immunocompromised patients and those undergoing immunosuppressant therapies, such as corticosteroids. We report an unusual case of disseminated strongyloidiasis in a patient undergoing chronic hemodialysis in Mali.

Case presentation

A 62-year-old woman from Mali with a past medical history of diabetic nephropathy was followed in our clinic. She has been undergoing chronic hemodialysis for two years due to diabetic nephropathy. She denied taking corticosteroids or immunosuppressant medications. Over three months, she presented with symptoms of non-specific abdominal pain, with alternating of diarrhea and constipation, and a dry cough with fever. At admission, physical examination found an altered general condition, blood pressure of 140/90 mmHg, heart rate of 97 beats per minute, and temperature of 38.7 °C. Ancillary tests, including urine culture, identified Strongyloides stercoralis. This was confirmed by parasitological examination of stool samples taken on three successive occasions. The patient was treated with oral 200 µg/kg ivermectin combined with 400 mg albendazole. His clinical presentation got improved significantly. One month later, the repeated parasitological and urinary tests were negative.

Conclusion

Severe strongyloidiasis is commonly seen in immunocompromised patients and usually have poor prognosis. This case highlights the need for thorough investigation of such infections in chronic immunodeficient individuals, often associated with end-stage renal failure. Therefore, we suggest parasitological monitoring or its prophylactic treatment at regular intervals for patients at high risk of developing disseminated and severe strongyloidiasis.

Background

Strongyloidiasis is a parasitic disease caused by the helminth Strongyloides stercoralis (S. Stercoralis). It is transmitted to humans through skin contact with contaminated soil, which can spread throughout different tissues [1]. The clinical manifestations are polymorphic and usually non-specific. These include gastrointestinal symptoms, urticaria, dry cough, and low-grade fever, among others. However, there is an exception for the very form of rare larva migrans (serpiginous rash), which is pathognomonic. Chronic and inconsistent blood hypereosinophilia, may be suggestive of the disease [2].

Disseminated strongyloidiasis presents in a severe form in immunocompromised patients or those undergoing prolonged corticosteroid therapy [3, 4]. Severe or disseminated strongyloidiasis is very rarely reported in hemodialysis patients in the literature [5]. Here we report an atypical presentation of disseminated strongyloidiasis in a patient undergoing chronic hemodialysis in Mali.

Case presentation

A 62-year-old woman from Mali, diagnosed with diabetic nephropathy, was undergoing chronic hemodialysis for two years via a left radial arteriovenous fistula. She did not report a history of corticosteroid medications or immunosuppressant drugs use.

She presented with symptoms including non-specific abdominal pain associated with alternating of diarrhea and constipation, and a dry cough with fever, for more than three months. At admission, physical examination found good general condition, blood pressure of 140/90 mmHg, heart rate of 97 beats per minute, and temperature of 38.7 °C. She weighed 61 kg and was 1.63 m in height, with a body mass index of 18.7 kg/m2. Lung auscultation found fine crackles and chest X-ray showed lesions consistent with right interstitial pneumonia (pulmonary infiltrates). The fundus examination was normal. The abdominal ultrasound was unremarkable. Blood count revealed leukocytosis at 14,000/mm3, predominated by neutrophils, normochromic normocytic anemia at 10.1 g/dl. In addition, C-reactive protein was 70 mg/l, procalcitonin at 1.2 ng/ml, and fasting blood glucose at 3 g/l. Cytobacteriological analysis of urine revealed a urinary tract infection with multi-resistant Escherichia coli. She was treated with meropenem 1 g/day for 14 days, with optimization of her diabetes treatment with insulin. The fever quickly resolved, and the urinary infection was cleared on follow-up urine analysis. She was discharged on day 15.

On day 20, she was readmitted to the hospital for fever at 38.5 °C, anorexia, and glycemic imbalance. A urine culture incidentally revealed the presence of Strongyloides stercoralis (L3 filariform larva of S. stercoralis) in a fresh state with a sterile bacteriological culture, which was confirmed by a second test three days later (Fig. 1A). Parasitological examination of stool samples taken three times consecutively detected the presence of filariform larva of S. stercolalis, one of which was alive in the second sample (Fig. 1B).

Fig. 1.

Parasitological examination of urine and stool samples. A: Presence of S. stercoralis larva on direct examination of fresh urine. B: Presence of S. stercoralis larva on direct examination of fresh stool after saline and iodine preparation.

The blood count showed normochromic normocytic anemia at 8 g/dl, leukocytosis 13,200/mm3 with a predominance of neutrophils (8,000/mm3) and eosinophils (589/mm3), a C-reactive protein level of 30 mg/l, and hypoalbuminemia at 33 g/l. Additionally, Human Immunodeficiency Virus (HIV) serology and two series of hemoculture were negative. All the details of biological and parasitological analyses are reported in Table 1.

Table 1.

Biological and bacteriological data

Biological data (Reference values)	First admission	Day 20	Day 30	Day 40
Haemoglobin (12-16 g/dl)	10.10	8.50	9.32	10.91
Leukocytes (4000-10000/mm3)	14000	12000	9000.41	6000.7
Platelets (150000-400000/mm3)	401000	378000	279	398
Neutrophils (2000-7500/mm3)	9000	8000	5649	4980
Eosinophils (40-4000/mm3)	389	589	394	276
CRP (< 6 mg/l)	70	30	21.3	8
Procalcitonin (< 0.1 ng/ml)	3.2 ng/ml	0.02	-	-
Blood sugar level (0.7-1.1 g/dl)	3	2.5	1.29	1.11
Glycosuria	Negative	-	-	-
Ketoneuria	Negative	-	-	-
Natraemia (135-145 mmol/l)	138.70	136.60	141.50	140
Potassium level (3.5-4.5 mmol/l)	5.03	5.80	3.34	4.41
Calcaemia (2.2-2.9 mmol/L)	2	2.03	2.1	2.09
Albumin (38-54 g/l)	-	33	35	36.80
Infectious disease assessment (Hbs antigen, HIV, HVC)	-	Normal	-	-
Bacteriological Data
Cytobacteriological studies of urine	E. coli urinary tract infection	S. strongyloides larva,Sterile culture	Sterile	Sterile
Stool culture	-	S. strongyloides larva,Sterile culture	Sterile	Sterile
Hemoculture	Negative	Negative	-	-

The patient was treated with oral ivermectin 200 µg/kg for 7 days combined with albendazole 400 mg for 3 days, repeated two weeks later. The clinical course was favorable, marked by apyrexia and a significant improvement in the digestive symptoms. Blood sugar levels were controlled with insulin therapy, and anemia was corrected by blood transfusion followed by erythropoietin injections on dialysis days. One month later, parasitological and urinary tests were negative.

Discussion and conclusion

Epidemiology of strongyloidiasis

Strongyloidiasis is a widespread parasitic infection that is very common in Africa, Central and South America, and Southeast Asia, where the tropical climate is conducive to the parasite’s development [6]. Our patient resided in the Kayes region of Mali, which has a semi-arid tropical climate characterized by high temperatures year-round. The overall prevalence of strongyloidiasis in the general population is estimated at around 8.1%, representing 614 million infected individuals, according to Buonfrate’s meta-analysis [1]. Among chronic hemodialysis patients in the Bolivian region of South America, the copro-parasitological prevalence of non-severe strongyloidiasis was 1.9% with a mean age of 51 years [7]. Severe or disseminated strongyloidiasis is very rarely reported in hemodialysis patients in the literature. In our African context, precise figures regarding the prevalence of strongyloidiasis are lacking, especially among dialysis patients. A case of severe strongyloidiasis in a 59-year-old chronic hemodialysis patient had been described in Morocco [5]. Our patient was 62 years old, and to our knowledge, this is the first case reported in West Africa in a patient on chronic hemodialysis.

Life cycle and risk factors associated with strongyloidiasis infection

The specific mechanisms by which the immune system is triggered in response to S. stercoralis infection have not been fully understood in humans [8]. The life cycle of S. stercoralis is more complex than that of most nematodes, with its alternating free-living stages and potential for self-infection. Rhabditiform larvae are excreted in feces and develop into free-living adults or infectious filariform larvae that penetrate human skin. In cases of autoinfection, some rhabditiform larvae transform into filariform larvae directly in the intestine, allowing the parasite to reinfect the host without passing through the external environment [9].

Adverse socioeconomic conditions and certain occupations (agriculture and mining) are generally believed to increase the risk of strongyloidiasis. As for disseminated and severe strongyloidiasis, several associated factors have been reported, including long-term corticosteroid therapy, immunosuppression following solid organ or allogeneic stem cell transplantation, HIV infection, human T-lymphotropic virus type 1 (HTLV-1) infection, diabetes, or chronic alcohol consumption [10, 11].

In this case, the patient was HIV-negative but had type 2 diabetes and did not have a high-risk occupation. There was no history of corticosteroid therapy or immunosuppressant drug use. In the case presented in Morocco by Hachim et al., the patient had received a high dose of corticosteroids and cyclophosphamide for her causal glomerulopathy [5]. In Buonfrate’s series, nine patients received corticosteroid treatment during the three months prior to recruitment, and diabetes was diagnosed in 48 patients [12].

There is no evidence in the literature that dialysis or end-stage renal failure are specific risk factors for S. stercoralis infection. However, dialysis patients have a significantly weakened immune system due to the consequences of chronic uremia, impaired phagocytic function of polymorphonuclear cells, and hyperreactivity of monocytes and dendritic cells, which lead to a reduced ability to eliminate infectious agents [7, 10].

Diagnosis

The disseminated and hyperinfestation syndrome of S. stercoralis can be accompanied by a wide range of symptoms without any pathognomonic features. The most common are respiratory symptoms (88.6%), fever (80.8%), and gastrointestinal symptoms (70.2%), which occur against a background of near-constant physical weakness [13]. In this case, the patient presented with fever and diffuse abdominal pain associated with a deterioration in general health. Our patient’s pulmonary symptoms and extensive bilateral infiltrates likely resulted from larval migration via the pulmonary route during the hyperinfestation syndrome. Hachim had reported in their case gastrointestinal symptoms such as profuse watery diarrhea, abdominal pain, vomiting, and gastrointestinal bleeding, without evidence of hypereosinophilia. The presence of hypereosinophilia is a strong indicator of helminthiasis. However, as it occurs in a cyclical, sawtooth pattern, it is not constant during strongyloidiasis [14]. In our patient, hypereosinophilia was present in only a single blood count sample.

While strongyloidiasis was not suspected initially, urine culture incidentally identified the parasite in the patient we report here. To confirm this finding was performed a second analysis by collecting new sample which confirmed the disease, which ruled out the possibility of sample contamination.

In cases of heavy infestation, the larvae can cross the intestinal barrier, carrying bacteria from the gut flora (enterobacteria, etc.) on their cuticle. These bacteria are transported into the bloodstream and organs, causing bacterial superinfections, particularly pyelonephritis or septicemia [15]. This hypothesis could explain the E. coli urinary tract infection observed in our patient at the initial presentation. Given the persistence of altered general condition associated with fever, the urine culture confirmed the S. stercoralis infection, reinforcing the possibility of a disseminated infection.

In clinical practice, distinguishing between a hyperinfestation syndrome and dissemination can be difficult in the absence of an autopsy. Analysis of two cases of urinary strongyloidiasis previously reported in the literature allowed us to conclude that this is a case of disseminated strongyloidiasis:

The first case, reported in 2018 [16], described strongyloidiasis with rhabdoid larvae excreted exclusively in the urine (negative stool culture) in a 72-year-old patient with chronic kidney disease (stage 2) and hydronephrosis caused by kidney stones. Urinary symptoms were predominant, with no fever or altered general condition. In a second case published in 2024 by Yamamoto, an 80-year-old patient presented with unexplained altered general condition in the context of febrile pneumonia. S. stercoralis larvae were identified in the urinary sediment, stool, and sputum [17]. The sequence of events described in our case report corresponded to that presented by Yamamoto, with the exception that bronchial aspirate analysis was not performed due to a lack of laboratory facilities in our setting.

Treatment and outcome

The treatment of S. stercoralis infection aims to be curative and preventive of self-infection and its potentially fatal complications. Unlike for other helminthiasis, whose treatment is included in public health programs, aim to reduce the parasite load to alter its transmission. The management of disseminated and severe strongyloidiasis is based on three therapeutic options, including ivermectin, thiabendazole and albendazole. In our case, treatment consisted of oral ivermectin 200 µg/kg for 7 days combined with albendazole 400 mg for 3 days. A significant clinical improvement was observed from day 3 of treatment. We repeated the treatment one month later to ensure that the parasite had been eliminated. The persistence of symptoms following treatment for a bacterial urinary tract infection, followed by rapid resolution after antiparasitic treatment, suggests that parasitic infection plays a significant role in the clinical course.

The efficacy of oral ivermectin at 200 µg/kg has been proven to eradicate larvae in stool for two weeks, although no randomized controlled trials are available to determine the exact duration of treatment. It has a dual effect against both adults and larvae, unlike albendazole, which targets only adults. As ivermectin is not eliminated via the kidneys, no dosage adjustment is necessary in cases of renal failure [18].

A study by Abad et al. reported that treatment with ivermectin is recommended as a first-line treatment and appears to be more effective when combined with another molecule, usually albendazole. Thiabendazole and albendazole should not be used alone in cases of severe strongyloidiasis due to their low efficacy [19].

Notably, some immunocompromised patients may have better prognosis in severe strongyloidiasis. However, severe pulmonary involvement is associated with higher risk of mortality [20]. In our case, the prognosis was favorable despite the presence of pneumonia.

Strongyloidiasis can be severe and life threatening in immunocompromised patients. Following this case presentation and given the chronic immunodeficiency associated with end-stage renal failure, antiparasitic treatment can be recommended every two weeks. In resource-limited settings, prioritizing parasitological monitoring among patients at high risk of severe strongyloidiasis, or alternatively providing regular prophylactic therapy, may be essential.

Ethical considerations

The patient's written consent was obtained for the writing and publication of this case. Anonymity was guaranteed.

Abbreviations

CRP

C-reactive protein

HIV

Human immunodeficiency virus

HTLV-1

Human T-lymphotropic virus

S. stercoralis

Strongyloides stercoralis

Author contributions

ASF: Data collection, analysis and interpretation, drafting first manuscript and incorporating subsequent revisions. MS, SS and HM: Editing for intellectual content of the manuscript. MS, AD: Data analysis and interpretation. AY: Language editing and proofreading of the manuscript. SOYD, YK, HY and SF: Editing for intellectual content of the manuscript.

Funding

This work received no financial support from any institution or individual.

Data availability

The authors confirm that the data supporting the findings of this study are available with the corresponding author (Dr FOFANA Aboubacar Sidiki, fofaboubacarsidiki@gmail.com) on reasonable request.

Declarations

Ethics approval and consent to participate

Not applicable.

Patient consent

We obtained informed consent from the patient to publish this case.

Consent for publication

We obtained written informed consent from the patient for publication of this case report including associated images.

Competing interests

The authors declare no competing interests.