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\begin{document}

\title{Septic shock, acute renal and liver failure following unsafe abortion
using bitter leaves and wandering jew in northern Uganda: a case series}



\author[1]{Gasthony Alobo}%
\author[2]{Cristina Reverzani}%
\author[2]{Violah Nahurira}%
\author[3]{Laura  Sarno}%
\author[4]{Alexandre Maia}%
\affil[1]{Lira University}%
\affil[2]{St. Mary’s Hospital Lacor}%
\affil[3]{University of Naples Federico II}%
\affil[4]{Affiliation not available}%


\vspace{-1em}



  
  \date{May 25, 2024}


\begingroup
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\selectlanguage{english}
\begin{abstract}
This case series describes the unusual severe toxicity of two herbal
medicines that are frequently used to induce abortion in Northern
Uganda. It highlights possible associations of Commelina Africana
(wandering jew) with uterine necrosis complicated by and sepsis, and of
Vernonia amygdalina (bitter leaf) with acute liver and renal failure%
\end{abstract}%



\sloppy


\textbf{Septic shock, acute renal and liver failure following unsafe
abortion using bitter leaves and wandering jew in northern Uganda: a
case series.}

Gasthony Alobo\textsuperscript{1,3}, Cristina
Reverzani\textsuperscript{3}, Violah Nahurira\textsuperscript{3}, Laura
Sarno\textsuperscript{2*}Correspondence: gasthonya@gmail.com

\textsuperscript{1} Department of Obstetrics and Gynaecology, Lira
University, Lira, Uganda

\textsuperscript{2}Department of Neurosciences, Reproductive Science and
Dentistry, University of Naples Federico II, Via Pansini 5, 80131,
Naples, Italy.

\textsuperscript{3}Department of Obstetrics and Gynaecology, St. Mary's
Hospital Lacor, P.O. Box 180 Gulu, Uganda.

Corresponding author: Dr. Alobo Gasthony, e-mail: gasthonya@gmail.com



\textbf{Abstract}

\textbf{Background:} Unsafe abortion is a major problem in Uganda, being
one of the leading causes of maternal morbidity and mortality. An
estimated 297,000 unsafe abortions are performed yearly, with an
abortion rate of 54 per 1,000 women aged 15-49; nearly 85,000 women have
been treated annually for complications of unsafe abortion, leading to
about 1,200 deaths. Abortions are performed mostly under unsafe
conditions, by people without medical training. In rural areas in
northern Uganda, women often resort to traditional providers, who use
local herbs as abortion remedies. Little is known about the biological
properties of these herbs and their toxicity profile.

\textbf{Case presentation} : Here we present the case series of two
women, of 31 and 24 years of age, who underwent unsafe abortion for
unintended pregnancy by using herbal medicines, i.e. \emph{Commelina
Africana} (wandering jew) and \emph{Vernonia amygdalina} (bitter leaf)
respectively. While the first case resulted in uterine necrosis and
pelvic peritonitis, which required multiple surgical interventions and
the use of reserve antibiotics, the second case resulted in liver and
renal failure that led to the death of the patient.

\textbf{Conclusion:} This case series describes the unusual severe
toxicity of two herbal medicines that are frequently used to induce
abortion in Northern Uganda. It highlights possible associations
of\emph{Commelina Africana} (wandering jew) with uterine necrosis
complicated by pyometra and sepsis, and of \emph{Vernonia
amygdalina}(bitter leaf) with acute liver failure and renal failure.

\textbf{Keywords:} Unsafe abortion, herbal medicines, herbs, northern
Uganda, case series

\textbf{Background}

Worldwide, the leading causes of maternal morbidity and mortality are
direct obstetric complications and include hemorrhage, sepsis,
hypertensive disorders, and abortion; the latter is responsible for
7.9\% of maternal deaths globally and 9.6\% in Sub-Saharan Africa (SSA)
{[}1{]}. The World Health Organization defines unsafe abortion as a
procedure for terminating a pregnancy performed by people lacking the
necessary skills or in an environment, not in conformity with minimal
medical standards, or both {[}2{]}.

In Uganda, although the official data of the Ministry of Health indicate
that abortion accounts for 5\% of maternal deaths {[}3{]}, the mortality
due to abortion complications could be higher due to restrictive laws.
It is estimated that 297,000 unsafe abortions are performed yearly, with
an abortion rate of 54 per 1,000 women aged 15-49. Nearly 85,000 women
have been treated annually for complications of unsafe that include
incomplete abortion, sepsis, and uterine perforations {[}4{]} making it
the main gynecologic cause of admission, leading to about 1,200 deaths
annually {[}5{]}.

The abortion rate is even higher in northern Uganda (70 per 1,000 women
aged 15-49 years) {[}4{]}, a predominantly rural region that is still
recovering from a 20-year conflict that left many people displaced from
their homes and economically disadvantaged. One of the factors
contributing to the high number of abortion complications is the unmet
need for contraception, which is still very high (28\%). Contraceptive
use in Uganda remains very low; only 17\% of all women of reproductive
age, and 18\% of married women, utilize modern contraception {[}6{]}.
This has resulted in a high total fertility rate (TFR) of 5.4 {[}7{]}.
It is estimated that almost half of the pregnancies in Uganda are
unintended, with 15\% of the total pregnancies ending in unsafe abortion
and constituting nearly one-third of the maternal deaths among the
country's young people {[}8{]}. The situation is even more dramatic
among rural, poor, and less educated women, such as in the northern
region.

Legal provisions for abortion in Uganda are very restrictive. Art. 22(2)
of the Constitution of Uganda (1995) quotes: ``\emph{No person has the
right to terminate the life of an unborn child except as may be
authorized by law} ''. The Penal Code Act (Cap. 120), as amended through
the Penal Code Amendment Act (No. 8 of 2007), Section 205, allows only
abortion if ``\emph{carried out in good faith to preserve the mother's
life''} . Therefore, safe `legal' abortion is not available and
accessible, except for rare cases where it is the only way to save a
woman's life, and many healthcare providers prefer not to offer safe
abortion to women who need it {[}9{]}. It is known that highly
restrictive laws do not reduce abortion rates, but rather increase the
likelihood of unsafe abortion {[}10{]}. Consequently, in a country like
Uganda where abortion is highly stigmatized {[}11, 12{]}, many women
seek illegal abortion with unsafe traditional methods, offered by
non-medical providers under unsafe conditions. While in urban areas the
use of prostaglandin analogs is the most common method of unsafe
abortion, in rural areas women resort to the intra-vaginal use of sharp
objects (safety pins, nails, knives or sticks), to the ingestion of
caustic substances (detergents or bleach) and more often to the use of
local herbs, such as \emph{Commelina Africana} and \emph{Vernonia
amygdalina} , which are readily available in the countryside {[}13{]}.

In this small case series, we described two cases of unsafe abortions
induced with very common herbs in northern Uganda, which ended up with
severe complications and, in one case, led to the death of the woman.

\textbf{Case presentation:}

\emph{Case 1}

N.A., a 31-year old female, para 2, abortus 1, at 5 weeks of amenorrhea
and HIV negative, was admitted to our Gynecology ward via the Emergency
Department. The patient presented with a 2-week history of lower
abdominal pain, 3 days of vomiting, and 2 days of loose stools. She did
not report any bleeding or discharge per vagina; the micturition habit
was normal. She reported not being pregnant in recent months and that
the symptoms started spontaneously, without any identifiable cause, and
worsened progressively.

At admission, the patient was conscious, with Glasgow Coma Scale (GCS)
of 15/15, but pale and in obvious discomfort; her blood pressure (BP)
was 96/56 mmHg, pulse rate (PR) was 112 beats per minute and temperature
was 38.7\selectlanguage{ngerman}°C. Abdominal examination revealed severe distension,
generalized tenderness, and guarding; bowel sounds were present. The
vaginal examination demonstrated no active bleeding but moderate
foul-smelling discharge; the cervical os was closed. At the bimanual
examination, the uterus was bulky, with severe cervical motion
tenderness. The physical examination of the other systems was
unremarkable.

Her blood investigations showed hemoglobin (Hb) of 6.5 gm/dl, white cell
count of 32.3×10\textsuperscript{9}/l, platelets of
105×10\textsuperscript{9}/l. The urine human chorionic gonadotropin
(hCG) quick test was positive. A pelvic ultrasound (US) scan showed an
empty and bulky uterus, normal-looking ovaries, and the presence of an
echogenic pelvic mass; a diagnosis of a pelvic abscess was made and an
exploratory laparotomy planned, after resuscitation of the patient.
During the exploratory laparotomy, the uterus was severely necrotic and
there was pus collection of 2 litres in the paracolic gutters and the
sub-diaphragmatic recess.

During the postoperative period, antibiotic therapy with intravenous
first line broad-spectrum antibiotics was performed, but the patient
remained febrile and started discharging pus from the laparotomy wound
on the 5\textsuperscript{th} postoperative day. A wound swab culture was
performed, revealing a multi-resistant \emph{Escherichia coli} ,
sensitive to Gentamicin and Chloramphenicol. Therapy with a combination
of these antibiotics did not show any improvement in the following days
and, on the 15\textsuperscript{th}postoperative day, the incision site
started gaping, with copious pus discharge.

A further pelvic ultrasound scan showed an echo-complex fluid collection
in the pouch of Douglas, with a volume of around 265ml; the findings
were in line with a pelvic abscess. A repeat laparotomy confirmed the
diagnostic hypothesis and an extensive pelvic lavage was done. The
patient was treated postoperatively with a reserve antibiotic
(intravenous Meropenem) and after 10 days was discharged home in good
general conditions, on oral antibiotics. At discharge from the hospital,
the patient reported having induced the abortion with a local herb,
known as ``wandering jew'', three weeks before admission, by inserting
some pieces of the stem of the plant in the vagina; a few days after the
expulsion of the fetus, she started developing lower abdominal pain and
abdominal distension, associated with per vagina foul-smelling
discharge.

\emph{Case 2}

A.E., a 24-year-old female, gravida 4, para 3, at unknown weeks of
amenorrhea, was admitted to our Gynecology ward with a history of fever
and chills, general body weakness, tea-colored urine and cramping lower
abdominal pain, radiating to the waist, that started spontaneously and
increased progressively in intensity. There was no history of vomiting
or nausea, vaginal bleeding, or discharge; the patient reported normal
micturition and bowel habits. The history of complaints of other systems
was unremarkable.

The patient, who was married with three living children, did not attend
antenatal care for the current pregnancy; obstetric and gynecological
histories were unremarkable. There was no history of chronic illnesses,
while the HIV status was unknown. The patient denied the use of herbal
medicine or any other medication in this pregnancy.

On physical examination, she was sick looking, with moderate pallor,
severe jaundice with dry mucous membranes, dry skin, and no edema. Her
BP was 93/61 mmHg, with PR of 94 beats per minute and a temperature of
36.8°C.

Abdominal examination revealed a normal fullness, with a moderate
tenderness in the hypogastric region; no organomegaly or masses were
palpable. On per vagina exam, vulva and vagina were normal, the cervical
os was closed and there was no active bleeding or discharge. The
physical examination of the other systems was unremarkable.

Her investigations showed a positive urine hCG quick test, while the
blood smear did not evidence any malaria parasites. The complete blood
count showed a white cell count of 28.1× 10\textsuperscript{9}/L, with
granulocytes of 20.5x10\textsuperscript{9}/L, Hb of 11.7g/dl, and red
blood cells of 3.66×10\textsuperscript{12}/L, platelets of
270×10\textsuperscript{9}/L and negative hepatitis B surface antigen
test. Liver function: Alanine transferase of 1,796U/L (0-40), Aspartate
transferase of 1,628U/L (0-37), Alkaline phosphatase of 159 U/L (98-279)
and albumin of 2.5g/dl (3.8-5.1). Renal function test: urea of 82mg/dl
(10-55), creatinine of 7.1mg/dl (0-1.3) and urea/creatinine ratio of
11.54. Serum electrolytes: sodium of 128.2mmol/L (134-146), potassium of
4.6mmol/L (3.5-5.5) and chloride of 105.9mmol/L (98-108).

A pelvic ultrasound scan showed a gravid uterus with an intrauterine
fetus in cephalic presentation, but no cardiac activity was present; the
amniotic fluid was reduced and the internal cervical os was open.
Moreover, the left maternal kidney was mildly enlarged and echogenic,
with normal margins. The findings of the ultrasound scan were in line
with a missed abortion at 14 weeks of gestation and maternal left
nephropathy. Our impression was a para 3, abortus 1, with missed
abortion at 14 weeks of gestation, acute hepatitis, and nephropathy. The
patient was stabilized and managed conservatively, without relevant
improvement.

On the 2\textsuperscript{nd} day of hospital stay, there was a new
complaint of bleeding per vagina; the patient was still sick looking,
afebrile, with moderate pallor and deep jaundice. Her BP was 110/65
mmHg, with PR of 69 beats per minute and random blood sugar (RBS) of 3.4
mmol/L. On per vagina examination, the cervical os was still closed but
fresh blood was found on the examining finger. The patient was treated
with dextrose, lactulose, and broad-spectrum antibiotics; after the
administration of one dose of Misoprostol, the fetus and the placenta
were expelled. Thereafter, the patient was restless, although the vital
parameters were in the normal range.

On the 3\textsuperscript{rd} day of hospital stay, the patient became
lethargic, with slurred speech and restless, moderately pale, and
increasingly jaundiced. Her BP was 119/73 mmHg, with PR of 69 beats per
minute, temperature of 36.7°C and RBS of 4.5mmol/l. GCS was 12/15 (E=4,
M=5, V=3), with pupils equal and reactive to light, normal tone, and
reflexes. The patient was in mild respiratory distress, with a
respiratory rate of 28 breaths/minute and oxygen saturation of 95\% on
room air. The urine was greenish, with a urine output of 300ml/24hrs. A
nasogastric tube was inserted and drained 200 ml of dark brown colored
fluids. The patient was lethargic and disoriented to time; a diagnosis
of hepatic encephalopathy grade 2, based on West Haven criteria, was
made and the plan was to continue the conservative therapy. On the early
morning of the 4\textsuperscript{th} day of hospital stay, the patient
passed away.

Only after her death, a collateral history could be obtained. The
patient's husband, who wanted more children, wasn't aware that his wife
was pregnant. The couple had previously argued on this issue since the
patient was not willing to face a new pregnancy, but the husband
prohibited her from using any modern contraceptive methods. As reported
by the mother in law, when the patient realized that she was pregnant,
she consulted a traditional healer, who provided her a local herb known
as ``bitter leaf''.

\textbf{Discussion and conclusion:}

In Uganda, medicinal plants are widely used by indigenous ethnic groups,
both as food vegetables and culinary herbs and in traditional medicine.
In a study conducted in western Uganda, 75 plants commonly used to
induce labor have been identified; most of them possess uterotonic
properties and, at unspecified high doses, their toxicity may be
life-threatening for both the mother and the fetus {[}14{]}.

In northern Uganda, two plants are commonly used to induce labor, i.e.
the \emph{Commelina Africana} , also known as \emph{``} wandering jew''
(Figure 1), and the \emph{Vernonia amygdalina} , also known
as\emph{``bitter leaf''} (Figure 2). The uterotonic properties of these
herbs have been already tested and confirmed {[}15{]}. \emph{Commelina
Africana} (\textbf{``} Wandering jew''; ``Lototo'' in Acholi language
and ``Otoro'' in Luo language), is known to have hypoglycemic effects
{[}10{]}, as well as uterotonic activity; in fact, it can increase both
the force of contractions and their frequency, with a dose-response
curve {[}15{]}. To induce abortion, the stem of the plant is normally
broken in small pieces and inserted in the vagina, adjacent to the
cervix, to induce it to dilate {[}14{]}. The severe complications due to
the use of this herb, as reported in Case 1, seem to be due to its
insertion in the vagina under unsterile conditions, which allow the
ascension of pathogens to the pelvic cavity passing through the cervix,
the uterus and the fallopian tubes, causing massive pelvic abscesses,
severe peritonitis, and septic shock. In our case, this condition
required multiple surgical interventions with extensive abdominal
lavage, as well as the use of reserve antibiotics.

\emph{Vernonia amygdalina} (``Bitter leaf''; ``Labwori'' in the Acholi
language and ``Olusia'' in Luo language) is an indigenous shrub that
grows in most parts of sub-Saharan Africa and may be found growing wild
along the edges of agricultural fields. It grows to a height of 1-2~m,
with elliptical leaves up to 20~cm long. It is commonly called ``bitter
leaf'' in English because of its bitter taste. As reported by Echemet
al.{[}16{]}, \emph{Vernonia amygdalina} plays a big role in the diet of
indigenous people throughout equatorial Africa because of the presence
of vitamins and mineral salts {[}15{]}. For numerous African ethnic
groups, it is also considered a very strong medicine in the treatment of
malarial fever, schistosomiasis, amoebic dysentery, and several other
intestinal parasites and stomach aches; extracts thereof have been also
used traditionally in the treatment of sexually transmitted diseases,
cough, constipation, and hypertension. Its ability to contract the
uterus, thereby inducing abortion, has been validated {[}15{]}.
\emph{Vernonia} species contain phytochemical principles, which include
bitter sesquiterpene lactones, vernolepin, vernodalin, vernomygdin, and
steroid glucosides, from which its biological properties were derived
{[}17{]}. \emph{Vernonia amygdalina,}especially those grown along heavy
traffic routes, can concentrate high levels of heavy metals such as
\emph{Iron (Fe), Manganese (Mn), Lead (Pb), chromium (Cr), Zinc (Zn) and
Cadmium (Cd)} ; which have the potential to act as biological poisons
even at parts per billion levels, {[}16{]}. The concentration of these
metals is highest in the leaves, which are commonly used for decoctions.

In case 2, the use of \emph{Vernonia amygdalina} led to complications
requiring admission to the hospital; the patient presented with reduced
GCS due to hepatic encephalopathy, associated with other signs of acute
renal and liver failure. Typical laboratory findings were hypoglycemia,
leucocytosis, and elevated liver enzymes, associated with elevated
creatinine and urea values. The course of the disease was deadly.

In conclusion, we reported two cases describing the unusual severe
toxicity of two herbal medicines that are frequently used to induce
abortion in northern Uganda. In particular, the use of \emph{Commelina
Africana} may be associated with pyometra and/or pyoperitoneum and
sepsis, while \emph{Vernonia amygdalina} may lead to acute liver and
renal failure, which can be fatal.

The ingestion of medicinal plants to induce abortion involves the risk
of severe maternal morbidity and mortality; patients should be informed
that the use of these medicinal plants as abortifacients can be
life-treating. Active policy to improve knowledge of contraception and
family planning is required.

Moreover, further field and laboratory research is needed to identify
the active principles contained in such herbal medicines and their
biological properties, to achieve a better understanding of their
pathophysiology, dosage levels, and toxicity. This would help in the
treatment of the associated complications and the development of
possible antidotes.

\textbf{Declarations:}

\textbf{List of abbreviations:}

BP: blood pressure; GCS: Glassgow coma scale; Hb: hemoglobin; hCG: human
chorionic gonadotropin; HIV: human immunodeficiency virus; PR: pulse
rate; SSA: sub-Saharan Africa; TFR: total fertility rate.

\textbf{Ethical approval and consent to participate:}

Ethical approval was provided by the Lacor Hospital Institutional
Research Ethics Committee. Before making this case series, written
informed consent was obtained from the patient (case 1) and the next of
kin of the deceased patient (Case 2). The patients' identities were duly
concealed.

\textbf{Consent for publication:}

Written informed consent for publication of this case series and the
accompanying images was obtained from the patient (Case 1) and the next
of kin of the deceased patient (Case 2).

\textbf{Availability of data and materials:}

All data generated or analyzed during this study are included in this
manuscript.

\textbf{Competing interests:}

The authors declare no conflicts of interest.

\textbf{Funding:}

There was no external funding to support this case report.

\textbf{Authors' contribution:}

CR and GA wrote the case report Background and Discussion; VN collected
the information on the patients and compiled the Case Presentation; LS
made the final review and editing of the manuscript before submission.
All authors have read and approved the manuscript.

\textbf{Acknowledgments:}

We would like to acknowledge the entire staff of the gynecology ward at
Lacor Hospital, especially the nurses who attended the patients during
their hospital stay. We would like to thank the patients' next of kin,
who consented to the preparation and publication of this case series. We
finally acknowledge the Mother-Child Health Lacor and South Sudan
(MoCHeLaSS) project, which facilitated the training of some team members
in research methods.

\textbf{References:}

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e323-e333.

2. Ganatra, B., et al., \emph{From concept to measurement:
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Public Health.

3. \emph{Ministry of Health,The Annual Health Sector Performance Report
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4. Singh, S., et al., \emph{The incidence of induced abortion in
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5. Mulumba, M., et al., \emph{Access to safe abortion in Uganda:
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6. Musoke, J.T. and B. Tolboom, Uganda Country Report - Country Needs
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7. Uganda Bureau of Statistcs (UBOS) and ICF, \emph{Uganda Demographic
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Rockville: Kampala, Uganda and Maryland, USA.

8. Hussain, R., \emph{Unintended pregnancy and abortion in
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9. Paul, M., et al., \emph{Barriers and facilitators in the provision of
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10. Singh, S., et al., \emph{Abortion worldwide 2017: uneven Progress
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11. Larsson, S., et al., \emph{The discourses on induced abortion in
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12. Cleeve, A., et al., \emph{Abortion as agentive action: reproductive
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13. Kiguba, R., et al., \emph{Herbal medicine use and linked suspected
adverse drug reactions in a prospective cohort of Ugandan
inpatients.}BMC complementary and alternative medicine, 2016.
\textbf{16} (1): p. 145.

14. Kamatenesi-Mugisha, M. and H. Oryem-Origa, \emph{Medicinal plants
used to induce labour during childbirth in western Uganda.} Journal of
ethnopharmacology, 2007. \textbf{109} (1): p. 1-9.

15. Rasch, V., et al., \emph{Unsafe abortion in rural Tanzania--the use
of traditional medicine from a patient and a provider perspective.} BMC
pregnancy and childbirth, 2014. \textbf{14} (1): p. 419.

16. Echem, O.G. and L. Kabari, \emph{Heavy metal content in Bitter Leaf
(Vernonia amygdalina) grown along heavy traffic routes in Port
Harcourt.} Agricultural Chemistry, 2013: p. 201-210.

17. Clement, E. et al., \emph{Significance of Bitter Leaf (Vernonia
Amagdalina) In Tropical Diseases and}

\emph{Beyond: A Review} . Malaria Chemotherapy Control and Elimination,
2014. \textbf{3} (1): p. 1-10.

\textbf{Figure Legends:}\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/image1/image1}

\end{center}
\end{figure}

Figure 1 -- \emph{Commelina Africana} or \emph{``} wandering jew''

Figures 1 and 2 are photographs of the herbs that were reportedly used
by the two cases following lead by the traditional herbalists who
administered them. The photographs were taken by the authors, CR and GA.\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/image2/image2}

\end{center}
\end{figure}

Figure 2 -- \emph{Vernoniaamygdalina} or ``bitter leaf''

\selectlanguage{english}
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